Bird Diversity and Distribution in relation to Urban Landscape Types in Northern Rwanda · 2016. 1....

12
Research Article Bird Diversity and Distribution in relation to Urban Landscape Types in Northern Rwanda T. Gatesire, 1,2 D. Nsabimana, 1 A. Nyiramana, 1 J. L. Seburanga, 1 and M. O. Mirville 2 1 University of Rwanda, P.O. Box 117, Butare, Rwanda 2 Karisoke Research Center, Dian Fossey Gorilla Fund International, 800 Cherokee Avenue Southeast, Atlanta, GA 30315-1440, USA Correspondence should be addressed to T. Gatesire; [email protected] Received 31 March 2014; Accepted 29 June 2014; Published 15 July 2014 Academic Editor: Getachew Dagne Copyright © 2014 T. Gatesire et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Using the point count method, linear mixed models, Shannon’s diversity index, and Bray-Curtis cluster analysis, we conducted a study of the effect of urban fabric layout on bird diversity and distribution in northern Rwanda. e results showed a significant effect of city landscapes on bird richness and relative abundance; residential neighborhoods, institutional grounds, and informal settlements had the highest species diversity in comparison to other microlandscape types. Riversides were characterized by specialized bird species, commonly known to be restricted to wetland environments. Built-up areas and open field landscapes had comparable results. One Albertine Riſt endemic bird species, the Ruwenzori Double-collared Sunbird (Cinnyris stuhlmanni), was recorded. ree migratory birds were found in Musanze city for the first time: the Common Sandpiper (Actitis hypoleucos), the Spotted Flycatcher (Muscicapa striata), and the Willow Warbler (Phylloscopus trochilus). Two bird species have not been previously reported in Rwanda: the Garden Warbler (Sylvia borin) and the Lesser Spotted Eagle (Aquila pomarina). e implications of this study are particularly relevant to urban decision makers who should consider the existence of a great diversity of avian fauna when developing and implementing master plans, especially when villages and cities are in proximity of protected areas or natural reserves. 1. Introduction By the year 2050, it is estimated that the majority of the global population will live in urban areas [1]. reats to biodiversity are particularly inherent to such rapid urbanization, which raises concern over the future of the already reduced diversity in settings surrounding urban neighborhoods [2]. In many developing countries, a large number of wildlife survive outside protected areas on farmlands, pasturelands, and in urban areas [3, 4]. Among all wildlife, birds are one of the most common wildlife in urban areas such as neighborhoods and cities, and many bird populations have been declining as a result of landscape changes due to urban expansion [58]. At the local level, these major changes include high rates of land conversion into urban uses and increasing human pressure on biodiversity due to rapid population growth. Due to the important role that birds play in maintaining ecosystems and supporting biodiversity, many seek their protection to manage biological threats and efficiently protect the environment [9]. Birds fulfill many ecological functions in their habitats. For instance, they are bioindicators of healthy ecosystems [10, 11]. In addition, insectivorous species and raptors regulate disease vectors, including mosquitoes and rodents. Scavenger birds, such as the Pied Crow (Corvus albus), contribute to biomass recycling and to some degree reduce levels of disposable wastes. Frugivorous birds play an important role in seed dispersal of fleshy fruit-producing plants [9]. Birds are also important in plant pollination as demonstrated by sun- birds, which participate in crossbreeding of flowering plants, especially those with bird-pollination syndrome [12]. ese ecosystem services are important for many communities, and to ensure that birds can fulfill these biological roles at an appropriate level for current and future generations, there is a pressing need to study the dynamics and socioeconomics Hindawi Publishing Corporation e Scientific World Journal Volume 2014, Article ID 157824, 12 pages http://dx.doi.org/10.1155/2014/157824

Transcript of Bird Diversity and Distribution in relation to Urban Landscape Types in Northern Rwanda · 2016. 1....

Page 1: Bird Diversity and Distribution in relation to Urban Landscape Types in Northern Rwanda · 2016. 1. 26. · ResearchArticle Bird Diversity and Distribution in relation to Urban Landscape

Research ArticleBird Diversity and Distribution in relation to Urban LandscapeTypes in Northern Rwanda

T Gatesire12 D Nsabimana1 A Nyiramana1 J L Seburanga1 and M O Mirville2

1 University of Rwanda PO Box 117 Butare Rwanda2 Karisoke Research Center Dian Fossey Gorilla Fund International 800 Cherokee Avenue Southeast Atlanta GA 30315-1440 USA

Correspondence should be addressed to T Gatesire gatesire2000yahoofr

Received 31 March 2014 Accepted 29 June 2014 Published 15 July 2014

Academic Editor Getachew Dagne

Copyright copy 2014 T Gatesire et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Using the point count method linear mixed models Shannonrsquos diversity index and Bray-Curtis cluster analysis we conducted astudy of the effect of urban fabric layout on bird diversity and distribution in northern Rwanda The results showed a significanteffect of city landscapes on bird richness and relative abundance residential neighborhoods institutional grounds and informalsettlements had the highest species diversity in comparison to other microlandscape types Riversides were characterized byspecialized bird species commonly known to be restricted to wetland environments Built-up areas and open field landscapeshad comparable results One Albertine Rift endemic bird species the Ruwenzori Double-collared Sunbird (Cinnyris stuhlmanni)was recordedThree migratory birds were found inMusanze city for the first time the Common Sandpiper (Actitis hypoleucos) theSpotted Flycatcher (Muscicapa striata) and theWillowWarbler (Phylloscopus trochilus) Two bird species have not been previouslyreported in Rwanda the Garden Warbler (Sylvia borin) and the Lesser Spotted Eagle (Aquila pomarina) The implications of thisstudy are particularly relevant to urban decision makers who should consider the existence of a great diversity of avian faunawhen developing and implementing master plans especially when villages and cities are in proximity of protected areas or naturalreserves

1 Introduction

By the year 2050 it is estimated that themajority of the globalpopulation will live in urban areas [1] Threats to biodiversityare particularly inherent to such rapid urbanization whichraises concern over the future of the already reduced diversityin settings surrounding urban neighborhoods [2] In manydeveloping countries a large number of wildlife surviveoutside protected areas on farmlands pasturelands and inurban areas [3 4] Among all wildlife birds are one of themost common wildlife in urban areas such as neighborhoodsand cities and many bird populations have been decliningas a result of landscape changes due to urban expansion [5ndash8] At the local level these major changes include high ratesof land conversion into urban uses and increasing humanpressure on biodiversity due to rapid population growth

Due to the important role that birds play in maintainingecosystems and supporting biodiversity many seek their

protection tomanage biological threats and efficiently protectthe environment [9]

Birds fulfill many ecological functions in their habitatsFor instance they are bioindicators of healthy ecosystems[10 11] In addition insectivorous species and raptors regulatedisease vectors includingmosquitoes and rodents Scavengerbirds such as the Pied Crow (Corvus albus) contributeto biomass recycling and to some degree reduce levels ofdisposable wastes Frugivorous birds play an important rolein seed dispersal of fleshy fruit-producing plants [9] Birds arealso important in plant pollination as demonstrated by sun-birds which participate in crossbreeding of flowering plantsespecially those with bird-pollination syndrome [12] Theseecosystem services are important formany communities andto ensure that birds can fulfill these biological roles at anappropriate level for current and future generations there isa pressing need to study the dynamics and socioeconomics

Hindawi Publishing Corporatione Scientific World JournalVolume 2014 Article ID 157824 12 pageshttpdxdoiorg1011552014157824

2 The Scientific World Journal

of bird diversity outside protected areas especially in urbanareas

The landscape of the Musanze District in the NorthernProvince of Rwanda has been undergoing major changesdue to rapid urbanization driven by a fast growing humanpopulation [13] Human density in this region can reach upto 1000 people per km2 [14] and it is estimated that morethan half of the total Rwandan population is expected tolive in urban areas in less than 40 years [15] High rates ofland conversion into urban use inMusanze is threatening thewild avian diversity as it is the case for other fast growingcities in the world [16] More than half of the total Rwandanpopulation is expected to live in urban areas in less than 40years [15]

While wild avian diversity has been a subject of researchin natural habitats of the Northern Province especially inthe Parc National des Volcans (PNV) and the Buhanga eco-park the biodiversity of the neighboring Musanze city likemany other anthropogenic landscapes remains understud-ied Thus this study aimed to address the issue of ecologicalbias in bird diversity and distribution in fast growing citiesand proposes strategies for effective conservation of birds inurban areas of Rwanda and of Musanze city in particularThe main objective of this study was to assess the diversityand distribution of birds in urban landscape types of theMusanze city Specifically the study aimed (1) to identify birdspecies that live in or visit Musanze city (2) to identify birdfeeding guilds bird abundance and bird diversity in differentlandscapes in Musanze (3) to locate areas of the city thatshow high bird diversity hereafter referred to as ldquourban birdhotspotsrdquo and (4) to compare the bird diversity in Musanzecity with the bird diversity found in the PNV and Buhangaeco-park which are two important ecological zones in theadministrative district where Musanze city is located Ourstudy therefore provides policy makers and conservationistswith scientific information about the ecological status of birdsin Musanze city and how species are distributed in the city inrelation to the urban fabric layout

2 Materials and Methods

21 Study Area Musanze District is situated in the north-western highlands of Rwanda and is one of the five admin-istrative districts within the Northern Province The studywas carried out within Musanze city which covers a totalarea of 6197 km2 and is comprised of four sectors MuhozaCyuve Musanze and Kimonyi Musanze is one of the largestand fastest growing urban centers in Rwanda and is a centralhub for businesses trade and tourism The PNV with itsfamous mountain gorillas the Buhanga eco-park and theRuhondo Lake are found in Musanze and make the city apopular destination for national and international tourists(httpwwwmusanzegovrw 30122012)

22 Landscape Stratification Landscapes ofMusanze city canbe classified into two major categories open fields and built-up areas Open fields can include agricultural land ceme-teries wastelands stream banks forests and the aerodrome

which is a nonpaved strip covered by a regularly mownlawn of about 15 km length Built-up areas include businesscenters institutional grounds settlements and residentialneighborhoods

In this study agricultural land referred to cultivated landslocated within Musanze surrounding urban areas wheremaize and beans are the most common crops We includedtwo cemeteries in our sampling sites which were located inthe Muhoza and Cyuve sectors Wastelands were defined asareas dedicated to household solid waste disposal Twowaste-lands were considered for the study one close to Musanzebusiness center and another in Cyuve We considered streambanks as land that encompassed habitats on both sides ofpermanent or seasonal river flows Forests included areascovered by tree plantations mainly Eucalypts Natural forestswere not found within the city boundaries The Musanzeaerodrome is a nonpaved strip covered by a regularly mownlawn of about 15 km length

Business centers included market places and areas witha high concentration of shops Institutional grounds werecomprised of large institution gardens including the districtoffice Musanze hospital one university one high schooland the city abattoir Informal and nonformal settlementsincluded organized village settlements and rural type scat-tered settlements where banana plantations were the mostcommon crop in the home gardens Residential neighbor-hoods were high standard settlement areas of the city

23 Data Collection DuringMarch 2012 data were collectedwithin plots using the point count method [17] The pointcount sampling design consisted of a series of points atwhich birds were counted within a defined radius [18] Forty50m radius plots were established using a global positioningsystem (GPS) unit twenty in open fields and other twentyin built-up areas (Table 1) Between two and five plots wererandomly selected for each microlandscape type (Table 1)within a 04 times 04 km grid at a rate of one plot per grid cellEach plot was visited four times for a ten-minute observationperiod [19] such that this study included 160 plot visitsin total Visits to each plot were equally distributed acrossfour periods during the day early morning (630ndash830)late morning (900ndash1100) early evening (1500ndash1700) andlate evening (1730ndash1830) As the weather can influence theoccurrence of some bird species [20] working during rain orstrong wind was avoided

In addition to a presurvey training of data collectorson bird identification a bird expert was present in 96of our field visits A pair of 8 times 42 resolution binoculars(Olympus mark) and a field guide book were also usedto identify the species of birds observed [9] Five minutesafter the plot was located the center was chosen wheneverpossible to observe any bird movement This time delay wasin place to allow birds to return to their natural behaviorin order to minimize potential impacts of human presenceon the survey The following variables were recorded duringeach 10min observation period number of plot type ofmicrolandscape arrival time departure time species namesof birds observed number of individuals from each observed

The Scientific World Journal 3

Table 1 Distribution of plots across microlandscape types and administrative sectors

Landscape types Category Sectors Number of plotsAerodrome Open field Muhoza 2Agrofields Open field Muhoza Cyuve 5Business centers Built-up Musanze Muhoza Cyuve 5Cemeteries Open field Muhoza 2Forests Open field Musanze Muhoza Cyuve 5Institutional grounds Built-up Musanze Muhoza 5Residential neighborhood Built-up Muhoza 5Riversides Open field Muhoza 2Informal settlements Built-up Kimonyi Muhoza 5Streamsides Open field Musanze 2Wastelands Open field Muhoza Cyuve 2

bird species weather conditions vegetation cover and anykind of disturbance such as extra human presence or noisefrom nearby vehicles

Birds encountered outside of our study plots wererecorded only when it was a locally novel species suchthat it had never been observed in the area before Theserecords were only considered for compiling a bird checklistof Musanze city and were therefore excluded from statisticalanalysis When a bird could not be identified in the fieldphotos from a high-resolution camera and descriptive noteswere taken for later identification by a bird expert

24 Data Analysis The linear mixed models (LMM)methodwas used to analyze the relationships between landscape birdabundance and species richness LMM recently became auseful tool used to analyze continuous repeated measuresdata from a sample of individuals in different areas [21] LMMis a statistical model that consists of both fixed effects andrandom-effects terms and was therefore themost appropriatechoice for our study [22] In this study LMM was used toassess whether urban landscape types have an effect on birdabundance and species richness Landscape types (macro-and microlandscapes) were fixed effects (covariates) whilesampling plots were treated as a random effect to control forrepeated measures in plots Bird species richness and relativeabundance were dependent variables assessed in differentLMMs

The Shannonrsquos diversity index (1198671015840 = minussum119901119894log119901119894 where

119901119894is the proportion of individuals belonging to the 119894th

species) was used to identify the 120572-diversity of bird speciesboth at city and landscape type levels in order to identify thelocal average species diversity of each particular habitat TheBray-Curtis cluster analysis (single link) method was usedto assess the level of similarity in bird composition betweenlandscape types [23]

Referring to Tuyisingize and Fawcett [24] fromwhich weretrieved the checklist of birds of the PNV and Buhanga eco-park the bird diversity and abundance of Musanze city werecompared with the two natural ecosystems of these parksin terms of bird species richness and composition using thehierarchical clustering method

To examine the relationship between bird species andfood availability in the city bird species were categorizedaccording to their feeding guilds The completeness of thesurvey was assessed by analyzing patterns of the species accu-mulation curves [25] The accumulation curves of speciesrichness in different microlandscape types globally reachedtheir plateau (Figure 1) giving us confidence to conclude thatour sampling efforts had covered the majority of species inMusanze

To determine the level of significance of the obtainedresults hypothesis testing tools were used including thetest of Studentrsquos 119905-test Bioprofessional MVSP Origin and Rsoftware packages were used for these analyses

3 Results

31 Species Richness A total of 94 bird species were observedin Musanze city 15 of which were found opportunisticallyoutside plots Only one Albertine Rift endemic species(Ruwenzori Double-collared Sunbird Cinnyris stuhlmanni)was observed and seven migrant bird species were recorded

311 Number of Bird Species by Macrolandscape Types Therewas no significant difference in the number of bird species inopen fields and built-up areas (119905 = minus042 119875 = 067 Figure 2)Similarly the total number of bird species observed in bothmacrolandscapes was not notably different (119873 built-up = 63119873 open fields = 61)

312 Number of Species by Microlandscape Types Amongthe different microlandscapes institutional grounds had thehighest number of species (119873 = 42) followed by residentialneighborhoods (119873 = 41) and informal settlements (119873 =37) Furthermore forest and riverside landscapes had similarnumber in terms of total number of species (119873 = 35 forboth) Finally wastelands and the aerodrome demonstratedthe smallest number of bird species (119873 = 16 and 119873 = 15resp) (Figure 3)

For the LMM that examined the impact of differentmicrolandscapes on the number of bird species residentialneighborhoods were used as the reference microlandscape

4 The Scientific World Journal

50

40

30

20

10

0

0 200 400 600 800

Number of individuals

Num

ber o

f spe

cies

Rarefaction plot

WastelandsAerodromeCemeteriesAgrofieldsForestRiverside

StreamsideBusiness centersInstitutional groundInformal settlementResidence neighborhood

Figure 1 Bird species rarefaction curves at the site considered inthis study

Built-up areas Open fields0123456789

101112

Mea

n nu

mbe

r of b

ird sp

ecie

s per

visi

t

Macrolandscape types

Figure 2Mean number of species observed during plot visits in thetwo macrolandscape types

type as it showed the highest average number of bird speciesper plot visit (Figure 4) Thus the average number of birdspecies found in any other microlandscape was compared tothe number of bird species found in residential neighbor-hoods The LMM analysis revealed that the average numberof bird species found in all microlandscapes excluding ceme-teries and riversides was significantly lower than the numberof bird species in residential Musanzersquos neighborhood areas(Table 2) The average number of bird species observed in

IG RN IS FT RD AF CM SS BC WL AM0

10

20

30

40

Num

ber o

f spe

cies

Microlandscape types

Figure 3 Total bird species in microlandscape types (AM aero-drome AG agrofields BC business centers CM cemeteries FTforests IS informal settlements IG institutional grounds RNresidential neighborhoods RS riversides SS streamside WLwasteland)

Table 2 LMM output showing parameter estimates of microland-scape types on the number of bird species

Landscape types Std error 119905 value 119875 valueIntercept 074 15338 lt0001Aerodrome 139 minus5502 lt0001Agrofield 105 minus3330 lt001Business centers 105 minus6374 lt0001Cemeteries 139 minus1816 0069Forests 105 minus3473 lt001Institutional ground 105 minus2807 lt001Riversides 139 minus0827 0408Informal settlements 105 minus3330 lt001Streamside 139 minus2445 lt005Wastelands 139 minus2625 lt001

plots located in cemeteries tended to be less than the averagenumber found in residential neighborhoods

32 Species Relative Abundance

321 Number of Individuals by Macrolandscape Types Therewas no significant difference between open fields and built-up areas in terms of number of bird individuals observed pervisit (119905 = 035 119875 = 073 Figure 5)

322 Number of Individuals by Microlandscape Types Therewere significantly less birds in all microlandscape typescompared to the number of birds encountered in plotslocated in residential neighborhoods except for cemeteries(where fewer birdswere observed) riversides andwastelands(Figure 6 and Table 3)

The Scientific World Journal 5

AM AG BC CM FT IS IG RN RS SS WL0

2

4

6

8

10

12

14

16

Microlandscape types

Mea

n nu

mbe

r of b

ird sp

ecie

s per

visi

t

Figure 4 Mean number of bird species observed during plot visitsin each microlandscape type (AM aerodrome AG agrofields BCbusiness centers CM cemeteries FT forests IS informal settle-ments IG institutional grounds RN residential neighborhoods RSriversides SS streamside WL wasteland)

0

5

10

15

20

25

30

35

40

Mea

n nu

mbe

r of b

ird in

divi

dual

s per

visi

t

Built-up areas Open fieldsMacrolandscape types

Figure 5Mean number of bird individuals encountered per visit bymacrolandscape type

323 Most Represented Species The Pied Crow (Corvusalbus) the Grey-headed Sparrow (Passer griseus) StreakySeedeater (Serinus striolatus) and the Black Kite (Milvusmigrans) were found to be the most abundant species in thisstudy (Figure 7)

33 Feeding Guild Categories

331 Feeding Guild Categories by Macrolandscape TypesAmong the eleven feeding guilds represented by bird speciesin Musanze city seedeaters were the most common in bothbuilt-up areas and open fields followed by insectivorousspecies and scavengers (Figure 8)

Table 3 LMM output showing parameter estimates of microland-scape types on the number of bird individuals

Landscape types Std error 119905 value 119875 valueIntercept 012 27250 lt0001Aerodrome 0224 minus4970 lt0001Agrofield 0169 minus2330 lt005Business centers 0169 minus6646 lt0001Cemeteries 0224 minus1919 0055Forests 0169 minus3615 lt0001Institutional ground 0169 minus2229 lt005Riversides 0224 minus016 0873Informal settlements 0169 minus2899 lt001Streamside 0224 minus2029 lt005Wastelands 0224 0173 0860

AM AG BC CM FT IS IG RN RS SS WL0

5

10

15

20

25

30

35

40

45

50

55

Mea

n nu

mbe

r of b

ird in

divi

dual

s per

visi

t

Microlandscape types

Figure 6 Mean number of bird individuals observed per plotvisit by microlandscape type (AM aerodrome AG agrofields BCbusiness centers CM cemeteries FT forests IS informal settle-ments IG institutional grounds RN residential neighborhoods RSriversides SS streamside WL wasteland)

332 Feeding Guild Categories by Microlandscapes Seed-eating bird species were the most common across allmicrolandscapes except for wastelands which were domi-nated by scavengers a feeding type that was also recorded inevery landscape Insectivorous species were also present in allmicrolandscape types unlike fishers that were only recordedin riverside landscapes Riverside landscapes were also whereflycatchers a feeding type that was present in all landscapetypes were most abundant

34 Species Diversity

341 Alpha Diversity in Macro- and Microlandscape TypesThe bird species diversity in both macro- and microland-scapes of Musanze are described using Whittaker curves(Figure 9) Using these curves built-up areas were slightlyhigher ranked in terms of bird diversity than open fields(Figure 9(a)) Amongmicrolandscapes institutional grounds

6 The Scientific World Journal

0 50 100 150 200 250 300Number of individuals

Spec

ies n

ame

Nectarinia kilimensis

Ploceus melanocephalus

Ploceus baglafecht

Estrilda astrild

Lagonosticta senegala

Lonchura cucullata

Milvus migrans

Serinus striolatus

Passer griseus

Corvus albus

Figure 7 Top ten most represented bird species in all sites of Musanze city

0 100 200 300 400 500 600 700Number of individuals

Aerial feeders

Butcherbirds

Fishers

Flycatchers

Frugivores

Insectivores

Nectar feeders

Raptors

Scavengers

Seedeaters

Shorerbirds

Feed

ing

guild

s

Open fields Built-up areas

Figure 8 Feeding guild categories of bird species as classified in microlandscapes types

had the highest diversity rank followed by residentialneighborhoods and informal settlements The aerodromeand Westland were ranked with the lowest bird diversity(Figure 9(b))

The Shannon diversity index was similar for bothmacrolandscape types built-up areas (1198671015840 = 1456) and itscounterpart open fields (1198671015840 = 1518) At the microland-scape level residential neighborhoods were the most diversefollowed by informal settlements and institutional groundsWastelands displayed the lowest bird diversity (Figure 10)

342 Species Similarity in Macro- and Microlandscape TypesOf the 94 bird species recorded in Musanze city 45 specieswere shared by both open fields and built-up landscapes Interms of species composition found in each microlandscape

type the riverside landscape was the most different fromthe remaining microlandscapes Residential neighborhoodsand informal settlements were most similar The differencesbetween the landscape types in terms of species compositionillustrated by the increasing distance from the root to thepoint where a given branch stems were as follows riversidelt aerodrome lt streamside lt wasteland lt agrofields lt ceme-teries lt forest lt institutional and business center lt informalsettlements and residences (Figure 11)

35 Bird Diversity in Musanze City and Nearby ProtectedAreas In addition to the internal comparison the level ofsimilarity between Musanze and its nearby protected areas(PNV and Buhanga eco-park) revealed important similaritiesbetween protected and urban habitats in terms of bird

The Scientific World Journal 7

0 5 10 15 20 25 30 35 4005

10

15

20

25

Rank

Open fieldsBuilt-up area

Log 1

0re

lativ

e abu

ndan

ce

(a)

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38

04

06

08

10

12

14

16

18

20

22

Rankminus2

AerodromeAgrofield Business centerCemeteriesForest

InstitutionalResidenceRiversideSettlementStreamside

WastelandLo

g 10

rela

tive a

bund

ance

(b)

Figure 9 Species rankabundance (a) in macrolandscape types and (b) in microlandscape types

Aerodrome

Agrofields

Business centers

Cemeteries

Forests

Institutional grounds

Residential neighborhoods

Riversides

Informal settlements

Streamsides

Wastelands

00 02 04 06 08 10 12 14Shannon index

Mic

rola

ndsc

ape t

ypes

Figure 10 Shannon index for microlandscape types of Musanze city

diversity (Figure 12) The total number of bird species inMusanze city was 94 105 in PNV and 81 in the Buhanga eco-park Of the 94 bird species recorded in Musanze 32 werealso present in Buhanga eco-park 51 in the PNV and 21 werefound in both the Buhanga eco-park and in PNV Moreoverwe found only one endemic bird species the RuwenzoriDouble-collared Sunbird (Cinnyris stuhlmanni) in Musanzeunlike the three endemic bird species present in Buhanga eco-park and the fifteen in the PNV This Albertine Rift endemic

species is also present in the PNV however it is absent fromthe Buhanga eco-park

In the comparison of the bird species found in the threesites Musanze city is unique in the number of migratory birdspecies observed Specifically seven migratory species wererecorded in Musanze city while only two are known to existin the PNV and none have been recorded in the Buhanga eco-park (Table 4) Musanzersquos microlandscapes that were visitedbymigratory birds include the riversides ofMukungwa River

8 The Scientific World Journal

RSWLSSISRNIGFTAFCMBCAM

1000 50

Similarity ()

Bray-Curtis cluster analysis (single link)

Figure 11 Species composition-based microlandscape clusters(AM aerodrome AG agrofields BC business centers CM ceme-teries FT forests IS informal settlements IG institutional groundsRN residential neighborhoods RS riversides SS streamside WLwasteland)

1000 50

Similarity ()

Bray-Curtis cluster analysis (single link)

PNV

Musanze

Buhanga

Figure 12 Musanze city PNV and Buhanga eco-park bird speciescomposition

informal settlements forests business centers and residentialneighborhoods

The majority of species in Musanze city were nativesuch that exotic bird species accounted for only 43 of thetotal number of bird species observed (Ficedula albicollisPloceus cucullatus Serinus canicollis and Serinus citrinel-loides) (Table 5) Up to 64 of the species observed hadno breeding opportunities within the study area (Actitishypoleucos Aquila pomarina Merops apiaster Muscicapastriata Phylloscopus trochilus and Sylvia borin)

4 Discussion

Our study of bird diversity in Musanze city has revealed thatcurrent wildlife conservation efforts do not coincide withareas of the highest bird abundance and species diversitywhich exist in urban areas Bird species richness in theurban areas of Musanze is greater than that of Buhangaeco-park and similar to that of the PNV two surroundingnatural habitats that are currently receiving the majority ofconservation efforts Furthermore species of high ecologicalimportance and therefore high conservation concern such

as endemic and migratory species were recorded across thecity landscapesThis study therefore indicates the importanceof protecting not only the natural habitats of native wildlifebut also urban areas where birds in particular are morecommonly existing

41 Species Richness The unique endemic species found inMusanze city the Ruwenzori Double-collared Sunbird haspreviously been observed in the VPN This species is knownto live in the high altitude habitats of the Albertine Rift[24] It is therefore not surprising that it was found in urbanlandscapes ofMusanze city which is located at a high altitudeof 1850m [26] Stevenson and Fanshawe [9] suggest thatthe sunbirdrsquos most preferred habitats are flowering bushes offorest edges and it may be unusual that the endemic specieswas observed foraging onMarkhamia lutea trees within openfields of Musanze city in this study Our study suggests thatthe species distribution of the Ruwenzori Double-collaredSunbird is not restricted to its natural habitat in the AlbertineRift as it can also exist in urban landscapesThis species maytherefore be able to adapt to human-dominated landscapesand it is likely that it may forage on vegetation such as urbangarden trees Our study suggests that the sunbird is capableof adapting its feeding preferences to the available plants incity landscapes potentially as a response to loss of its naturalhabitat caused by park reductions [27]

The seven migrant bird species found in the studysite were regular September-April visitors from Palearcticregions Two of them the Red-chested Cuckoo (Cucu-lus solitarius) and the European Bee-eater (Merops api-aster) had previously been sighted in the gallery forestsof the Rwandanrsquos Eastern Province [28] and in the PNV[24] The Common Sandpiper Spotted Flycatcher andWillow Warbler have also been reported to visit Rwanda(httpwwwrwandabirdingorg 02092012) and Musanzecity but have never been sighted in the Lava Plain or inthe Volcano Range of Rwanda The remaining two migrantsthe Garden Warbler (Sylvia borin) and the Lesser SpottedEagle (Aquila pomarina) have been reported in Rwandafor the first time as a result of this study Importantly theseven migrant species have never been reported to occurin urban environments of Rwanda and only two had beenreported to visit its highlands [24] However the AfricanPitta (Pitta angolensis) which is an intra-African breedingmigrant bird sighted in the Buhanga eco-park in 2006 and2008 [29] was not recorded in this study The findings of ourstudy encourage the development of bird watching activitiesin Musanze city which may be of particular interest tointernational tourists due to the high number of urban-livingand therefore easily observed unique bird species

411 Number of Species by Macrolandscape Types Thehypothesis that bird species inhabit open fields more thanbuilt-up areas was not supported in this study This maybe due to the fact that some built-up areas including insti-tutional grounds residential neighborhoods and informalsettlements are specifically designed with plant communi-ties to attract birds [30] These communities often include

The Scientific World Journal 9

Table 4 Migratory birds in Musanze city PNV and Buhanga eco-park

Common name Scientific name Musanze city Protected areasPNV Buhanga eco-park

Common Sandpiper Actitis hypoleucos

European Bee-eater Merops apiaster

Garden Warbler Sylvia borin

Lesser-spotted Eagle Aquila pomarina

Red-chested Cuckoo Cuculus solitarius

Spotted Flycatcher Muscicapa striata

WillowWarbler Phylloscopus trochilus

Table 5 Exotic birds in Musanze city PNV and Buhanga eco-park

Common name Scientific name Musanze city Protected areasPNV Buhanga eco-park

Collared Flycatcher Ficedula albicollis

Black-headed Weaver Ploceus cucullatus

Yellow-crowned Canary Serinus canicollis

Abyssinian Citril Serinus citrinelloides

a number of trees with a substantial canopy as well asornamental plants such as vegetation that exists as bushesAlternatively some microlandscapes within open fields havea low number of species such as the Musanze aerodromewhich is a grassland habitat and is regularly maintained tofacilitate airplane landing This habitat offers little feedingopportunities to wildlife and is an unsuitable habitat for mostbird species as it may for instance expose small-sized birdsto predators [31]

412 Number of Species by Microlandscape Types In supportof Koellner et al [32] different landscapes in Musanze werecorrelated with differences in bird species richness Theinstitutional grounds had a relatively high species richnessperhaps due to a high variety of plant assemblages Simi-larly the high number of bird species found in residentialneighborhoods and informal settlements can be explained bythe diversity of plant resources in these areas These plantresources include nectar-producing flowers such as bananaplants that attract sunbirds fruit-bearing trees and shrubssuch as guava plants that frugivorous species can feed on Inaddition the high concentrations of domestic wastes (such asresidues food disposable and waste-water) in the homesteadenvironment offer a unique opportunity to predators suchas insectivorous birds that feed on small mammals (egmice frogs) and insects (eg flies mosquitoes) and arecommon to this type of microhabitats Domestic waste mayalso attract scavenger species Finally informal settlementsthat are surrounded by a mosaic of vegetation types offermany opportunities for bird foraging and nesting [30] Thisdiversity in urban landscape vegetation structure and typemay therefore reflect the vast diversity of bird species in urbanareas which has not previously been investigated in Rwanda

42 Species Relative Abundance

421 Number of Individuals by Macrolandscape Types Thenonsignificant effect of macrolandscapes on the total numberof birds in an area may be linked to the fact that landscapetype had no significant influence on bird species richnessMore importantly due to the historical nonformal nature ofurban design in Musanze both macrolandscapes appeared tohave similar types and levels of bird-exploitable resourcesincluding appropriate plant coverage and sites for birds tonest [33]

422 Number of Individuals byMicrolandscape Types Ceme-teries riverside landscapes and wastelands did not differin the total number of birds in comparison to residentialneighborhoods (Table 3) This may be attributed to the factthat these four landscapes appear to be intrinsically hetero-geneous suggesting that there may be possible confoundingfactors that have overshadowed the expected relationshipbetween microlandscapes and relative bird abundance Forinstance wastelands attract many scavengers and raptorscemeteries and agrofields provide appropriate plant assem-blages for seed eaters and riversides offer easy water accessand shelter for aquatic bird species [4] Therefore theabundance of birds across the different microlandscapes ofMusanze is relatively uniform due to the fact that eachlandscape offers a range of suitable habitats for a range of birdspecies

423 Most Represented Species in Musanze City The PiedCrow (Corvus albus) was the most common species inMusanze and seemed to be the most adapted to human-dominated landscapes (Figure 7) For instance unlike many

10 The Scientific World Journal

other bird species in the area the Pied Crow was observedclose to many human facilities such food markets abattoirswastelands domestic yards and croplands In addition thePied Crow was found in high abundance where its foodsources including small reptiles small mammals grainpeanuts carrion scraps of human food fruits insects andother small invertebrates were most available [9] To a lesserextent the urban habitat appeared to favor the Grey-headedSparrow (Passer griseus) The occurrence of the Grey-headedSparrow was associated with open woodlands and humansettlements where this species can easily access required foodand habitat resources The third most represented specieswas the Streaky Seedeater (Serinus striolatus) which is acommon bird of highlands and is generally found above1300m in gardens and cultivated areas woodland edgesheath and scrub vegetation areas The Streaky Seedeateris therefore adept at living in human altered landscapeswhich is not unlike the Black Kite (Milvus migrans) whichwas also common to densely human-populated areas Thesehuman-used landscapes are also a popular habitat of theBlackKitersquos prey which includes small birds bats and rodents Inparticular our study revealed the common occurrence of theBlack Kite circling near the abattoir and scavenging in thecityrsquos wastelands

43 Feeding Guild Categories

431 Feeding Guild Categories by Macrolandscape TypesSeed-eating birds were the best represented guild inMusanze(Figure 8) This may be partially due to the fact that datacollection was completed during a maize-harvesting periodDuring this period urban fields have an exceptionally largeabundance of seeds that can be exploited by birds and mayhave therefore selectively attracted seed-eating species [34]It was also observed that seed-eating species fed from arange of fruits According to Holland and DeAngelis [35]this habit allows seed-eating species to contribute to plantreproduction through pollination Insectivorous species werealso prominent in Musanzersquos urban landscapes Similarly tothe findings of Austin and Smith [5] insectivores were mostabundant in insect-rich landscapes including streamsideareas forests and informal settlements

432 FeedingGuild Categories byMicrolandscapes Althoughseedeaters especially the Grey-headed Sparrow (Passergriseus) dominated almost all microlandscapes it is impor-tant to consider that in wastelands scavengers were the mostabundant (Figure 13) This finding is likely due to the factthat different microlandscapes aremore appropriate for somespecies more than others especially those with differentfeeding habits

Our study confirms that bird species found in Musanzecity like urban-living bird species in other cities contributeto biomass recycling [36] Interestingly although there wereonly a few species of scavenging birds in Musanze theirabundance was high enough to compensate for their lowspecies richness in order to make a notable biomass recyclingimpact to city dwellersThis was particularly true for the Pied

Figure 13 Abundance of Pied Crows in a landfill within Musanzecity (Photo Author 2012)

Crow (Corvus albus) a species whose abundance amountedto more than seven times the average number of individualsper species whichwas almost 10of the total number of birdsobserved

44 Species Diversity

441 Alpha Diversity The bird diversity found in built-up areas was comparable to the bird diversity in urbanopen fields in Musanze city (Figure 9(a)) This finding pro-vides support for the increasingly recognized idea that birddiversity in urban areas can be as high as that in naturalenvironments [37 38] Previous research suggests that thismay be due to a relatively high number of nonnative speciespresent in cities as well as the heterogeneous habitat thaturban landscapes provide [39] which was not supportedin this study perhaps because of close proximity of thestudy area to a network of natural environments (PNVGishwati forest and Buhanga eco-park Rugezi Mukungwaand Bihinga wetlands and Karago Bulera and Ruhondolakes) Moreover Luck [40] suggested that there is a positivecorrelation between human population density and birdspecies richness This relationship was demonstrated in ourstudy as species such as the Pied Crowwere found to bemostabundant throughout urban landscapes and therefore welladapted to an environment where high human densities existInterestingly even the Albertine Rift endemic species theRuwenzori Double-collared Sunbird was sighted foraging inhuman populated areas on garden plants

Overall residential neighborhoods institutionalgrounds and informal settlements can be considered asthe major bird hotspots in Musanze city (Figure 9(b)) Thesethree landscapes share a great floristic diversity providingmany important stimuli for bird life (such as fruits seedsnectar domestic residues insects small mammals reptilesand amphibians) [30] Finally contrary to rural areas andnatural forests that undergo seasonal shortages of resources[3] cities do not experience strong seasonal variation due toa continuous supply of recourses from remote areas

442 Species Similarity The macrolandscapes all appearedto have similar bird species composition which may bedue to landscape heterogeneity [39] This heterogeneity islikely a result of the lack of historical professional landscapeplanning and design leaving a mosaic landscape structure inboth built-up and open fields instead of a uniform landscapespecialization Our results suggest that residential areas and

The Scientific World Journal 11

informal settlements were the most similar in terms ofspecies composition These landscapes ultimately functionto host family life The only difference between residentialareas and informal settlements resides in their socioeconomicstatus which is reflected in the landscape structure Howeverboth landscapes are more similar to each other than toother landscapes Furthermore the species composition ofcemeteries was similar to both forests and some of the built-up microlandscapes which may be attributed to the fact thatthese areas are all surrounded by trees Additionally ceme-teries are characterized by low human disturbance whichmay compare to that of forests and some urban landscapesThese landscapes all harbor a wide variety of floweringplants which in the case of cemeteries are mainly plantedby bereaved ones Moreover the vegetation of graveyardsincludes a range of regeneration stages resulting in a widerange of habitats from the vegetation-free areas of newly duggraves to the reconstructed thickets around old graves [41]Finally riverside landscapes emerged as the most specializedlandscape type as expected with many distinctive speciesobserved in this landscape only Almost all the species foundin riverside areas were specialists of wetlands and were notfound elsewhere As a result it was the most dissimilar to allother microlandscapes

The high degree of similarity in terms of bird diversitybetween Musanze city and the protected natural habitatsnearby provide further support that wildlife does not exclu-sively inhabit protected areas [33 37 42] Although the twonatural habitats are at eight km from Musanze city morethan half of the species found in the city were also found inVPN The lower degree of similarity between Musanze andBuhanga eco-park may be linked to the relative geographiclocation of the two sites as Musanze city is almost half waybetween the two protected areas This finding may also beattributed to the fact that the diversity ofmicrohabitats withinBuhanga eco-park is lower than that of Musanze and VPN[13] which may be due to the relatively small size of Buhangaeco-park Interestingly the species found in more than onelandscape type were also recorded both inside and beyondthe city limits Conversely Ficedula albicollis was recorded inonly one landscape type (cemeteries) and was absent in bothPNV and Buhanga eco-park

5 Conclusions

This study contributes to the knowledge of bird diversity inurban landscapes and provides the most recent status of birddiversity in Musanze city Our findings confirm that birddiversity in urban areas such as a densely populated city canbe as great as that in surrounding natural forests Specificallythe total number of bird species in Musanze city was verysimilar to that of the nearest protected forests VolcanoesNational Park and Buhanga eco-park Endemic and migra-tory birdswere also found inMusanze cityOneAlbertine Riftendemic bird species the Ruwenzori Double-collared Sun-bird was observed in Musanze during this study which hasnot been previously recorded Similarly threemigratory birdswere found inMusanze region for the first time the Common

Sandpiper the Spotted Flycatcher and theWillowWarbler Inaddition two bird species were observed that have not beenpreviously reported in Rwanda the Garden Warbler (Sylviaborin) and the Lesser Spotted Eagle (Aquila pomarina) Theeffect of landscape types on bird species richness and relativeabundance was also illustrated Residential neighborhoodsinstitutional grounds and informal settlements had thehighest species diversity indices and rankabundance relativeto the rest of the microlandscapes in this study Riversidelandscapes emerged with the most specialized bird faunaincluding species that are restricted to wetland environmentsand water bodies This study confirmed that scavengers inMusanze city contribute more to biomass recycling than anyother bird feeding groups Our study provides a current anduseful reference for urban decision makers and confirms theexistence of a great diversity of wildlife within cities Wesuggest that the development and implementation of cityland-use plans should consider this biodiversity especiallywhen villages and cities are in close proximity of protectedareas or natural reserves Finally it may be important thatbotanical gardens and public parks are included in themasterplan of the city as our study indicates that their designrequires an understanding of biodiversity in particular ofavian populations

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors acknowledge technical support from staffat DFGFI-Karisoke Research Center namely Dr WinnieEckardt Mr Deogratias Tuyisingize Mr Emmanuel Faidaand Mrs Keiko Mori

References

[1] S R Loss M O Ruiz and J D Brawn ldquoRelationships betweenavian diversity neighborhood age income and environmentalcharacteristics of an urban landscaperdquo Biological Conservationvol 142 no 11 pp 2578ndash2585 2009

[2] K L Evans D E Chamberlain B J Hatchwell R D Gregoryand K J Gaston ldquoWhat makes an urban birdrdquo Global ChangeBiology vol 17 no 1 pp 32ndash44 2011

[3] S Bolwig D Pomeroy H Tushabe and D Mushabe ldquoCropstrees and birds biodiversity change under agricultural inten-sification in Ugandas farmed landscapesrdquo Danish Journal ofGeography vol 106 no 2 pp 115ndash130 2006

[4] J Hitchmough and N Dunnett ldquoIntroduction to naturalisticplanting in urban landscapesrdquo in The Dynamic LandscapeJ Hitchmough and N Dunnatt Eds pp 1ndash32 Spon PressLondon UK 2004

[5] G T Austin and E L Smith ldquoWinter foraging ecology of mixedinsectivorous bird flocks in oakwoodland in southernArizonardquoThe Condor vol 74 pp 17ndash24 1972

[6] B R Coppedge D M Engle R E Masters and M S GregoryldquoAvian response to landscape change in fragmented southern

12 The Scientific World Journal

great plains grasslandsrdquo Ecological Applications vol 11 no 1 pp47ndash59 2001

[7] K L Evans S E Newson and K J Gaston ldquoHabitat influenceson urban avian assemblagesrdquo Ibis vol 151 no 1 pp 19ndash39 2009

[8] MW Strohbach D Haase and N Kabisch ldquoBirds and the cityUrban biodiversity land use and socioeconomicsrdquo Ecology andSociety vol 14 no 2 pp 31ndash45 2009

[9] T Stevenson and J Fanshawe Field Guide to the Birds of EastAfrica Kenya Tanzania Uganda Rwanda Burundi T amp A DPoyser London UK 2002

[10] J Mistry A Berardi and M Simpson ldquoBirds as indicators ofwetland status and change in the North Rupununi GuyanardquoBiodiversity and Conservation vol 17 no 10 pp 2383ndash24092008

[11] H Slabbekoorn and E A P Ripmeester ldquoBirdsong and anthro-pogenic noise implications and applications for conservationrdquoMolecular Ecology vol 17 no 1 pp 72ndash83 2008

[12] W S Judd C S Campbell E A Kellogg P F Stevens andM JDonoghue Plant Systematics A Phylogenetic Approach SinauerAssociates Sunderland Mass USA 3rd edition 2008

[13] W Weber ldquoRuhengeri and its resources an environmentalprofile of the Ruhengeri prefecturerdquo ETMAUSAID KigaliRwanda

[14] E Sabuhoro and G Bush ldquoThe Dian Fossey Gorilla FundInternationalPADGEF Assessing the Benefit Stream fromIllegal Activities in the Parc National des Volcansrdquo TargetingCommunity Conservation Interventions Musanze Rwanda2008

[15] J C Sano Urban Environmental Infrastructure in Kigali CityRwanda Challenges and Opportunities for Modernized Decen-tralized Sanitation Systems in Poor Neighborhoods WageningenUniversity Wageningen The Netherlands 2007

[16] R J Staniforth ldquoEffects of urbanization on bird populations inthe Canadian Central Arcticrdquo Arctic vol 55 no 1 pp 87ndash932002

[17] DWGibbons andRD Gregory ldquoBirdsrdquo in Ecological CensusesTechniques W L Sutherland Ed pp 308ndash350 CambridgeUniversity 2nd edition 2006

[18] D H Johnson ldquoPoint counts of birds what are we estimatingrdquoTech Rep PSW-GTR-149 USDA Forest Service 1995

[19] A Haslem and A F Bennett ldquoBirds in agricultural mosaics theinfluence of landscape pattern and countryside heterogeneityrdquoEcological Applications vol 18 no 1 pp 185ndash196 2008

[20] M L Rurangwa Feeding Ecology of Albertine Rift Endemic Birdsin the Volcanoes National Park Regal Sunbird Rwenzori Double-Collared Sunbird and Rwenzori Turako National University ofRwanda 2011

[21] R B Arellano-Valle H Bolfarine and V H Lachos ldquoSkew-normal linear mixedmodelsrdquo Journal of Data Science vol 3 pp415ndash438 2005

[22] D Bates Fitting LinearMixedModels in RTheNewsletter of theR Project Volume 51 University of Wisconsin Madison WisUSA 2005

[23] A E Magurran Measuring Biological Diversity Blackwell Sci-ence Malden Mass USA 2004

[24] D Tuyisingize and K Fawcett ldquoThe common bird distributionin the Parc National des Volcans and its surrounding patternsconservation and future challengesrdquo DFGF Technical Report2011

[25] A T Peterson and N A Slade ldquoExtrapolating inventory resultsinto biodiversity estimates and the importance of stoppingrulesrdquoDiversity and Distributions vol 4 no 3 pp 95ndash105 1998

[26] M Salek J Svobodova and P Zasadil ldquoEdge effect of low-trafficforest roads on bird communities in secondary productionforests in central Europerdquo Landscape Ecology vol 25 no 7 pp1113ndash1124 2010

[27] S Murererehe ldquoCollecte et analyse de donnees pourlrsquoamenagement durable des forets -Joindre les efforts nationauxet internationaux Etat des ressources forestieres au RwandardquoTech Rep FAO Rome Italy 2000

[28] S J Nsengimana M Ndimukaga L Gakwerere et al ldquoBiodi-versity surveyrdquo Tech Rep Rufford Small Grant FoundationLondon UK 2009

[29] C Nsabagasani ldquoA Migratory Species African Pitta ldquoPittaangolensisrdquo passed Buhanga relict forestrdquo Backbone vol 17 pp6ndash8 2008

[30] J Jokimaki and M Kaisanlahti-Jokimaki ldquoThe role of residen-tial habitat type on the temporal variation of wintering birdassemblages in northern Finlandrdquo Ornis Fennica vol 88 2011

[31] T M Bergin L B Best K E Freemark and K J KoehlerldquoEffects of landscape structure on nest predation in roadsides ofa midwestern agroecosystem a multiscale analysisrdquo LandscapeEcology vol 15 no 2 pp 131ndash143 2000

[32] T Koellner AMHersperger andTWohlgemuth ldquoRarefactionmethod for assessing plant species diversity on a regional scalerdquoEcography vol 27 no 4 pp 532ndash544 2004

[33] S H Faeth P S Warren E Shochat and W A MarussichldquoTrophic dynamics in urban communitiesrdquo BioScience vol 55no 5 pp 399ndash407 2005

[34] R J Fuller and J D Wilson ldquoThe ecology of seed-eating birdsin relation to agricultural practices current research and futuredirectionsrdquo British Trust for Ornithology Research Report no149 1995

[35] J N Holland andD L DeAngelis ldquoEcological and evolutionaryconditions for fruit abortion to regulate pollinating seed-eaters and increase plant reproductionrdquo Theoretical PopulationBiology vol 61 no 3 pp 251ndash263 2002

[36] C J Whelan D G Wenny and R J Marquis ldquoEcosystemservices provided by birdsrdquo Annals of the New York Academyof Sciences vol 1134 pp 25ndash60 2008

[37] O Gilbert The Ecology of Urban Habitats Chapman amp HallLondon UK 1989

[38] A Millard ldquoSemi-natural vegetation and its relationship todesignated urban green space at the landscape scale in LeedsUKrdquo Landscape Ecology vol 23 no 10 pp 1231ndash1241 2008

[39] I Kowarik ldquoOn the role of alien species in urban flora andvegetationrdquo in Plant Invasions General Aspects and SpecialProblems P Pysek K Prach M Rejmanek and M WadeEds pp 85ndash103 SPB Academic Publishing Amsterdam TheNetherlands 1995

[40] G W Luck ldquoA review of the relationships between humanpopulation density and biodiversityrdquo Biological Reviews vol 82no 4 pp 607ndash645 2007

[41] Victorian Government Department of Sustainability and Envi-ronment (VGDSE) Managing Native Vegetation in VictorianCemeteries Victorian Government Department of Sustainabil-ity and Environment Melbourne Australia 2009

[42] C Dowd ldquoEffect of development on bird species compositionof two urban forested wetlands in Staten Island New YorkrdquoJournal of Field Ornithology vol 63 no 4 pp 455ndash461 1992

Page 2: Bird Diversity and Distribution in relation to Urban Landscape Types in Northern Rwanda · 2016. 1. 26. · ResearchArticle Bird Diversity and Distribution in relation to Urban Landscape

2 The Scientific World Journal

of bird diversity outside protected areas especially in urbanareas

The landscape of the Musanze District in the NorthernProvince of Rwanda has been undergoing major changesdue to rapid urbanization driven by a fast growing humanpopulation [13] Human density in this region can reach upto 1000 people per km2 [14] and it is estimated that morethan half of the total Rwandan population is expected tolive in urban areas in less than 40 years [15] High rates ofland conversion into urban use inMusanze is threatening thewild avian diversity as it is the case for other fast growingcities in the world [16] More than half of the total Rwandanpopulation is expected to live in urban areas in less than 40years [15]

While wild avian diversity has been a subject of researchin natural habitats of the Northern Province especially inthe Parc National des Volcans (PNV) and the Buhanga eco-park the biodiversity of the neighboring Musanze city likemany other anthropogenic landscapes remains understud-ied Thus this study aimed to address the issue of ecologicalbias in bird diversity and distribution in fast growing citiesand proposes strategies for effective conservation of birds inurban areas of Rwanda and of Musanze city in particularThe main objective of this study was to assess the diversityand distribution of birds in urban landscape types of theMusanze city Specifically the study aimed (1) to identify birdspecies that live in or visit Musanze city (2) to identify birdfeeding guilds bird abundance and bird diversity in differentlandscapes in Musanze (3) to locate areas of the city thatshow high bird diversity hereafter referred to as ldquourban birdhotspotsrdquo and (4) to compare the bird diversity in Musanzecity with the bird diversity found in the PNV and Buhangaeco-park which are two important ecological zones in theadministrative district where Musanze city is located Ourstudy therefore provides policy makers and conservationistswith scientific information about the ecological status of birdsin Musanze city and how species are distributed in the city inrelation to the urban fabric layout

2 Materials and Methods

21 Study Area Musanze District is situated in the north-western highlands of Rwanda and is one of the five admin-istrative districts within the Northern Province The studywas carried out within Musanze city which covers a totalarea of 6197 km2 and is comprised of four sectors MuhozaCyuve Musanze and Kimonyi Musanze is one of the largestand fastest growing urban centers in Rwanda and is a centralhub for businesses trade and tourism The PNV with itsfamous mountain gorillas the Buhanga eco-park and theRuhondo Lake are found in Musanze and make the city apopular destination for national and international tourists(httpwwwmusanzegovrw 30122012)

22 Landscape Stratification Landscapes ofMusanze city canbe classified into two major categories open fields and built-up areas Open fields can include agricultural land ceme-teries wastelands stream banks forests and the aerodrome

which is a nonpaved strip covered by a regularly mownlawn of about 15 km length Built-up areas include businesscenters institutional grounds settlements and residentialneighborhoods

In this study agricultural land referred to cultivated landslocated within Musanze surrounding urban areas wheremaize and beans are the most common crops We includedtwo cemeteries in our sampling sites which were located inthe Muhoza and Cyuve sectors Wastelands were defined asareas dedicated to household solid waste disposal Twowaste-lands were considered for the study one close to Musanzebusiness center and another in Cyuve We considered streambanks as land that encompassed habitats on both sides ofpermanent or seasonal river flows Forests included areascovered by tree plantations mainly Eucalypts Natural forestswere not found within the city boundaries The Musanzeaerodrome is a nonpaved strip covered by a regularly mownlawn of about 15 km length

Business centers included market places and areas witha high concentration of shops Institutional grounds werecomprised of large institution gardens including the districtoffice Musanze hospital one university one high schooland the city abattoir Informal and nonformal settlementsincluded organized village settlements and rural type scat-tered settlements where banana plantations were the mostcommon crop in the home gardens Residential neighbor-hoods were high standard settlement areas of the city

23 Data Collection DuringMarch 2012 data were collectedwithin plots using the point count method [17] The pointcount sampling design consisted of a series of points atwhich birds were counted within a defined radius [18] Forty50m radius plots were established using a global positioningsystem (GPS) unit twenty in open fields and other twentyin built-up areas (Table 1) Between two and five plots wererandomly selected for each microlandscape type (Table 1)within a 04 times 04 km grid at a rate of one plot per grid cellEach plot was visited four times for a ten-minute observationperiod [19] such that this study included 160 plot visitsin total Visits to each plot were equally distributed acrossfour periods during the day early morning (630ndash830)late morning (900ndash1100) early evening (1500ndash1700) andlate evening (1730ndash1830) As the weather can influence theoccurrence of some bird species [20] working during rain orstrong wind was avoided

In addition to a presurvey training of data collectorson bird identification a bird expert was present in 96of our field visits A pair of 8 times 42 resolution binoculars(Olympus mark) and a field guide book were also usedto identify the species of birds observed [9] Five minutesafter the plot was located the center was chosen wheneverpossible to observe any bird movement This time delay wasin place to allow birds to return to their natural behaviorin order to minimize potential impacts of human presenceon the survey The following variables were recorded duringeach 10min observation period number of plot type ofmicrolandscape arrival time departure time species namesof birds observed number of individuals from each observed

The Scientific World Journal 3

Table 1 Distribution of plots across microlandscape types and administrative sectors

Landscape types Category Sectors Number of plotsAerodrome Open field Muhoza 2Agrofields Open field Muhoza Cyuve 5Business centers Built-up Musanze Muhoza Cyuve 5Cemeteries Open field Muhoza 2Forests Open field Musanze Muhoza Cyuve 5Institutional grounds Built-up Musanze Muhoza 5Residential neighborhood Built-up Muhoza 5Riversides Open field Muhoza 2Informal settlements Built-up Kimonyi Muhoza 5Streamsides Open field Musanze 2Wastelands Open field Muhoza Cyuve 2

bird species weather conditions vegetation cover and anykind of disturbance such as extra human presence or noisefrom nearby vehicles

Birds encountered outside of our study plots wererecorded only when it was a locally novel species suchthat it had never been observed in the area before Theserecords were only considered for compiling a bird checklistof Musanze city and were therefore excluded from statisticalanalysis When a bird could not be identified in the fieldphotos from a high-resolution camera and descriptive noteswere taken for later identification by a bird expert

24 Data Analysis The linear mixed models (LMM)methodwas used to analyze the relationships between landscape birdabundance and species richness LMM recently became auseful tool used to analyze continuous repeated measuresdata from a sample of individuals in different areas [21] LMMis a statistical model that consists of both fixed effects andrandom-effects terms and was therefore themost appropriatechoice for our study [22] In this study LMM was used toassess whether urban landscape types have an effect on birdabundance and species richness Landscape types (macro-and microlandscapes) were fixed effects (covariates) whilesampling plots were treated as a random effect to control forrepeated measures in plots Bird species richness and relativeabundance were dependent variables assessed in differentLMMs

The Shannonrsquos diversity index (1198671015840 = minussum119901119894log119901119894 where

119901119894is the proportion of individuals belonging to the 119894th

species) was used to identify the 120572-diversity of bird speciesboth at city and landscape type levels in order to identify thelocal average species diversity of each particular habitat TheBray-Curtis cluster analysis (single link) method was usedto assess the level of similarity in bird composition betweenlandscape types [23]

Referring to Tuyisingize and Fawcett [24] fromwhich weretrieved the checklist of birds of the PNV and Buhanga eco-park the bird diversity and abundance of Musanze city werecompared with the two natural ecosystems of these parksin terms of bird species richness and composition using thehierarchical clustering method

To examine the relationship between bird species andfood availability in the city bird species were categorizedaccording to their feeding guilds The completeness of thesurvey was assessed by analyzing patterns of the species accu-mulation curves [25] The accumulation curves of speciesrichness in different microlandscape types globally reachedtheir plateau (Figure 1) giving us confidence to conclude thatour sampling efforts had covered the majority of species inMusanze

To determine the level of significance of the obtainedresults hypothesis testing tools were used including thetest of Studentrsquos 119905-test Bioprofessional MVSP Origin and Rsoftware packages were used for these analyses

3 Results

31 Species Richness A total of 94 bird species were observedin Musanze city 15 of which were found opportunisticallyoutside plots Only one Albertine Rift endemic species(Ruwenzori Double-collared Sunbird Cinnyris stuhlmanni)was observed and seven migrant bird species were recorded

311 Number of Bird Species by Macrolandscape Types Therewas no significant difference in the number of bird species inopen fields and built-up areas (119905 = minus042 119875 = 067 Figure 2)Similarly the total number of bird species observed in bothmacrolandscapes was not notably different (119873 built-up = 63119873 open fields = 61)

312 Number of Species by Microlandscape Types Amongthe different microlandscapes institutional grounds had thehighest number of species (119873 = 42) followed by residentialneighborhoods (119873 = 41) and informal settlements (119873 =37) Furthermore forest and riverside landscapes had similarnumber in terms of total number of species (119873 = 35 forboth) Finally wastelands and the aerodrome demonstratedthe smallest number of bird species (119873 = 16 and 119873 = 15resp) (Figure 3)

For the LMM that examined the impact of differentmicrolandscapes on the number of bird species residentialneighborhoods were used as the reference microlandscape

4 The Scientific World Journal

50

40

30

20

10

0

0 200 400 600 800

Number of individuals

Num

ber o

f spe

cies

Rarefaction plot

WastelandsAerodromeCemeteriesAgrofieldsForestRiverside

StreamsideBusiness centersInstitutional groundInformal settlementResidence neighborhood

Figure 1 Bird species rarefaction curves at the site considered inthis study

Built-up areas Open fields0123456789

101112

Mea

n nu

mbe

r of b

ird sp

ecie

s per

visi

t

Macrolandscape types

Figure 2Mean number of species observed during plot visits in thetwo macrolandscape types

type as it showed the highest average number of bird speciesper plot visit (Figure 4) Thus the average number of birdspecies found in any other microlandscape was compared tothe number of bird species found in residential neighbor-hoods The LMM analysis revealed that the average numberof bird species found in all microlandscapes excluding ceme-teries and riversides was significantly lower than the numberof bird species in residential Musanzersquos neighborhood areas(Table 2) The average number of bird species observed in

IG RN IS FT RD AF CM SS BC WL AM0

10

20

30

40

Num

ber o

f spe

cies

Microlandscape types

Figure 3 Total bird species in microlandscape types (AM aero-drome AG agrofields BC business centers CM cemeteries FTforests IS informal settlements IG institutional grounds RNresidential neighborhoods RS riversides SS streamside WLwasteland)

Table 2 LMM output showing parameter estimates of microland-scape types on the number of bird species

Landscape types Std error 119905 value 119875 valueIntercept 074 15338 lt0001Aerodrome 139 minus5502 lt0001Agrofield 105 minus3330 lt001Business centers 105 minus6374 lt0001Cemeteries 139 minus1816 0069Forests 105 minus3473 lt001Institutional ground 105 minus2807 lt001Riversides 139 minus0827 0408Informal settlements 105 minus3330 lt001Streamside 139 minus2445 lt005Wastelands 139 minus2625 lt001

plots located in cemeteries tended to be less than the averagenumber found in residential neighborhoods

32 Species Relative Abundance

321 Number of Individuals by Macrolandscape Types Therewas no significant difference between open fields and built-up areas in terms of number of bird individuals observed pervisit (119905 = 035 119875 = 073 Figure 5)

322 Number of Individuals by Microlandscape Types Therewere significantly less birds in all microlandscape typescompared to the number of birds encountered in plotslocated in residential neighborhoods except for cemeteries(where fewer birdswere observed) riversides andwastelands(Figure 6 and Table 3)

The Scientific World Journal 5

AM AG BC CM FT IS IG RN RS SS WL0

2

4

6

8

10

12

14

16

Microlandscape types

Mea

n nu

mbe

r of b

ird sp

ecie

s per

visi

t

Figure 4 Mean number of bird species observed during plot visitsin each microlandscape type (AM aerodrome AG agrofields BCbusiness centers CM cemeteries FT forests IS informal settle-ments IG institutional grounds RN residential neighborhoods RSriversides SS streamside WL wasteland)

0

5

10

15

20

25

30

35

40

Mea

n nu

mbe

r of b

ird in

divi

dual

s per

visi

t

Built-up areas Open fieldsMacrolandscape types

Figure 5Mean number of bird individuals encountered per visit bymacrolandscape type

323 Most Represented Species The Pied Crow (Corvusalbus) the Grey-headed Sparrow (Passer griseus) StreakySeedeater (Serinus striolatus) and the Black Kite (Milvusmigrans) were found to be the most abundant species in thisstudy (Figure 7)

33 Feeding Guild Categories

331 Feeding Guild Categories by Macrolandscape TypesAmong the eleven feeding guilds represented by bird speciesin Musanze city seedeaters were the most common in bothbuilt-up areas and open fields followed by insectivorousspecies and scavengers (Figure 8)

Table 3 LMM output showing parameter estimates of microland-scape types on the number of bird individuals

Landscape types Std error 119905 value 119875 valueIntercept 012 27250 lt0001Aerodrome 0224 minus4970 lt0001Agrofield 0169 minus2330 lt005Business centers 0169 minus6646 lt0001Cemeteries 0224 minus1919 0055Forests 0169 minus3615 lt0001Institutional ground 0169 minus2229 lt005Riversides 0224 minus016 0873Informal settlements 0169 minus2899 lt001Streamside 0224 minus2029 lt005Wastelands 0224 0173 0860

AM AG BC CM FT IS IG RN RS SS WL0

5

10

15

20

25

30

35

40

45

50

55

Mea

n nu

mbe

r of b

ird in

divi

dual

s per

visi

t

Microlandscape types

Figure 6 Mean number of bird individuals observed per plotvisit by microlandscape type (AM aerodrome AG agrofields BCbusiness centers CM cemeteries FT forests IS informal settle-ments IG institutional grounds RN residential neighborhoods RSriversides SS streamside WL wasteland)

332 Feeding Guild Categories by Microlandscapes Seed-eating bird species were the most common across allmicrolandscapes except for wastelands which were domi-nated by scavengers a feeding type that was also recorded inevery landscape Insectivorous species were also present in allmicrolandscape types unlike fishers that were only recordedin riverside landscapes Riverside landscapes were also whereflycatchers a feeding type that was present in all landscapetypes were most abundant

34 Species Diversity

341 Alpha Diversity in Macro- and Microlandscape TypesThe bird species diversity in both macro- and microland-scapes of Musanze are described using Whittaker curves(Figure 9) Using these curves built-up areas were slightlyhigher ranked in terms of bird diversity than open fields(Figure 9(a)) Amongmicrolandscapes institutional grounds

6 The Scientific World Journal

0 50 100 150 200 250 300Number of individuals

Spec

ies n

ame

Nectarinia kilimensis

Ploceus melanocephalus

Ploceus baglafecht

Estrilda astrild

Lagonosticta senegala

Lonchura cucullata

Milvus migrans

Serinus striolatus

Passer griseus

Corvus albus

Figure 7 Top ten most represented bird species in all sites of Musanze city

0 100 200 300 400 500 600 700Number of individuals

Aerial feeders

Butcherbirds

Fishers

Flycatchers

Frugivores

Insectivores

Nectar feeders

Raptors

Scavengers

Seedeaters

Shorerbirds

Feed

ing

guild

s

Open fields Built-up areas

Figure 8 Feeding guild categories of bird species as classified in microlandscapes types

had the highest diversity rank followed by residentialneighborhoods and informal settlements The aerodromeand Westland were ranked with the lowest bird diversity(Figure 9(b))

The Shannon diversity index was similar for bothmacrolandscape types built-up areas (1198671015840 = 1456) and itscounterpart open fields (1198671015840 = 1518) At the microland-scape level residential neighborhoods were the most diversefollowed by informal settlements and institutional groundsWastelands displayed the lowest bird diversity (Figure 10)

342 Species Similarity in Macro- and Microlandscape TypesOf the 94 bird species recorded in Musanze city 45 specieswere shared by both open fields and built-up landscapes Interms of species composition found in each microlandscape

type the riverside landscape was the most different fromthe remaining microlandscapes Residential neighborhoodsand informal settlements were most similar The differencesbetween the landscape types in terms of species compositionillustrated by the increasing distance from the root to thepoint where a given branch stems were as follows riversidelt aerodrome lt streamside lt wasteland lt agrofields lt ceme-teries lt forest lt institutional and business center lt informalsettlements and residences (Figure 11)

35 Bird Diversity in Musanze City and Nearby ProtectedAreas In addition to the internal comparison the level ofsimilarity between Musanze and its nearby protected areas(PNV and Buhanga eco-park) revealed important similaritiesbetween protected and urban habitats in terms of bird

The Scientific World Journal 7

0 5 10 15 20 25 30 35 4005

10

15

20

25

Rank

Open fieldsBuilt-up area

Log 1

0re

lativ

e abu

ndan

ce

(a)

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38

04

06

08

10

12

14

16

18

20

22

Rankminus2

AerodromeAgrofield Business centerCemeteriesForest

InstitutionalResidenceRiversideSettlementStreamside

WastelandLo

g 10

rela

tive a

bund

ance

(b)

Figure 9 Species rankabundance (a) in macrolandscape types and (b) in microlandscape types

Aerodrome

Agrofields

Business centers

Cemeteries

Forests

Institutional grounds

Residential neighborhoods

Riversides

Informal settlements

Streamsides

Wastelands

00 02 04 06 08 10 12 14Shannon index

Mic

rola

ndsc

ape t

ypes

Figure 10 Shannon index for microlandscape types of Musanze city

diversity (Figure 12) The total number of bird species inMusanze city was 94 105 in PNV and 81 in the Buhanga eco-park Of the 94 bird species recorded in Musanze 32 werealso present in Buhanga eco-park 51 in the PNV and 21 werefound in both the Buhanga eco-park and in PNV Moreoverwe found only one endemic bird species the RuwenzoriDouble-collared Sunbird (Cinnyris stuhlmanni) in Musanzeunlike the three endemic bird species present in Buhanga eco-park and the fifteen in the PNV This Albertine Rift endemic

species is also present in the PNV however it is absent fromthe Buhanga eco-park

In the comparison of the bird species found in the threesites Musanze city is unique in the number of migratory birdspecies observed Specifically seven migratory species wererecorded in Musanze city while only two are known to existin the PNV and none have been recorded in the Buhanga eco-park (Table 4) Musanzersquos microlandscapes that were visitedbymigratory birds include the riversides ofMukungwa River

8 The Scientific World Journal

RSWLSSISRNIGFTAFCMBCAM

1000 50

Similarity ()

Bray-Curtis cluster analysis (single link)

Figure 11 Species composition-based microlandscape clusters(AM aerodrome AG agrofields BC business centers CM ceme-teries FT forests IS informal settlements IG institutional groundsRN residential neighborhoods RS riversides SS streamside WLwasteland)

1000 50

Similarity ()

Bray-Curtis cluster analysis (single link)

PNV

Musanze

Buhanga

Figure 12 Musanze city PNV and Buhanga eco-park bird speciescomposition

informal settlements forests business centers and residentialneighborhoods

The majority of species in Musanze city were nativesuch that exotic bird species accounted for only 43 of thetotal number of bird species observed (Ficedula albicollisPloceus cucullatus Serinus canicollis and Serinus citrinel-loides) (Table 5) Up to 64 of the species observed hadno breeding opportunities within the study area (Actitishypoleucos Aquila pomarina Merops apiaster Muscicapastriata Phylloscopus trochilus and Sylvia borin)

4 Discussion

Our study of bird diversity in Musanze city has revealed thatcurrent wildlife conservation efforts do not coincide withareas of the highest bird abundance and species diversitywhich exist in urban areas Bird species richness in theurban areas of Musanze is greater than that of Buhangaeco-park and similar to that of the PNV two surroundingnatural habitats that are currently receiving the majority ofconservation efforts Furthermore species of high ecologicalimportance and therefore high conservation concern such

as endemic and migratory species were recorded across thecity landscapesThis study therefore indicates the importanceof protecting not only the natural habitats of native wildlifebut also urban areas where birds in particular are morecommonly existing

41 Species Richness The unique endemic species found inMusanze city the Ruwenzori Double-collared Sunbird haspreviously been observed in the VPN This species is knownto live in the high altitude habitats of the Albertine Rift[24] It is therefore not surprising that it was found in urbanlandscapes ofMusanze city which is located at a high altitudeof 1850m [26] Stevenson and Fanshawe [9] suggest thatthe sunbirdrsquos most preferred habitats are flowering bushes offorest edges and it may be unusual that the endemic specieswas observed foraging onMarkhamia lutea trees within openfields of Musanze city in this study Our study suggests thatthe species distribution of the Ruwenzori Double-collaredSunbird is not restricted to its natural habitat in the AlbertineRift as it can also exist in urban landscapesThis species maytherefore be able to adapt to human-dominated landscapesand it is likely that it may forage on vegetation such as urbangarden trees Our study suggests that the sunbird is capableof adapting its feeding preferences to the available plants incity landscapes potentially as a response to loss of its naturalhabitat caused by park reductions [27]

The seven migrant bird species found in the studysite were regular September-April visitors from Palearcticregions Two of them the Red-chested Cuckoo (Cucu-lus solitarius) and the European Bee-eater (Merops api-aster) had previously been sighted in the gallery forestsof the Rwandanrsquos Eastern Province [28] and in the PNV[24] The Common Sandpiper Spotted Flycatcher andWillow Warbler have also been reported to visit Rwanda(httpwwwrwandabirdingorg 02092012) and Musanzecity but have never been sighted in the Lava Plain or inthe Volcano Range of Rwanda The remaining two migrantsthe Garden Warbler (Sylvia borin) and the Lesser SpottedEagle (Aquila pomarina) have been reported in Rwandafor the first time as a result of this study Importantly theseven migrant species have never been reported to occurin urban environments of Rwanda and only two had beenreported to visit its highlands [24] However the AfricanPitta (Pitta angolensis) which is an intra-African breedingmigrant bird sighted in the Buhanga eco-park in 2006 and2008 [29] was not recorded in this study The findings of ourstudy encourage the development of bird watching activitiesin Musanze city which may be of particular interest tointernational tourists due to the high number of urban-livingand therefore easily observed unique bird species

411 Number of Species by Macrolandscape Types Thehypothesis that bird species inhabit open fields more thanbuilt-up areas was not supported in this study This maybe due to the fact that some built-up areas including insti-tutional grounds residential neighborhoods and informalsettlements are specifically designed with plant communi-ties to attract birds [30] These communities often include

The Scientific World Journal 9

Table 4 Migratory birds in Musanze city PNV and Buhanga eco-park

Common name Scientific name Musanze city Protected areasPNV Buhanga eco-park

Common Sandpiper Actitis hypoleucos

European Bee-eater Merops apiaster

Garden Warbler Sylvia borin

Lesser-spotted Eagle Aquila pomarina

Red-chested Cuckoo Cuculus solitarius

Spotted Flycatcher Muscicapa striata

WillowWarbler Phylloscopus trochilus

Table 5 Exotic birds in Musanze city PNV and Buhanga eco-park

Common name Scientific name Musanze city Protected areasPNV Buhanga eco-park

Collared Flycatcher Ficedula albicollis

Black-headed Weaver Ploceus cucullatus

Yellow-crowned Canary Serinus canicollis

Abyssinian Citril Serinus citrinelloides

a number of trees with a substantial canopy as well asornamental plants such as vegetation that exists as bushesAlternatively some microlandscapes within open fields havea low number of species such as the Musanze aerodromewhich is a grassland habitat and is regularly maintained tofacilitate airplane landing This habitat offers little feedingopportunities to wildlife and is an unsuitable habitat for mostbird species as it may for instance expose small-sized birdsto predators [31]

412 Number of Species by Microlandscape Types In supportof Koellner et al [32] different landscapes in Musanze werecorrelated with differences in bird species richness Theinstitutional grounds had a relatively high species richnessperhaps due to a high variety of plant assemblages Simi-larly the high number of bird species found in residentialneighborhoods and informal settlements can be explained bythe diversity of plant resources in these areas These plantresources include nectar-producing flowers such as bananaplants that attract sunbirds fruit-bearing trees and shrubssuch as guava plants that frugivorous species can feed on Inaddition the high concentrations of domestic wastes (such asresidues food disposable and waste-water) in the homesteadenvironment offer a unique opportunity to predators suchas insectivorous birds that feed on small mammals (egmice frogs) and insects (eg flies mosquitoes) and arecommon to this type of microhabitats Domestic waste mayalso attract scavenger species Finally informal settlementsthat are surrounded by a mosaic of vegetation types offermany opportunities for bird foraging and nesting [30] Thisdiversity in urban landscape vegetation structure and typemay therefore reflect the vast diversity of bird species in urbanareas which has not previously been investigated in Rwanda

42 Species Relative Abundance

421 Number of Individuals by Macrolandscape Types Thenonsignificant effect of macrolandscapes on the total numberof birds in an area may be linked to the fact that landscapetype had no significant influence on bird species richnessMore importantly due to the historical nonformal nature ofurban design in Musanze both macrolandscapes appeared tohave similar types and levels of bird-exploitable resourcesincluding appropriate plant coverage and sites for birds tonest [33]

422 Number of Individuals byMicrolandscape Types Ceme-teries riverside landscapes and wastelands did not differin the total number of birds in comparison to residentialneighborhoods (Table 3) This may be attributed to the factthat these four landscapes appear to be intrinsically hetero-geneous suggesting that there may be possible confoundingfactors that have overshadowed the expected relationshipbetween microlandscapes and relative bird abundance Forinstance wastelands attract many scavengers and raptorscemeteries and agrofields provide appropriate plant assem-blages for seed eaters and riversides offer easy water accessand shelter for aquatic bird species [4] Therefore theabundance of birds across the different microlandscapes ofMusanze is relatively uniform due to the fact that eachlandscape offers a range of suitable habitats for a range of birdspecies

423 Most Represented Species in Musanze City The PiedCrow (Corvus albus) was the most common species inMusanze and seemed to be the most adapted to human-dominated landscapes (Figure 7) For instance unlike many

10 The Scientific World Journal

other bird species in the area the Pied Crow was observedclose to many human facilities such food markets abattoirswastelands domestic yards and croplands In addition thePied Crow was found in high abundance where its foodsources including small reptiles small mammals grainpeanuts carrion scraps of human food fruits insects andother small invertebrates were most available [9] To a lesserextent the urban habitat appeared to favor the Grey-headedSparrow (Passer griseus) The occurrence of the Grey-headedSparrow was associated with open woodlands and humansettlements where this species can easily access required foodand habitat resources The third most represented specieswas the Streaky Seedeater (Serinus striolatus) which is acommon bird of highlands and is generally found above1300m in gardens and cultivated areas woodland edgesheath and scrub vegetation areas The Streaky Seedeateris therefore adept at living in human altered landscapeswhich is not unlike the Black Kite (Milvus migrans) whichwas also common to densely human-populated areas Thesehuman-used landscapes are also a popular habitat of theBlackKitersquos prey which includes small birds bats and rodents Inparticular our study revealed the common occurrence of theBlack Kite circling near the abattoir and scavenging in thecityrsquos wastelands

43 Feeding Guild Categories

431 Feeding Guild Categories by Macrolandscape TypesSeed-eating birds were the best represented guild inMusanze(Figure 8) This may be partially due to the fact that datacollection was completed during a maize-harvesting periodDuring this period urban fields have an exceptionally largeabundance of seeds that can be exploited by birds and mayhave therefore selectively attracted seed-eating species [34]It was also observed that seed-eating species fed from arange of fruits According to Holland and DeAngelis [35]this habit allows seed-eating species to contribute to plantreproduction through pollination Insectivorous species werealso prominent in Musanzersquos urban landscapes Similarly tothe findings of Austin and Smith [5] insectivores were mostabundant in insect-rich landscapes including streamsideareas forests and informal settlements

432 FeedingGuild Categories byMicrolandscapes Althoughseedeaters especially the Grey-headed Sparrow (Passergriseus) dominated almost all microlandscapes it is impor-tant to consider that in wastelands scavengers were the mostabundant (Figure 13) This finding is likely due to the factthat different microlandscapes aremore appropriate for somespecies more than others especially those with differentfeeding habits

Our study confirms that bird species found in Musanzecity like urban-living bird species in other cities contributeto biomass recycling [36] Interestingly although there wereonly a few species of scavenging birds in Musanze theirabundance was high enough to compensate for their lowspecies richness in order to make a notable biomass recyclingimpact to city dwellersThis was particularly true for the Pied

Figure 13 Abundance of Pied Crows in a landfill within Musanzecity (Photo Author 2012)

Crow (Corvus albus) a species whose abundance amountedto more than seven times the average number of individualsper species whichwas almost 10of the total number of birdsobserved

44 Species Diversity

441 Alpha Diversity The bird diversity found in built-up areas was comparable to the bird diversity in urbanopen fields in Musanze city (Figure 9(a)) This finding pro-vides support for the increasingly recognized idea that birddiversity in urban areas can be as high as that in naturalenvironments [37 38] Previous research suggests that thismay be due to a relatively high number of nonnative speciespresent in cities as well as the heterogeneous habitat thaturban landscapes provide [39] which was not supportedin this study perhaps because of close proximity of thestudy area to a network of natural environments (PNVGishwati forest and Buhanga eco-park Rugezi Mukungwaand Bihinga wetlands and Karago Bulera and Ruhondolakes) Moreover Luck [40] suggested that there is a positivecorrelation between human population density and birdspecies richness This relationship was demonstrated in ourstudy as species such as the Pied Crowwere found to bemostabundant throughout urban landscapes and therefore welladapted to an environment where high human densities existInterestingly even the Albertine Rift endemic species theRuwenzori Double-collared Sunbird was sighted foraging inhuman populated areas on garden plants

Overall residential neighborhoods institutionalgrounds and informal settlements can be considered asthe major bird hotspots in Musanze city (Figure 9(b)) Thesethree landscapes share a great floristic diversity providingmany important stimuli for bird life (such as fruits seedsnectar domestic residues insects small mammals reptilesand amphibians) [30] Finally contrary to rural areas andnatural forests that undergo seasonal shortages of resources[3] cities do not experience strong seasonal variation due toa continuous supply of recourses from remote areas

442 Species Similarity The macrolandscapes all appearedto have similar bird species composition which may bedue to landscape heterogeneity [39] This heterogeneity islikely a result of the lack of historical professional landscapeplanning and design leaving a mosaic landscape structure inboth built-up and open fields instead of a uniform landscapespecialization Our results suggest that residential areas and

The Scientific World Journal 11

informal settlements were the most similar in terms ofspecies composition These landscapes ultimately functionto host family life The only difference between residentialareas and informal settlements resides in their socioeconomicstatus which is reflected in the landscape structure Howeverboth landscapes are more similar to each other than toother landscapes Furthermore the species composition ofcemeteries was similar to both forests and some of the built-up microlandscapes which may be attributed to the fact thatthese areas are all surrounded by trees Additionally ceme-teries are characterized by low human disturbance whichmay compare to that of forests and some urban landscapesThese landscapes all harbor a wide variety of floweringplants which in the case of cemeteries are mainly plantedby bereaved ones Moreover the vegetation of graveyardsincludes a range of regeneration stages resulting in a widerange of habitats from the vegetation-free areas of newly duggraves to the reconstructed thickets around old graves [41]Finally riverside landscapes emerged as the most specializedlandscape type as expected with many distinctive speciesobserved in this landscape only Almost all the species foundin riverside areas were specialists of wetlands and were notfound elsewhere As a result it was the most dissimilar to allother microlandscapes

The high degree of similarity in terms of bird diversitybetween Musanze city and the protected natural habitatsnearby provide further support that wildlife does not exclu-sively inhabit protected areas [33 37 42] Although the twonatural habitats are at eight km from Musanze city morethan half of the species found in the city were also found inVPN The lower degree of similarity between Musanze andBuhanga eco-park may be linked to the relative geographiclocation of the two sites as Musanze city is almost half waybetween the two protected areas This finding may also beattributed to the fact that the diversity ofmicrohabitats withinBuhanga eco-park is lower than that of Musanze and VPN[13] which may be due to the relatively small size of Buhangaeco-park Interestingly the species found in more than onelandscape type were also recorded both inside and beyondthe city limits Conversely Ficedula albicollis was recorded inonly one landscape type (cemeteries) and was absent in bothPNV and Buhanga eco-park

5 Conclusions

This study contributes to the knowledge of bird diversity inurban landscapes and provides the most recent status of birddiversity in Musanze city Our findings confirm that birddiversity in urban areas such as a densely populated city canbe as great as that in surrounding natural forests Specificallythe total number of bird species in Musanze city was verysimilar to that of the nearest protected forests VolcanoesNational Park and Buhanga eco-park Endemic and migra-tory birdswere also found inMusanze cityOneAlbertine Riftendemic bird species the Ruwenzori Double-collared Sun-bird was observed in Musanze during this study which hasnot been previously recorded Similarly threemigratory birdswere found inMusanze region for the first time the Common

Sandpiper the Spotted Flycatcher and theWillowWarbler Inaddition two bird species were observed that have not beenpreviously reported in Rwanda the Garden Warbler (Sylviaborin) and the Lesser Spotted Eagle (Aquila pomarina) Theeffect of landscape types on bird species richness and relativeabundance was also illustrated Residential neighborhoodsinstitutional grounds and informal settlements had thehighest species diversity indices and rankabundance relativeto the rest of the microlandscapes in this study Riversidelandscapes emerged with the most specialized bird faunaincluding species that are restricted to wetland environmentsand water bodies This study confirmed that scavengers inMusanze city contribute more to biomass recycling than anyother bird feeding groups Our study provides a current anduseful reference for urban decision makers and confirms theexistence of a great diversity of wildlife within cities Wesuggest that the development and implementation of cityland-use plans should consider this biodiversity especiallywhen villages and cities are in close proximity of protectedareas or natural reserves Finally it may be important thatbotanical gardens and public parks are included in themasterplan of the city as our study indicates that their designrequires an understanding of biodiversity in particular ofavian populations

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors acknowledge technical support from staffat DFGFI-Karisoke Research Center namely Dr WinnieEckardt Mr Deogratias Tuyisingize Mr Emmanuel Faidaand Mrs Keiko Mori

References

[1] S R Loss M O Ruiz and J D Brawn ldquoRelationships betweenavian diversity neighborhood age income and environmentalcharacteristics of an urban landscaperdquo Biological Conservationvol 142 no 11 pp 2578ndash2585 2009

[2] K L Evans D E Chamberlain B J Hatchwell R D Gregoryand K J Gaston ldquoWhat makes an urban birdrdquo Global ChangeBiology vol 17 no 1 pp 32ndash44 2011

[3] S Bolwig D Pomeroy H Tushabe and D Mushabe ldquoCropstrees and birds biodiversity change under agricultural inten-sification in Ugandas farmed landscapesrdquo Danish Journal ofGeography vol 106 no 2 pp 115ndash130 2006

[4] J Hitchmough and N Dunnett ldquoIntroduction to naturalisticplanting in urban landscapesrdquo in The Dynamic LandscapeJ Hitchmough and N Dunnatt Eds pp 1ndash32 Spon PressLondon UK 2004

[5] G T Austin and E L Smith ldquoWinter foraging ecology of mixedinsectivorous bird flocks in oakwoodland in southernArizonardquoThe Condor vol 74 pp 17ndash24 1972

[6] B R Coppedge D M Engle R E Masters and M S GregoryldquoAvian response to landscape change in fragmented southern

12 The Scientific World Journal

great plains grasslandsrdquo Ecological Applications vol 11 no 1 pp47ndash59 2001

[7] K L Evans S E Newson and K J Gaston ldquoHabitat influenceson urban avian assemblagesrdquo Ibis vol 151 no 1 pp 19ndash39 2009

[8] MW Strohbach D Haase and N Kabisch ldquoBirds and the cityUrban biodiversity land use and socioeconomicsrdquo Ecology andSociety vol 14 no 2 pp 31ndash45 2009

[9] T Stevenson and J Fanshawe Field Guide to the Birds of EastAfrica Kenya Tanzania Uganda Rwanda Burundi T amp A DPoyser London UK 2002

[10] J Mistry A Berardi and M Simpson ldquoBirds as indicators ofwetland status and change in the North Rupununi GuyanardquoBiodiversity and Conservation vol 17 no 10 pp 2383ndash24092008

[11] H Slabbekoorn and E A P Ripmeester ldquoBirdsong and anthro-pogenic noise implications and applications for conservationrdquoMolecular Ecology vol 17 no 1 pp 72ndash83 2008

[12] W S Judd C S Campbell E A Kellogg P F Stevens andM JDonoghue Plant Systematics A Phylogenetic Approach SinauerAssociates Sunderland Mass USA 3rd edition 2008

[13] W Weber ldquoRuhengeri and its resources an environmentalprofile of the Ruhengeri prefecturerdquo ETMAUSAID KigaliRwanda

[14] E Sabuhoro and G Bush ldquoThe Dian Fossey Gorilla FundInternationalPADGEF Assessing the Benefit Stream fromIllegal Activities in the Parc National des Volcansrdquo TargetingCommunity Conservation Interventions Musanze Rwanda2008

[15] J C Sano Urban Environmental Infrastructure in Kigali CityRwanda Challenges and Opportunities for Modernized Decen-tralized Sanitation Systems in Poor Neighborhoods WageningenUniversity Wageningen The Netherlands 2007

[16] R J Staniforth ldquoEffects of urbanization on bird populations inthe Canadian Central Arcticrdquo Arctic vol 55 no 1 pp 87ndash932002

[17] DWGibbons andRD Gregory ldquoBirdsrdquo in Ecological CensusesTechniques W L Sutherland Ed pp 308ndash350 CambridgeUniversity 2nd edition 2006

[18] D H Johnson ldquoPoint counts of birds what are we estimatingrdquoTech Rep PSW-GTR-149 USDA Forest Service 1995

[19] A Haslem and A F Bennett ldquoBirds in agricultural mosaics theinfluence of landscape pattern and countryside heterogeneityrdquoEcological Applications vol 18 no 1 pp 185ndash196 2008

[20] M L Rurangwa Feeding Ecology of Albertine Rift Endemic Birdsin the Volcanoes National Park Regal Sunbird Rwenzori Double-Collared Sunbird and Rwenzori Turako National University ofRwanda 2011

[21] R B Arellano-Valle H Bolfarine and V H Lachos ldquoSkew-normal linear mixedmodelsrdquo Journal of Data Science vol 3 pp415ndash438 2005

[22] D Bates Fitting LinearMixedModels in RTheNewsletter of theR Project Volume 51 University of Wisconsin Madison WisUSA 2005

[23] A E Magurran Measuring Biological Diversity Blackwell Sci-ence Malden Mass USA 2004

[24] D Tuyisingize and K Fawcett ldquoThe common bird distributionin the Parc National des Volcans and its surrounding patternsconservation and future challengesrdquo DFGF Technical Report2011

[25] A T Peterson and N A Slade ldquoExtrapolating inventory resultsinto biodiversity estimates and the importance of stoppingrulesrdquoDiversity and Distributions vol 4 no 3 pp 95ndash105 1998

[26] M Salek J Svobodova and P Zasadil ldquoEdge effect of low-trafficforest roads on bird communities in secondary productionforests in central Europerdquo Landscape Ecology vol 25 no 7 pp1113ndash1124 2010

[27] S Murererehe ldquoCollecte et analyse de donnees pourlrsquoamenagement durable des forets -Joindre les efforts nationauxet internationaux Etat des ressources forestieres au RwandardquoTech Rep FAO Rome Italy 2000

[28] S J Nsengimana M Ndimukaga L Gakwerere et al ldquoBiodi-versity surveyrdquo Tech Rep Rufford Small Grant FoundationLondon UK 2009

[29] C Nsabagasani ldquoA Migratory Species African Pitta ldquoPittaangolensisrdquo passed Buhanga relict forestrdquo Backbone vol 17 pp6ndash8 2008

[30] J Jokimaki and M Kaisanlahti-Jokimaki ldquoThe role of residen-tial habitat type on the temporal variation of wintering birdassemblages in northern Finlandrdquo Ornis Fennica vol 88 2011

[31] T M Bergin L B Best K E Freemark and K J KoehlerldquoEffects of landscape structure on nest predation in roadsides ofa midwestern agroecosystem a multiscale analysisrdquo LandscapeEcology vol 15 no 2 pp 131ndash143 2000

[32] T Koellner AMHersperger andTWohlgemuth ldquoRarefactionmethod for assessing plant species diversity on a regional scalerdquoEcography vol 27 no 4 pp 532ndash544 2004

[33] S H Faeth P S Warren E Shochat and W A MarussichldquoTrophic dynamics in urban communitiesrdquo BioScience vol 55no 5 pp 399ndash407 2005

[34] R J Fuller and J D Wilson ldquoThe ecology of seed-eating birdsin relation to agricultural practices current research and futuredirectionsrdquo British Trust for Ornithology Research Report no149 1995

[35] J N Holland andD L DeAngelis ldquoEcological and evolutionaryconditions for fruit abortion to regulate pollinating seed-eaters and increase plant reproductionrdquo Theoretical PopulationBiology vol 61 no 3 pp 251ndash263 2002

[36] C J Whelan D G Wenny and R J Marquis ldquoEcosystemservices provided by birdsrdquo Annals of the New York Academyof Sciences vol 1134 pp 25ndash60 2008

[37] O Gilbert The Ecology of Urban Habitats Chapman amp HallLondon UK 1989

[38] A Millard ldquoSemi-natural vegetation and its relationship todesignated urban green space at the landscape scale in LeedsUKrdquo Landscape Ecology vol 23 no 10 pp 1231ndash1241 2008

[39] I Kowarik ldquoOn the role of alien species in urban flora andvegetationrdquo in Plant Invasions General Aspects and SpecialProblems P Pysek K Prach M Rejmanek and M WadeEds pp 85ndash103 SPB Academic Publishing Amsterdam TheNetherlands 1995

[40] G W Luck ldquoA review of the relationships between humanpopulation density and biodiversityrdquo Biological Reviews vol 82no 4 pp 607ndash645 2007

[41] Victorian Government Department of Sustainability and Envi-ronment (VGDSE) Managing Native Vegetation in VictorianCemeteries Victorian Government Department of Sustainabil-ity and Environment Melbourne Australia 2009

[42] C Dowd ldquoEffect of development on bird species compositionof two urban forested wetlands in Staten Island New YorkrdquoJournal of Field Ornithology vol 63 no 4 pp 455ndash461 1992

Page 3: Bird Diversity and Distribution in relation to Urban Landscape Types in Northern Rwanda · 2016. 1. 26. · ResearchArticle Bird Diversity and Distribution in relation to Urban Landscape

The Scientific World Journal 3

Table 1 Distribution of plots across microlandscape types and administrative sectors

Landscape types Category Sectors Number of plotsAerodrome Open field Muhoza 2Agrofields Open field Muhoza Cyuve 5Business centers Built-up Musanze Muhoza Cyuve 5Cemeteries Open field Muhoza 2Forests Open field Musanze Muhoza Cyuve 5Institutional grounds Built-up Musanze Muhoza 5Residential neighborhood Built-up Muhoza 5Riversides Open field Muhoza 2Informal settlements Built-up Kimonyi Muhoza 5Streamsides Open field Musanze 2Wastelands Open field Muhoza Cyuve 2

bird species weather conditions vegetation cover and anykind of disturbance such as extra human presence or noisefrom nearby vehicles

Birds encountered outside of our study plots wererecorded only when it was a locally novel species suchthat it had never been observed in the area before Theserecords were only considered for compiling a bird checklistof Musanze city and were therefore excluded from statisticalanalysis When a bird could not be identified in the fieldphotos from a high-resolution camera and descriptive noteswere taken for later identification by a bird expert

24 Data Analysis The linear mixed models (LMM)methodwas used to analyze the relationships between landscape birdabundance and species richness LMM recently became auseful tool used to analyze continuous repeated measuresdata from a sample of individuals in different areas [21] LMMis a statistical model that consists of both fixed effects andrandom-effects terms and was therefore themost appropriatechoice for our study [22] In this study LMM was used toassess whether urban landscape types have an effect on birdabundance and species richness Landscape types (macro-and microlandscapes) were fixed effects (covariates) whilesampling plots were treated as a random effect to control forrepeated measures in plots Bird species richness and relativeabundance were dependent variables assessed in differentLMMs

The Shannonrsquos diversity index (1198671015840 = minussum119901119894log119901119894 where

119901119894is the proportion of individuals belonging to the 119894th

species) was used to identify the 120572-diversity of bird speciesboth at city and landscape type levels in order to identify thelocal average species diversity of each particular habitat TheBray-Curtis cluster analysis (single link) method was usedto assess the level of similarity in bird composition betweenlandscape types [23]

Referring to Tuyisingize and Fawcett [24] fromwhich weretrieved the checklist of birds of the PNV and Buhanga eco-park the bird diversity and abundance of Musanze city werecompared with the two natural ecosystems of these parksin terms of bird species richness and composition using thehierarchical clustering method

To examine the relationship between bird species andfood availability in the city bird species were categorizedaccording to their feeding guilds The completeness of thesurvey was assessed by analyzing patterns of the species accu-mulation curves [25] The accumulation curves of speciesrichness in different microlandscape types globally reachedtheir plateau (Figure 1) giving us confidence to conclude thatour sampling efforts had covered the majority of species inMusanze

To determine the level of significance of the obtainedresults hypothesis testing tools were used including thetest of Studentrsquos 119905-test Bioprofessional MVSP Origin and Rsoftware packages were used for these analyses

3 Results

31 Species Richness A total of 94 bird species were observedin Musanze city 15 of which were found opportunisticallyoutside plots Only one Albertine Rift endemic species(Ruwenzori Double-collared Sunbird Cinnyris stuhlmanni)was observed and seven migrant bird species were recorded

311 Number of Bird Species by Macrolandscape Types Therewas no significant difference in the number of bird species inopen fields and built-up areas (119905 = minus042 119875 = 067 Figure 2)Similarly the total number of bird species observed in bothmacrolandscapes was not notably different (119873 built-up = 63119873 open fields = 61)

312 Number of Species by Microlandscape Types Amongthe different microlandscapes institutional grounds had thehighest number of species (119873 = 42) followed by residentialneighborhoods (119873 = 41) and informal settlements (119873 =37) Furthermore forest and riverside landscapes had similarnumber in terms of total number of species (119873 = 35 forboth) Finally wastelands and the aerodrome demonstratedthe smallest number of bird species (119873 = 16 and 119873 = 15resp) (Figure 3)

For the LMM that examined the impact of differentmicrolandscapes on the number of bird species residentialneighborhoods were used as the reference microlandscape

4 The Scientific World Journal

50

40

30

20

10

0

0 200 400 600 800

Number of individuals

Num

ber o

f spe

cies

Rarefaction plot

WastelandsAerodromeCemeteriesAgrofieldsForestRiverside

StreamsideBusiness centersInstitutional groundInformal settlementResidence neighborhood

Figure 1 Bird species rarefaction curves at the site considered inthis study

Built-up areas Open fields0123456789

101112

Mea

n nu

mbe

r of b

ird sp

ecie

s per

visi

t

Macrolandscape types

Figure 2Mean number of species observed during plot visits in thetwo macrolandscape types

type as it showed the highest average number of bird speciesper plot visit (Figure 4) Thus the average number of birdspecies found in any other microlandscape was compared tothe number of bird species found in residential neighbor-hoods The LMM analysis revealed that the average numberof bird species found in all microlandscapes excluding ceme-teries and riversides was significantly lower than the numberof bird species in residential Musanzersquos neighborhood areas(Table 2) The average number of bird species observed in

IG RN IS FT RD AF CM SS BC WL AM0

10

20

30

40

Num

ber o

f spe

cies

Microlandscape types

Figure 3 Total bird species in microlandscape types (AM aero-drome AG agrofields BC business centers CM cemeteries FTforests IS informal settlements IG institutional grounds RNresidential neighborhoods RS riversides SS streamside WLwasteland)

Table 2 LMM output showing parameter estimates of microland-scape types on the number of bird species

Landscape types Std error 119905 value 119875 valueIntercept 074 15338 lt0001Aerodrome 139 minus5502 lt0001Agrofield 105 minus3330 lt001Business centers 105 minus6374 lt0001Cemeteries 139 minus1816 0069Forests 105 minus3473 lt001Institutional ground 105 minus2807 lt001Riversides 139 minus0827 0408Informal settlements 105 minus3330 lt001Streamside 139 minus2445 lt005Wastelands 139 minus2625 lt001

plots located in cemeteries tended to be less than the averagenumber found in residential neighborhoods

32 Species Relative Abundance

321 Number of Individuals by Macrolandscape Types Therewas no significant difference between open fields and built-up areas in terms of number of bird individuals observed pervisit (119905 = 035 119875 = 073 Figure 5)

322 Number of Individuals by Microlandscape Types Therewere significantly less birds in all microlandscape typescompared to the number of birds encountered in plotslocated in residential neighborhoods except for cemeteries(where fewer birdswere observed) riversides andwastelands(Figure 6 and Table 3)

The Scientific World Journal 5

AM AG BC CM FT IS IG RN RS SS WL0

2

4

6

8

10

12

14

16

Microlandscape types

Mea

n nu

mbe

r of b

ird sp

ecie

s per

visi

t

Figure 4 Mean number of bird species observed during plot visitsin each microlandscape type (AM aerodrome AG agrofields BCbusiness centers CM cemeteries FT forests IS informal settle-ments IG institutional grounds RN residential neighborhoods RSriversides SS streamside WL wasteland)

0

5

10

15

20

25

30

35

40

Mea

n nu

mbe

r of b

ird in

divi

dual

s per

visi

t

Built-up areas Open fieldsMacrolandscape types

Figure 5Mean number of bird individuals encountered per visit bymacrolandscape type

323 Most Represented Species The Pied Crow (Corvusalbus) the Grey-headed Sparrow (Passer griseus) StreakySeedeater (Serinus striolatus) and the Black Kite (Milvusmigrans) were found to be the most abundant species in thisstudy (Figure 7)

33 Feeding Guild Categories

331 Feeding Guild Categories by Macrolandscape TypesAmong the eleven feeding guilds represented by bird speciesin Musanze city seedeaters were the most common in bothbuilt-up areas and open fields followed by insectivorousspecies and scavengers (Figure 8)

Table 3 LMM output showing parameter estimates of microland-scape types on the number of bird individuals

Landscape types Std error 119905 value 119875 valueIntercept 012 27250 lt0001Aerodrome 0224 minus4970 lt0001Agrofield 0169 minus2330 lt005Business centers 0169 minus6646 lt0001Cemeteries 0224 minus1919 0055Forests 0169 minus3615 lt0001Institutional ground 0169 minus2229 lt005Riversides 0224 minus016 0873Informal settlements 0169 minus2899 lt001Streamside 0224 minus2029 lt005Wastelands 0224 0173 0860

AM AG BC CM FT IS IG RN RS SS WL0

5

10

15

20

25

30

35

40

45

50

55

Mea

n nu

mbe

r of b

ird in

divi

dual

s per

visi

t

Microlandscape types

Figure 6 Mean number of bird individuals observed per plotvisit by microlandscape type (AM aerodrome AG agrofields BCbusiness centers CM cemeteries FT forests IS informal settle-ments IG institutional grounds RN residential neighborhoods RSriversides SS streamside WL wasteland)

332 Feeding Guild Categories by Microlandscapes Seed-eating bird species were the most common across allmicrolandscapes except for wastelands which were domi-nated by scavengers a feeding type that was also recorded inevery landscape Insectivorous species were also present in allmicrolandscape types unlike fishers that were only recordedin riverside landscapes Riverside landscapes were also whereflycatchers a feeding type that was present in all landscapetypes were most abundant

34 Species Diversity

341 Alpha Diversity in Macro- and Microlandscape TypesThe bird species diversity in both macro- and microland-scapes of Musanze are described using Whittaker curves(Figure 9) Using these curves built-up areas were slightlyhigher ranked in terms of bird diversity than open fields(Figure 9(a)) Amongmicrolandscapes institutional grounds

6 The Scientific World Journal

0 50 100 150 200 250 300Number of individuals

Spec

ies n

ame

Nectarinia kilimensis

Ploceus melanocephalus

Ploceus baglafecht

Estrilda astrild

Lagonosticta senegala

Lonchura cucullata

Milvus migrans

Serinus striolatus

Passer griseus

Corvus albus

Figure 7 Top ten most represented bird species in all sites of Musanze city

0 100 200 300 400 500 600 700Number of individuals

Aerial feeders

Butcherbirds

Fishers

Flycatchers

Frugivores

Insectivores

Nectar feeders

Raptors

Scavengers

Seedeaters

Shorerbirds

Feed

ing

guild

s

Open fields Built-up areas

Figure 8 Feeding guild categories of bird species as classified in microlandscapes types

had the highest diversity rank followed by residentialneighborhoods and informal settlements The aerodromeand Westland were ranked with the lowest bird diversity(Figure 9(b))

The Shannon diversity index was similar for bothmacrolandscape types built-up areas (1198671015840 = 1456) and itscounterpart open fields (1198671015840 = 1518) At the microland-scape level residential neighborhoods were the most diversefollowed by informal settlements and institutional groundsWastelands displayed the lowest bird diversity (Figure 10)

342 Species Similarity in Macro- and Microlandscape TypesOf the 94 bird species recorded in Musanze city 45 specieswere shared by both open fields and built-up landscapes Interms of species composition found in each microlandscape

type the riverside landscape was the most different fromthe remaining microlandscapes Residential neighborhoodsand informal settlements were most similar The differencesbetween the landscape types in terms of species compositionillustrated by the increasing distance from the root to thepoint where a given branch stems were as follows riversidelt aerodrome lt streamside lt wasteland lt agrofields lt ceme-teries lt forest lt institutional and business center lt informalsettlements and residences (Figure 11)

35 Bird Diversity in Musanze City and Nearby ProtectedAreas In addition to the internal comparison the level ofsimilarity between Musanze and its nearby protected areas(PNV and Buhanga eco-park) revealed important similaritiesbetween protected and urban habitats in terms of bird

The Scientific World Journal 7

0 5 10 15 20 25 30 35 4005

10

15

20

25

Rank

Open fieldsBuilt-up area

Log 1

0re

lativ

e abu

ndan

ce

(a)

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38

04

06

08

10

12

14

16

18

20

22

Rankminus2

AerodromeAgrofield Business centerCemeteriesForest

InstitutionalResidenceRiversideSettlementStreamside

WastelandLo

g 10

rela

tive a

bund

ance

(b)

Figure 9 Species rankabundance (a) in macrolandscape types and (b) in microlandscape types

Aerodrome

Agrofields

Business centers

Cemeteries

Forests

Institutional grounds

Residential neighborhoods

Riversides

Informal settlements

Streamsides

Wastelands

00 02 04 06 08 10 12 14Shannon index

Mic

rola

ndsc

ape t

ypes

Figure 10 Shannon index for microlandscape types of Musanze city

diversity (Figure 12) The total number of bird species inMusanze city was 94 105 in PNV and 81 in the Buhanga eco-park Of the 94 bird species recorded in Musanze 32 werealso present in Buhanga eco-park 51 in the PNV and 21 werefound in both the Buhanga eco-park and in PNV Moreoverwe found only one endemic bird species the RuwenzoriDouble-collared Sunbird (Cinnyris stuhlmanni) in Musanzeunlike the three endemic bird species present in Buhanga eco-park and the fifteen in the PNV This Albertine Rift endemic

species is also present in the PNV however it is absent fromthe Buhanga eco-park

In the comparison of the bird species found in the threesites Musanze city is unique in the number of migratory birdspecies observed Specifically seven migratory species wererecorded in Musanze city while only two are known to existin the PNV and none have been recorded in the Buhanga eco-park (Table 4) Musanzersquos microlandscapes that were visitedbymigratory birds include the riversides ofMukungwa River

8 The Scientific World Journal

RSWLSSISRNIGFTAFCMBCAM

1000 50

Similarity ()

Bray-Curtis cluster analysis (single link)

Figure 11 Species composition-based microlandscape clusters(AM aerodrome AG agrofields BC business centers CM ceme-teries FT forests IS informal settlements IG institutional groundsRN residential neighborhoods RS riversides SS streamside WLwasteland)

1000 50

Similarity ()

Bray-Curtis cluster analysis (single link)

PNV

Musanze

Buhanga

Figure 12 Musanze city PNV and Buhanga eco-park bird speciescomposition

informal settlements forests business centers and residentialneighborhoods

The majority of species in Musanze city were nativesuch that exotic bird species accounted for only 43 of thetotal number of bird species observed (Ficedula albicollisPloceus cucullatus Serinus canicollis and Serinus citrinel-loides) (Table 5) Up to 64 of the species observed hadno breeding opportunities within the study area (Actitishypoleucos Aquila pomarina Merops apiaster Muscicapastriata Phylloscopus trochilus and Sylvia borin)

4 Discussion

Our study of bird diversity in Musanze city has revealed thatcurrent wildlife conservation efforts do not coincide withareas of the highest bird abundance and species diversitywhich exist in urban areas Bird species richness in theurban areas of Musanze is greater than that of Buhangaeco-park and similar to that of the PNV two surroundingnatural habitats that are currently receiving the majority ofconservation efforts Furthermore species of high ecologicalimportance and therefore high conservation concern such

as endemic and migratory species were recorded across thecity landscapesThis study therefore indicates the importanceof protecting not only the natural habitats of native wildlifebut also urban areas where birds in particular are morecommonly existing

41 Species Richness The unique endemic species found inMusanze city the Ruwenzori Double-collared Sunbird haspreviously been observed in the VPN This species is knownto live in the high altitude habitats of the Albertine Rift[24] It is therefore not surprising that it was found in urbanlandscapes ofMusanze city which is located at a high altitudeof 1850m [26] Stevenson and Fanshawe [9] suggest thatthe sunbirdrsquos most preferred habitats are flowering bushes offorest edges and it may be unusual that the endemic specieswas observed foraging onMarkhamia lutea trees within openfields of Musanze city in this study Our study suggests thatthe species distribution of the Ruwenzori Double-collaredSunbird is not restricted to its natural habitat in the AlbertineRift as it can also exist in urban landscapesThis species maytherefore be able to adapt to human-dominated landscapesand it is likely that it may forage on vegetation such as urbangarden trees Our study suggests that the sunbird is capableof adapting its feeding preferences to the available plants incity landscapes potentially as a response to loss of its naturalhabitat caused by park reductions [27]

The seven migrant bird species found in the studysite were regular September-April visitors from Palearcticregions Two of them the Red-chested Cuckoo (Cucu-lus solitarius) and the European Bee-eater (Merops api-aster) had previously been sighted in the gallery forestsof the Rwandanrsquos Eastern Province [28] and in the PNV[24] The Common Sandpiper Spotted Flycatcher andWillow Warbler have also been reported to visit Rwanda(httpwwwrwandabirdingorg 02092012) and Musanzecity but have never been sighted in the Lava Plain or inthe Volcano Range of Rwanda The remaining two migrantsthe Garden Warbler (Sylvia borin) and the Lesser SpottedEagle (Aquila pomarina) have been reported in Rwandafor the first time as a result of this study Importantly theseven migrant species have never been reported to occurin urban environments of Rwanda and only two had beenreported to visit its highlands [24] However the AfricanPitta (Pitta angolensis) which is an intra-African breedingmigrant bird sighted in the Buhanga eco-park in 2006 and2008 [29] was not recorded in this study The findings of ourstudy encourage the development of bird watching activitiesin Musanze city which may be of particular interest tointernational tourists due to the high number of urban-livingand therefore easily observed unique bird species

411 Number of Species by Macrolandscape Types Thehypothesis that bird species inhabit open fields more thanbuilt-up areas was not supported in this study This maybe due to the fact that some built-up areas including insti-tutional grounds residential neighborhoods and informalsettlements are specifically designed with plant communi-ties to attract birds [30] These communities often include

The Scientific World Journal 9

Table 4 Migratory birds in Musanze city PNV and Buhanga eco-park

Common name Scientific name Musanze city Protected areasPNV Buhanga eco-park

Common Sandpiper Actitis hypoleucos

European Bee-eater Merops apiaster

Garden Warbler Sylvia borin

Lesser-spotted Eagle Aquila pomarina

Red-chested Cuckoo Cuculus solitarius

Spotted Flycatcher Muscicapa striata

WillowWarbler Phylloscopus trochilus

Table 5 Exotic birds in Musanze city PNV and Buhanga eco-park

Common name Scientific name Musanze city Protected areasPNV Buhanga eco-park

Collared Flycatcher Ficedula albicollis

Black-headed Weaver Ploceus cucullatus

Yellow-crowned Canary Serinus canicollis

Abyssinian Citril Serinus citrinelloides

a number of trees with a substantial canopy as well asornamental plants such as vegetation that exists as bushesAlternatively some microlandscapes within open fields havea low number of species such as the Musanze aerodromewhich is a grassland habitat and is regularly maintained tofacilitate airplane landing This habitat offers little feedingopportunities to wildlife and is an unsuitable habitat for mostbird species as it may for instance expose small-sized birdsto predators [31]

412 Number of Species by Microlandscape Types In supportof Koellner et al [32] different landscapes in Musanze werecorrelated with differences in bird species richness Theinstitutional grounds had a relatively high species richnessperhaps due to a high variety of plant assemblages Simi-larly the high number of bird species found in residentialneighborhoods and informal settlements can be explained bythe diversity of plant resources in these areas These plantresources include nectar-producing flowers such as bananaplants that attract sunbirds fruit-bearing trees and shrubssuch as guava plants that frugivorous species can feed on Inaddition the high concentrations of domestic wastes (such asresidues food disposable and waste-water) in the homesteadenvironment offer a unique opportunity to predators suchas insectivorous birds that feed on small mammals (egmice frogs) and insects (eg flies mosquitoes) and arecommon to this type of microhabitats Domestic waste mayalso attract scavenger species Finally informal settlementsthat are surrounded by a mosaic of vegetation types offermany opportunities for bird foraging and nesting [30] Thisdiversity in urban landscape vegetation structure and typemay therefore reflect the vast diversity of bird species in urbanareas which has not previously been investigated in Rwanda

42 Species Relative Abundance

421 Number of Individuals by Macrolandscape Types Thenonsignificant effect of macrolandscapes on the total numberof birds in an area may be linked to the fact that landscapetype had no significant influence on bird species richnessMore importantly due to the historical nonformal nature ofurban design in Musanze both macrolandscapes appeared tohave similar types and levels of bird-exploitable resourcesincluding appropriate plant coverage and sites for birds tonest [33]

422 Number of Individuals byMicrolandscape Types Ceme-teries riverside landscapes and wastelands did not differin the total number of birds in comparison to residentialneighborhoods (Table 3) This may be attributed to the factthat these four landscapes appear to be intrinsically hetero-geneous suggesting that there may be possible confoundingfactors that have overshadowed the expected relationshipbetween microlandscapes and relative bird abundance Forinstance wastelands attract many scavengers and raptorscemeteries and agrofields provide appropriate plant assem-blages for seed eaters and riversides offer easy water accessand shelter for aquatic bird species [4] Therefore theabundance of birds across the different microlandscapes ofMusanze is relatively uniform due to the fact that eachlandscape offers a range of suitable habitats for a range of birdspecies

423 Most Represented Species in Musanze City The PiedCrow (Corvus albus) was the most common species inMusanze and seemed to be the most adapted to human-dominated landscapes (Figure 7) For instance unlike many

10 The Scientific World Journal

other bird species in the area the Pied Crow was observedclose to many human facilities such food markets abattoirswastelands domestic yards and croplands In addition thePied Crow was found in high abundance where its foodsources including small reptiles small mammals grainpeanuts carrion scraps of human food fruits insects andother small invertebrates were most available [9] To a lesserextent the urban habitat appeared to favor the Grey-headedSparrow (Passer griseus) The occurrence of the Grey-headedSparrow was associated with open woodlands and humansettlements where this species can easily access required foodand habitat resources The third most represented specieswas the Streaky Seedeater (Serinus striolatus) which is acommon bird of highlands and is generally found above1300m in gardens and cultivated areas woodland edgesheath and scrub vegetation areas The Streaky Seedeateris therefore adept at living in human altered landscapeswhich is not unlike the Black Kite (Milvus migrans) whichwas also common to densely human-populated areas Thesehuman-used landscapes are also a popular habitat of theBlackKitersquos prey which includes small birds bats and rodents Inparticular our study revealed the common occurrence of theBlack Kite circling near the abattoir and scavenging in thecityrsquos wastelands

43 Feeding Guild Categories

431 Feeding Guild Categories by Macrolandscape TypesSeed-eating birds were the best represented guild inMusanze(Figure 8) This may be partially due to the fact that datacollection was completed during a maize-harvesting periodDuring this period urban fields have an exceptionally largeabundance of seeds that can be exploited by birds and mayhave therefore selectively attracted seed-eating species [34]It was also observed that seed-eating species fed from arange of fruits According to Holland and DeAngelis [35]this habit allows seed-eating species to contribute to plantreproduction through pollination Insectivorous species werealso prominent in Musanzersquos urban landscapes Similarly tothe findings of Austin and Smith [5] insectivores were mostabundant in insect-rich landscapes including streamsideareas forests and informal settlements

432 FeedingGuild Categories byMicrolandscapes Althoughseedeaters especially the Grey-headed Sparrow (Passergriseus) dominated almost all microlandscapes it is impor-tant to consider that in wastelands scavengers were the mostabundant (Figure 13) This finding is likely due to the factthat different microlandscapes aremore appropriate for somespecies more than others especially those with differentfeeding habits

Our study confirms that bird species found in Musanzecity like urban-living bird species in other cities contributeto biomass recycling [36] Interestingly although there wereonly a few species of scavenging birds in Musanze theirabundance was high enough to compensate for their lowspecies richness in order to make a notable biomass recyclingimpact to city dwellersThis was particularly true for the Pied

Figure 13 Abundance of Pied Crows in a landfill within Musanzecity (Photo Author 2012)

Crow (Corvus albus) a species whose abundance amountedto more than seven times the average number of individualsper species whichwas almost 10of the total number of birdsobserved

44 Species Diversity

441 Alpha Diversity The bird diversity found in built-up areas was comparable to the bird diversity in urbanopen fields in Musanze city (Figure 9(a)) This finding pro-vides support for the increasingly recognized idea that birddiversity in urban areas can be as high as that in naturalenvironments [37 38] Previous research suggests that thismay be due to a relatively high number of nonnative speciespresent in cities as well as the heterogeneous habitat thaturban landscapes provide [39] which was not supportedin this study perhaps because of close proximity of thestudy area to a network of natural environments (PNVGishwati forest and Buhanga eco-park Rugezi Mukungwaand Bihinga wetlands and Karago Bulera and Ruhondolakes) Moreover Luck [40] suggested that there is a positivecorrelation between human population density and birdspecies richness This relationship was demonstrated in ourstudy as species such as the Pied Crowwere found to bemostabundant throughout urban landscapes and therefore welladapted to an environment where high human densities existInterestingly even the Albertine Rift endemic species theRuwenzori Double-collared Sunbird was sighted foraging inhuman populated areas on garden plants

Overall residential neighborhoods institutionalgrounds and informal settlements can be considered asthe major bird hotspots in Musanze city (Figure 9(b)) Thesethree landscapes share a great floristic diversity providingmany important stimuli for bird life (such as fruits seedsnectar domestic residues insects small mammals reptilesand amphibians) [30] Finally contrary to rural areas andnatural forests that undergo seasonal shortages of resources[3] cities do not experience strong seasonal variation due toa continuous supply of recourses from remote areas

442 Species Similarity The macrolandscapes all appearedto have similar bird species composition which may bedue to landscape heterogeneity [39] This heterogeneity islikely a result of the lack of historical professional landscapeplanning and design leaving a mosaic landscape structure inboth built-up and open fields instead of a uniform landscapespecialization Our results suggest that residential areas and

The Scientific World Journal 11

informal settlements were the most similar in terms ofspecies composition These landscapes ultimately functionto host family life The only difference between residentialareas and informal settlements resides in their socioeconomicstatus which is reflected in the landscape structure Howeverboth landscapes are more similar to each other than toother landscapes Furthermore the species composition ofcemeteries was similar to both forests and some of the built-up microlandscapes which may be attributed to the fact thatthese areas are all surrounded by trees Additionally ceme-teries are characterized by low human disturbance whichmay compare to that of forests and some urban landscapesThese landscapes all harbor a wide variety of floweringplants which in the case of cemeteries are mainly plantedby bereaved ones Moreover the vegetation of graveyardsincludes a range of regeneration stages resulting in a widerange of habitats from the vegetation-free areas of newly duggraves to the reconstructed thickets around old graves [41]Finally riverside landscapes emerged as the most specializedlandscape type as expected with many distinctive speciesobserved in this landscape only Almost all the species foundin riverside areas were specialists of wetlands and were notfound elsewhere As a result it was the most dissimilar to allother microlandscapes

The high degree of similarity in terms of bird diversitybetween Musanze city and the protected natural habitatsnearby provide further support that wildlife does not exclu-sively inhabit protected areas [33 37 42] Although the twonatural habitats are at eight km from Musanze city morethan half of the species found in the city were also found inVPN The lower degree of similarity between Musanze andBuhanga eco-park may be linked to the relative geographiclocation of the two sites as Musanze city is almost half waybetween the two protected areas This finding may also beattributed to the fact that the diversity ofmicrohabitats withinBuhanga eco-park is lower than that of Musanze and VPN[13] which may be due to the relatively small size of Buhangaeco-park Interestingly the species found in more than onelandscape type were also recorded both inside and beyondthe city limits Conversely Ficedula albicollis was recorded inonly one landscape type (cemeteries) and was absent in bothPNV and Buhanga eco-park

5 Conclusions

This study contributes to the knowledge of bird diversity inurban landscapes and provides the most recent status of birddiversity in Musanze city Our findings confirm that birddiversity in urban areas such as a densely populated city canbe as great as that in surrounding natural forests Specificallythe total number of bird species in Musanze city was verysimilar to that of the nearest protected forests VolcanoesNational Park and Buhanga eco-park Endemic and migra-tory birdswere also found inMusanze cityOneAlbertine Riftendemic bird species the Ruwenzori Double-collared Sun-bird was observed in Musanze during this study which hasnot been previously recorded Similarly threemigratory birdswere found inMusanze region for the first time the Common

Sandpiper the Spotted Flycatcher and theWillowWarbler Inaddition two bird species were observed that have not beenpreviously reported in Rwanda the Garden Warbler (Sylviaborin) and the Lesser Spotted Eagle (Aquila pomarina) Theeffect of landscape types on bird species richness and relativeabundance was also illustrated Residential neighborhoodsinstitutional grounds and informal settlements had thehighest species diversity indices and rankabundance relativeto the rest of the microlandscapes in this study Riversidelandscapes emerged with the most specialized bird faunaincluding species that are restricted to wetland environmentsand water bodies This study confirmed that scavengers inMusanze city contribute more to biomass recycling than anyother bird feeding groups Our study provides a current anduseful reference for urban decision makers and confirms theexistence of a great diversity of wildlife within cities Wesuggest that the development and implementation of cityland-use plans should consider this biodiversity especiallywhen villages and cities are in close proximity of protectedareas or natural reserves Finally it may be important thatbotanical gardens and public parks are included in themasterplan of the city as our study indicates that their designrequires an understanding of biodiversity in particular ofavian populations

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors acknowledge technical support from staffat DFGFI-Karisoke Research Center namely Dr WinnieEckardt Mr Deogratias Tuyisingize Mr Emmanuel Faidaand Mrs Keiko Mori

References

[1] S R Loss M O Ruiz and J D Brawn ldquoRelationships betweenavian diversity neighborhood age income and environmentalcharacteristics of an urban landscaperdquo Biological Conservationvol 142 no 11 pp 2578ndash2585 2009

[2] K L Evans D E Chamberlain B J Hatchwell R D Gregoryand K J Gaston ldquoWhat makes an urban birdrdquo Global ChangeBiology vol 17 no 1 pp 32ndash44 2011

[3] S Bolwig D Pomeroy H Tushabe and D Mushabe ldquoCropstrees and birds biodiversity change under agricultural inten-sification in Ugandas farmed landscapesrdquo Danish Journal ofGeography vol 106 no 2 pp 115ndash130 2006

[4] J Hitchmough and N Dunnett ldquoIntroduction to naturalisticplanting in urban landscapesrdquo in The Dynamic LandscapeJ Hitchmough and N Dunnatt Eds pp 1ndash32 Spon PressLondon UK 2004

[5] G T Austin and E L Smith ldquoWinter foraging ecology of mixedinsectivorous bird flocks in oakwoodland in southernArizonardquoThe Condor vol 74 pp 17ndash24 1972

[6] B R Coppedge D M Engle R E Masters and M S GregoryldquoAvian response to landscape change in fragmented southern

12 The Scientific World Journal

great plains grasslandsrdquo Ecological Applications vol 11 no 1 pp47ndash59 2001

[7] K L Evans S E Newson and K J Gaston ldquoHabitat influenceson urban avian assemblagesrdquo Ibis vol 151 no 1 pp 19ndash39 2009

[8] MW Strohbach D Haase and N Kabisch ldquoBirds and the cityUrban biodiversity land use and socioeconomicsrdquo Ecology andSociety vol 14 no 2 pp 31ndash45 2009

[9] T Stevenson and J Fanshawe Field Guide to the Birds of EastAfrica Kenya Tanzania Uganda Rwanda Burundi T amp A DPoyser London UK 2002

[10] J Mistry A Berardi and M Simpson ldquoBirds as indicators ofwetland status and change in the North Rupununi GuyanardquoBiodiversity and Conservation vol 17 no 10 pp 2383ndash24092008

[11] H Slabbekoorn and E A P Ripmeester ldquoBirdsong and anthro-pogenic noise implications and applications for conservationrdquoMolecular Ecology vol 17 no 1 pp 72ndash83 2008

[12] W S Judd C S Campbell E A Kellogg P F Stevens andM JDonoghue Plant Systematics A Phylogenetic Approach SinauerAssociates Sunderland Mass USA 3rd edition 2008

[13] W Weber ldquoRuhengeri and its resources an environmentalprofile of the Ruhengeri prefecturerdquo ETMAUSAID KigaliRwanda

[14] E Sabuhoro and G Bush ldquoThe Dian Fossey Gorilla FundInternationalPADGEF Assessing the Benefit Stream fromIllegal Activities in the Parc National des Volcansrdquo TargetingCommunity Conservation Interventions Musanze Rwanda2008

[15] J C Sano Urban Environmental Infrastructure in Kigali CityRwanda Challenges and Opportunities for Modernized Decen-tralized Sanitation Systems in Poor Neighborhoods WageningenUniversity Wageningen The Netherlands 2007

[16] R J Staniforth ldquoEffects of urbanization on bird populations inthe Canadian Central Arcticrdquo Arctic vol 55 no 1 pp 87ndash932002

[17] DWGibbons andRD Gregory ldquoBirdsrdquo in Ecological CensusesTechniques W L Sutherland Ed pp 308ndash350 CambridgeUniversity 2nd edition 2006

[18] D H Johnson ldquoPoint counts of birds what are we estimatingrdquoTech Rep PSW-GTR-149 USDA Forest Service 1995

[19] A Haslem and A F Bennett ldquoBirds in agricultural mosaics theinfluence of landscape pattern and countryside heterogeneityrdquoEcological Applications vol 18 no 1 pp 185ndash196 2008

[20] M L Rurangwa Feeding Ecology of Albertine Rift Endemic Birdsin the Volcanoes National Park Regal Sunbird Rwenzori Double-Collared Sunbird and Rwenzori Turako National University ofRwanda 2011

[21] R B Arellano-Valle H Bolfarine and V H Lachos ldquoSkew-normal linear mixedmodelsrdquo Journal of Data Science vol 3 pp415ndash438 2005

[22] D Bates Fitting LinearMixedModels in RTheNewsletter of theR Project Volume 51 University of Wisconsin Madison WisUSA 2005

[23] A E Magurran Measuring Biological Diversity Blackwell Sci-ence Malden Mass USA 2004

[24] D Tuyisingize and K Fawcett ldquoThe common bird distributionin the Parc National des Volcans and its surrounding patternsconservation and future challengesrdquo DFGF Technical Report2011

[25] A T Peterson and N A Slade ldquoExtrapolating inventory resultsinto biodiversity estimates and the importance of stoppingrulesrdquoDiversity and Distributions vol 4 no 3 pp 95ndash105 1998

[26] M Salek J Svobodova and P Zasadil ldquoEdge effect of low-trafficforest roads on bird communities in secondary productionforests in central Europerdquo Landscape Ecology vol 25 no 7 pp1113ndash1124 2010

[27] S Murererehe ldquoCollecte et analyse de donnees pourlrsquoamenagement durable des forets -Joindre les efforts nationauxet internationaux Etat des ressources forestieres au RwandardquoTech Rep FAO Rome Italy 2000

[28] S J Nsengimana M Ndimukaga L Gakwerere et al ldquoBiodi-versity surveyrdquo Tech Rep Rufford Small Grant FoundationLondon UK 2009

[29] C Nsabagasani ldquoA Migratory Species African Pitta ldquoPittaangolensisrdquo passed Buhanga relict forestrdquo Backbone vol 17 pp6ndash8 2008

[30] J Jokimaki and M Kaisanlahti-Jokimaki ldquoThe role of residen-tial habitat type on the temporal variation of wintering birdassemblages in northern Finlandrdquo Ornis Fennica vol 88 2011

[31] T M Bergin L B Best K E Freemark and K J KoehlerldquoEffects of landscape structure on nest predation in roadsides ofa midwestern agroecosystem a multiscale analysisrdquo LandscapeEcology vol 15 no 2 pp 131ndash143 2000

[32] T Koellner AMHersperger andTWohlgemuth ldquoRarefactionmethod for assessing plant species diversity on a regional scalerdquoEcography vol 27 no 4 pp 532ndash544 2004

[33] S H Faeth P S Warren E Shochat and W A MarussichldquoTrophic dynamics in urban communitiesrdquo BioScience vol 55no 5 pp 399ndash407 2005

[34] R J Fuller and J D Wilson ldquoThe ecology of seed-eating birdsin relation to agricultural practices current research and futuredirectionsrdquo British Trust for Ornithology Research Report no149 1995

[35] J N Holland andD L DeAngelis ldquoEcological and evolutionaryconditions for fruit abortion to regulate pollinating seed-eaters and increase plant reproductionrdquo Theoretical PopulationBiology vol 61 no 3 pp 251ndash263 2002

[36] C J Whelan D G Wenny and R J Marquis ldquoEcosystemservices provided by birdsrdquo Annals of the New York Academyof Sciences vol 1134 pp 25ndash60 2008

[37] O Gilbert The Ecology of Urban Habitats Chapman amp HallLondon UK 1989

[38] A Millard ldquoSemi-natural vegetation and its relationship todesignated urban green space at the landscape scale in LeedsUKrdquo Landscape Ecology vol 23 no 10 pp 1231ndash1241 2008

[39] I Kowarik ldquoOn the role of alien species in urban flora andvegetationrdquo in Plant Invasions General Aspects and SpecialProblems P Pysek K Prach M Rejmanek and M WadeEds pp 85ndash103 SPB Academic Publishing Amsterdam TheNetherlands 1995

[40] G W Luck ldquoA review of the relationships between humanpopulation density and biodiversityrdquo Biological Reviews vol 82no 4 pp 607ndash645 2007

[41] Victorian Government Department of Sustainability and Envi-ronment (VGDSE) Managing Native Vegetation in VictorianCemeteries Victorian Government Department of Sustainabil-ity and Environment Melbourne Australia 2009

[42] C Dowd ldquoEffect of development on bird species compositionof two urban forested wetlands in Staten Island New YorkrdquoJournal of Field Ornithology vol 63 no 4 pp 455ndash461 1992

Page 4: Bird Diversity and Distribution in relation to Urban Landscape Types in Northern Rwanda · 2016. 1. 26. · ResearchArticle Bird Diversity and Distribution in relation to Urban Landscape

4 The Scientific World Journal

50

40

30

20

10

0

0 200 400 600 800

Number of individuals

Num

ber o

f spe

cies

Rarefaction plot

WastelandsAerodromeCemeteriesAgrofieldsForestRiverside

StreamsideBusiness centersInstitutional groundInformal settlementResidence neighborhood

Figure 1 Bird species rarefaction curves at the site considered inthis study

Built-up areas Open fields0123456789

101112

Mea

n nu

mbe

r of b

ird sp

ecie

s per

visi

t

Macrolandscape types

Figure 2Mean number of species observed during plot visits in thetwo macrolandscape types

type as it showed the highest average number of bird speciesper plot visit (Figure 4) Thus the average number of birdspecies found in any other microlandscape was compared tothe number of bird species found in residential neighbor-hoods The LMM analysis revealed that the average numberof bird species found in all microlandscapes excluding ceme-teries and riversides was significantly lower than the numberof bird species in residential Musanzersquos neighborhood areas(Table 2) The average number of bird species observed in

IG RN IS FT RD AF CM SS BC WL AM0

10

20

30

40

Num

ber o

f spe

cies

Microlandscape types

Figure 3 Total bird species in microlandscape types (AM aero-drome AG agrofields BC business centers CM cemeteries FTforests IS informal settlements IG institutional grounds RNresidential neighborhoods RS riversides SS streamside WLwasteland)

Table 2 LMM output showing parameter estimates of microland-scape types on the number of bird species

Landscape types Std error 119905 value 119875 valueIntercept 074 15338 lt0001Aerodrome 139 minus5502 lt0001Agrofield 105 minus3330 lt001Business centers 105 minus6374 lt0001Cemeteries 139 minus1816 0069Forests 105 minus3473 lt001Institutional ground 105 minus2807 lt001Riversides 139 minus0827 0408Informal settlements 105 minus3330 lt001Streamside 139 minus2445 lt005Wastelands 139 minus2625 lt001

plots located in cemeteries tended to be less than the averagenumber found in residential neighborhoods

32 Species Relative Abundance

321 Number of Individuals by Macrolandscape Types Therewas no significant difference between open fields and built-up areas in terms of number of bird individuals observed pervisit (119905 = 035 119875 = 073 Figure 5)

322 Number of Individuals by Microlandscape Types Therewere significantly less birds in all microlandscape typescompared to the number of birds encountered in plotslocated in residential neighborhoods except for cemeteries(where fewer birdswere observed) riversides andwastelands(Figure 6 and Table 3)

The Scientific World Journal 5

AM AG BC CM FT IS IG RN RS SS WL0

2

4

6

8

10

12

14

16

Microlandscape types

Mea

n nu

mbe

r of b

ird sp

ecie

s per

visi

t

Figure 4 Mean number of bird species observed during plot visitsin each microlandscape type (AM aerodrome AG agrofields BCbusiness centers CM cemeteries FT forests IS informal settle-ments IG institutional grounds RN residential neighborhoods RSriversides SS streamside WL wasteland)

0

5

10

15

20

25

30

35

40

Mea

n nu

mbe

r of b

ird in

divi

dual

s per

visi

t

Built-up areas Open fieldsMacrolandscape types

Figure 5Mean number of bird individuals encountered per visit bymacrolandscape type

323 Most Represented Species The Pied Crow (Corvusalbus) the Grey-headed Sparrow (Passer griseus) StreakySeedeater (Serinus striolatus) and the Black Kite (Milvusmigrans) were found to be the most abundant species in thisstudy (Figure 7)

33 Feeding Guild Categories

331 Feeding Guild Categories by Macrolandscape TypesAmong the eleven feeding guilds represented by bird speciesin Musanze city seedeaters were the most common in bothbuilt-up areas and open fields followed by insectivorousspecies and scavengers (Figure 8)

Table 3 LMM output showing parameter estimates of microland-scape types on the number of bird individuals

Landscape types Std error 119905 value 119875 valueIntercept 012 27250 lt0001Aerodrome 0224 minus4970 lt0001Agrofield 0169 minus2330 lt005Business centers 0169 minus6646 lt0001Cemeteries 0224 minus1919 0055Forests 0169 minus3615 lt0001Institutional ground 0169 minus2229 lt005Riversides 0224 minus016 0873Informal settlements 0169 minus2899 lt001Streamside 0224 minus2029 lt005Wastelands 0224 0173 0860

AM AG BC CM FT IS IG RN RS SS WL0

5

10

15

20

25

30

35

40

45

50

55

Mea

n nu

mbe

r of b

ird in

divi

dual

s per

visi

t

Microlandscape types

Figure 6 Mean number of bird individuals observed per plotvisit by microlandscape type (AM aerodrome AG agrofields BCbusiness centers CM cemeteries FT forests IS informal settle-ments IG institutional grounds RN residential neighborhoods RSriversides SS streamside WL wasteland)

332 Feeding Guild Categories by Microlandscapes Seed-eating bird species were the most common across allmicrolandscapes except for wastelands which were domi-nated by scavengers a feeding type that was also recorded inevery landscape Insectivorous species were also present in allmicrolandscape types unlike fishers that were only recordedin riverside landscapes Riverside landscapes were also whereflycatchers a feeding type that was present in all landscapetypes were most abundant

34 Species Diversity

341 Alpha Diversity in Macro- and Microlandscape TypesThe bird species diversity in both macro- and microland-scapes of Musanze are described using Whittaker curves(Figure 9) Using these curves built-up areas were slightlyhigher ranked in terms of bird diversity than open fields(Figure 9(a)) Amongmicrolandscapes institutional grounds

6 The Scientific World Journal

0 50 100 150 200 250 300Number of individuals

Spec

ies n

ame

Nectarinia kilimensis

Ploceus melanocephalus

Ploceus baglafecht

Estrilda astrild

Lagonosticta senegala

Lonchura cucullata

Milvus migrans

Serinus striolatus

Passer griseus

Corvus albus

Figure 7 Top ten most represented bird species in all sites of Musanze city

0 100 200 300 400 500 600 700Number of individuals

Aerial feeders

Butcherbirds

Fishers

Flycatchers

Frugivores

Insectivores

Nectar feeders

Raptors

Scavengers

Seedeaters

Shorerbirds

Feed

ing

guild

s

Open fields Built-up areas

Figure 8 Feeding guild categories of bird species as classified in microlandscapes types

had the highest diversity rank followed by residentialneighborhoods and informal settlements The aerodromeand Westland were ranked with the lowest bird diversity(Figure 9(b))

The Shannon diversity index was similar for bothmacrolandscape types built-up areas (1198671015840 = 1456) and itscounterpart open fields (1198671015840 = 1518) At the microland-scape level residential neighborhoods were the most diversefollowed by informal settlements and institutional groundsWastelands displayed the lowest bird diversity (Figure 10)

342 Species Similarity in Macro- and Microlandscape TypesOf the 94 bird species recorded in Musanze city 45 specieswere shared by both open fields and built-up landscapes Interms of species composition found in each microlandscape

type the riverside landscape was the most different fromthe remaining microlandscapes Residential neighborhoodsand informal settlements were most similar The differencesbetween the landscape types in terms of species compositionillustrated by the increasing distance from the root to thepoint where a given branch stems were as follows riversidelt aerodrome lt streamside lt wasteland lt agrofields lt ceme-teries lt forest lt institutional and business center lt informalsettlements and residences (Figure 11)

35 Bird Diversity in Musanze City and Nearby ProtectedAreas In addition to the internal comparison the level ofsimilarity between Musanze and its nearby protected areas(PNV and Buhanga eco-park) revealed important similaritiesbetween protected and urban habitats in terms of bird

The Scientific World Journal 7

0 5 10 15 20 25 30 35 4005

10

15

20

25

Rank

Open fieldsBuilt-up area

Log 1

0re

lativ

e abu

ndan

ce

(a)

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38

04

06

08

10

12

14

16

18

20

22

Rankminus2

AerodromeAgrofield Business centerCemeteriesForest

InstitutionalResidenceRiversideSettlementStreamside

WastelandLo

g 10

rela

tive a

bund

ance

(b)

Figure 9 Species rankabundance (a) in macrolandscape types and (b) in microlandscape types

Aerodrome

Agrofields

Business centers

Cemeteries

Forests

Institutional grounds

Residential neighborhoods

Riversides

Informal settlements

Streamsides

Wastelands

00 02 04 06 08 10 12 14Shannon index

Mic

rola

ndsc

ape t

ypes

Figure 10 Shannon index for microlandscape types of Musanze city

diversity (Figure 12) The total number of bird species inMusanze city was 94 105 in PNV and 81 in the Buhanga eco-park Of the 94 bird species recorded in Musanze 32 werealso present in Buhanga eco-park 51 in the PNV and 21 werefound in both the Buhanga eco-park and in PNV Moreoverwe found only one endemic bird species the RuwenzoriDouble-collared Sunbird (Cinnyris stuhlmanni) in Musanzeunlike the three endemic bird species present in Buhanga eco-park and the fifteen in the PNV This Albertine Rift endemic

species is also present in the PNV however it is absent fromthe Buhanga eco-park

In the comparison of the bird species found in the threesites Musanze city is unique in the number of migratory birdspecies observed Specifically seven migratory species wererecorded in Musanze city while only two are known to existin the PNV and none have been recorded in the Buhanga eco-park (Table 4) Musanzersquos microlandscapes that were visitedbymigratory birds include the riversides ofMukungwa River

8 The Scientific World Journal

RSWLSSISRNIGFTAFCMBCAM

1000 50

Similarity ()

Bray-Curtis cluster analysis (single link)

Figure 11 Species composition-based microlandscape clusters(AM aerodrome AG agrofields BC business centers CM ceme-teries FT forests IS informal settlements IG institutional groundsRN residential neighborhoods RS riversides SS streamside WLwasteland)

1000 50

Similarity ()

Bray-Curtis cluster analysis (single link)

PNV

Musanze

Buhanga

Figure 12 Musanze city PNV and Buhanga eco-park bird speciescomposition

informal settlements forests business centers and residentialneighborhoods

The majority of species in Musanze city were nativesuch that exotic bird species accounted for only 43 of thetotal number of bird species observed (Ficedula albicollisPloceus cucullatus Serinus canicollis and Serinus citrinel-loides) (Table 5) Up to 64 of the species observed hadno breeding opportunities within the study area (Actitishypoleucos Aquila pomarina Merops apiaster Muscicapastriata Phylloscopus trochilus and Sylvia borin)

4 Discussion

Our study of bird diversity in Musanze city has revealed thatcurrent wildlife conservation efforts do not coincide withareas of the highest bird abundance and species diversitywhich exist in urban areas Bird species richness in theurban areas of Musanze is greater than that of Buhangaeco-park and similar to that of the PNV two surroundingnatural habitats that are currently receiving the majority ofconservation efforts Furthermore species of high ecologicalimportance and therefore high conservation concern such

as endemic and migratory species were recorded across thecity landscapesThis study therefore indicates the importanceof protecting not only the natural habitats of native wildlifebut also urban areas where birds in particular are morecommonly existing

41 Species Richness The unique endemic species found inMusanze city the Ruwenzori Double-collared Sunbird haspreviously been observed in the VPN This species is knownto live in the high altitude habitats of the Albertine Rift[24] It is therefore not surprising that it was found in urbanlandscapes ofMusanze city which is located at a high altitudeof 1850m [26] Stevenson and Fanshawe [9] suggest thatthe sunbirdrsquos most preferred habitats are flowering bushes offorest edges and it may be unusual that the endemic specieswas observed foraging onMarkhamia lutea trees within openfields of Musanze city in this study Our study suggests thatthe species distribution of the Ruwenzori Double-collaredSunbird is not restricted to its natural habitat in the AlbertineRift as it can also exist in urban landscapesThis species maytherefore be able to adapt to human-dominated landscapesand it is likely that it may forage on vegetation such as urbangarden trees Our study suggests that the sunbird is capableof adapting its feeding preferences to the available plants incity landscapes potentially as a response to loss of its naturalhabitat caused by park reductions [27]

The seven migrant bird species found in the studysite were regular September-April visitors from Palearcticregions Two of them the Red-chested Cuckoo (Cucu-lus solitarius) and the European Bee-eater (Merops api-aster) had previously been sighted in the gallery forestsof the Rwandanrsquos Eastern Province [28] and in the PNV[24] The Common Sandpiper Spotted Flycatcher andWillow Warbler have also been reported to visit Rwanda(httpwwwrwandabirdingorg 02092012) and Musanzecity but have never been sighted in the Lava Plain or inthe Volcano Range of Rwanda The remaining two migrantsthe Garden Warbler (Sylvia borin) and the Lesser SpottedEagle (Aquila pomarina) have been reported in Rwandafor the first time as a result of this study Importantly theseven migrant species have never been reported to occurin urban environments of Rwanda and only two had beenreported to visit its highlands [24] However the AfricanPitta (Pitta angolensis) which is an intra-African breedingmigrant bird sighted in the Buhanga eco-park in 2006 and2008 [29] was not recorded in this study The findings of ourstudy encourage the development of bird watching activitiesin Musanze city which may be of particular interest tointernational tourists due to the high number of urban-livingand therefore easily observed unique bird species

411 Number of Species by Macrolandscape Types Thehypothesis that bird species inhabit open fields more thanbuilt-up areas was not supported in this study This maybe due to the fact that some built-up areas including insti-tutional grounds residential neighborhoods and informalsettlements are specifically designed with plant communi-ties to attract birds [30] These communities often include

The Scientific World Journal 9

Table 4 Migratory birds in Musanze city PNV and Buhanga eco-park

Common name Scientific name Musanze city Protected areasPNV Buhanga eco-park

Common Sandpiper Actitis hypoleucos

European Bee-eater Merops apiaster

Garden Warbler Sylvia borin

Lesser-spotted Eagle Aquila pomarina

Red-chested Cuckoo Cuculus solitarius

Spotted Flycatcher Muscicapa striata

WillowWarbler Phylloscopus trochilus

Table 5 Exotic birds in Musanze city PNV and Buhanga eco-park

Common name Scientific name Musanze city Protected areasPNV Buhanga eco-park

Collared Flycatcher Ficedula albicollis

Black-headed Weaver Ploceus cucullatus

Yellow-crowned Canary Serinus canicollis

Abyssinian Citril Serinus citrinelloides

a number of trees with a substantial canopy as well asornamental plants such as vegetation that exists as bushesAlternatively some microlandscapes within open fields havea low number of species such as the Musanze aerodromewhich is a grassland habitat and is regularly maintained tofacilitate airplane landing This habitat offers little feedingopportunities to wildlife and is an unsuitable habitat for mostbird species as it may for instance expose small-sized birdsto predators [31]

412 Number of Species by Microlandscape Types In supportof Koellner et al [32] different landscapes in Musanze werecorrelated with differences in bird species richness Theinstitutional grounds had a relatively high species richnessperhaps due to a high variety of plant assemblages Simi-larly the high number of bird species found in residentialneighborhoods and informal settlements can be explained bythe diversity of plant resources in these areas These plantresources include nectar-producing flowers such as bananaplants that attract sunbirds fruit-bearing trees and shrubssuch as guava plants that frugivorous species can feed on Inaddition the high concentrations of domestic wastes (such asresidues food disposable and waste-water) in the homesteadenvironment offer a unique opportunity to predators suchas insectivorous birds that feed on small mammals (egmice frogs) and insects (eg flies mosquitoes) and arecommon to this type of microhabitats Domestic waste mayalso attract scavenger species Finally informal settlementsthat are surrounded by a mosaic of vegetation types offermany opportunities for bird foraging and nesting [30] Thisdiversity in urban landscape vegetation structure and typemay therefore reflect the vast diversity of bird species in urbanareas which has not previously been investigated in Rwanda

42 Species Relative Abundance

421 Number of Individuals by Macrolandscape Types Thenonsignificant effect of macrolandscapes on the total numberof birds in an area may be linked to the fact that landscapetype had no significant influence on bird species richnessMore importantly due to the historical nonformal nature ofurban design in Musanze both macrolandscapes appeared tohave similar types and levels of bird-exploitable resourcesincluding appropriate plant coverage and sites for birds tonest [33]

422 Number of Individuals byMicrolandscape Types Ceme-teries riverside landscapes and wastelands did not differin the total number of birds in comparison to residentialneighborhoods (Table 3) This may be attributed to the factthat these four landscapes appear to be intrinsically hetero-geneous suggesting that there may be possible confoundingfactors that have overshadowed the expected relationshipbetween microlandscapes and relative bird abundance Forinstance wastelands attract many scavengers and raptorscemeteries and agrofields provide appropriate plant assem-blages for seed eaters and riversides offer easy water accessand shelter for aquatic bird species [4] Therefore theabundance of birds across the different microlandscapes ofMusanze is relatively uniform due to the fact that eachlandscape offers a range of suitable habitats for a range of birdspecies

423 Most Represented Species in Musanze City The PiedCrow (Corvus albus) was the most common species inMusanze and seemed to be the most adapted to human-dominated landscapes (Figure 7) For instance unlike many

10 The Scientific World Journal

other bird species in the area the Pied Crow was observedclose to many human facilities such food markets abattoirswastelands domestic yards and croplands In addition thePied Crow was found in high abundance where its foodsources including small reptiles small mammals grainpeanuts carrion scraps of human food fruits insects andother small invertebrates were most available [9] To a lesserextent the urban habitat appeared to favor the Grey-headedSparrow (Passer griseus) The occurrence of the Grey-headedSparrow was associated with open woodlands and humansettlements where this species can easily access required foodand habitat resources The third most represented specieswas the Streaky Seedeater (Serinus striolatus) which is acommon bird of highlands and is generally found above1300m in gardens and cultivated areas woodland edgesheath and scrub vegetation areas The Streaky Seedeateris therefore adept at living in human altered landscapeswhich is not unlike the Black Kite (Milvus migrans) whichwas also common to densely human-populated areas Thesehuman-used landscapes are also a popular habitat of theBlackKitersquos prey which includes small birds bats and rodents Inparticular our study revealed the common occurrence of theBlack Kite circling near the abattoir and scavenging in thecityrsquos wastelands

43 Feeding Guild Categories

431 Feeding Guild Categories by Macrolandscape TypesSeed-eating birds were the best represented guild inMusanze(Figure 8) This may be partially due to the fact that datacollection was completed during a maize-harvesting periodDuring this period urban fields have an exceptionally largeabundance of seeds that can be exploited by birds and mayhave therefore selectively attracted seed-eating species [34]It was also observed that seed-eating species fed from arange of fruits According to Holland and DeAngelis [35]this habit allows seed-eating species to contribute to plantreproduction through pollination Insectivorous species werealso prominent in Musanzersquos urban landscapes Similarly tothe findings of Austin and Smith [5] insectivores were mostabundant in insect-rich landscapes including streamsideareas forests and informal settlements

432 FeedingGuild Categories byMicrolandscapes Althoughseedeaters especially the Grey-headed Sparrow (Passergriseus) dominated almost all microlandscapes it is impor-tant to consider that in wastelands scavengers were the mostabundant (Figure 13) This finding is likely due to the factthat different microlandscapes aremore appropriate for somespecies more than others especially those with differentfeeding habits

Our study confirms that bird species found in Musanzecity like urban-living bird species in other cities contributeto biomass recycling [36] Interestingly although there wereonly a few species of scavenging birds in Musanze theirabundance was high enough to compensate for their lowspecies richness in order to make a notable biomass recyclingimpact to city dwellersThis was particularly true for the Pied

Figure 13 Abundance of Pied Crows in a landfill within Musanzecity (Photo Author 2012)

Crow (Corvus albus) a species whose abundance amountedto more than seven times the average number of individualsper species whichwas almost 10of the total number of birdsobserved

44 Species Diversity

441 Alpha Diversity The bird diversity found in built-up areas was comparable to the bird diversity in urbanopen fields in Musanze city (Figure 9(a)) This finding pro-vides support for the increasingly recognized idea that birddiversity in urban areas can be as high as that in naturalenvironments [37 38] Previous research suggests that thismay be due to a relatively high number of nonnative speciespresent in cities as well as the heterogeneous habitat thaturban landscapes provide [39] which was not supportedin this study perhaps because of close proximity of thestudy area to a network of natural environments (PNVGishwati forest and Buhanga eco-park Rugezi Mukungwaand Bihinga wetlands and Karago Bulera and Ruhondolakes) Moreover Luck [40] suggested that there is a positivecorrelation between human population density and birdspecies richness This relationship was demonstrated in ourstudy as species such as the Pied Crowwere found to bemostabundant throughout urban landscapes and therefore welladapted to an environment where high human densities existInterestingly even the Albertine Rift endemic species theRuwenzori Double-collared Sunbird was sighted foraging inhuman populated areas on garden plants

Overall residential neighborhoods institutionalgrounds and informal settlements can be considered asthe major bird hotspots in Musanze city (Figure 9(b)) Thesethree landscapes share a great floristic diversity providingmany important stimuli for bird life (such as fruits seedsnectar domestic residues insects small mammals reptilesand amphibians) [30] Finally contrary to rural areas andnatural forests that undergo seasonal shortages of resources[3] cities do not experience strong seasonal variation due toa continuous supply of recourses from remote areas

442 Species Similarity The macrolandscapes all appearedto have similar bird species composition which may bedue to landscape heterogeneity [39] This heterogeneity islikely a result of the lack of historical professional landscapeplanning and design leaving a mosaic landscape structure inboth built-up and open fields instead of a uniform landscapespecialization Our results suggest that residential areas and

The Scientific World Journal 11

informal settlements were the most similar in terms ofspecies composition These landscapes ultimately functionto host family life The only difference between residentialareas and informal settlements resides in their socioeconomicstatus which is reflected in the landscape structure Howeverboth landscapes are more similar to each other than toother landscapes Furthermore the species composition ofcemeteries was similar to both forests and some of the built-up microlandscapes which may be attributed to the fact thatthese areas are all surrounded by trees Additionally ceme-teries are characterized by low human disturbance whichmay compare to that of forests and some urban landscapesThese landscapes all harbor a wide variety of floweringplants which in the case of cemeteries are mainly plantedby bereaved ones Moreover the vegetation of graveyardsincludes a range of regeneration stages resulting in a widerange of habitats from the vegetation-free areas of newly duggraves to the reconstructed thickets around old graves [41]Finally riverside landscapes emerged as the most specializedlandscape type as expected with many distinctive speciesobserved in this landscape only Almost all the species foundin riverside areas were specialists of wetlands and were notfound elsewhere As a result it was the most dissimilar to allother microlandscapes

The high degree of similarity in terms of bird diversitybetween Musanze city and the protected natural habitatsnearby provide further support that wildlife does not exclu-sively inhabit protected areas [33 37 42] Although the twonatural habitats are at eight km from Musanze city morethan half of the species found in the city were also found inVPN The lower degree of similarity between Musanze andBuhanga eco-park may be linked to the relative geographiclocation of the two sites as Musanze city is almost half waybetween the two protected areas This finding may also beattributed to the fact that the diversity ofmicrohabitats withinBuhanga eco-park is lower than that of Musanze and VPN[13] which may be due to the relatively small size of Buhangaeco-park Interestingly the species found in more than onelandscape type were also recorded both inside and beyondthe city limits Conversely Ficedula albicollis was recorded inonly one landscape type (cemeteries) and was absent in bothPNV and Buhanga eco-park

5 Conclusions

This study contributes to the knowledge of bird diversity inurban landscapes and provides the most recent status of birddiversity in Musanze city Our findings confirm that birddiversity in urban areas such as a densely populated city canbe as great as that in surrounding natural forests Specificallythe total number of bird species in Musanze city was verysimilar to that of the nearest protected forests VolcanoesNational Park and Buhanga eco-park Endemic and migra-tory birdswere also found inMusanze cityOneAlbertine Riftendemic bird species the Ruwenzori Double-collared Sun-bird was observed in Musanze during this study which hasnot been previously recorded Similarly threemigratory birdswere found inMusanze region for the first time the Common

Sandpiper the Spotted Flycatcher and theWillowWarbler Inaddition two bird species were observed that have not beenpreviously reported in Rwanda the Garden Warbler (Sylviaborin) and the Lesser Spotted Eagle (Aquila pomarina) Theeffect of landscape types on bird species richness and relativeabundance was also illustrated Residential neighborhoodsinstitutional grounds and informal settlements had thehighest species diversity indices and rankabundance relativeto the rest of the microlandscapes in this study Riversidelandscapes emerged with the most specialized bird faunaincluding species that are restricted to wetland environmentsand water bodies This study confirmed that scavengers inMusanze city contribute more to biomass recycling than anyother bird feeding groups Our study provides a current anduseful reference for urban decision makers and confirms theexistence of a great diversity of wildlife within cities Wesuggest that the development and implementation of cityland-use plans should consider this biodiversity especiallywhen villages and cities are in close proximity of protectedareas or natural reserves Finally it may be important thatbotanical gardens and public parks are included in themasterplan of the city as our study indicates that their designrequires an understanding of biodiversity in particular ofavian populations

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors acknowledge technical support from staffat DFGFI-Karisoke Research Center namely Dr WinnieEckardt Mr Deogratias Tuyisingize Mr Emmanuel Faidaand Mrs Keiko Mori

References

[1] S R Loss M O Ruiz and J D Brawn ldquoRelationships betweenavian diversity neighborhood age income and environmentalcharacteristics of an urban landscaperdquo Biological Conservationvol 142 no 11 pp 2578ndash2585 2009

[2] K L Evans D E Chamberlain B J Hatchwell R D Gregoryand K J Gaston ldquoWhat makes an urban birdrdquo Global ChangeBiology vol 17 no 1 pp 32ndash44 2011

[3] S Bolwig D Pomeroy H Tushabe and D Mushabe ldquoCropstrees and birds biodiversity change under agricultural inten-sification in Ugandas farmed landscapesrdquo Danish Journal ofGeography vol 106 no 2 pp 115ndash130 2006

[4] J Hitchmough and N Dunnett ldquoIntroduction to naturalisticplanting in urban landscapesrdquo in The Dynamic LandscapeJ Hitchmough and N Dunnatt Eds pp 1ndash32 Spon PressLondon UK 2004

[5] G T Austin and E L Smith ldquoWinter foraging ecology of mixedinsectivorous bird flocks in oakwoodland in southernArizonardquoThe Condor vol 74 pp 17ndash24 1972

[6] B R Coppedge D M Engle R E Masters and M S GregoryldquoAvian response to landscape change in fragmented southern

12 The Scientific World Journal

great plains grasslandsrdquo Ecological Applications vol 11 no 1 pp47ndash59 2001

[7] K L Evans S E Newson and K J Gaston ldquoHabitat influenceson urban avian assemblagesrdquo Ibis vol 151 no 1 pp 19ndash39 2009

[8] MW Strohbach D Haase and N Kabisch ldquoBirds and the cityUrban biodiversity land use and socioeconomicsrdquo Ecology andSociety vol 14 no 2 pp 31ndash45 2009

[9] T Stevenson and J Fanshawe Field Guide to the Birds of EastAfrica Kenya Tanzania Uganda Rwanda Burundi T amp A DPoyser London UK 2002

[10] J Mistry A Berardi and M Simpson ldquoBirds as indicators ofwetland status and change in the North Rupununi GuyanardquoBiodiversity and Conservation vol 17 no 10 pp 2383ndash24092008

[11] H Slabbekoorn and E A P Ripmeester ldquoBirdsong and anthro-pogenic noise implications and applications for conservationrdquoMolecular Ecology vol 17 no 1 pp 72ndash83 2008

[12] W S Judd C S Campbell E A Kellogg P F Stevens andM JDonoghue Plant Systematics A Phylogenetic Approach SinauerAssociates Sunderland Mass USA 3rd edition 2008

[13] W Weber ldquoRuhengeri and its resources an environmentalprofile of the Ruhengeri prefecturerdquo ETMAUSAID KigaliRwanda

[14] E Sabuhoro and G Bush ldquoThe Dian Fossey Gorilla FundInternationalPADGEF Assessing the Benefit Stream fromIllegal Activities in the Parc National des Volcansrdquo TargetingCommunity Conservation Interventions Musanze Rwanda2008

[15] J C Sano Urban Environmental Infrastructure in Kigali CityRwanda Challenges and Opportunities for Modernized Decen-tralized Sanitation Systems in Poor Neighborhoods WageningenUniversity Wageningen The Netherlands 2007

[16] R J Staniforth ldquoEffects of urbanization on bird populations inthe Canadian Central Arcticrdquo Arctic vol 55 no 1 pp 87ndash932002

[17] DWGibbons andRD Gregory ldquoBirdsrdquo in Ecological CensusesTechniques W L Sutherland Ed pp 308ndash350 CambridgeUniversity 2nd edition 2006

[18] D H Johnson ldquoPoint counts of birds what are we estimatingrdquoTech Rep PSW-GTR-149 USDA Forest Service 1995

[19] A Haslem and A F Bennett ldquoBirds in agricultural mosaics theinfluence of landscape pattern and countryside heterogeneityrdquoEcological Applications vol 18 no 1 pp 185ndash196 2008

[20] M L Rurangwa Feeding Ecology of Albertine Rift Endemic Birdsin the Volcanoes National Park Regal Sunbird Rwenzori Double-Collared Sunbird and Rwenzori Turako National University ofRwanda 2011

[21] R B Arellano-Valle H Bolfarine and V H Lachos ldquoSkew-normal linear mixedmodelsrdquo Journal of Data Science vol 3 pp415ndash438 2005

[22] D Bates Fitting LinearMixedModels in RTheNewsletter of theR Project Volume 51 University of Wisconsin Madison WisUSA 2005

[23] A E Magurran Measuring Biological Diversity Blackwell Sci-ence Malden Mass USA 2004

[24] D Tuyisingize and K Fawcett ldquoThe common bird distributionin the Parc National des Volcans and its surrounding patternsconservation and future challengesrdquo DFGF Technical Report2011

[25] A T Peterson and N A Slade ldquoExtrapolating inventory resultsinto biodiversity estimates and the importance of stoppingrulesrdquoDiversity and Distributions vol 4 no 3 pp 95ndash105 1998

[26] M Salek J Svobodova and P Zasadil ldquoEdge effect of low-trafficforest roads on bird communities in secondary productionforests in central Europerdquo Landscape Ecology vol 25 no 7 pp1113ndash1124 2010

[27] S Murererehe ldquoCollecte et analyse de donnees pourlrsquoamenagement durable des forets -Joindre les efforts nationauxet internationaux Etat des ressources forestieres au RwandardquoTech Rep FAO Rome Italy 2000

[28] S J Nsengimana M Ndimukaga L Gakwerere et al ldquoBiodi-versity surveyrdquo Tech Rep Rufford Small Grant FoundationLondon UK 2009

[29] C Nsabagasani ldquoA Migratory Species African Pitta ldquoPittaangolensisrdquo passed Buhanga relict forestrdquo Backbone vol 17 pp6ndash8 2008

[30] J Jokimaki and M Kaisanlahti-Jokimaki ldquoThe role of residen-tial habitat type on the temporal variation of wintering birdassemblages in northern Finlandrdquo Ornis Fennica vol 88 2011

[31] T M Bergin L B Best K E Freemark and K J KoehlerldquoEffects of landscape structure on nest predation in roadsides ofa midwestern agroecosystem a multiscale analysisrdquo LandscapeEcology vol 15 no 2 pp 131ndash143 2000

[32] T Koellner AMHersperger andTWohlgemuth ldquoRarefactionmethod for assessing plant species diversity on a regional scalerdquoEcography vol 27 no 4 pp 532ndash544 2004

[33] S H Faeth P S Warren E Shochat and W A MarussichldquoTrophic dynamics in urban communitiesrdquo BioScience vol 55no 5 pp 399ndash407 2005

[34] R J Fuller and J D Wilson ldquoThe ecology of seed-eating birdsin relation to agricultural practices current research and futuredirectionsrdquo British Trust for Ornithology Research Report no149 1995

[35] J N Holland andD L DeAngelis ldquoEcological and evolutionaryconditions for fruit abortion to regulate pollinating seed-eaters and increase plant reproductionrdquo Theoretical PopulationBiology vol 61 no 3 pp 251ndash263 2002

[36] C J Whelan D G Wenny and R J Marquis ldquoEcosystemservices provided by birdsrdquo Annals of the New York Academyof Sciences vol 1134 pp 25ndash60 2008

[37] O Gilbert The Ecology of Urban Habitats Chapman amp HallLondon UK 1989

[38] A Millard ldquoSemi-natural vegetation and its relationship todesignated urban green space at the landscape scale in LeedsUKrdquo Landscape Ecology vol 23 no 10 pp 1231ndash1241 2008

[39] I Kowarik ldquoOn the role of alien species in urban flora andvegetationrdquo in Plant Invasions General Aspects and SpecialProblems P Pysek K Prach M Rejmanek and M WadeEds pp 85ndash103 SPB Academic Publishing Amsterdam TheNetherlands 1995

[40] G W Luck ldquoA review of the relationships between humanpopulation density and biodiversityrdquo Biological Reviews vol 82no 4 pp 607ndash645 2007

[41] Victorian Government Department of Sustainability and Envi-ronment (VGDSE) Managing Native Vegetation in VictorianCemeteries Victorian Government Department of Sustainabil-ity and Environment Melbourne Australia 2009

[42] C Dowd ldquoEffect of development on bird species compositionof two urban forested wetlands in Staten Island New YorkrdquoJournal of Field Ornithology vol 63 no 4 pp 455ndash461 1992

Page 5: Bird Diversity and Distribution in relation to Urban Landscape Types in Northern Rwanda · 2016. 1. 26. · ResearchArticle Bird Diversity and Distribution in relation to Urban Landscape

The Scientific World Journal 5

AM AG BC CM FT IS IG RN RS SS WL0

2

4

6

8

10

12

14

16

Microlandscape types

Mea

n nu

mbe

r of b

ird sp

ecie

s per

visi

t

Figure 4 Mean number of bird species observed during plot visitsin each microlandscape type (AM aerodrome AG agrofields BCbusiness centers CM cemeteries FT forests IS informal settle-ments IG institutional grounds RN residential neighborhoods RSriversides SS streamside WL wasteland)

0

5

10

15

20

25

30

35

40

Mea

n nu

mbe

r of b

ird in

divi

dual

s per

visi

t

Built-up areas Open fieldsMacrolandscape types

Figure 5Mean number of bird individuals encountered per visit bymacrolandscape type

323 Most Represented Species The Pied Crow (Corvusalbus) the Grey-headed Sparrow (Passer griseus) StreakySeedeater (Serinus striolatus) and the Black Kite (Milvusmigrans) were found to be the most abundant species in thisstudy (Figure 7)

33 Feeding Guild Categories

331 Feeding Guild Categories by Macrolandscape TypesAmong the eleven feeding guilds represented by bird speciesin Musanze city seedeaters were the most common in bothbuilt-up areas and open fields followed by insectivorousspecies and scavengers (Figure 8)

Table 3 LMM output showing parameter estimates of microland-scape types on the number of bird individuals

Landscape types Std error 119905 value 119875 valueIntercept 012 27250 lt0001Aerodrome 0224 minus4970 lt0001Agrofield 0169 minus2330 lt005Business centers 0169 minus6646 lt0001Cemeteries 0224 minus1919 0055Forests 0169 minus3615 lt0001Institutional ground 0169 minus2229 lt005Riversides 0224 minus016 0873Informal settlements 0169 minus2899 lt001Streamside 0224 minus2029 lt005Wastelands 0224 0173 0860

AM AG BC CM FT IS IG RN RS SS WL0

5

10

15

20

25

30

35

40

45

50

55

Mea

n nu

mbe

r of b

ird in

divi

dual

s per

visi

t

Microlandscape types

Figure 6 Mean number of bird individuals observed per plotvisit by microlandscape type (AM aerodrome AG agrofields BCbusiness centers CM cemeteries FT forests IS informal settle-ments IG institutional grounds RN residential neighborhoods RSriversides SS streamside WL wasteland)

332 Feeding Guild Categories by Microlandscapes Seed-eating bird species were the most common across allmicrolandscapes except for wastelands which were domi-nated by scavengers a feeding type that was also recorded inevery landscape Insectivorous species were also present in allmicrolandscape types unlike fishers that were only recordedin riverside landscapes Riverside landscapes were also whereflycatchers a feeding type that was present in all landscapetypes were most abundant

34 Species Diversity

341 Alpha Diversity in Macro- and Microlandscape TypesThe bird species diversity in both macro- and microland-scapes of Musanze are described using Whittaker curves(Figure 9) Using these curves built-up areas were slightlyhigher ranked in terms of bird diversity than open fields(Figure 9(a)) Amongmicrolandscapes institutional grounds

6 The Scientific World Journal

0 50 100 150 200 250 300Number of individuals

Spec

ies n

ame

Nectarinia kilimensis

Ploceus melanocephalus

Ploceus baglafecht

Estrilda astrild

Lagonosticta senegala

Lonchura cucullata

Milvus migrans

Serinus striolatus

Passer griseus

Corvus albus

Figure 7 Top ten most represented bird species in all sites of Musanze city

0 100 200 300 400 500 600 700Number of individuals

Aerial feeders

Butcherbirds

Fishers

Flycatchers

Frugivores

Insectivores

Nectar feeders

Raptors

Scavengers

Seedeaters

Shorerbirds

Feed

ing

guild

s

Open fields Built-up areas

Figure 8 Feeding guild categories of bird species as classified in microlandscapes types

had the highest diversity rank followed by residentialneighborhoods and informal settlements The aerodromeand Westland were ranked with the lowest bird diversity(Figure 9(b))

The Shannon diversity index was similar for bothmacrolandscape types built-up areas (1198671015840 = 1456) and itscounterpart open fields (1198671015840 = 1518) At the microland-scape level residential neighborhoods were the most diversefollowed by informal settlements and institutional groundsWastelands displayed the lowest bird diversity (Figure 10)

342 Species Similarity in Macro- and Microlandscape TypesOf the 94 bird species recorded in Musanze city 45 specieswere shared by both open fields and built-up landscapes Interms of species composition found in each microlandscape

type the riverside landscape was the most different fromthe remaining microlandscapes Residential neighborhoodsand informal settlements were most similar The differencesbetween the landscape types in terms of species compositionillustrated by the increasing distance from the root to thepoint where a given branch stems were as follows riversidelt aerodrome lt streamside lt wasteland lt agrofields lt ceme-teries lt forest lt institutional and business center lt informalsettlements and residences (Figure 11)

35 Bird Diversity in Musanze City and Nearby ProtectedAreas In addition to the internal comparison the level ofsimilarity between Musanze and its nearby protected areas(PNV and Buhanga eco-park) revealed important similaritiesbetween protected and urban habitats in terms of bird

The Scientific World Journal 7

0 5 10 15 20 25 30 35 4005

10

15

20

25

Rank

Open fieldsBuilt-up area

Log 1

0re

lativ

e abu

ndan

ce

(a)

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38

04

06

08

10

12

14

16

18

20

22

Rankminus2

AerodromeAgrofield Business centerCemeteriesForest

InstitutionalResidenceRiversideSettlementStreamside

WastelandLo

g 10

rela

tive a

bund

ance

(b)

Figure 9 Species rankabundance (a) in macrolandscape types and (b) in microlandscape types

Aerodrome

Agrofields

Business centers

Cemeteries

Forests

Institutional grounds

Residential neighborhoods

Riversides

Informal settlements

Streamsides

Wastelands

00 02 04 06 08 10 12 14Shannon index

Mic

rola

ndsc

ape t

ypes

Figure 10 Shannon index for microlandscape types of Musanze city

diversity (Figure 12) The total number of bird species inMusanze city was 94 105 in PNV and 81 in the Buhanga eco-park Of the 94 bird species recorded in Musanze 32 werealso present in Buhanga eco-park 51 in the PNV and 21 werefound in both the Buhanga eco-park and in PNV Moreoverwe found only one endemic bird species the RuwenzoriDouble-collared Sunbird (Cinnyris stuhlmanni) in Musanzeunlike the three endemic bird species present in Buhanga eco-park and the fifteen in the PNV This Albertine Rift endemic

species is also present in the PNV however it is absent fromthe Buhanga eco-park

In the comparison of the bird species found in the threesites Musanze city is unique in the number of migratory birdspecies observed Specifically seven migratory species wererecorded in Musanze city while only two are known to existin the PNV and none have been recorded in the Buhanga eco-park (Table 4) Musanzersquos microlandscapes that were visitedbymigratory birds include the riversides ofMukungwa River

8 The Scientific World Journal

RSWLSSISRNIGFTAFCMBCAM

1000 50

Similarity ()

Bray-Curtis cluster analysis (single link)

Figure 11 Species composition-based microlandscape clusters(AM aerodrome AG agrofields BC business centers CM ceme-teries FT forests IS informal settlements IG institutional groundsRN residential neighborhoods RS riversides SS streamside WLwasteland)

1000 50

Similarity ()

Bray-Curtis cluster analysis (single link)

PNV

Musanze

Buhanga

Figure 12 Musanze city PNV and Buhanga eco-park bird speciescomposition

informal settlements forests business centers and residentialneighborhoods

The majority of species in Musanze city were nativesuch that exotic bird species accounted for only 43 of thetotal number of bird species observed (Ficedula albicollisPloceus cucullatus Serinus canicollis and Serinus citrinel-loides) (Table 5) Up to 64 of the species observed hadno breeding opportunities within the study area (Actitishypoleucos Aquila pomarina Merops apiaster Muscicapastriata Phylloscopus trochilus and Sylvia borin)

4 Discussion

Our study of bird diversity in Musanze city has revealed thatcurrent wildlife conservation efforts do not coincide withareas of the highest bird abundance and species diversitywhich exist in urban areas Bird species richness in theurban areas of Musanze is greater than that of Buhangaeco-park and similar to that of the PNV two surroundingnatural habitats that are currently receiving the majority ofconservation efforts Furthermore species of high ecologicalimportance and therefore high conservation concern such

as endemic and migratory species were recorded across thecity landscapesThis study therefore indicates the importanceof protecting not only the natural habitats of native wildlifebut also urban areas where birds in particular are morecommonly existing

41 Species Richness The unique endemic species found inMusanze city the Ruwenzori Double-collared Sunbird haspreviously been observed in the VPN This species is knownto live in the high altitude habitats of the Albertine Rift[24] It is therefore not surprising that it was found in urbanlandscapes ofMusanze city which is located at a high altitudeof 1850m [26] Stevenson and Fanshawe [9] suggest thatthe sunbirdrsquos most preferred habitats are flowering bushes offorest edges and it may be unusual that the endemic specieswas observed foraging onMarkhamia lutea trees within openfields of Musanze city in this study Our study suggests thatthe species distribution of the Ruwenzori Double-collaredSunbird is not restricted to its natural habitat in the AlbertineRift as it can also exist in urban landscapesThis species maytherefore be able to adapt to human-dominated landscapesand it is likely that it may forage on vegetation such as urbangarden trees Our study suggests that the sunbird is capableof adapting its feeding preferences to the available plants incity landscapes potentially as a response to loss of its naturalhabitat caused by park reductions [27]

The seven migrant bird species found in the studysite were regular September-April visitors from Palearcticregions Two of them the Red-chested Cuckoo (Cucu-lus solitarius) and the European Bee-eater (Merops api-aster) had previously been sighted in the gallery forestsof the Rwandanrsquos Eastern Province [28] and in the PNV[24] The Common Sandpiper Spotted Flycatcher andWillow Warbler have also been reported to visit Rwanda(httpwwwrwandabirdingorg 02092012) and Musanzecity but have never been sighted in the Lava Plain or inthe Volcano Range of Rwanda The remaining two migrantsthe Garden Warbler (Sylvia borin) and the Lesser SpottedEagle (Aquila pomarina) have been reported in Rwandafor the first time as a result of this study Importantly theseven migrant species have never been reported to occurin urban environments of Rwanda and only two had beenreported to visit its highlands [24] However the AfricanPitta (Pitta angolensis) which is an intra-African breedingmigrant bird sighted in the Buhanga eco-park in 2006 and2008 [29] was not recorded in this study The findings of ourstudy encourage the development of bird watching activitiesin Musanze city which may be of particular interest tointernational tourists due to the high number of urban-livingand therefore easily observed unique bird species

411 Number of Species by Macrolandscape Types Thehypothesis that bird species inhabit open fields more thanbuilt-up areas was not supported in this study This maybe due to the fact that some built-up areas including insti-tutional grounds residential neighborhoods and informalsettlements are specifically designed with plant communi-ties to attract birds [30] These communities often include

The Scientific World Journal 9

Table 4 Migratory birds in Musanze city PNV and Buhanga eco-park

Common name Scientific name Musanze city Protected areasPNV Buhanga eco-park

Common Sandpiper Actitis hypoleucos

European Bee-eater Merops apiaster

Garden Warbler Sylvia borin

Lesser-spotted Eagle Aquila pomarina

Red-chested Cuckoo Cuculus solitarius

Spotted Flycatcher Muscicapa striata

WillowWarbler Phylloscopus trochilus

Table 5 Exotic birds in Musanze city PNV and Buhanga eco-park

Common name Scientific name Musanze city Protected areasPNV Buhanga eco-park

Collared Flycatcher Ficedula albicollis

Black-headed Weaver Ploceus cucullatus

Yellow-crowned Canary Serinus canicollis

Abyssinian Citril Serinus citrinelloides

a number of trees with a substantial canopy as well asornamental plants such as vegetation that exists as bushesAlternatively some microlandscapes within open fields havea low number of species such as the Musanze aerodromewhich is a grassland habitat and is regularly maintained tofacilitate airplane landing This habitat offers little feedingopportunities to wildlife and is an unsuitable habitat for mostbird species as it may for instance expose small-sized birdsto predators [31]

412 Number of Species by Microlandscape Types In supportof Koellner et al [32] different landscapes in Musanze werecorrelated with differences in bird species richness Theinstitutional grounds had a relatively high species richnessperhaps due to a high variety of plant assemblages Simi-larly the high number of bird species found in residentialneighborhoods and informal settlements can be explained bythe diversity of plant resources in these areas These plantresources include nectar-producing flowers such as bananaplants that attract sunbirds fruit-bearing trees and shrubssuch as guava plants that frugivorous species can feed on Inaddition the high concentrations of domestic wastes (such asresidues food disposable and waste-water) in the homesteadenvironment offer a unique opportunity to predators suchas insectivorous birds that feed on small mammals (egmice frogs) and insects (eg flies mosquitoes) and arecommon to this type of microhabitats Domestic waste mayalso attract scavenger species Finally informal settlementsthat are surrounded by a mosaic of vegetation types offermany opportunities for bird foraging and nesting [30] Thisdiversity in urban landscape vegetation structure and typemay therefore reflect the vast diversity of bird species in urbanareas which has not previously been investigated in Rwanda

42 Species Relative Abundance

421 Number of Individuals by Macrolandscape Types Thenonsignificant effect of macrolandscapes on the total numberof birds in an area may be linked to the fact that landscapetype had no significant influence on bird species richnessMore importantly due to the historical nonformal nature ofurban design in Musanze both macrolandscapes appeared tohave similar types and levels of bird-exploitable resourcesincluding appropriate plant coverage and sites for birds tonest [33]

422 Number of Individuals byMicrolandscape Types Ceme-teries riverside landscapes and wastelands did not differin the total number of birds in comparison to residentialneighborhoods (Table 3) This may be attributed to the factthat these four landscapes appear to be intrinsically hetero-geneous suggesting that there may be possible confoundingfactors that have overshadowed the expected relationshipbetween microlandscapes and relative bird abundance Forinstance wastelands attract many scavengers and raptorscemeteries and agrofields provide appropriate plant assem-blages for seed eaters and riversides offer easy water accessand shelter for aquatic bird species [4] Therefore theabundance of birds across the different microlandscapes ofMusanze is relatively uniform due to the fact that eachlandscape offers a range of suitable habitats for a range of birdspecies

423 Most Represented Species in Musanze City The PiedCrow (Corvus albus) was the most common species inMusanze and seemed to be the most adapted to human-dominated landscapes (Figure 7) For instance unlike many

10 The Scientific World Journal

other bird species in the area the Pied Crow was observedclose to many human facilities such food markets abattoirswastelands domestic yards and croplands In addition thePied Crow was found in high abundance where its foodsources including small reptiles small mammals grainpeanuts carrion scraps of human food fruits insects andother small invertebrates were most available [9] To a lesserextent the urban habitat appeared to favor the Grey-headedSparrow (Passer griseus) The occurrence of the Grey-headedSparrow was associated with open woodlands and humansettlements where this species can easily access required foodand habitat resources The third most represented specieswas the Streaky Seedeater (Serinus striolatus) which is acommon bird of highlands and is generally found above1300m in gardens and cultivated areas woodland edgesheath and scrub vegetation areas The Streaky Seedeateris therefore adept at living in human altered landscapeswhich is not unlike the Black Kite (Milvus migrans) whichwas also common to densely human-populated areas Thesehuman-used landscapes are also a popular habitat of theBlackKitersquos prey which includes small birds bats and rodents Inparticular our study revealed the common occurrence of theBlack Kite circling near the abattoir and scavenging in thecityrsquos wastelands

43 Feeding Guild Categories

431 Feeding Guild Categories by Macrolandscape TypesSeed-eating birds were the best represented guild inMusanze(Figure 8) This may be partially due to the fact that datacollection was completed during a maize-harvesting periodDuring this period urban fields have an exceptionally largeabundance of seeds that can be exploited by birds and mayhave therefore selectively attracted seed-eating species [34]It was also observed that seed-eating species fed from arange of fruits According to Holland and DeAngelis [35]this habit allows seed-eating species to contribute to plantreproduction through pollination Insectivorous species werealso prominent in Musanzersquos urban landscapes Similarly tothe findings of Austin and Smith [5] insectivores were mostabundant in insect-rich landscapes including streamsideareas forests and informal settlements

432 FeedingGuild Categories byMicrolandscapes Althoughseedeaters especially the Grey-headed Sparrow (Passergriseus) dominated almost all microlandscapes it is impor-tant to consider that in wastelands scavengers were the mostabundant (Figure 13) This finding is likely due to the factthat different microlandscapes aremore appropriate for somespecies more than others especially those with differentfeeding habits

Our study confirms that bird species found in Musanzecity like urban-living bird species in other cities contributeto biomass recycling [36] Interestingly although there wereonly a few species of scavenging birds in Musanze theirabundance was high enough to compensate for their lowspecies richness in order to make a notable biomass recyclingimpact to city dwellersThis was particularly true for the Pied

Figure 13 Abundance of Pied Crows in a landfill within Musanzecity (Photo Author 2012)

Crow (Corvus albus) a species whose abundance amountedto more than seven times the average number of individualsper species whichwas almost 10of the total number of birdsobserved

44 Species Diversity

441 Alpha Diversity The bird diversity found in built-up areas was comparable to the bird diversity in urbanopen fields in Musanze city (Figure 9(a)) This finding pro-vides support for the increasingly recognized idea that birddiversity in urban areas can be as high as that in naturalenvironments [37 38] Previous research suggests that thismay be due to a relatively high number of nonnative speciespresent in cities as well as the heterogeneous habitat thaturban landscapes provide [39] which was not supportedin this study perhaps because of close proximity of thestudy area to a network of natural environments (PNVGishwati forest and Buhanga eco-park Rugezi Mukungwaand Bihinga wetlands and Karago Bulera and Ruhondolakes) Moreover Luck [40] suggested that there is a positivecorrelation between human population density and birdspecies richness This relationship was demonstrated in ourstudy as species such as the Pied Crowwere found to bemostabundant throughout urban landscapes and therefore welladapted to an environment where high human densities existInterestingly even the Albertine Rift endemic species theRuwenzori Double-collared Sunbird was sighted foraging inhuman populated areas on garden plants

Overall residential neighborhoods institutionalgrounds and informal settlements can be considered asthe major bird hotspots in Musanze city (Figure 9(b)) Thesethree landscapes share a great floristic diversity providingmany important stimuli for bird life (such as fruits seedsnectar domestic residues insects small mammals reptilesand amphibians) [30] Finally contrary to rural areas andnatural forests that undergo seasonal shortages of resources[3] cities do not experience strong seasonal variation due toa continuous supply of recourses from remote areas

442 Species Similarity The macrolandscapes all appearedto have similar bird species composition which may bedue to landscape heterogeneity [39] This heterogeneity islikely a result of the lack of historical professional landscapeplanning and design leaving a mosaic landscape structure inboth built-up and open fields instead of a uniform landscapespecialization Our results suggest that residential areas and

The Scientific World Journal 11

informal settlements were the most similar in terms ofspecies composition These landscapes ultimately functionto host family life The only difference between residentialareas and informal settlements resides in their socioeconomicstatus which is reflected in the landscape structure Howeverboth landscapes are more similar to each other than toother landscapes Furthermore the species composition ofcemeteries was similar to both forests and some of the built-up microlandscapes which may be attributed to the fact thatthese areas are all surrounded by trees Additionally ceme-teries are characterized by low human disturbance whichmay compare to that of forests and some urban landscapesThese landscapes all harbor a wide variety of floweringplants which in the case of cemeteries are mainly plantedby bereaved ones Moreover the vegetation of graveyardsincludes a range of regeneration stages resulting in a widerange of habitats from the vegetation-free areas of newly duggraves to the reconstructed thickets around old graves [41]Finally riverside landscapes emerged as the most specializedlandscape type as expected with many distinctive speciesobserved in this landscape only Almost all the species foundin riverside areas were specialists of wetlands and were notfound elsewhere As a result it was the most dissimilar to allother microlandscapes

The high degree of similarity in terms of bird diversitybetween Musanze city and the protected natural habitatsnearby provide further support that wildlife does not exclu-sively inhabit protected areas [33 37 42] Although the twonatural habitats are at eight km from Musanze city morethan half of the species found in the city were also found inVPN The lower degree of similarity between Musanze andBuhanga eco-park may be linked to the relative geographiclocation of the two sites as Musanze city is almost half waybetween the two protected areas This finding may also beattributed to the fact that the diversity ofmicrohabitats withinBuhanga eco-park is lower than that of Musanze and VPN[13] which may be due to the relatively small size of Buhangaeco-park Interestingly the species found in more than onelandscape type were also recorded both inside and beyondthe city limits Conversely Ficedula albicollis was recorded inonly one landscape type (cemeteries) and was absent in bothPNV and Buhanga eco-park

5 Conclusions

This study contributes to the knowledge of bird diversity inurban landscapes and provides the most recent status of birddiversity in Musanze city Our findings confirm that birddiversity in urban areas such as a densely populated city canbe as great as that in surrounding natural forests Specificallythe total number of bird species in Musanze city was verysimilar to that of the nearest protected forests VolcanoesNational Park and Buhanga eco-park Endemic and migra-tory birdswere also found inMusanze cityOneAlbertine Riftendemic bird species the Ruwenzori Double-collared Sun-bird was observed in Musanze during this study which hasnot been previously recorded Similarly threemigratory birdswere found inMusanze region for the first time the Common

Sandpiper the Spotted Flycatcher and theWillowWarbler Inaddition two bird species were observed that have not beenpreviously reported in Rwanda the Garden Warbler (Sylviaborin) and the Lesser Spotted Eagle (Aquila pomarina) Theeffect of landscape types on bird species richness and relativeabundance was also illustrated Residential neighborhoodsinstitutional grounds and informal settlements had thehighest species diversity indices and rankabundance relativeto the rest of the microlandscapes in this study Riversidelandscapes emerged with the most specialized bird faunaincluding species that are restricted to wetland environmentsand water bodies This study confirmed that scavengers inMusanze city contribute more to biomass recycling than anyother bird feeding groups Our study provides a current anduseful reference for urban decision makers and confirms theexistence of a great diversity of wildlife within cities Wesuggest that the development and implementation of cityland-use plans should consider this biodiversity especiallywhen villages and cities are in close proximity of protectedareas or natural reserves Finally it may be important thatbotanical gardens and public parks are included in themasterplan of the city as our study indicates that their designrequires an understanding of biodiversity in particular ofavian populations

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors acknowledge technical support from staffat DFGFI-Karisoke Research Center namely Dr WinnieEckardt Mr Deogratias Tuyisingize Mr Emmanuel Faidaand Mrs Keiko Mori

References

[1] S R Loss M O Ruiz and J D Brawn ldquoRelationships betweenavian diversity neighborhood age income and environmentalcharacteristics of an urban landscaperdquo Biological Conservationvol 142 no 11 pp 2578ndash2585 2009

[2] K L Evans D E Chamberlain B J Hatchwell R D Gregoryand K J Gaston ldquoWhat makes an urban birdrdquo Global ChangeBiology vol 17 no 1 pp 32ndash44 2011

[3] S Bolwig D Pomeroy H Tushabe and D Mushabe ldquoCropstrees and birds biodiversity change under agricultural inten-sification in Ugandas farmed landscapesrdquo Danish Journal ofGeography vol 106 no 2 pp 115ndash130 2006

[4] J Hitchmough and N Dunnett ldquoIntroduction to naturalisticplanting in urban landscapesrdquo in The Dynamic LandscapeJ Hitchmough and N Dunnatt Eds pp 1ndash32 Spon PressLondon UK 2004

[5] G T Austin and E L Smith ldquoWinter foraging ecology of mixedinsectivorous bird flocks in oakwoodland in southernArizonardquoThe Condor vol 74 pp 17ndash24 1972

[6] B R Coppedge D M Engle R E Masters and M S GregoryldquoAvian response to landscape change in fragmented southern

12 The Scientific World Journal

great plains grasslandsrdquo Ecological Applications vol 11 no 1 pp47ndash59 2001

[7] K L Evans S E Newson and K J Gaston ldquoHabitat influenceson urban avian assemblagesrdquo Ibis vol 151 no 1 pp 19ndash39 2009

[8] MW Strohbach D Haase and N Kabisch ldquoBirds and the cityUrban biodiversity land use and socioeconomicsrdquo Ecology andSociety vol 14 no 2 pp 31ndash45 2009

[9] T Stevenson and J Fanshawe Field Guide to the Birds of EastAfrica Kenya Tanzania Uganda Rwanda Burundi T amp A DPoyser London UK 2002

[10] J Mistry A Berardi and M Simpson ldquoBirds as indicators ofwetland status and change in the North Rupununi GuyanardquoBiodiversity and Conservation vol 17 no 10 pp 2383ndash24092008

[11] H Slabbekoorn and E A P Ripmeester ldquoBirdsong and anthro-pogenic noise implications and applications for conservationrdquoMolecular Ecology vol 17 no 1 pp 72ndash83 2008

[12] W S Judd C S Campbell E A Kellogg P F Stevens andM JDonoghue Plant Systematics A Phylogenetic Approach SinauerAssociates Sunderland Mass USA 3rd edition 2008

[13] W Weber ldquoRuhengeri and its resources an environmentalprofile of the Ruhengeri prefecturerdquo ETMAUSAID KigaliRwanda

[14] E Sabuhoro and G Bush ldquoThe Dian Fossey Gorilla FundInternationalPADGEF Assessing the Benefit Stream fromIllegal Activities in the Parc National des Volcansrdquo TargetingCommunity Conservation Interventions Musanze Rwanda2008

[15] J C Sano Urban Environmental Infrastructure in Kigali CityRwanda Challenges and Opportunities for Modernized Decen-tralized Sanitation Systems in Poor Neighborhoods WageningenUniversity Wageningen The Netherlands 2007

[16] R J Staniforth ldquoEffects of urbanization on bird populations inthe Canadian Central Arcticrdquo Arctic vol 55 no 1 pp 87ndash932002

[17] DWGibbons andRD Gregory ldquoBirdsrdquo in Ecological CensusesTechniques W L Sutherland Ed pp 308ndash350 CambridgeUniversity 2nd edition 2006

[18] D H Johnson ldquoPoint counts of birds what are we estimatingrdquoTech Rep PSW-GTR-149 USDA Forest Service 1995

[19] A Haslem and A F Bennett ldquoBirds in agricultural mosaics theinfluence of landscape pattern and countryside heterogeneityrdquoEcological Applications vol 18 no 1 pp 185ndash196 2008

[20] M L Rurangwa Feeding Ecology of Albertine Rift Endemic Birdsin the Volcanoes National Park Regal Sunbird Rwenzori Double-Collared Sunbird and Rwenzori Turako National University ofRwanda 2011

[21] R B Arellano-Valle H Bolfarine and V H Lachos ldquoSkew-normal linear mixedmodelsrdquo Journal of Data Science vol 3 pp415ndash438 2005

[22] D Bates Fitting LinearMixedModels in RTheNewsletter of theR Project Volume 51 University of Wisconsin Madison WisUSA 2005

[23] A E Magurran Measuring Biological Diversity Blackwell Sci-ence Malden Mass USA 2004

[24] D Tuyisingize and K Fawcett ldquoThe common bird distributionin the Parc National des Volcans and its surrounding patternsconservation and future challengesrdquo DFGF Technical Report2011

[25] A T Peterson and N A Slade ldquoExtrapolating inventory resultsinto biodiversity estimates and the importance of stoppingrulesrdquoDiversity and Distributions vol 4 no 3 pp 95ndash105 1998

[26] M Salek J Svobodova and P Zasadil ldquoEdge effect of low-trafficforest roads on bird communities in secondary productionforests in central Europerdquo Landscape Ecology vol 25 no 7 pp1113ndash1124 2010

[27] S Murererehe ldquoCollecte et analyse de donnees pourlrsquoamenagement durable des forets -Joindre les efforts nationauxet internationaux Etat des ressources forestieres au RwandardquoTech Rep FAO Rome Italy 2000

[28] S J Nsengimana M Ndimukaga L Gakwerere et al ldquoBiodi-versity surveyrdquo Tech Rep Rufford Small Grant FoundationLondon UK 2009

[29] C Nsabagasani ldquoA Migratory Species African Pitta ldquoPittaangolensisrdquo passed Buhanga relict forestrdquo Backbone vol 17 pp6ndash8 2008

[30] J Jokimaki and M Kaisanlahti-Jokimaki ldquoThe role of residen-tial habitat type on the temporal variation of wintering birdassemblages in northern Finlandrdquo Ornis Fennica vol 88 2011

[31] T M Bergin L B Best K E Freemark and K J KoehlerldquoEffects of landscape structure on nest predation in roadsides ofa midwestern agroecosystem a multiscale analysisrdquo LandscapeEcology vol 15 no 2 pp 131ndash143 2000

[32] T Koellner AMHersperger andTWohlgemuth ldquoRarefactionmethod for assessing plant species diversity on a regional scalerdquoEcography vol 27 no 4 pp 532ndash544 2004

[33] S H Faeth P S Warren E Shochat and W A MarussichldquoTrophic dynamics in urban communitiesrdquo BioScience vol 55no 5 pp 399ndash407 2005

[34] R J Fuller and J D Wilson ldquoThe ecology of seed-eating birdsin relation to agricultural practices current research and futuredirectionsrdquo British Trust for Ornithology Research Report no149 1995

[35] J N Holland andD L DeAngelis ldquoEcological and evolutionaryconditions for fruit abortion to regulate pollinating seed-eaters and increase plant reproductionrdquo Theoretical PopulationBiology vol 61 no 3 pp 251ndash263 2002

[36] C J Whelan D G Wenny and R J Marquis ldquoEcosystemservices provided by birdsrdquo Annals of the New York Academyof Sciences vol 1134 pp 25ndash60 2008

[37] O Gilbert The Ecology of Urban Habitats Chapman amp HallLondon UK 1989

[38] A Millard ldquoSemi-natural vegetation and its relationship todesignated urban green space at the landscape scale in LeedsUKrdquo Landscape Ecology vol 23 no 10 pp 1231ndash1241 2008

[39] I Kowarik ldquoOn the role of alien species in urban flora andvegetationrdquo in Plant Invasions General Aspects and SpecialProblems P Pysek K Prach M Rejmanek and M WadeEds pp 85ndash103 SPB Academic Publishing Amsterdam TheNetherlands 1995

[40] G W Luck ldquoA review of the relationships between humanpopulation density and biodiversityrdquo Biological Reviews vol 82no 4 pp 607ndash645 2007

[41] Victorian Government Department of Sustainability and Envi-ronment (VGDSE) Managing Native Vegetation in VictorianCemeteries Victorian Government Department of Sustainabil-ity and Environment Melbourne Australia 2009

[42] C Dowd ldquoEffect of development on bird species compositionof two urban forested wetlands in Staten Island New YorkrdquoJournal of Field Ornithology vol 63 no 4 pp 455ndash461 1992

Page 6: Bird Diversity and Distribution in relation to Urban Landscape Types in Northern Rwanda · 2016. 1. 26. · ResearchArticle Bird Diversity and Distribution in relation to Urban Landscape

6 The Scientific World Journal

0 50 100 150 200 250 300Number of individuals

Spec

ies n

ame

Nectarinia kilimensis

Ploceus melanocephalus

Ploceus baglafecht

Estrilda astrild

Lagonosticta senegala

Lonchura cucullata

Milvus migrans

Serinus striolatus

Passer griseus

Corvus albus

Figure 7 Top ten most represented bird species in all sites of Musanze city

0 100 200 300 400 500 600 700Number of individuals

Aerial feeders

Butcherbirds

Fishers

Flycatchers

Frugivores

Insectivores

Nectar feeders

Raptors

Scavengers

Seedeaters

Shorerbirds

Feed

ing

guild

s

Open fields Built-up areas

Figure 8 Feeding guild categories of bird species as classified in microlandscapes types

had the highest diversity rank followed by residentialneighborhoods and informal settlements The aerodromeand Westland were ranked with the lowest bird diversity(Figure 9(b))

The Shannon diversity index was similar for bothmacrolandscape types built-up areas (1198671015840 = 1456) and itscounterpart open fields (1198671015840 = 1518) At the microland-scape level residential neighborhoods were the most diversefollowed by informal settlements and institutional groundsWastelands displayed the lowest bird diversity (Figure 10)

342 Species Similarity in Macro- and Microlandscape TypesOf the 94 bird species recorded in Musanze city 45 specieswere shared by both open fields and built-up landscapes Interms of species composition found in each microlandscape

type the riverside landscape was the most different fromthe remaining microlandscapes Residential neighborhoodsand informal settlements were most similar The differencesbetween the landscape types in terms of species compositionillustrated by the increasing distance from the root to thepoint where a given branch stems were as follows riversidelt aerodrome lt streamside lt wasteland lt agrofields lt ceme-teries lt forest lt institutional and business center lt informalsettlements and residences (Figure 11)

35 Bird Diversity in Musanze City and Nearby ProtectedAreas In addition to the internal comparison the level ofsimilarity between Musanze and its nearby protected areas(PNV and Buhanga eco-park) revealed important similaritiesbetween protected and urban habitats in terms of bird

The Scientific World Journal 7

0 5 10 15 20 25 30 35 4005

10

15

20

25

Rank

Open fieldsBuilt-up area

Log 1

0re

lativ

e abu

ndan

ce

(a)

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38

04

06

08

10

12

14

16

18

20

22

Rankminus2

AerodromeAgrofield Business centerCemeteriesForest

InstitutionalResidenceRiversideSettlementStreamside

WastelandLo

g 10

rela

tive a

bund

ance

(b)

Figure 9 Species rankabundance (a) in macrolandscape types and (b) in microlandscape types

Aerodrome

Agrofields

Business centers

Cemeteries

Forests

Institutional grounds

Residential neighborhoods

Riversides

Informal settlements

Streamsides

Wastelands

00 02 04 06 08 10 12 14Shannon index

Mic

rola

ndsc

ape t

ypes

Figure 10 Shannon index for microlandscape types of Musanze city

diversity (Figure 12) The total number of bird species inMusanze city was 94 105 in PNV and 81 in the Buhanga eco-park Of the 94 bird species recorded in Musanze 32 werealso present in Buhanga eco-park 51 in the PNV and 21 werefound in both the Buhanga eco-park and in PNV Moreoverwe found only one endemic bird species the RuwenzoriDouble-collared Sunbird (Cinnyris stuhlmanni) in Musanzeunlike the three endemic bird species present in Buhanga eco-park and the fifteen in the PNV This Albertine Rift endemic

species is also present in the PNV however it is absent fromthe Buhanga eco-park

In the comparison of the bird species found in the threesites Musanze city is unique in the number of migratory birdspecies observed Specifically seven migratory species wererecorded in Musanze city while only two are known to existin the PNV and none have been recorded in the Buhanga eco-park (Table 4) Musanzersquos microlandscapes that were visitedbymigratory birds include the riversides ofMukungwa River

8 The Scientific World Journal

RSWLSSISRNIGFTAFCMBCAM

1000 50

Similarity ()

Bray-Curtis cluster analysis (single link)

Figure 11 Species composition-based microlandscape clusters(AM aerodrome AG agrofields BC business centers CM ceme-teries FT forests IS informal settlements IG institutional groundsRN residential neighborhoods RS riversides SS streamside WLwasteland)

1000 50

Similarity ()

Bray-Curtis cluster analysis (single link)

PNV

Musanze

Buhanga

Figure 12 Musanze city PNV and Buhanga eco-park bird speciescomposition

informal settlements forests business centers and residentialneighborhoods

The majority of species in Musanze city were nativesuch that exotic bird species accounted for only 43 of thetotal number of bird species observed (Ficedula albicollisPloceus cucullatus Serinus canicollis and Serinus citrinel-loides) (Table 5) Up to 64 of the species observed hadno breeding opportunities within the study area (Actitishypoleucos Aquila pomarina Merops apiaster Muscicapastriata Phylloscopus trochilus and Sylvia borin)

4 Discussion

Our study of bird diversity in Musanze city has revealed thatcurrent wildlife conservation efforts do not coincide withareas of the highest bird abundance and species diversitywhich exist in urban areas Bird species richness in theurban areas of Musanze is greater than that of Buhangaeco-park and similar to that of the PNV two surroundingnatural habitats that are currently receiving the majority ofconservation efforts Furthermore species of high ecologicalimportance and therefore high conservation concern such

as endemic and migratory species were recorded across thecity landscapesThis study therefore indicates the importanceof protecting not only the natural habitats of native wildlifebut also urban areas where birds in particular are morecommonly existing

41 Species Richness The unique endemic species found inMusanze city the Ruwenzori Double-collared Sunbird haspreviously been observed in the VPN This species is knownto live in the high altitude habitats of the Albertine Rift[24] It is therefore not surprising that it was found in urbanlandscapes ofMusanze city which is located at a high altitudeof 1850m [26] Stevenson and Fanshawe [9] suggest thatthe sunbirdrsquos most preferred habitats are flowering bushes offorest edges and it may be unusual that the endemic specieswas observed foraging onMarkhamia lutea trees within openfields of Musanze city in this study Our study suggests thatthe species distribution of the Ruwenzori Double-collaredSunbird is not restricted to its natural habitat in the AlbertineRift as it can also exist in urban landscapesThis species maytherefore be able to adapt to human-dominated landscapesand it is likely that it may forage on vegetation such as urbangarden trees Our study suggests that the sunbird is capableof adapting its feeding preferences to the available plants incity landscapes potentially as a response to loss of its naturalhabitat caused by park reductions [27]

The seven migrant bird species found in the studysite were regular September-April visitors from Palearcticregions Two of them the Red-chested Cuckoo (Cucu-lus solitarius) and the European Bee-eater (Merops api-aster) had previously been sighted in the gallery forestsof the Rwandanrsquos Eastern Province [28] and in the PNV[24] The Common Sandpiper Spotted Flycatcher andWillow Warbler have also been reported to visit Rwanda(httpwwwrwandabirdingorg 02092012) and Musanzecity but have never been sighted in the Lava Plain or inthe Volcano Range of Rwanda The remaining two migrantsthe Garden Warbler (Sylvia borin) and the Lesser SpottedEagle (Aquila pomarina) have been reported in Rwandafor the first time as a result of this study Importantly theseven migrant species have never been reported to occurin urban environments of Rwanda and only two had beenreported to visit its highlands [24] However the AfricanPitta (Pitta angolensis) which is an intra-African breedingmigrant bird sighted in the Buhanga eco-park in 2006 and2008 [29] was not recorded in this study The findings of ourstudy encourage the development of bird watching activitiesin Musanze city which may be of particular interest tointernational tourists due to the high number of urban-livingand therefore easily observed unique bird species

411 Number of Species by Macrolandscape Types Thehypothesis that bird species inhabit open fields more thanbuilt-up areas was not supported in this study This maybe due to the fact that some built-up areas including insti-tutional grounds residential neighborhoods and informalsettlements are specifically designed with plant communi-ties to attract birds [30] These communities often include

The Scientific World Journal 9

Table 4 Migratory birds in Musanze city PNV and Buhanga eco-park

Common name Scientific name Musanze city Protected areasPNV Buhanga eco-park

Common Sandpiper Actitis hypoleucos

European Bee-eater Merops apiaster

Garden Warbler Sylvia borin

Lesser-spotted Eagle Aquila pomarina

Red-chested Cuckoo Cuculus solitarius

Spotted Flycatcher Muscicapa striata

WillowWarbler Phylloscopus trochilus

Table 5 Exotic birds in Musanze city PNV and Buhanga eco-park

Common name Scientific name Musanze city Protected areasPNV Buhanga eco-park

Collared Flycatcher Ficedula albicollis

Black-headed Weaver Ploceus cucullatus

Yellow-crowned Canary Serinus canicollis

Abyssinian Citril Serinus citrinelloides

a number of trees with a substantial canopy as well asornamental plants such as vegetation that exists as bushesAlternatively some microlandscapes within open fields havea low number of species such as the Musanze aerodromewhich is a grassland habitat and is regularly maintained tofacilitate airplane landing This habitat offers little feedingopportunities to wildlife and is an unsuitable habitat for mostbird species as it may for instance expose small-sized birdsto predators [31]

412 Number of Species by Microlandscape Types In supportof Koellner et al [32] different landscapes in Musanze werecorrelated with differences in bird species richness Theinstitutional grounds had a relatively high species richnessperhaps due to a high variety of plant assemblages Simi-larly the high number of bird species found in residentialneighborhoods and informal settlements can be explained bythe diversity of plant resources in these areas These plantresources include nectar-producing flowers such as bananaplants that attract sunbirds fruit-bearing trees and shrubssuch as guava plants that frugivorous species can feed on Inaddition the high concentrations of domestic wastes (such asresidues food disposable and waste-water) in the homesteadenvironment offer a unique opportunity to predators suchas insectivorous birds that feed on small mammals (egmice frogs) and insects (eg flies mosquitoes) and arecommon to this type of microhabitats Domestic waste mayalso attract scavenger species Finally informal settlementsthat are surrounded by a mosaic of vegetation types offermany opportunities for bird foraging and nesting [30] Thisdiversity in urban landscape vegetation structure and typemay therefore reflect the vast diversity of bird species in urbanareas which has not previously been investigated in Rwanda

42 Species Relative Abundance

421 Number of Individuals by Macrolandscape Types Thenonsignificant effect of macrolandscapes on the total numberof birds in an area may be linked to the fact that landscapetype had no significant influence on bird species richnessMore importantly due to the historical nonformal nature ofurban design in Musanze both macrolandscapes appeared tohave similar types and levels of bird-exploitable resourcesincluding appropriate plant coverage and sites for birds tonest [33]

422 Number of Individuals byMicrolandscape Types Ceme-teries riverside landscapes and wastelands did not differin the total number of birds in comparison to residentialneighborhoods (Table 3) This may be attributed to the factthat these four landscapes appear to be intrinsically hetero-geneous suggesting that there may be possible confoundingfactors that have overshadowed the expected relationshipbetween microlandscapes and relative bird abundance Forinstance wastelands attract many scavengers and raptorscemeteries and agrofields provide appropriate plant assem-blages for seed eaters and riversides offer easy water accessand shelter for aquatic bird species [4] Therefore theabundance of birds across the different microlandscapes ofMusanze is relatively uniform due to the fact that eachlandscape offers a range of suitable habitats for a range of birdspecies

423 Most Represented Species in Musanze City The PiedCrow (Corvus albus) was the most common species inMusanze and seemed to be the most adapted to human-dominated landscapes (Figure 7) For instance unlike many

10 The Scientific World Journal

other bird species in the area the Pied Crow was observedclose to many human facilities such food markets abattoirswastelands domestic yards and croplands In addition thePied Crow was found in high abundance where its foodsources including small reptiles small mammals grainpeanuts carrion scraps of human food fruits insects andother small invertebrates were most available [9] To a lesserextent the urban habitat appeared to favor the Grey-headedSparrow (Passer griseus) The occurrence of the Grey-headedSparrow was associated with open woodlands and humansettlements where this species can easily access required foodand habitat resources The third most represented specieswas the Streaky Seedeater (Serinus striolatus) which is acommon bird of highlands and is generally found above1300m in gardens and cultivated areas woodland edgesheath and scrub vegetation areas The Streaky Seedeateris therefore adept at living in human altered landscapeswhich is not unlike the Black Kite (Milvus migrans) whichwas also common to densely human-populated areas Thesehuman-used landscapes are also a popular habitat of theBlackKitersquos prey which includes small birds bats and rodents Inparticular our study revealed the common occurrence of theBlack Kite circling near the abattoir and scavenging in thecityrsquos wastelands

43 Feeding Guild Categories

431 Feeding Guild Categories by Macrolandscape TypesSeed-eating birds were the best represented guild inMusanze(Figure 8) This may be partially due to the fact that datacollection was completed during a maize-harvesting periodDuring this period urban fields have an exceptionally largeabundance of seeds that can be exploited by birds and mayhave therefore selectively attracted seed-eating species [34]It was also observed that seed-eating species fed from arange of fruits According to Holland and DeAngelis [35]this habit allows seed-eating species to contribute to plantreproduction through pollination Insectivorous species werealso prominent in Musanzersquos urban landscapes Similarly tothe findings of Austin and Smith [5] insectivores were mostabundant in insect-rich landscapes including streamsideareas forests and informal settlements

432 FeedingGuild Categories byMicrolandscapes Althoughseedeaters especially the Grey-headed Sparrow (Passergriseus) dominated almost all microlandscapes it is impor-tant to consider that in wastelands scavengers were the mostabundant (Figure 13) This finding is likely due to the factthat different microlandscapes aremore appropriate for somespecies more than others especially those with differentfeeding habits

Our study confirms that bird species found in Musanzecity like urban-living bird species in other cities contributeto biomass recycling [36] Interestingly although there wereonly a few species of scavenging birds in Musanze theirabundance was high enough to compensate for their lowspecies richness in order to make a notable biomass recyclingimpact to city dwellersThis was particularly true for the Pied

Figure 13 Abundance of Pied Crows in a landfill within Musanzecity (Photo Author 2012)

Crow (Corvus albus) a species whose abundance amountedto more than seven times the average number of individualsper species whichwas almost 10of the total number of birdsobserved

44 Species Diversity

441 Alpha Diversity The bird diversity found in built-up areas was comparable to the bird diversity in urbanopen fields in Musanze city (Figure 9(a)) This finding pro-vides support for the increasingly recognized idea that birddiversity in urban areas can be as high as that in naturalenvironments [37 38] Previous research suggests that thismay be due to a relatively high number of nonnative speciespresent in cities as well as the heterogeneous habitat thaturban landscapes provide [39] which was not supportedin this study perhaps because of close proximity of thestudy area to a network of natural environments (PNVGishwati forest and Buhanga eco-park Rugezi Mukungwaand Bihinga wetlands and Karago Bulera and Ruhondolakes) Moreover Luck [40] suggested that there is a positivecorrelation between human population density and birdspecies richness This relationship was demonstrated in ourstudy as species such as the Pied Crowwere found to bemostabundant throughout urban landscapes and therefore welladapted to an environment where high human densities existInterestingly even the Albertine Rift endemic species theRuwenzori Double-collared Sunbird was sighted foraging inhuman populated areas on garden plants

Overall residential neighborhoods institutionalgrounds and informal settlements can be considered asthe major bird hotspots in Musanze city (Figure 9(b)) Thesethree landscapes share a great floristic diversity providingmany important stimuli for bird life (such as fruits seedsnectar domestic residues insects small mammals reptilesand amphibians) [30] Finally contrary to rural areas andnatural forests that undergo seasonal shortages of resources[3] cities do not experience strong seasonal variation due toa continuous supply of recourses from remote areas

442 Species Similarity The macrolandscapes all appearedto have similar bird species composition which may bedue to landscape heterogeneity [39] This heterogeneity islikely a result of the lack of historical professional landscapeplanning and design leaving a mosaic landscape structure inboth built-up and open fields instead of a uniform landscapespecialization Our results suggest that residential areas and

The Scientific World Journal 11

informal settlements were the most similar in terms ofspecies composition These landscapes ultimately functionto host family life The only difference between residentialareas and informal settlements resides in their socioeconomicstatus which is reflected in the landscape structure Howeverboth landscapes are more similar to each other than toother landscapes Furthermore the species composition ofcemeteries was similar to both forests and some of the built-up microlandscapes which may be attributed to the fact thatthese areas are all surrounded by trees Additionally ceme-teries are characterized by low human disturbance whichmay compare to that of forests and some urban landscapesThese landscapes all harbor a wide variety of floweringplants which in the case of cemeteries are mainly plantedby bereaved ones Moreover the vegetation of graveyardsincludes a range of regeneration stages resulting in a widerange of habitats from the vegetation-free areas of newly duggraves to the reconstructed thickets around old graves [41]Finally riverside landscapes emerged as the most specializedlandscape type as expected with many distinctive speciesobserved in this landscape only Almost all the species foundin riverside areas were specialists of wetlands and were notfound elsewhere As a result it was the most dissimilar to allother microlandscapes

The high degree of similarity in terms of bird diversitybetween Musanze city and the protected natural habitatsnearby provide further support that wildlife does not exclu-sively inhabit protected areas [33 37 42] Although the twonatural habitats are at eight km from Musanze city morethan half of the species found in the city were also found inVPN The lower degree of similarity between Musanze andBuhanga eco-park may be linked to the relative geographiclocation of the two sites as Musanze city is almost half waybetween the two protected areas This finding may also beattributed to the fact that the diversity ofmicrohabitats withinBuhanga eco-park is lower than that of Musanze and VPN[13] which may be due to the relatively small size of Buhangaeco-park Interestingly the species found in more than onelandscape type were also recorded both inside and beyondthe city limits Conversely Ficedula albicollis was recorded inonly one landscape type (cemeteries) and was absent in bothPNV and Buhanga eco-park

5 Conclusions

This study contributes to the knowledge of bird diversity inurban landscapes and provides the most recent status of birddiversity in Musanze city Our findings confirm that birddiversity in urban areas such as a densely populated city canbe as great as that in surrounding natural forests Specificallythe total number of bird species in Musanze city was verysimilar to that of the nearest protected forests VolcanoesNational Park and Buhanga eco-park Endemic and migra-tory birdswere also found inMusanze cityOneAlbertine Riftendemic bird species the Ruwenzori Double-collared Sun-bird was observed in Musanze during this study which hasnot been previously recorded Similarly threemigratory birdswere found inMusanze region for the first time the Common

Sandpiper the Spotted Flycatcher and theWillowWarbler Inaddition two bird species were observed that have not beenpreviously reported in Rwanda the Garden Warbler (Sylviaborin) and the Lesser Spotted Eagle (Aquila pomarina) Theeffect of landscape types on bird species richness and relativeabundance was also illustrated Residential neighborhoodsinstitutional grounds and informal settlements had thehighest species diversity indices and rankabundance relativeto the rest of the microlandscapes in this study Riversidelandscapes emerged with the most specialized bird faunaincluding species that are restricted to wetland environmentsand water bodies This study confirmed that scavengers inMusanze city contribute more to biomass recycling than anyother bird feeding groups Our study provides a current anduseful reference for urban decision makers and confirms theexistence of a great diversity of wildlife within cities Wesuggest that the development and implementation of cityland-use plans should consider this biodiversity especiallywhen villages and cities are in close proximity of protectedareas or natural reserves Finally it may be important thatbotanical gardens and public parks are included in themasterplan of the city as our study indicates that their designrequires an understanding of biodiversity in particular ofavian populations

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors acknowledge technical support from staffat DFGFI-Karisoke Research Center namely Dr WinnieEckardt Mr Deogratias Tuyisingize Mr Emmanuel Faidaand Mrs Keiko Mori

References

[1] S R Loss M O Ruiz and J D Brawn ldquoRelationships betweenavian diversity neighborhood age income and environmentalcharacteristics of an urban landscaperdquo Biological Conservationvol 142 no 11 pp 2578ndash2585 2009

[2] K L Evans D E Chamberlain B J Hatchwell R D Gregoryand K J Gaston ldquoWhat makes an urban birdrdquo Global ChangeBiology vol 17 no 1 pp 32ndash44 2011

[3] S Bolwig D Pomeroy H Tushabe and D Mushabe ldquoCropstrees and birds biodiversity change under agricultural inten-sification in Ugandas farmed landscapesrdquo Danish Journal ofGeography vol 106 no 2 pp 115ndash130 2006

[4] J Hitchmough and N Dunnett ldquoIntroduction to naturalisticplanting in urban landscapesrdquo in The Dynamic LandscapeJ Hitchmough and N Dunnatt Eds pp 1ndash32 Spon PressLondon UK 2004

[5] G T Austin and E L Smith ldquoWinter foraging ecology of mixedinsectivorous bird flocks in oakwoodland in southernArizonardquoThe Condor vol 74 pp 17ndash24 1972

[6] B R Coppedge D M Engle R E Masters and M S GregoryldquoAvian response to landscape change in fragmented southern

12 The Scientific World Journal

great plains grasslandsrdquo Ecological Applications vol 11 no 1 pp47ndash59 2001

[7] K L Evans S E Newson and K J Gaston ldquoHabitat influenceson urban avian assemblagesrdquo Ibis vol 151 no 1 pp 19ndash39 2009

[8] MW Strohbach D Haase and N Kabisch ldquoBirds and the cityUrban biodiversity land use and socioeconomicsrdquo Ecology andSociety vol 14 no 2 pp 31ndash45 2009

[9] T Stevenson and J Fanshawe Field Guide to the Birds of EastAfrica Kenya Tanzania Uganda Rwanda Burundi T amp A DPoyser London UK 2002

[10] J Mistry A Berardi and M Simpson ldquoBirds as indicators ofwetland status and change in the North Rupununi GuyanardquoBiodiversity and Conservation vol 17 no 10 pp 2383ndash24092008

[11] H Slabbekoorn and E A P Ripmeester ldquoBirdsong and anthro-pogenic noise implications and applications for conservationrdquoMolecular Ecology vol 17 no 1 pp 72ndash83 2008

[12] W S Judd C S Campbell E A Kellogg P F Stevens andM JDonoghue Plant Systematics A Phylogenetic Approach SinauerAssociates Sunderland Mass USA 3rd edition 2008

[13] W Weber ldquoRuhengeri and its resources an environmentalprofile of the Ruhengeri prefecturerdquo ETMAUSAID KigaliRwanda

[14] E Sabuhoro and G Bush ldquoThe Dian Fossey Gorilla FundInternationalPADGEF Assessing the Benefit Stream fromIllegal Activities in the Parc National des Volcansrdquo TargetingCommunity Conservation Interventions Musanze Rwanda2008

[15] J C Sano Urban Environmental Infrastructure in Kigali CityRwanda Challenges and Opportunities for Modernized Decen-tralized Sanitation Systems in Poor Neighborhoods WageningenUniversity Wageningen The Netherlands 2007

[16] R J Staniforth ldquoEffects of urbanization on bird populations inthe Canadian Central Arcticrdquo Arctic vol 55 no 1 pp 87ndash932002

[17] DWGibbons andRD Gregory ldquoBirdsrdquo in Ecological CensusesTechniques W L Sutherland Ed pp 308ndash350 CambridgeUniversity 2nd edition 2006

[18] D H Johnson ldquoPoint counts of birds what are we estimatingrdquoTech Rep PSW-GTR-149 USDA Forest Service 1995

[19] A Haslem and A F Bennett ldquoBirds in agricultural mosaics theinfluence of landscape pattern and countryside heterogeneityrdquoEcological Applications vol 18 no 1 pp 185ndash196 2008

[20] M L Rurangwa Feeding Ecology of Albertine Rift Endemic Birdsin the Volcanoes National Park Regal Sunbird Rwenzori Double-Collared Sunbird and Rwenzori Turako National University ofRwanda 2011

[21] R B Arellano-Valle H Bolfarine and V H Lachos ldquoSkew-normal linear mixedmodelsrdquo Journal of Data Science vol 3 pp415ndash438 2005

[22] D Bates Fitting LinearMixedModels in RTheNewsletter of theR Project Volume 51 University of Wisconsin Madison WisUSA 2005

[23] A E Magurran Measuring Biological Diversity Blackwell Sci-ence Malden Mass USA 2004

[24] D Tuyisingize and K Fawcett ldquoThe common bird distributionin the Parc National des Volcans and its surrounding patternsconservation and future challengesrdquo DFGF Technical Report2011

[25] A T Peterson and N A Slade ldquoExtrapolating inventory resultsinto biodiversity estimates and the importance of stoppingrulesrdquoDiversity and Distributions vol 4 no 3 pp 95ndash105 1998

[26] M Salek J Svobodova and P Zasadil ldquoEdge effect of low-trafficforest roads on bird communities in secondary productionforests in central Europerdquo Landscape Ecology vol 25 no 7 pp1113ndash1124 2010

[27] S Murererehe ldquoCollecte et analyse de donnees pourlrsquoamenagement durable des forets -Joindre les efforts nationauxet internationaux Etat des ressources forestieres au RwandardquoTech Rep FAO Rome Italy 2000

[28] S J Nsengimana M Ndimukaga L Gakwerere et al ldquoBiodi-versity surveyrdquo Tech Rep Rufford Small Grant FoundationLondon UK 2009

[29] C Nsabagasani ldquoA Migratory Species African Pitta ldquoPittaangolensisrdquo passed Buhanga relict forestrdquo Backbone vol 17 pp6ndash8 2008

[30] J Jokimaki and M Kaisanlahti-Jokimaki ldquoThe role of residen-tial habitat type on the temporal variation of wintering birdassemblages in northern Finlandrdquo Ornis Fennica vol 88 2011

[31] T M Bergin L B Best K E Freemark and K J KoehlerldquoEffects of landscape structure on nest predation in roadsides ofa midwestern agroecosystem a multiscale analysisrdquo LandscapeEcology vol 15 no 2 pp 131ndash143 2000

[32] T Koellner AMHersperger andTWohlgemuth ldquoRarefactionmethod for assessing plant species diversity on a regional scalerdquoEcography vol 27 no 4 pp 532ndash544 2004

[33] S H Faeth P S Warren E Shochat and W A MarussichldquoTrophic dynamics in urban communitiesrdquo BioScience vol 55no 5 pp 399ndash407 2005

[34] R J Fuller and J D Wilson ldquoThe ecology of seed-eating birdsin relation to agricultural practices current research and futuredirectionsrdquo British Trust for Ornithology Research Report no149 1995

[35] J N Holland andD L DeAngelis ldquoEcological and evolutionaryconditions for fruit abortion to regulate pollinating seed-eaters and increase plant reproductionrdquo Theoretical PopulationBiology vol 61 no 3 pp 251ndash263 2002

[36] C J Whelan D G Wenny and R J Marquis ldquoEcosystemservices provided by birdsrdquo Annals of the New York Academyof Sciences vol 1134 pp 25ndash60 2008

[37] O Gilbert The Ecology of Urban Habitats Chapman amp HallLondon UK 1989

[38] A Millard ldquoSemi-natural vegetation and its relationship todesignated urban green space at the landscape scale in LeedsUKrdquo Landscape Ecology vol 23 no 10 pp 1231ndash1241 2008

[39] I Kowarik ldquoOn the role of alien species in urban flora andvegetationrdquo in Plant Invasions General Aspects and SpecialProblems P Pysek K Prach M Rejmanek and M WadeEds pp 85ndash103 SPB Academic Publishing Amsterdam TheNetherlands 1995

[40] G W Luck ldquoA review of the relationships between humanpopulation density and biodiversityrdquo Biological Reviews vol 82no 4 pp 607ndash645 2007

[41] Victorian Government Department of Sustainability and Envi-ronment (VGDSE) Managing Native Vegetation in VictorianCemeteries Victorian Government Department of Sustainabil-ity and Environment Melbourne Australia 2009

[42] C Dowd ldquoEffect of development on bird species compositionof two urban forested wetlands in Staten Island New YorkrdquoJournal of Field Ornithology vol 63 no 4 pp 455ndash461 1992

Page 7: Bird Diversity and Distribution in relation to Urban Landscape Types in Northern Rwanda · 2016. 1. 26. · ResearchArticle Bird Diversity and Distribution in relation to Urban Landscape

The Scientific World Journal 7

0 5 10 15 20 25 30 35 4005

10

15

20

25

Rank

Open fieldsBuilt-up area

Log 1

0re

lativ

e abu

ndan

ce

(a)

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38

04

06

08

10

12

14

16

18

20

22

Rankminus2

AerodromeAgrofield Business centerCemeteriesForest

InstitutionalResidenceRiversideSettlementStreamside

WastelandLo

g 10

rela

tive a

bund

ance

(b)

Figure 9 Species rankabundance (a) in macrolandscape types and (b) in microlandscape types

Aerodrome

Agrofields

Business centers

Cemeteries

Forests

Institutional grounds

Residential neighborhoods

Riversides

Informal settlements

Streamsides

Wastelands

00 02 04 06 08 10 12 14Shannon index

Mic

rola

ndsc

ape t

ypes

Figure 10 Shannon index for microlandscape types of Musanze city

diversity (Figure 12) The total number of bird species inMusanze city was 94 105 in PNV and 81 in the Buhanga eco-park Of the 94 bird species recorded in Musanze 32 werealso present in Buhanga eco-park 51 in the PNV and 21 werefound in both the Buhanga eco-park and in PNV Moreoverwe found only one endemic bird species the RuwenzoriDouble-collared Sunbird (Cinnyris stuhlmanni) in Musanzeunlike the three endemic bird species present in Buhanga eco-park and the fifteen in the PNV This Albertine Rift endemic

species is also present in the PNV however it is absent fromthe Buhanga eco-park

In the comparison of the bird species found in the threesites Musanze city is unique in the number of migratory birdspecies observed Specifically seven migratory species wererecorded in Musanze city while only two are known to existin the PNV and none have been recorded in the Buhanga eco-park (Table 4) Musanzersquos microlandscapes that were visitedbymigratory birds include the riversides ofMukungwa River

8 The Scientific World Journal

RSWLSSISRNIGFTAFCMBCAM

1000 50

Similarity ()

Bray-Curtis cluster analysis (single link)

Figure 11 Species composition-based microlandscape clusters(AM aerodrome AG agrofields BC business centers CM ceme-teries FT forests IS informal settlements IG institutional groundsRN residential neighborhoods RS riversides SS streamside WLwasteland)

1000 50

Similarity ()

Bray-Curtis cluster analysis (single link)

PNV

Musanze

Buhanga

Figure 12 Musanze city PNV and Buhanga eco-park bird speciescomposition

informal settlements forests business centers and residentialneighborhoods

The majority of species in Musanze city were nativesuch that exotic bird species accounted for only 43 of thetotal number of bird species observed (Ficedula albicollisPloceus cucullatus Serinus canicollis and Serinus citrinel-loides) (Table 5) Up to 64 of the species observed hadno breeding opportunities within the study area (Actitishypoleucos Aquila pomarina Merops apiaster Muscicapastriata Phylloscopus trochilus and Sylvia borin)

4 Discussion

Our study of bird diversity in Musanze city has revealed thatcurrent wildlife conservation efforts do not coincide withareas of the highest bird abundance and species diversitywhich exist in urban areas Bird species richness in theurban areas of Musanze is greater than that of Buhangaeco-park and similar to that of the PNV two surroundingnatural habitats that are currently receiving the majority ofconservation efforts Furthermore species of high ecologicalimportance and therefore high conservation concern such

as endemic and migratory species were recorded across thecity landscapesThis study therefore indicates the importanceof protecting not only the natural habitats of native wildlifebut also urban areas where birds in particular are morecommonly existing

41 Species Richness The unique endemic species found inMusanze city the Ruwenzori Double-collared Sunbird haspreviously been observed in the VPN This species is knownto live in the high altitude habitats of the Albertine Rift[24] It is therefore not surprising that it was found in urbanlandscapes ofMusanze city which is located at a high altitudeof 1850m [26] Stevenson and Fanshawe [9] suggest thatthe sunbirdrsquos most preferred habitats are flowering bushes offorest edges and it may be unusual that the endemic specieswas observed foraging onMarkhamia lutea trees within openfields of Musanze city in this study Our study suggests thatthe species distribution of the Ruwenzori Double-collaredSunbird is not restricted to its natural habitat in the AlbertineRift as it can also exist in urban landscapesThis species maytherefore be able to adapt to human-dominated landscapesand it is likely that it may forage on vegetation such as urbangarden trees Our study suggests that the sunbird is capableof adapting its feeding preferences to the available plants incity landscapes potentially as a response to loss of its naturalhabitat caused by park reductions [27]

The seven migrant bird species found in the studysite were regular September-April visitors from Palearcticregions Two of them the Red-chested Cuckoo (Cucu-lus solitarius) and the European Bee-eater (Merops api-aster) had previously been sighted in the gallery forestsof the Rwandanrsquos Eastern Province [28] and in the PNV[24] The Common Sandpiper Spotted Flycatcher andWillow Warbler have also been reported to visit Rwanda(httpwwwrwandabirdingorg 02092012) and Musanzecity but have never been sighted in the Lava Plain or inthe Volcano Range of Rwanda The remaining two migrantsthe Garden Warbler (Sylvia borin) and the Lesser SpottedEagle (Aquila pomarina) have been reported in Rwandafor the first time as a result of this study Importantly theseven migrant species have never been reported to occurin urban environments of Rwanda and only two had beenreported to visit its highlands [24] However the AfricanPitta (Pitta angolensis) which is an intra-African breedingmigrant bird sighted in the Buhanga eco-park in 2006 and2008 [29] was not recorded in this study The findings of ourstudy encourage the development of bird watching activitiesin Musanze city which may be of particular interest tointernational tourists due to the high number of urban-livingand therefore easily observed unique bird species

411 Number of Species by Macrolandscape Types Thehypothesis that bird species inhabit open fields more thanbuilt-up areas was not supported in this study This maybe due to the fact that some built-up areas including insti-tutional grounds residential neighborhoods and informalsettlements are specifically designed with plant communi-ties to attract birds [30] These communities often include

The Scientific World Journal 9

Table 4 Migratory birds in Musanze city PNV and Buhanga eco-park

Common name Scientific name Musanze city Protected areasPNV Buhanga eco-park

Common Sandpiper Actitis hypoleucos

European Bee-eater Merops apiaster

Garden Warbler Sylvia borin

Lesser-spotted Eagle Aquila pomarina

Red-chested Cuckoo Cuculus solitarius

Spotted Flycatcher Muscicapa striata

WillowWarbler Phylloscopus trochilus

Table 5 Exotic birds in Musanze city PNV and Buhanga eco-park

Common name Scientific name Musanze city Protected areasPNV Buhanga eco-park

Collared Flycatcher Ficedula albicollis

Black-headed Weaver Ploceus cucullatus

Yellow-crowned Canary Serinus canicollis

Abyssinian Citril Serinus citrinelloides

a number of trees with a substantial canopy as well asornamental plants such as vegetation that exists as bushesAlternatively some microlandscapes within open fields havea low number of species such as the Musanze aerodromewhich is a grassland habitat and is regularly maintained tofacilitate airplane landing This habitat offers little feedingopportunities to wildlife and is an unsuitable habitat for mostbird species as it may for instance expose small-sized birdsto predators [31]

412 Number of Species by Microlandscape Types In supportof Koellner et al [32] different landscapes in Musanze werecorrelated with differences in bird species richness Theinstitutional grounds had a relatively high species richnessperhaps due to a high variety of plant assemblages Simi-larly the high number of bird species found in residentialneighborhoods and informal settlements can be explained bythe diversity of plant resources in these areas These plantresources include nectar-producing flowers such as bananaplants that attract sunbirds fruit-bearing trees and shrubssuch as guava plants that frugivorous species can feed on Inaddition the high concentrations of domestic wastes (such asresidues food disposable and waste-water) in the homesteadenvironment offer a unique opportunity to predators suchas insectivorous birds that feed on small mammals (egmice frogs) and insects (eg flies mosquitoes) and arecommon to this type of microhabitats Domestic waste mayalso attract scavenger species Finally informal settlementsthat are surrounded by a mosaic of vegetation types offermany opportunities for bird foraging and nesting [30] Thisdiversity in urban landscape vegetation structure and typemay therefore reflect the vast diversity of bird species in urbanareas which has not previously been investigated in Rwanda

42 Species Relative Abundance

421 Number of Individuals by Macrolandscape Types Thenonsignificant effect of macrolandscapes on the total numberof birds in an area may be linked to the fact that landscapetype had no significant influence on bird species richnessMore importantly due to the historical nonformal nature ofurban design in Musanze both macrolandscapes appeared tohave similar types and levels of bird-exploitable resourcesincluding appropriate plant coverage and sites for birds tonest [33]

422 Number of Individuals byMicrolandscape Types Ceme-teries riverside landscapes and wastelands did not differin the total number of birds in comparison to residentialneighborhoods (Table 3) This may be attributed to the factthat these four landscapes appear to be intrinsically hetero-geneous suggesting that there may be possible confoundingfactors that have overshadowed the expected relationshipbetween microlandscapes and relative bird abundance Forinstance wastelands attract many scavengers and raptorscemeteries and agrofields provide appropriate plant assem-blages for seed eaters and riversides offer easy water accessand shelter for aquatic bird species [4] Therefore theabundance of birds across the different microlandscapes ofMusanze is relatively uniform due to the fact that eachlandscape offers a range of suitable habitats for a range of birdspecies

423 Most Represented Species in Musanze City The PiedCrow (Corvus albus) was the most common species inMusanze and seemed to be the most adapted to human-dominated landscapes (Figure 7) For instance unlike many

10 The Scientific World Journal

other bird species in the area the Pied Crow was observedclose to many human facilities such food markets abattoirswastelands domestic yards and croplands In addition thePied Crow was found in high abundance where its foodsources including small reptiles small mammals grainpeanuts carrion scraps of human food fruits insects andother small invertebrates were most available [9] To a lesserextent the urban habitat appeared to favor the Grey-headedSparrow (Passer griseus) The occurrence of the Grey-headedSparrow was associated with open woodlands and humansettlements where this species can easily access required foodand habitat resources The third most represented specieswas the Streaky Seedeater (Serinus striolatus) which is acommon bird of highlands and is generally found above1300m in gardens and cultivated areas woodland edgesheath and scrub vegetation areas The Streaky Seedeateris therefore adept at living in human altered landscapeswhich is not unlike the Black Kite (Milvus migrans) whichwas also common to densely human-populated areas Thesehuman-used landscapes are also a popular habitat of theBlackKitersquos prey which includes small birds bats and rodents Inparticular our study revealed the common occurrence of theBlack Kite circling near the abattoir and scavenging in thecityrsquos wastelands

43 Feeding Guild Categories

431 Feeding Guild Categories by Macrolandscape TypesSeed-eating birds were the best represented guild inMusanze(Figure 8) This may be partially due to the fact that datacollection was completed during a maize-harvesting periodDuring this period urban fields have an exceptionally largeabundance of seeds that can be exploited by birds and mayhave therefore selectively attracted seed-eating species [34]It was also observed that seed-eating species fed from arange of fruits According to Holland and DeAngelis [35]this habit allows seed-eating species to contribute to plantreproduction through pollination Insectivorous species werealso prominent in Musanzersquos urban landscapes Similarly tothe findings of Austin and Smith [5] insectivores were mostabundant in insect-rich landscapes including streamsideareas forests and informal settlements

432 FeedingGuild Categories byMicrolandscapes Althoughseedeaters especially the Grey-headed Sparrow (Passergriseus) dominated almost all microlandscapes it is impor-tant to consider that in wastelands scavengers were the mostabundant (Figure 13) This finding is likely due to the factthat different microlandscapes aremore appropriate for somespecies more than others especially those with differentfeeding habits

Our study confirms that bird species found in Musanzecity like urban-living bird species in other cities contributeto biomass recycling [36] Interestingly although there wereonly a few species of scavenging birds in Musanze theirabundance was high enough to compensate for their lowspecies richness in order to make a notable biomass recyclingimpact to city dwellersThis was particularly true for the Pied

Figure 13 Abundance of Pied Crows in a landfill within Musanzecity (Photo Author 2012)

Crow (Corvus albus) a species whose abundance amountedto more than seven times the average number of individualsper species whichwas almost 10of the total number of birdsobserved

44 Species Diversity

441 Alpha Diversity The bird diversity found in built-up areas was comparable to the bird diversity in urbanopen fields in Musanze city (Figure 9(a)) This finding pro-vides support for the increasingly recognized idea that birddiversity in urban areas can be as high as that in naturalenvironments [37 38] Previous research suggests that thismay be due to a relatively high number of nonnative speciespresent in cities as well as the heterogeneous habitat thaturban landscapes provide [39] which was not supportedin this study perhaps because of close proximity of thestudy area to a network of natural environments (PNVGishwati forest and Buhanga eco-park Rugezi Mukungwaand Bihinga wetlands and Karago Bulera and Ruhondolakes) Moreover Luck [40] suggested that there is a positivecorrelation between human population density and birdspecies richness This relationship was demonstrated in ourstudy as species such as the Pied Crowwere found to bemostabundant throughout urban landscapes and therefore welladapted to an environment where high human densities existInterestingly even the Albertine Rift endemic species theRuwenzori Double-collared Sunbird was sighted foraging inhuman populated areas on garden plants

Overall residential neighborhoods institutionalgrounds and informal settlements can be considered asthe major bird hotspots in Musanze city (Figure 9(b)) Thesethree landscapes share a great floristic diversity providingmany important stimuli for bird life (such as fruits seedsnectar domestic residues insects small mammals reptilesand amphibians) [30] Finally contrary to rural areas andnatural forests that undergo seasonal shortages of resources[3] cities do not experience strong seasonal variation due toa continuous supply of recourses from remote areas

442 Species Similarity The macrolandscapes all appearedto have similar bird species composition which may bedue to landscape heterogeneity [39] This heterogeneity islikely a result of the lack of historical professional landscapeplanning and design leaving a mosaic landscape structure inboth built-up and open fields instead of a uniform landscapespecialization Our results suggest that residential areas and

The Scientific World Journal 11

informal settlements were the most similar in terms ofspecies composition These landscapes ultimately functionto host family life The only difference between residentialareas and informal settlements resides in their socioeconomicstatus which is reflected in the landscape structure Howeverboth landscapes are more similar to each other than toother landscapes Furthermore the species composition ofcemeteries was similar to both forests and some of the built-up microlandscapes which may be attributed to the fact thatthese areas are all surrounded by trees Additionally ceme-teries are characterized by low human disturbance whichmay compare to that of forests and some urban landscapesThese landscapes all harbor a wide variety of floweringplants which in the case of cemeteries are mainly plantedby bereaved ones Moreover the vegetation of graveyardsincludes a range of regeneration stages resulting in a widerange of habitats from the vegetation-free areas of newly duggraves to the reconstructed thickets around old graves [41]Finally riverside landscapes emerged as the most specializedlandscape type as expected with many distinctive speciesobserved in this landscape only Almost all the species foundin riverside areas were specialists of wetlands and were notfound elsewhere As a result it was the most dissimilar to allother microlandscapes

The high degree of similarity in terms of bird diversitybetween Musanze city and the protected natural habitatsnearby provide further support that wildlife does not exclu-sively inhabit protected areas [33 37 42] Although the twonatural habitats are at eight km from Musanze city morethan half of the species found in the city were also found inVPN The lower degree of similarity between Musanze andBuhanga eco-park may be linked to the relative geographiclocation of the two sites as Musanze city is almost half waybetween the two protected areas This finding may also beattributed to the fact that the diversity ofmicrohabitats withinBuhanga eco-park is lower than that of Musanze and VPN[13] which may be due to the relatively small size of Buhangaeco-park Interestingly the species found in more than onelandscape type were also recorded both inside and beyondthe city limits Conversely Ficedula albicollis was recorded inonly one landscape type (cemeteries) and was absent in bothPNV and Buhanga eco-park

5 Conclusions

This study contributes to the knowledge of bird diversity inurban landscapes and provides the most recent status of birddiversity in Musanze city Our findings confirm that birddiversity in urban areas such as a densely populated city canbe as great as that in surrounding natural forests Specificallythe total number of bird species in Musanze city was verysimilar to that of the nearest protected forests VolcanoesNational Park and Buhanga eco-park Endemic and migra-tory birdswere also found inMusanze cityOneAlbertine Riftendemic bird species the Ruwenzori Double-collared Sun-bird was observed in Musanze during this study which hasnot been previously recorded Similarly threemigratory birdswere found inMusanze region for the first time the Common

Sandpiper the Spotted Flycatcher and theWillowWarbler Inaddition two bird species were observed that have not beenpreviously reported in Rwanda the Garden Warbler (Sylviaborin) and the Lesser Spotted Eagle (Aquila pomarina) Theeffect of landscape types on bird species richness and relativeabundance was also illustrated Residential neighborhoodsinstitutional grounds and informal settlements had thehighest species diversity indices and rankabundance relativeto the rest of the microlandscapes in this study Riversidelandscapes emerged with the most specialized bird faunaincluding species that are restricted to wetland environmentsand water bodies This study confirmed that scavengers inMusanze city contribute more to biomass recycling than anyother bird feeding groups Our study provides a current anduseful reference for urban decision makers and confirms theexistence of a great diversity of wildlife within cities Wesuggest that the development and implementation of cityland-use plans should consider this biodiversity especiallywhen villages and cities are in close proximity of protectedareas or natural reserves Finally it may be important thatbotanical gardens and public parks are included in themasterplan of the city as our study indicates that their designrequires an understanding of biodiversity in particular ofavian populations

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors acknowledge technical support from staffat DFGFI-Karisoke Research Center namely Dr WinnieEckardt Mr Deogratias Tuyisingize Mr Emmanuel Faidaand Mrs Keiko Mori

References

[1] S R Loss M O Ruiz and J D Brawn ldquoRelationships betweenavian diversity neighborhood age income and environmentalcharacteristics of an urban landscaperdquo Biological Conservationvol 142 no 11 pp 2578ndash2585 2009

[2] K L Evans D E Chamberlain B J Hatchwell R D Gregoryand K J Gaston ldquoWhat makes an urban birdrdquo Global ChangeBiology vol 17 no 1 pp 32ndash44 2011

[3] S Bolwig D Pomeroy H Tushabe and D Mushabe ldquoCropstrees and birds biodiversity change under agricultural inten-sification in Ugandas farmed landscapesrdquo Danish Journal ofGeography vol 106 no 2 pp 115ndash130 2006

[4] J Hitchmough and N Dunnett ldquoIntroduction to naturalisticplanting in urban landscapesrdquo in The Dynamic LandscapeJ Hitchmough and N Dunnatt Eds pp 1ndash32 Spon PressLondon UK 2004

[5] G T Austin and E L Smith ldquoWinter foraging ecology of mixedinsectivorous bird flocks in oakwoodland in southernArizonardquoThe Condor vol 74 pp 17ndash24 1972

[6] B R Coppedge D M Engle R E Masters and M S GregoryldquoAvian response to landscape change in fragmented southern

12 The Scientific World Journal

great plains grasslandsrdquo Ecological Applications vol 11 no 1 pp47ndash59 2001

[7] K L Evans S E Newson and K J Gaston ldquoHabitat influenceson urban avian assemblagesrdquo Ibis vol 151 no 1 pp 19ndash39 2009

[8] MW Strohbach D Haase and N Kabisch ldquoBirds and the cityUrban biodiversity land use and socioeconomicsrdquo Ecology andSociety vol 14 no 2 pp 31ndash45 2009

[9] T Stevenson and J Fanshawe Field Guide to the Birds of EastAfrica Kenya Tanzania Uganda Rwanda Burundi T amp A DPoyser London UK 2002

[10] J Mistry A Berardi and M Simpson ldquoBirds as indicators ofwetland status and change in the North Rupununi GuyanardquoBiodiversity and Conservation vol 17 no 10 pp 2383ndash24092008

[11] H Slabbekoorn and E A P Ripmeester ldquoBirdsong and anthro-pogenic noise implications and applications for conservationrdquoMolecular Ecology vol 17 no 1 pp 72ndash83 2008

[12] W S Judd C S Campbell E A Kellogg P F Stevens andM JDonoghue Plant Systematics A Phylogenetic Approach SinauerAssociates Sunderland Mass USA 3rd edition 2008

[13] W Weber ldquoRuhengeri and its resources an environmentalprofile of the Ruhengeri prefecturerdquo ETMAUSAID KigaliRwanda

[14] E Sabuhoro and G Bush ldquoThe Dian Fossey Gorilla FundInternationalPADGEF Assessing the Benefit Stream fromIllegal Activities in the Parc National des Volcansrdquo TargetingCommunity Conservation Interventions Musanze Rwanda2008

[15] J C Sano Urban Environmental Infrastructure in Kigali CityRwanda Challenges and Opportunities for Modernized Decen-tralized Sanitation Systems in Poor Neighborhoods WageningenUniversity Wageningen The Netherlands 2007

[16] R J Staniforth ldquoEffects of urbanization on bird populations inthe Canadian Central Arcticrdquo Arctic vol 55 no 1 pp 87ndash932002

[17] DWGibbons andRD Gregory ldquoBirdsrdquo in Ecological CensusesTechniques W L Sutherland Ed pp 308ndash350 CambridgeUniversity 2nd edition 2006

[18] D H Johnson ldquoPoint counts of birds what are we estimatingrdquoTech Rep PSW-GTR-149 USDA Forest Service 1995

[19] A Haslem and A F Bennett ldquoBirds in agricultural mosaics theinfluence of landscape pattern and countryside heterogeneityrdquoEcological Applications vol 18 no 1 pp 185ndash196 2008

[20] M L Rurangwa Feeding Ecology of Albertine Rift Endemic Birdsin the Volcanoes National Park Regal Sunbird Rwenzori Double-Collared Sunbird and Rwenzori Turako National University ofRwanda 2011

[21] R B Arellano-Valle H Bolfarine and V H Lachos ldquoSkew-normal linear mixedmodelsrdquo Journal of Data Science vol 3 pp415ndash438 2005

[22] D Bates Fitting LinearMixedModels in RTheNewsletter of theR Project Volume 51 University of Wisconsin Madison WisUSA 2005

[23] A E Magurran Measuring Biological Diversity Blackwell Sci-ence Malden Mass USA 2004

[24] D Tuyisingize and K Fawcett ldquoThe common bird distributionin the Parc National des Volcans and its surrounding patternsconservation and future challengesrdquo DFGF Technical Report2011

[25] A T Peterson and N A Slade ldquoExtrapolating inventory resultsinto biodiversity estimates and the importance of stoppingrulesrdquoDiversity and Distributions vol 4 no 3 pp 95ndash105 1998

[26] M Salek J Svobodova and P Zasadil ldquoEdge effect of low-trafficforest roads on bird communities in secondary productionforests in central Europerdquo Landscape Ecology vol 25 no 7 pp1113ndash1124 2010

[27] S Murererehe ldquoCollecte et analyse de donnees pourlrsquoamenagement durable des forets -Joindre les efforts nationauxet internationaux Etat des ressources forestieres au RwandardquoTech Rep FAO Rome Italy 2000

[28] S J Nsengimana M Ndimukaga L Gakwerere et al ldquoBiodi-versity surveyrdquo Tech Rep Rufford Small Grant FoundationLondon UK 2009

[29] C Nsabagasani ldquoA Migratory Species African Pitta ldquoPittaangolensisrdquo passed Buhanga relict forestrdquo Backbone vol 17 pp6ndash8 2008

[30] J Jokimaki and M Kaisanlahti-Jokimaki ldquoThe role of residen-tial habitat type on the temporal variation of wintering birdassemblages in northern Finlandrdquo Ornis Fennica vol 88 2011

[31] T M Bergin L B Best K E Freemark and K J KoehlerldquoEffects of landscape structure on nest predation in roadsides ofa midwestern agroecosystem a multiscale analysisrdquo LandscapeEcology vol 15 no 2 pp 131ndash143 2000

[32] T Koellner AMHersperger andTWohlgemuth ldquoRarefactionmethod for assessing plant species diversity on a regional scalerdquoEcography vol 27 no 4 pp 532ndash544 2004

[33] S H Faeth P S Warren E Shochat and W A MarussichldquoTrophic dynamics in urban communitiesrdquo BioScience vol 55no 5 pp 399ndash407 2005

[34] R J Fuller and J D Wilson ldquoThe ecology of seed-eating birdsin relation to agricultural practices current research and futuredirectionsrdquo British Trust for Ornithology Research Report no149 1995

[35] J N Holland andD L DeAngelis ldquoEcological and evolutionaryconditions for fruit abortion to regulate pollinating seed-eaters and increase plant reproductionrdquo Theoretical PopulationBiology vol 61 no 3 pp 251ndash263 2002

[36] C J Whelan D G Wenny and R J Marquis ldquoEcosystemservices provided by birdsrdquo Annals of the New York Academyof Sciences vol 1134 pp 25ndash60 2008

[37] O Gilbert The Ecology of Urban Habitats Chapman amp HallLondon UK 1989

[38] A Millard ldquoSemi-natural vegetation and its relationship todesignated urban green space at the landscape scale in LeedsUKrdquo Landscape Ecology vol 23 no 10 pp 1231ndash1241 2008

[39] I Kowarik ldquoOn the role of alien species in urban flora andvegetationrdquo in Plant Invasions General Aspects and SpecialProblems P Pysek K Prach M Rejmanek and M WadeEds pp 85ndash103 SPB Academic Publishing Amsterdam TheNetherlands 1995

[40] G W Luck ldquoA review of the relationships between humanpopulation density and biodiversityrdquo Biological Reviews vol 82no 4 pp 607ndash645 2007

[41] Victorian Government Department of Sustainability and Envi-ronment (VGDSE) Managing Native Vegetation in VictorianCemeteries Victorian Government Department of Sustainabil-ity and Environment Melbourne Australia 2009

[42] C Dowd ldquoEffect of development on bird species compositionof two urban forested wetlands in Staten Island New YorkrdquoJournal of Field Ornithology vol 63 no 4 pp 455ndash461 1992

Page 8: Bird Diversity and Distribution in relation to Urban Landscape Types in Northern Rwanda · 2016. 1. 26. · ResearchArticle Bird Diversity and Distribution in relation to Urban Landscape

8 The Scientific World Journal

RSWLSSISRNIGFTAFCMBCAM

1000 50

Similarity ()

Bray-Curtis cluster analysis (single link)

Figure 11 Species composition-based microlandscape clusters(AM aerodrome AG agrofields BC business centers CM ceme-teries FT forests IS informal settlements IG institutional groundsRN residential neighborhoods RS riversides SS streamside WLwasteland)

1000 50

Similarity ()

Bray-Curtis cluster analysis (single link)

PNV

Musanze

Buhanga

Figure 12 Musanze city PNV and Buhanga eco-park bird speciescomposition

informal settlements forests business centers and residentialneighborhoods

The majority of species in Musanze city were nativesuch that exotic bird species accounted for only 43 of thetotal number of bird species observed (Ficedula albicollisPloceus cucullatus Serinus canicollis and Serinus citrinel-loides) (Table 5) Up to 64 of the species observed hadno breeding opportunities within the study area (Actitishypoleucos Aquila pomarina Merops apiaster Muscicapastriata Phylloscopus trochilus and Sylvia borin)

4 Discussion

Our study of bird diversity in Musanze city has revealed thatcurrent wildlife conservation efforts do not coincide withareas of the highest bird abundance and species diversitywhich exist in urban areas Bird species richness in theurban areas of Musanze is greater than that of Buhangaeco-park and similar to that of the PNV two surroundingnatural habitats that are currently receiving the majority ofconservation efforts Furthermore species of high ecologicalimportance and therefore high conservation concern such

as endemic and migratory species were recorded across thecity landscapesThis study therefore indicates the importanceof protecting not only the natural habitats of native wildlifebut also urban areas where birds in particular are morecommonly existing

41 Species Richness The unique endemic species found inMusanze city the Ruwenzori Double-collared Sunbird haspreviously been observed in the VPN This species is knownto live in the high altitude habitats of the Albertine Rift[24] It is therefore not surprising that it was found in urbanlandscapes ofMusanze city which is located at a high altitudeof 1850m [26] Stevenson and Fanshawe [9] suggest thatthe sunbirdrsquos most preferred habitats are flowering bushes offorest edges and it may be unusual that the endemic specieswas observed foraging onMarkhamia lutea trees within openfields of Musanze city in this study Our study suggests thatthe species distribution of the Ruwenzori Double-collaredSunbird is not restricted to its natural habitat in the AlbertineRift as it can also exist in urban landscapesThis species maytherefore be able to adapt to human-dominated landscapesand it is likely that it may forage on vegetation such as urbangarden trees Our study suggests that the sunbird is capableof adapting its feeding preferences to the available plants incity landscapes potentially as a response to loss of its naturalhabitat caused by park reductions [27]

The seven migrant bird species found in the studysite were regular September-April visitors from Palearcticregions Two of them the Red-chested Cuckoo (Cucu-lus solitarius) and the European Bee-eater (Merops api-aster) had previously been sighted in the gallery forestsof the Rwandanrsquos Eastern Province [28] and in the PNV[24] The Common Sandpiper Spotted Flycatcher andWillow Warbler have also been reported to visit Rwanda(httpwwwrwandabirdingorg 02092012) and Musanzecity but have never been sighted in the Lava Plain or inthe Volcano Range of Rwanda The remaining two migrantsthe Garden Warbler (Sylvia borin) and the Lesser SpottedEagle (Aquila pomarina) have been reported in Rwandafor the first time as a result of this study Importantly theseven migrant species have never been reported to occurin urban environments of Rwanda and only two had beenreported to visit its highlands [24] However the AfricanPitta (Pitta angolensis) which is an intra-African breedingmigrant bird sighted in the Buhanga eco-park in 2006 and2008 [29] was not recorded in this study The findings of ourstudy encourage the development of bird watching activitiesin Musanze city which may be of particular interest tointernational tourists due to the high number of urban-livingand therefore easily observed unique bird species

411 Number of Species by Macrolandscape Types Thehypothesis that bird species inhabit open fields more thanbuilt-up areas was not supported in this study This maybe due to the fact that some built-up areas including insti-tutional grounds residential neighborhoods and informalsettlements are specifically designed with plant communi-ties to attract birds [30] These communities often include

The Scientific World Journal 9

Table 4 Migratory birds in Musanze city PNV and Buhanga eco-park

Common name Scientific name Musanze city Protected areasPNV Buhanga eco-park

Common Sandpiper Actitis hypoleucos

European Bee-eater Merops apiaster

Garden Warbler Sylvia borin

Lesser-spotted Eagle Aquila pomarina

Red-chested Cuckoo Cuculus solitarius

Spotted Flycatcher Muscicapa striata

WillowWarbler Phylloscopus trochilus

Table 5 Exotic birds in Musanze city PNV and Buhanga eco-park

Common name Scientific name Musanze city Protected areasPNV Buhanga eco-park

Collared Flycatcher Ficedula albicollis

Black-headed Weaver Ploceus cucullatus

Yellow-crowned Canary Serinus canicollis

Abyssinian Citril Serinus citrinelloides

a number of trees with a substantial canopy as well asornamental plants such as vegetation that exists as bushesAlternatively some microlandscapes within open fields havea low number of species such as the Musanze aerodromewhich is a grassland habitat and is regularly maintained tofacilitate airplane landing This habitat offers little feedingopportunities to wildlife and is an unsuitable habitat for mostbird species as it may for instance expose small-sized birdsto predators [31]

412 Number of Species by Microlandscape Types In supportof Koellner et al [32] different landscapes in Musanze werecorrelated with differences in bird species richness Theinstitutional grounds had a relatively high species richnessperhaps due to a high variety of plant assemblages Simi-larly the high number of bird species found in residentialneighborhoods and informal settlements can be explained bythe diversity of plant resources in these areas These plantresources include nectar-producing flowers such as bananaplants that attract sunbirds fruit-bearing trees and shrubssuch as guava plants that frugivorous species can feed on Inaddition the high concentrations of domestic wastes (such asresidues food disposable and waste-water) in the homesteadenvironment offer a unique opportunity to predators suchas insectivorous birds that feed on small mammals (egmice frogs) and insects (eg flies mosquitoes) and arecommon to this type of microhabitats Domestic waste mayalso attract scavenger species Finally informal settlementsthat are surrounded by a mosaic of vegetation types offermany opportunities for bird foraging and nesting [30] Thisdiversity in urban landscape vegetation structure and typemay therefore reflect the vast diversity of bird species in urbanareas which has not previously been investigated in Rwanda

42 Species Relative Abundance

421 Number of Individuals by Macrolandscape Types Thenonsignificant effect of macrolandscapes on the total numberof birds in an area may be linked to the fact that landscapetype had no significant influence on bird species richnessMore importantly due to the historical nonformal nature ofurban design in Musanze both macrolandscapes appeared tohave similar types and levels of bird-exploitable resourcesincluding appropriate plant coverage and sites for birds tonest [33]

422 Number of Individuals byMicrolandscape Types Ceme-teries riverside landscapes and wastelands did not differin the total number of birds in comparison to residentialneighborhoods (Table 3) This may be attributed to the factthat these four landscapes appear to be intrinsically hetero-geneous suggesting that there may be possible confoundingfactors that have overshadowed the expected relationshipbetween microlandscapes and relative bird abundance Forinstance wastelands attract many scavengers and raptorscemeteries and agrofields provide appropriate plant assem-blages for seed eaters and riversides offer easy water accessand shelter for aquatic bird species [4] Therefore theabundance of birds across the different microlandscapes ofMusanze is relatively uniform due to the fact that eachlandscape offers a range of suitable habitats for a range of birdspecies

423 Most Represented Species in Musanze City The PiedCrow (Corvus albus) was the most common species inMusanze and seemed to be the most adapted to human-dominated landscapes (Figure 7) For instance unlike many

10 The Scientific World Journal

other bird species in the area the Pied Crow was observedclose to many human facilities such food markets abattoirswastelands domestic yards and croplands In addition thePied Crow was found in high abundance where its foodsources including small reptiles small mammals grainpeanuts carrion scraps of human food fruits insects andother small invertebrates were most available [9] To a lesserextent the urban habitat appeared to favor the Grey-headedSparrow (Passer griseus) The occurrence of the Grey-headedSparrow was associated with open woodlands and humansettlements where this species can easily access required foodand habitat resources The third most represented specieswas the Streaky Seedeater (Serinus striolatus) which is acommon bird of highlands and is generally found above1300m in gardens and cultivated areas woodland edgesheath and scrub vegetation areas The Streaky Seedeateris therefore adept at living in human altered landscapeswhich is not unlike the Black Kite (Milvus migrans) whichwas also common to densely human-populated areas Thesehuman-used landscapes are also a popular habitat of theBlackKitersquos prey which includes small birds bats and rodents Inparticular our study revealed the common occurrence of theBlack Kite circling near the abattoir and scavenging in thecityrsquos wastelands

43 Feeding Guild Categories

431 Feeding Guild Categories by Macrolandscape TypesSeed-eating birds were the best represented guild inMusanze(Figure 8) This may be partially due to the fact that datacollection was completed during a maize-harvesting periodDuring this period urban fields have an exceptionally largeabundance of seeds that can be exploited by birds and mayhave therefore selectively attracted seed-eating species [34]It was also observed that seed-eating species fed from arange of fruits According to Holland and DeAngelis [35]this habit allows seed-eating species to contribute to plantreproduction through pollination Insectivorous species werealso prominent in Musanzersquos urban landscapes Similarly tothe findings of Austin and Smith [5] insectivores were mostabundant in insect-rich landscapes including streamsideareas forests and informal settlements

432 FeedingGuild Categories byMicrolandscapes Althoughseedeaters especially the Grey-headed Sparrow (Passergriseus) dominated almost all microlandscapes it is impor-tant to consider that in wastelands scavengers were the mostabundant (Figure 13) This finding is likely due to the factthat different microlandscapes aremore appropriate for somespecies more than others especially those with differentfeeding habits

Our study confirms that bird species found in Musanzecity like urban-living bird species in other cities contributeto biomass recycling [36] Interestingly although there wereonly a few species of scavenging birds in Musanze theirabundance was high enough to compensate for their lowspecies richness in order to make a notable biomass recyclingimpact to city dwellersThis was particularly true for the Pied

Figure 13 Abundance of Pied Crows in a landfill within Musanzecity (Photo Author 2012)

Crow (Corvus albus) a species whose abundance amountedto more than seven times the average number of individualsper species whichwas almost 10of the total number of birdsobserved

44 Species Diversity

441 Alpha Diversity The bird diversity found in built-up areas was comparable to the bird diversity in urbanopen fields in Musanze city (Figure 9(a)) This finding pro-vides support for the increasingly recognized idea that birddiversity in urban areas can be as high as that in naturalenvironments [37 38] Previous research suggests that thismay be due to a relatively high number of nonnative speciespresent in cities as well as the heterogeneous habitat thaturban landscapes provide [39] which was not supportedin this study perhaps because of close proximity of thestudy area to a network of natural environments (PNVGishwati forest and Buhanga eco-park Rugezi Mukungwaand Bihinga wetlands and Karago Bulera and Ruhondolakes) Moreover Luck [40] suggested that there is a positivecorrelation between human population density and birdspecies richness This relationship was demonstrated in ourstudy as species such as the Pied Crowwere found to bemostabundant throughout urban landscapes and therefore welladapted to an environment where high human densities existInterestingly even the Albertine Rift endemic species theRuwenzori Double-collared Sunbird was sighted foraging inhuman populated areas on garden plants

Overall residential neighborhoods institutionalgrounds and informal settlements can be considered asthe major bird hotspots in Musanze city (Figure 9(b)) Thesethree landscapes share a great floristic diversity providingmany important stimuli for bird life (such as fruits seedsnectar domestic residues insects small mammals reptilesand amphibians) [30] Finally contrary to rural areas andnatural forests that undergo seasonal shortages of resources[3] cities do not experience strong seasonal variation due toa continuous supply of recourses from remote areas

442 Species Similarity The macrolandscapes all appearedto have similar bird species composition which may bedue to landscape heterogeneity [39] This heterogeneity islikely a result of the lack of historical professional landscapeplanning and design leaving a mosaic landscape structure inboth built-up and open fields instead of a uniform landscapespecialization Our results suggest that residential areas and

The Scientific World Journal 11

informal settlements were the most similar in terms ofspecies composition These landscapes ultimately functionto host family life The only difference between residentialareas and informal settlements resides in their socioeconomicstatus which is reflected in the landscape structure Howeverboth landscapes are more similar to each other than toother landscapes Furthermore the species composition ofcemeteries was similar to both forests and some of the built-up microlandscapes which may be attributed to the fact thatthese areas are all surrounded by trees Additionally ceme-teries are characterized by low human disturbance whichmay compare to that of forests and some urban landscapesThese landscapes all harbor a wide variety of floweringplants which in the case of cemeteries are mainly plantedby bereaved ones Moreover the vegetation of graveyardsincludes a range of regeneration stages resulting in a widerange of habitats from the vegetation-free areas of newly duggraves to the reconstructed thickets around old graves [41]Finally riverside landscapes emerged as the most specializedlandscape type as expected with many distinctive speciesobserved in this landscape only Almost all the species foundin riverside areas were specialists of wetlands and were notfound elsewhere As a result it was the most dissimilar to allother microlandscapes

The high degree of similarity in terms of bird diversitybetween Musanze city and the protected natural habitatsnearby provide further support that wildlife does not exclu-sively inhabit protected areas [33 37 42] Although the twonatural habitats are at eight km from Musanze city morethan half of the species found in the city were also found inVPN The lower degree of similarity between Musanze andBuhanga eco-park may be linked to the relative geographiclocation of the two sites as Musanze city is almost half waybetween the two protected areas This finding may also beattributed to the fact that the diversity ofmicrohabitats withinBuhanga eco-park is lower than that of Musanze and VPN[13] which may be due to the relatively small size of Buhangaeco-park Interestingly the species found in more than onelandscape type were also recorded both inside and beyondthe city limits Conversely Ficedula albicollis was recorded inonly one landscape type (cemeteries) and was absent in bothPNV and Buhanga eco-park

5 Conclusions

This study contributes to the knowledge of bird diversity inurban landscapes and provides the most recent status of birddiversity in Musanze city Our findings confirm that birddiversity in urban areas such as a densely populated city canbe as great as that in surrounding natural forests Specificallythe total number of bird species in Musanze city was verysimilar to that of the nearest protected forests VolcanoesNational Park and Buhanga eco-park Endemic and migra-tory birdswere also found inMusanze cityOneAlbertine Riftendemic bird species the Ruwenzori Double-collared Sun-bird was observed in Musanze during this study which hasnot been previously recorded Similarly threemigratory birdswere found inMusanze region for the first time the Common

Sandpiper the Spotted Flycatcher and theWillowWarbler Inaddition two bird species were observed that have not beenpreviously reported in Rwanda the Garden Warbler (Sylviaborin) and the Lesser Spotted Eagle (Aquila pomarina) Theeffect of landscape types on bird species richness and relativeabundance was also illustrated Residential neighborhoodsinstitutional grounds and informal settlements had thehighest species diversity indices and rankabundance relativeto the rest of the microlandscapes in this study Riversidelandscapes emerged with the most specialized bird faunaincluding species that are restricted to wetland environmentsand water bodies This study confirmed that scavengers inMusanze city contribute more to biomass recycling than anyother bird feeding groups Our study provides a current anduseful reference for urban decision makers and confirms theexistence of a great diversity of wildlife within cities Wesuggest that the development and implementation of cityland-use plans should consider this biodiversity especiallywhen villages and cities are in close proximity of protectedareas or natural reserves Finally it may be important thatbotanical gardens and public parks are included in themasterplan of the city as our study indicates that their designrequires an understanding of biodiversity in particular ofavian populations

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors acknowledge technical support from staffat DFGFI-Karisoke Research Center namely Dr WinnieEckardt Mr Deogratias Tuyisingize Mr Emmanuel Faidaand Mrs Keiko Mori

References

[1] S R Loss M O Ruiz and J D Brawn ldquoRelationships betweenavian diversity neighborhood age income and environmentalcharacteristics of an urban landscaperdquo Biological Conservationvol 142 no 11 pp 2578ndash2585 2009

[2] K L Evans D E Chamberlain B J Hatchwell R D Gregoryand K J Gaston ldquoWhat makes an urban birdrdquo Global ChangeBiology vol 17 no 1 pp 32ndash44 2011

[3] S Bolwig D Pomeroy H Tushabe and D Mushabe ldquoCropstrees and birds biodiversity change under agricultural inten-sification in Ugandas farmed landscapesrdquo Danish Journal ofGeography vol 106 no 2 pp 115ndash130 2006

[4] J Hitchmough and N Dunnett ldquoIntroduction to naturalisticplanting in urban landscapesrdquo in The Dynamic LandscapeJ Hitchmough and N Dunnatt Eds pp 1ndash32 Spon PressLondon UK 2004

[5] G T Austin and E L Smith ldquoWinter foraging ecology of mixedinsectivorous bird flocks in oakwoodland in southernArizonardquoThe Condor vol 74 pp 17ndash24 1972

[6] B R Coppedge D M Engle R E Masters and M S GregoryldquoAvian response to landscape change in fragmented southern

12 The Scientific World Journal

great plains grasslandsrdquo Ecological Applications vol 11 no 1 pp47ndash59 2001

[7] K L Evans S E Newson and K J Gaston ldquoHabitat influenceson urban avian assemblagesrdquo Ibis vol 151 no 1 pp 19ndash39 2009

[8] MW Strohbach D Haase and N Kabisch ldquoBirds and the cityUrban biodiversity land use and socioeconomicsrdquo Ecology andSociety vol 14 no 2 pp 31ndash45 2009

[9] T Stevenson and J Fanshawe Field Guide to the Birds of EastAfrica Kenya Tanzania Uganda Rwanda Burundi T amp A DPoyser London UK 2002

[10] J Mistry A Berardi and M Simpson ldquoBirds as indicators ofwetland status and change in the North Rupununi GuyanardquoBiodiversity and Conservation vol 17 no 10 pp 2383ndash24092008

[11] H Slabbekoorn and E A P Ripmeester ldquoBirdsong and anthro-pogenic noise implications and applications for conservationrdquoMolecular Ecology vol 17 no 1 pp 72ndash83 2008

[12] W S Judd C S Campbell E A Kellogg P F Stevens andM JDonoghue Plant Systematics A Phylogenetic Approach SinauerAssociates Sunderland Mass USA 3rd edition 2008

[13] W Weber ldquoRuhengeri and its resources an environmentalprofile of the Ruhengeri prefecturerdquo ETMAUSAID KigaliRwanda

[14] E Sabuhoro and G Bush ldquoThe Dian Fossey Gorilla FundInternationalPADGEF Assessing the Benefit Stream fromIllegal Activities in the Parc National des Volcansrdquo TargetingCommunity Conservation Interventions Musanze Rwanda2008

[15] J C Sano Urban Environmental Infrastructure in Kigali CityRwanda Challenges and Opportunities for Modernized Decen-tralized Sanitation Systems in Poor Neighborhoods WageningenUniversity Wageningen The Netherlands 2007

[16] R J Staniforth ldquoEffects of urbanization on bird populations inthe Canadian Central Arcticrdquo Arctic vol 55 no 1 pp 87ndash932002

[17] DWGibbons andRD Gregory ldquoBirdsrdquo in Ecological CensusesTechniques W L Sutherland Ed pp 308ndash350 CambridgeUniversity 2nd edition 2006

[18] D H Johnson ldquoPoint counts of birds what are we estimatingrdquoTech Rep PSW-GTR-149 USDA Forest Service 1995

[19] A Haslem and A F Bennett ldquoBirds in agricultural mosaics theinfluence of landscape pattern and countryside heterogeneityrdquoEcological Applications vol 18 no 1 pp 185ndash196 2008

[20] M L Rurangwa Feeding Ecology of Albertine Rift Endemic Birdsin the Volcanoes National Park Regal Sunbird Rwenzori Double-Collared Sunbird and Rwenzori Turako National University ofRwanda 2011

[21] R B Arellano-Valle H Bolfarine and V H Lachos ldquoSkew-normal linear mixedmodelsrdquo Journal of Data Science vol 3 pp415ndash438 2005

[22] D Bates Fitting LinearMixedModels in RTheNewsletter of theR Project Volume 51 University of Wisconsin Madison WisUSA 2005

[23] A E Magurran Measuring Biological Diversity Blackwell Sci-ence Malden Mass USA 2004

[24] D Tuyisingize and K Fawcett ldquoThe common bird distributionin the Parc National des Volcans and its surrounding patternsconservation and future challengesrdquo DFGF Technical Report2011

[25] A T Peterson and N A Slade ldquoExtrapolating inventory resultsinto biodiversity estimates and the importance of stoppingrulesrdquoDiversity and Distributions vol 4 no 3 pp 95ndash105 1998

[26] M Salek J Svobodova and P Zasadil ldquoEdge effect of low-trafficforest roads on bird communities in secondary productionforests in central Europerdquo Landscape Ecology vol 25 no 7 pp1113ndash1124 2010

[27] S Murererehe ldquoCollecte et analyse de donnees pourlrsquoamenagement durable des forets -Joindre les efforts nationauxet internationaux Etat des ressources forestieres au RwandardquoTech Rep FAO Rome Italy 2000

[28] S J Nsengimana M Ndimukaga L Gakwerere et al ldquoBiodi-versity surveyrdquo Tech Rep Rufford Small Grant FoundationLondon UK 2009

[29] C Nsabagasani ldquoA Migratory Species African Pitta ldquoPittaangolensisrdquo passed Buhanga relict forestrdquo Backbone vol 17 pp6ndash8 2008

[30] J Jokimaki and M Kaisanlahti-Jokimaki ldquoThe role of residen-tial habitat type on the temporal variation of wintering birdassemblages in northern Finlandrdquo Ornis Fennica vol 88 2011

[31] T M Bergin L B Best K E Freemark and K J KoehlerldquoEffects of landscape structure on nest predation in roadsides ofa midwestern agroecosystem a multiscale analysisrdquo LandscapeEcology vol 15 no 2 pp 131ndash143 2000

[32] T Koellner AMHersperger andTWohlgemuth ldquoRarefactionmethod for assessing plant species diversity on a regional scalerdquoEcography vol 27 no 4 pp 532ndash544 2004

[33] S H Faeth P S Warren E Shochat and W A MarussichldquoTrophic dynamics in urban communitiesrdquo BioScience vol 55no 5 pp 399ndash407 2005

[34] R J Fuller and J D Wilson ldquoThe ecology of seed-eating birdsin relation to agricultural practices current research and futuredirectionsrdquo British Trust for Ornithology Research Report no149 1995

[35] J N Holland andD L DeAngelis ldquoEcological and evolutionaryconditions for fruit abortion to regulate pollinating seed-eaters and increase plant reproductionrdquo Theoretical PopulationBiology vol 61 no 3 pp 251ndash263 2002

[36] C J Whelan D G Wenny and R J Marquis ldquoEcosystemservices provided by birdsrdquo Annals of the New York Academyof Sciences vol 1134 pp 25ndash60 2008

[37] O Gilbert The Ecology of Urban Habitats Chapman amp HallLondon UK 1989

[38] A Millard ldquoSemi-natural vegetation and its relationship todesignated urban green space at the landscape scale in LeedsUKrdquo Landscape Ecology vol 23 no 10 pp 1231ndash1241 2008

[39] I Kowarik ldquoOn the role of alien species in urban flora andvegetationrdquo in Plant Invasions General Aspects and SpecialProblems P Pysek K Prach M Rejmanek and M WadeEds pp 85ndash103 SPB Academic Publishing Amsterdam TheNetherlands 1995

[40] G W Luck ldquoA review of the relationships between humanpopulation density and biodiversityrdquo Biological Reviews vol 82no 4 pp 607ndash645 2007

[41] Victorian Government Department of Sustainability and Envi-ronment (VGDSE) Managing Native Vegetation in VictorianCemeteries Victorian Government Department of Sustainabil-ity and Environment Melbourne Australia 2009

[42] C Dowd ldquoEffect of development on bird species compositionof two urban forested wetlands in Staten Island New YorkrdquoJournal of Field Ornithology vol 63 no 4 pp 455ndash461 1992

Page 9: Bird Diversity and Distribution in relation to Urban Landscape Types in Northern Rwanda · 2016. 1. 26. · ResearchArticle Bird Diversity and Distribution in relation to Urban Landscape

The Scientific World Journal 9

Table 4 Migratory birds in Musanze city PNV and Buhanga eco-park

Common name Scientific name Musanze city Protected areasPNV Buhanga eco-park

Common Sandpiper Actitis hypoleucos

European Bee-eater Merops apiaster

Garden Warbler Sylvia borin

Lesser-spotted Eagle Aquila pomarina

Red-chested Cuckoo Cuculus solitarius

Spotted Flycatcher Muscicapa striata

WillowWarbler Phylloscopus trochilus

Table 5 Exotic birds in Musanze city PNV and Buhanga eco-park

Common name Scientific name Musanze city Protected areasPNV Buhanga eco-park

Collared Flycatcher Ficedula albicollis

Black-headed Weaver Ploceus cucullatus

Yellow-crowned Canary Serinus canicollis

Abyssinian Citril Serinus citrinelloides

a number of trees with a substantial canopy as well asornamental plants such as vegetation that exists as bushesAlternatively some microlandscapes within open fields havea low number of species such as the Musanze aerodromewhich is a grassland habitat and is regularly maintained tofacilitate airplane landing This habitat offers little feedingopportunities to wildlife and is an unsuitable habitat for mostbird species as it may for instance expose small-sized birdsto predators [31]

412 Number of Species by Microlandscape Types In supportof Koellner et al [32] different landscapes in Musanze werecorrelated with differences in bird species richness Theinstitutional grounds had a relatively high species richnessperhaps due to a high variety of plant assemblages Simi-larly the high number of bird species found in residentialneighborhoods and informal settlements can be explained bythe diversity of plant resources in these areas These plantresources include nectar-producing flowers such as bananaplants that attract sunbirds fruit-bearing trees and shrubssuch as guava plants that frugivorous species can feed on Inaddition the high concentrations of domestic wastes (such asresidues food disposable and waste-water) in the homesteadenvironment offer a unique opportunity to predators suchas insectivorous birds that feed on small mammals (egmice frogs) and insects (eg flies mosquitoes) and arecommon to this type of microhabitats Domestic waste mayalso attract scavenger species Finally informal settlementsthat are surrounded by a mosaic of vegetation types offermany opportunities for bird foraging and nesting [30] Thisdiversity in urban landscape vegetation structure and typemay therefore reflect the vast diversity of bird species in urbanareas which has not previously been investigated in Rwanda

42 Species Relative Abundance

421 Number of Individuals by Macrolandscape Types Thenonsignificant effect of macrolandscapes on the total numberof birds in an area may be linked to the fact that landscapetype had no significant influence on bird species richnessMore importantly due to the historical nonformal nature ofurban design in Musanze both macrolandscapes appeared tohave similar types and levels of bird-exploitable resourcesincluding appropriate plant coverage and sites for birds tonest [33]

422 Number of Individuals byMicrolandscape Types Ceme-teries riverside landscapes and wastelands did not differin the total number of birds in comparison to residentialneighborhoods (Table 3) This may be attributed to the factthat these four landscapes appear to be intrinsically hetero-geneous suggesting that there may be possible confoundingfactors that have overshadowed the expected relationshipbetween microlandscapes and relative bird abundance Forinstance wastelands attract many scavengers and raptorscemeteries and agrofields provide appropriate plant assem-blages for seed eaters and riversides offer easy water accessand shelter for aquatic bird species [4] Therefore theabundance of birds across the different microlandscapes ofMusanze is relatively uniform due to the fact that eachlandscape offers a range of suitable habitats for a range of birdspecies

423 Most Represented Species in Musanze City The PiedCrow (Corvus albus) was the most common species inMusanze and seemed to be the most adapted to human-dominated landscapes (Figure 7) For instance unlike many

10 The Scientific World Journal

other bird species in the area the Pied Crow was observedclose to many human facilities such food markets abattoirswastelands domestic yards and croplands In addition thePied Crow was found in high abundance where its foodsources including small reptiles small mammals grainpeanuts carrion scraps of human food fruits insects andother small invertebrates were most available [9] To a lesserextent the urban habitat appeared to favor the Grey-headedSparrow (Passer griseus) The occurrence of the Grey-headedSparrow was associated with open woodlands and humansettlements where this species can easily access required foodand habitat resources The third most represented specieswas the Streaky Seedeater (Serinus striolatus) which is acommon bird of highlands and is generally found above1300m in gardens and cultivated areas woodland edgesheath and scrub vegetation areas The Streaky Seedeateris therefore adept at living in human altered landscapeswhich is not unlike the Black Kite (Milvus migrans) whichwas also common to densely human-populated areas Thesehuman-used landscapes are also a popular habitat of theBlackKitersquos prey which includes small birds bats and rodents Inparticular our study revealed the common occurrence of theBlack Kite circling near the abattoir and scavenging in thecityrsquos wastelands

43 Feeding Guild Categories

431 Feeding Guild Categories by Macrolandscape TypesSeed-eating birds were the best represented guild inMusanze(Figure 8) This may be partially due to the fact that datacollection was completed during a maize-harvesting periodDuring this period urban fields have an exceptionally largeabundance of seeds that can be exploited by birds and mayhave therefore selectively attracted seed-eating species [34]It was also observed that seed-eating species fed from arange of fruits According to Holland and DeAngelis [35]this habit allows seed-eating species to contribute to plantreproduction through pollination Insectivorous species werealso prominent in Musanzersquos urban landscapes Similarly tothe findings of Austin and Smith [5] insectivores were mostabundant in insect-rich landscapes including streamsideareas forests and informal settlements

432 FeedingGuild Categories byMicrolandscapes Althoughseedeaters especially the Grey-headed Sparrow (Passergriseus) dominated almost all microlandscapes it is impor-tant to consider that in wastelands scavengers were the mostabundant (Figure 13) This finding is likely due to the factthat different microlandscapes aremore appropriate for somespecies more than others especially those with differentfeeding habits

Our study confirms that bird species found in Musanzecity like urban-living bird species in other cities contributeto biomass recycling [36] Interestingly although there wereonly a few species of scavenging birds in Musanze theirabundance was high enough to compensate for their lowspecies richness in order to make a notable biomass recyclingimpact to city dwellersThis was particularly true for the Pied

Figure 13 Abundance of Pied Crows in a landfill within Musanzecity (Photo Author 2012)

Crow (Corvus albus) a species whose abundance amountedto more than seven times the average number of individualsper species whichwas almost 10of the total number of birdsobserved

44 Species Diversity

441 Alpha Diversity The bird diversity found in built-up areas was comparable to the bird diversity in urbanopen fields in Musanze city (Figure 9(a)) This finding pro-vides support for the increasingly recognized idea that birddiversity in urban areas can be as high as that in naturalenvironments [37 38] Previous research suggests that thismay be due to a relatively high number of nonnative speciespresent in cities as well as the heterogeneous habitat thaturban landscapes provide [39] which was not supportedin this study perhaps because of close proximity of thestudy area to a network of natural environments (PNVGishwati forest and Buhanga eco-park Rugezi Mukungwaand Bihinga wetlands and Karago Bulera and Ruhondolakes) Moreover Luck [40] suggested that there is a positivecorrelation between human population density and birdspecies richness This relationship was demonstrated in ourstudy as species such as the Pied Crowwere found to bemostabundant throughout urban landscapes and therefore welladapted to an environment where high human densities existInterestingly even the Albertine Rift endemic species theRuwenzori Double-collared Sunbird was sighted foraging inhuman populated areas on garden plants

Overall residential neighborhoods institutionalgrounds and informal settlements can be considered asthe major bird hotspots in Musanze city (Figure 9(b)) Thesethree landscapes share a great floristic diversity providingmany important stimuli for bird life (such as fruits seedsnectar domestic residues insects small mammals reptilesand amphibians) [30] Finally contrary to rural areas andnatural forests that undergo seasonal shortages of resources[3] cities do not experience strong seasonal variation due toa continuous supply of recourses from remote areas

442 Species Similarity The macrolandscapes all appearedto have similar bird species composition which may bedue to landscape heterogeneity [39] This heterogeneity islikely a result of the lack of historical professional landscapeplanning and design leaving a mosaic landscape structure inboth built-up and open fields instead of a uniform landscapespecialization Our results suggest that residential areas and

The Scientific World Journal 11

informal settlements were the most similar in terms ofspecies composition These landscapes ultimately functionto host family life The only difference between residentialareas and informal settlements resides in their socioeconomicstatus which is reflected in the landscape structure Howeverboth landscapes are more similar to each other than toother landscapes Furthermore the species composition ofcemeteries was similar to both forests and some of the built-up microlandscapes which may be attributed to the fact thatthese areas are all surrounded by trees Additionally ceme-teries are characterized by low human disturbance whichmay compare to that of forests and some urban landscapesThese landscapes all harbor a wide variety of floweringplants which in the case of cemeteries are mainly plantedby bereaved ones Moreover the vegetation of graveyardsincludes a range of regeneration stages resulting in a widerange of habitats from the vegetation-free areas of newly duggraves to the reconstructed thickets around old graves [41]Finally riverside landscapes emerged as the most specializedlandscape type as expected with many distinctive speciesobserved in this landscape only Almost all the species foundin riverside areas were specialists of wetlands and were notfound elsewhere As a result it was the most dissimilar to allother microlandscapes

The high degree of similarity in terms of bird diversitybetween Musanze city and the protected natural habitatsnearby provide further support that wildlife does not exclu-sively inhabit protected areas [33 37 42] Although the twonatural habitats are at eight km from Musanze city morethan half of the species found in the city were also found inVPN The lower degree of similarity between Musanze andBuhanga eco-park may be linked to the relative geographiclocation of the two sites as Musanze city is almost half waybetween the two protected areas This finding may also beattributed to the fact that the diversity ofmicrohabitats withinBuhanga eco-park is lower than that of Musanze and VPN[13] which may be due to the relatively small size of Buhangaeco-park Interestingly the species found in more than onelandscape type were also recorded both inside and beyondthe city limits Conversely Ficedula albicollis was recorded inonly one landscape type (cemeteries) and was absent in bothPNV and Buhanga eco-park

5 Conclusions

This study contributes to the knowledge of bird diversity inurban landscapes and provides the most recent status of birddiversity in Musanze city Our findings confirm that birddiversity in urban areas such as a densely populated city canbe as great as that in surrounding natural forests Specificallythe total number of bird species in Musanze city was verysimilar to that of the nearest protected forests VolcanoesNational Park and Buhanga eco-park Endemic and migra-tory birdswere also found inMusanze cityOneAlbertine Riftendemic bird species the Ruwenzori Double-collared Sun-bird was observed in Musanze during this study which hasnot been previously recorded Similarly threemigratory birdswere found inMusanze region for the first time the Common

Sandpiper the Spotted Flycatcher and theWillowWarbler Inaddition two bird species were observed that have not beenpreviously reported in Rwanda the Garden Warbler (Sylviaborin) and the Lesser Spotted Eagle (Aquila pomarina) Theeffect of landscape types on bird species richness and relativeabundance was also illustrated Residential neighborhoodsinstitutional grounds and informal settlements had thehighest species diversity indices and rankabundance relativeto the rest of the microlandscapes in this study Riversidelandscapes emerged with the most specialized bird faunaincluding species that are restricted to wetland environmentsand water bodies This study confirmed that scavengers inMusanze city contribute more to biomass recycling than anyother bird feeding groups Our study provides a current anduseful reference for urban decision makers and confirms theexistence of a great diversity of wildlife within cities Wesuggest that the development and implementation of cityland-use plans should consider this biodiversity especiallywhen villages and cities are in close proximity of protectedareas or natural reserves Finally it may be important thatbotanical gardens and public parks are included in themasterplan of the city as our study indicates that their designrequires an understanding of biodiversity in particular ofavian populations

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors acknowledge technical support from staffat DFGFI-Karisoke Research Center namely Dr WinnieEckardt Mr Deogratias Tuyisingize Mr Emmanuel Faidaand Mrs Keiko Mori

References

[1] S R Loss M O Ruiz and J D Brawn ldquoRelationships betweenavian diversity neighborhood age income and environmentalcharacteristics of an urban landscaperdquo Biological Conservationvol 142 no 11 pp 2578ndash2585 2009

[2] K L Evans D E Chamberlain B J Hatchwell R D Gregoryand K J Gaston ldquoWhat makes an urban birdrdquo Global ChangeBiology vol 17 no 1 pp 32ndash44 2011

[3] S Bolwig D Pomeroy H Tushabe and D Mushabe ldquoCropstrees and birds biodiversity change under agricultural inten-sification in Ugandas farmed landscapesrdquo Danish Journal ofGeography vol 106 no 2 pp 115ndash130 2006

[4] J Hitchmough and N Dunnett ldquoIntroduction to naturalisticplanting in urban landscapesrdquo in The Dynamic LandscapeJ Hitchmough and N Dunnatt Eds pp 1ndash32 Spon PressLondon UK 2004

[5] G T Austin and E L Smith ldquoWinter foraging ecology of mixedinsectivorous bird flocks in oakwoodland in southernArizonardquoThe Condor vol 74 pp 17ndash24 1972

[6] B R Coppedge D M Engle R E Masters and M S GregoryldquoAvian response to landscape change in fragmented southern

12 The Scientific World Journal

great plains grasslandsrdquo Ecological Applications vol 11 no 1 pp47ndash59 2001

[7] K L Evans S E Newson and K J Gaston ldquoHabitat influenceson urban avian assemblagesrdquo Ibis vol 151 no 1 pp 19ndash39 2009

[8] MW Strohbach D Haase and N Kabisch ldquoBirds and the cityUrban biodiversity land use and socioeconomicsrdquo Ecology andSociety vol 14 no 2 pp 31ndash45 2009

[9] T Stevenson and J Fanshawe Field Guide to the Birds of EastAfrica Kenya Tanzania Uganda Rwanda Burundi T amp A DPoyser London UK 2002

[10] J Mistry A Berardi and M Simpson ldquoBirds as indicators ofwetland status and change in the North Rupununi GuyanardquoBiodiversity and Conservation vol 17 no 10 pp 2383ndash24092008

[11] H Slabbekoorn and E A P Ripmeester ldquoBirdsong and anthro-pogenic noise implications and applications for conservationrdquoMolecular Ecology vol 17 no 1 pp 72ndash83 2008

[12] W S Judd C S Campbell E A Kellogg P F Stevens andM JDonoghue Plant Systematics A Phylogenetic Approach SinauerAssociates Sunderland Mass USA 3rd edition 2008

[13] W Weber ldquoRuhengeri and its resources an environmentalprofile of the Ruhengeri prefecturerdquo ETMAUSAID KigaliRwanda

[14] E Sabuhoro and G Bush ldquoThe Dian Fossey Gorilla FundInternationalPADGEF Assessing the Benefit Stream fromIllegal Activities in the Parc National des Volcansrdquo TargetingCommunity Conservation Interventions Musanze Rwanda2008

[15] J C Sano Urban Environmental Infrastructure in Kigali CityRwanda Challenges and Opportunities for Modernized Decen-tralized Sanitation Systems in Poor Neighborhoods WageningenUniversity Wageningen The Netherlands 2007

[16] R J Staniforth ldquoEffects of urbanization on bird populations inthe Canadian Central Arcticrdquo Arctic vol 55 no 1 pp 87ndash932002

[17] DWGibbons andRD Gregory ldquoBirdsrdquo in Ecological CensusesTechniques W L Sutherland Ed pp 308ndash350 CambridgeUniversity 2nd edition 2006

[18] D H Johnson ldquoPoint counts of birds what are we estimatingrdquoTech Rep PSW-GTR-149 USDA Forest Service 1995

[19] A Haslem and A F Bennett ldquoBirds in agricultural mosaics theinfluence of landscape pattern and countryside heterogeneityrdquoEcological Applications vol 18 no 1 pp 185ndash196 2008

[20] M L Rurangwa Feeding Ecology of Albertine Rift Endemic Birdsin the Volcanoes National Park Regal Sunbird Rwenzori Double-Collared Sunbird and Rwenzori Turako National University ofRwanda 2011

[21] R B Arellano-Valle H Bolfarine and V H Lachos ldquoSkew-normal linear mixedmodelsrdquo Journal of Data Science vol 3 pp415ndash438 2005

[22] D Bates Fitting LinearMixedModels in RTheNewsletter of theR Project Volume 51 University of Wisconsin Madison WisUSA 2005

[23] A E Magurran Measuring Biological Diversity Blackwell Sci-ence Malden Mass USA 2004

[24] D Tuyisingize and K Fawcett ldquoThe common bird distributionin the Parc National des Volcans and its surrounding patternsconservation and future challengesrdquo DFGF Technical Report2011

[25] A T Peterson and N A Slade ldquoExtrapolating inventory resultsinto biodiversity estimates and the importance of stoppingrulesrdquoDiversity and Distributions vol 4 no 3 pp 95ndash105 1998

[26] M Salek J Svobodova and P Zasadil ldquoEdge effect of low-trafficforest roads on bird communities in secondary productionforests in central Europerdquo Landscape Ecology vol 25 no 7 pp1113ndash1124 2010

[27] S Murererehe ldquoCollecte et analyse de donnees pourlrsquoamenagement durable des forets -Joindre les efforts nationauxet internationaux Etat des ressources forestieres au RwandardquoTech Rep FAO Rome Italy 2000

[28] S J Nsengimana M Ndimukaga L Gakwerere et al ldquoBiodi-versity surveyrdquo Tech Rep Rufford Small Grant FoundationLondon UK 2009

[29] C Nsabagasani ldquoA Migratory Species African Pitta ldquoPittaangolensisrdquo passed Buhanga relict forestrdquo Backbone vol 17 pp6ndash8 2008

[30] J Jokimaki and M Kaisanlahti-Jokimaki ldquoThe role of residen-tial habitat type on the temporal variation of wintering birdassemblages in northern Finlandrdquo Ornis Fennica vol 88 2011

[31] T M Bergin L B Best K E Freemark and K J KoehlerldquoEffects of landscape structure on nest predation in roadsides ofa midwestern agroecosystem a multiscale analysisrdquo LandscapeEcology vol 15 no 2 pp 131ndash143 2000

[32] T Koellner AMHersperger andTWohlgemuth ldquoRarefactionmethod for assessing plant species diversity on a regional scalerdquoEcography vol 27 no 4 pp 532ndash544 2004

[33] S H Faeth P S Warren E Shochat and W A MarussichldquoTrophic dynamics in urban communitiesrdquo BioScience vol 55no 5 pp 399ndash407 2005

[34] R J Fuller and J D Wilson ldquoThe ecology of seed-eating birdsin relation to agricultural practices current research and futuredirectionsrdquo British Trust for Ornithology Research Report no149 1995

[35] J N Holland andD L DeAngelis ldquoEcological and evolutionaryconditions for fruit abortion to regulate pollinating seed-eaters and increase plant reproductionrdquo Theoretical PopulationBiology vol 61 no 3 pp 251ndash263 2002

[36] C J Whelan D G Wenny and R J Marquis ldquoEcosystemservices provided by birdsrdquo Annals of the New York Academyof Sciences vol 1134 pp 25ndash60 2008

[37] O Gilbert The Ecology of Urban Habitats Chapman amp HallLondon UK 1989

[38] A Millard ldquoSemi-natural vegetation and its relationship todesignated urban green space at the landscape scale in LeedsUKrdquo Landscape Ecology vol 23 no 10 pp 1231ndash1241 2008

[39] I Kowarik ldquoOn the role of alien species in urban flora andvegetationrdquo in Plant Invasions General Aspects and SpecialProblems P Pysek K Prach M Rejmanek and M WadeEds pp 85ndash103 SPB Academic Publishing Amsterdam TheNetherlands 1995

[40] G W Luck ldquoA review of the relationships between humanpopulation density and biodiversityrdquo Biological Reviews vol 82no 4 pp 607ndash645 2007

[41] Victorian Government Department of Sustainability and Envi-ronment (VGDSE) Managing Native Vegetation in VictorianCemeteries Victorian Government Department of Sustainabil-ity and Environment Melbourne Australia 2009

[42] C Dowd ldquoEffect of development on bird species compositionof two urban forested wetlands in Staten Island New YorkrdquoJournal of Field Ornithology vol 63 no 4 pp 455ndash461 1992

Page 10: Bird Diversity and Distribution in relation to Urban Landscape Types in Northern Rwanda · 2016. 1. 26. · ResearchArticle Bird Diversity and Distribution in relation to Urban Landscape

10 The Scientific World Journal

other bird species in the area the Pied Crow was observedclose to many human facilities such food markets abattoirswastelands domestic yards and croplands In addition thePied Crow was found in high abundance where its foodsources including small reptiles small mammals grainpeanuts carrion scraps of human food fruits insects andother small invertebrates were most available [9] To a lesserextent the urban habitat appeared to favor the Grey-headedSparrow (Passer griseus) The occurrence of the Grey-headedSparrow was associated with open woodlands and humansettlements where this species can easily access required foodand habitat resources The third most represented specieswas the Streaky Seedeater (Serinus striolatus) which is acommon bird of highlands and is generally found above1300m in gardens and cultivated areas woodland edgesheath and scrub vegetation areas The Streaky Seedeateris therefore adept at living in human altered landscapeswhich is not unlike the Black Kite (Milvus migrans) whichwas also common to densely human-populated areas Thesehuman-used landscapes are also a popular habitat of theBlackKitersquos prey which includes small birds bats and rodents Inparticular our study revealed the common occurrence of theBlack Kite circling near the abattoir and scavenging in thecityrsquos wastelands

43 Feeding Guild Categories

431 Feeding Guild Categories by Macrolandscape TypesSeed-eating birds were the best represented guild inMusanze(Figure 8) This may be partially due to the fact that datacollection was completed during a maize-harvesting periodDuring this period urban fields have an exceptionally largeabundance of seeds that can be exploited by birds and mayhave therefore selectively attracted seed-eating species [34]It was also observed that seed-eating species fed from arange of fruits According to Holland and DeAngelis [35]this habit allows seed-eating species to contribute to plantreproduction through pollination Insectivorous species werealso prominent in Musanzersquos urban landscapes Similarly tothe findings of Austin and Smith [5] insectivores were mostabundant in insect-rich landscapes including streamsideareas forests and informal settlements

432 FeedingGuild Categories byMicrolandscapes Althoughseedeaters especially the Grey-headed Sparrow (Passergriseus) dominated almost all microlandscapes it is impor-tant to consider that in wastelands scavengers were the mostabundant (Figure 13) This finding is likely due to the factthat different microlandscapes aremore appropriate for somespecies more than others especially those with differentfeeding habits

Our study confirms that bird species found in Musanzecity like urban-living bird species in other cities contributeto biomass recycling [36] Interestingly although there wereonly a few species of scavenging birds in Musanze theirabundance was high enough to compensate for their lowspecies richness in order to make a notable biomass recyclingimpact to city dwellersThis was particularly true for the Pied

Figure 13 Abundance of Pied Crows in a landfill within Musanzecity (Photo Author 2012)

Crow (Corvus albus) a species whose abundance amountedto more than seven times the average number of individualsper species whichwas almost 10of the total number of birdsobserved

44 Species Diversity

441 Alpha Diversity The bird diversity found in built-up areas was comparable to the bird diversity in urbanopen fields in Musanze city (Figure 9(a)) This finding pro-vides support for the increasingly recognized idea that birddiversity in urban areas can be as high as that in naturalenvironments [37 38] Previous research suggests that thismay be due to a relatively high number of nonnative speciespresent in cities as well as the heterogeneous habitat thaturban landscapes provide [39] which was not supportedin this study perhaps because of close proximity of thestudy area to a network of natural environments (PNVGishwati forest and Buhanga eco-park Rugezi Mukungwaand Bihinga wetlands and Karago Bulera and Ruhondolakes) Moreover Luck [40] suggested that there is a positivecorrelation between human population density and birdspecies richness This relationship was demonstrated in ourstudy as species such as the Pied Crowwere found to bemostabundant throughout urban landscapes and therefore welladapted to an environment where high human densities existInterestingly even the Albertine Rift endemic species theRuwenzori Double-collared Sunbird was sighted foraging inhuman populated areas on garden plants

Overall residential neighborhoods institutionalgrounds and informal settlements can be considered asthe major bird hotspots in Musanze city (Figure 9(b)) Thesethree landscapes share a great floristic diversity providingmany important stimuli for bird life (such as fruits seedsnectar domestic residues insects small mammals reptilesand amphibians) [30] Finally contrary to rural areas andnatural forests that undergo seasonal shortages of resources[3] cities do not experience strong seasonal variation due toa continuous supply of recourses from remote areas

442 Species Similarity The macrolandscapes all appearedto have similar bird species composition which may bedue to landscape heterogeneity [39] This heterogeneity islikely a result of the lack of historical professional landscapeplanning and design leaving a mosaic landscape structure inboth built-up and open fields instead of a uniform landscapespecialization Our results suggest that residential areas and

The Scientific World Journal 11

informal settlements were the most similar in terms ofspecies composition These landscapes ultimately functionto host family life The only difference between residentialareas and informal settlements resides in their socioeconomicstatus which is reflected in the landscape structure Howeverboth landscapes are more similar to each other than toother landscapes Furthermore the species composition ofcemeteries was similar to both forests and some of the built-up microlandscapes which may be attributed to the fact thatthese areas are all surrounded by trees Additionally ceme-teries are characterized by low human disturbance whichmay compare to that of forests and some urban landscapesThese landscapes all harbor a wide variety of floweringplants which in the case of cemeteries are mainly plantedby bereaved ones Moreover the vegetation of graveyardsincludes a range of regeneration stages resulting in a widerange of habitats from the vegetation-free areas of newly duggraves to the reconstructed thickets around old graves [41]Finally riverside landscapes emerged as the most specializedlandscape type as expected with many distinctive speciesobserved in this landscape only Almost all the species foundin riverside areas were specialists of wetlands and were notfound elsewhere As a result it was the most dissimilar to allother microlandscapes

The high degree of similarity in terms of bird diversitybetween Musanze city and the protected natural habitatsnearby provide further support that wildlife does not exclu-sively inhabit protected areas [33 37 42] Although the twonatural habitats are at eight km from Musanze city morethan half of the species found in the city were also found inVPN The lower degree of similarity between Musanze andBuhanga eco-park may be linked to the relative geographiclocation of the two sites as Musanze city is almost half waybetween the two protected areas This finding may also beattributed to the fact that the diversity ofmicrohabitats withinBuhanga eco-park is lower than that of Musanze and VPN[13] which may be due to the relatively small size of Buhangaeco-park Interestingly the species found in more than onelandscape type were also recorded both inside and beyondthe city limits Conversely Ficedula albicollis was recorded inonly one landscape type (cemeteries) and was absent in bothPNV and Buhanga eco-park

5 Conclusions

This study contributes to the knowledge of bird diversity inurban landscapes and provides the most recent status of birddiversity in Musanze city Our findings confirm that birddiversity in urban areas such as a densely populated city canbe as great as that in surrounding natural forests Specificallythe total number of bird species in Musanze city was verysimilar to that of the nearest protected forests VolcanoesNational Park and Buhanga eco-park Endemic and migra-tory birdswere also found inMusanze cityOneAlbertine Riftendemic bird species the Ruwenzori Double-collared Sun-bird was observed in Musanze during this study which hasnot been previously recorded Similarly threemigratory birdswere found inMusanze region for the first time the Common

Sandpiper the Spotted Flycatcher and theWillowWarbler Inaddition two bird species were observed that have not beenpreviously reported in Rwanda the Garden Warbler (Sylviaborin) and the Lesser Spotted Eagle (Aquila pomarina) Theeffect of landscape types on bird species richness and relativeabundance was also illustrated Residential neighborhoodsinstitutional grounds and informal settlements had thehighest species diversity indices and rankabundance relativeto the rest of the microlandscapes in this study Riversidelandscapes emerged with the most specialized bird faunaincluding species that are restricted to wetland environmentsand water bodies This study confirmed that scavengers inMusanze city contribute more to biomass recycling than anyother bird feeding groups Our study provides a current anduseful reference for urban decision makers and confirms theexistence of a great diversity of wildlife within cities Wesuggest that the development and implementation of cityland-use plans should consider this biodiversity especiallywhen villages and cities are in close proximity of protectedareas or natural reserves Finally it may be important thatbotanical gardens and public parks are included in themasterplan of the city as our study indicates that their designrequires an understanding of biodiversity in particular ofavian populations

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors acknowledge technical support from staffat DFGFI-Karisoke Research Center namely Dr WinnieEckardt Mr Deogratias Tuyisingize Mr Emmanuel Faidaand Mrs Keiko Mori

References

[1] S R Loss M O Ruiz and J D Brawn ldquoRelationships betweenavian diversity neighborhood age income and environmentalcharacteristics of an urban landscaperdquo Biological Conservationvol 142 no 11 pp 2578ndash2585 2009

[2] K L Evans D E Chamberlain B J Hatchwell R D Gregoryand K J Gaston ldquoWhat makes an urban birdrdquo Global ChangeBiology vol 17 no 1 pp 32ndash44 2011

[3] S Bolwig D Pomeroy H Tushabe and D Mushabe ldquoCropstrees and birds biodiversity change under agricultural inten-sification in Ugandas farmed landscapesrdquo Danish Journal ofGeography vol 106 no 2 pp 115ndash130 2006

[4] J Hitchmough and N Dunnett ldquoIntroduction to naturalisticplanting in urban landscapesrdquo in The Dynamic LandscapeJ Hitchmough and N Dunnatt Eds pp 1ndash32 Spon PressLondon UK 2004

[5] G T Austin and E L Smith ldquoWinter foraging ecology of mixedinsectivorous bird flocks in oakwoodland in southernArizonardquoThe Condor vol 74 pp 17ndash24 1972

[6] B R Coppedge D M Engle R E Masters and M S GregoryldquoAvian response to landscape change in fragmented southern

12 The Scientific World Journal

great plains grasslandsrdquo Ecological Applications vol 11 no 1 pp47ndash59 2001

[7] K L Evans S E Newson and K J Gaston ldquoHabitat influenceson urban avian assemblagesrdquo Ibis vol 151 no 1 pp 19ndash39 2009

[8] MW Strohbach D Haase and N Kabisch ldquoBirds and the cityUrban biodiversity land use and socioeconomicsrdquo Ecology andSociety vol 14 no 2 pp 31ndash45 2009

[9] T Stevenson and J Fanshawe Field Guide to the Birds of EastAfrica Kenya Tanzania Uganda Rwanda Burundi T amp A DPoyser London UK 2002

[10] J Mistry A Berardi and M Simpson ldquoBirds as indicators ofwetland status and change in the North Rupununi GuyanardquoBiodiversity and Conservation vol 17 no 10 pp 2383ndash24092008

[11] H Slabbekoorn and E A P Ripmeester ldquoBirdsong and anthro-pogenic noise implications and applications for conservationrdquoMolecular Ecology vol 17 no 1 pp 72ndash83 2008

[12] W S Judd C S Campbell E A Kellogg P F Stevens andM JDonoghue Plant Systematics A Phylogenetic Approach SinauerAssociates Sunderland Mass USA 3rd edition 2008

[13] W Weber ldquoRuhengeri and its resources an environmentalprofile of the Ruhengeri prefecturerdquo ETMAUSAID KigaliRwanda

[14] E Sabuhoro and G Bush ldquoThe Dian Fossey Gorilla FundInternationalPADGEF Assessing the Benefit Stream fromIllegal Activities in the Parc National des Volcansrdquo TargetingCommunity Conservation Interventions Musanze Rwanda2008

[15] J C Sano Urban Environmental Infrastructure in Kigali CityRwanda Challenges and Opportunities for Modernized Decen-tralized Sanitation Systems in Poor Neighborhoods WageningenUniversity Wageningen The Netherlands 2007

[16] R J Staniforth ldquoEffects of urbanization on bird populations inthe Canadian Central Arcticrdquo Arctic vol 55 no 1 pp 87ndash932002

[17] DWGibbons andRD Gregory ldquoBirdsrdquo in Ecological CensusesTechniques W L Sutherland Ed pp 308ndash350 CambridgeUniversity 2nd edition 2006

[18] D H Johnson ldquoPoint counts of birds what are we estimatingrdquoTech Rep PSW-GTR-149 USDA Forest Service 1995

[19] A Haslem and A F Bennett ldquoBirds in agricultural mosaics theinfluence of landscape pattern and countryside heterogeneityrdquoEcological Applications vol 18 no 1 pp 185ndash196 2008

[20] M L Rurangwa Feeding Ecology of Albertine Rift Endemic Birdsin the Volcanoes National Park Regal Sunbird Rwenzori Double-Collared Sunbird and Rwenzori Turako National University ofRwanda 2011

[21] R B Arellano-Valle H Bolfarine and V H Lachos ldquoSkew-normal linear mixedmodelsrdquo Journal of Data Science vol 3 pp415ndash438 2005

[22] D Bates Fitting LinearMixedModels in RTheNewsletter of theR Project Volume 51 University of Wisconsin Madison WisUSA 2005

[23] A E Magurran Measuring Biological Diversity Blackwell Sci-ence Malden Mass USA 2004

[24] D Tuyisingize and K Fawcett ldquoThe common bird distributionin the Parc National des Volcans and its surrounding patternsconservation and future challengesrdquo DFGF Technical Report2011

[25] A T Peterson and N A Slade ldquoExtrapolating inventory resultsinto biodiversity estimates and the importance of stoppingrulesrdquoDiversity and Distributions vol 4 no 3 pp 95ndash105 1998

[26] M Salek J Svobodova and P Zasadil ldquoEdge effect of low-trafficforest roads on bird communities in secondary productionforests in central Europerdquo Landscape Ecology vol 25 no 7 pp1113ndash1124 2010

[27] S Murererehe ldquoCollecte et analyse de donnees pourlrsquoamenagement durable des forets -Joindre les efforts nationauxet internationaux Etat des ressources forestieres au RwandardquoTech Rep FAO Rome Italy 2000

[28] S J Nsengimana M Ndimukaga L Gakwerere et al ldquoBiodi-versity surveyrdquo Tech Rep Rufford Small Grant FoundationLondon UK 2009

[29] C Nsabagasani ldquoA Migratory Species African Pitta ldquoPittaangolensisrdquo passed Buhanga relict forestrdquo Backbone vol 17 pp6ndash8 2008

[30] J Jokimaki and M Kaisanlahti-Jokimaki ldquoThe role of residen-tial habitat type on the temporal variation of wintering birdassemblages in northern Finlandrdquo Ornis Fennica vol 88 2011

[31] T M Bergin L B Best K E Freemark and K J KoehlerldquoEffects of landscape structure on nest predation in roadsides ofa midwestern agroecosystem a multiscale analysisrdquo LandscapeEcology vol 15 no 2 pp 131ndash143 2000

[32] T Koellner AMHersperger andTWohlgemuth ldquoRarefactionmethod for assessing plant species diversity on a regional scalerdquoEcography vol 27 no 4 pp 532ndash544 2004

[33] S H Faeth P S Warren E Shochat and W A MarussichldquoTrophic dynamics in urban communitiesrdquo BioScience vol 55no 5 pp 399ndash407 2005

[34] R J Fuller and J D Wilson ldquoThe ecology of seed-eating birdsin relation to agricultural practices current research and futuredirectionsrdquo British Trust for Ornithology Research Report no149 1995

[35] J N Holland andD L DeAngelis ldquoEcological and evolutionaryconditions for fruit abortion to regulate pollinating seed-eaters and increase plant reproductionrdquo Theoretical PopulationBiology vol 61 no 3 pp 251ndash263 2002

[36] C J Whelan D G Wenny and R J Marquis ldquoEcosystemservices provided by birdsrdquo Annals of the New York Academyof Sciences vol 1134 pp 25ndash60 2008

[37] O Gilbert The Ecology of Urban Habitats Chapman amp HallLondon UK 1989

[38] A Millard ldquoSemi-natural vegetation and its relationship todesignated urban green space at the landscape scale in LeedsUKrdquo Landscape Ecology vol 23 no 10 pp 1231ndash1241 2008

[39] I Kowarik ldquoOn the role of alien species in urban flora andvegetationrdquo in Plant Invasions General Aspects and SpecialProblems P Pysek K Prach M Rejmanek and M WadeEds pp 85ndash103 SPB Academic Publishing Amsterdam TheNetherlands 1995

[40] G W Luck ldquoA review of the relationships between humanpopulation density and biodiversityrdquo Biological Reviews vol 82no 4 pp 607ndash645 2007

[41] Victorian Government Department of Sustainability and Envi-ronment (VGDSE) Managing Native Vegetation in VictorianCemeteries Victorian Government Department of Sustainabil-ity and Environment Melbourne Australia 2009

[42] C Dowd ldquoEffect of development on bird species compositionof two urban forested wetlands in Staten Island New YorkrdquoJournal of Field Ornithology vol 63 no 4 pp 455ndash461 1992

Page 11: Bird Diversity and Distribution in relation to Urban Landscape Types in Northern Rwanda · 2016. 1. 26. · ResearchArticle Bird Diversity and Distribution in relation to Urban Landscape

The Scientific World Journal 11

informal settlements were the most similar in terms ofspecies composition These landscapes ultimately functionto host family life The only difference between residentialareas and informal settlements resides in their socioeconomicstatus which is reflected in the landscape structure Howeverboth landscapes are more similar to each other than toother landscapes Furthermore the species composition ofcemeteries was similar to both forests and some of the built-up microlandscapes which may be attributed to the fact thatthese areas are all surrounded by trees Additionally ceme-teries are characterized by low human disturbance whichmay compare to that of forests and some urban landscapesThese landscapes all harbor a wide variety of floweringplants which in the case of cemeteries are mainly plantedby bereaved ones Moreover the vegetation of graveyardsincludes a range of regeneration stages resulting in a widerange of habitats from the vegetation-free areas of newly duggraves to the reconstructed thickets around old graves [41]Finally riverside landscapes emerged as the most specializedlandscape type as expected with many distinctive speciesobserved in this landscape only Almost all the species foundin riverside areas were specialists of wetlands and were notfound elsewhere As a result it was the most dissimilar to allother microlandscapes

The high degree of similarity in terms of bird diversitybetween Musanze city and the protected natural habitatsnearby provide further support that wildlife does not exclu-sively inhabit protected areas [33 37 42] Although the twonatural habitats are at eight km from Musanze city morethan half of the species found in the city were also found inVPN The lower degree of similarity between Musanze andBuhanga eco-park may be linked to the relative geographiclocation of the two sites as Musanze city is almost half waybetween the two protected areas This finding may also beattributed to the fact that the diversity ofmicrohabitats withinBuhanga eco-park is lower than that of Musanze and VPN[13] which may be due to the relatively small size of Buhangaeco-park Interestingly the species found in more than onelandscape type were also recorded both inside and beyondthe city limits Conversely Ficedula albicollis was recorded inonly one landscape type (cemeteries) and was absent in bothPNV and Buhanga eco-park

5 Conclusions

This study contributes to the knowledge of bird diversity inurban landscapes and provides the most recent status of birddiversity in Musanze city Our findings confirm that birddiversity in urban areas such as a densely populated city canbe as great as that in surrounding natural forests Specificallythe total number of bird species in Musanze city was verysimilar to that of the nearest protected forests VolcanoesNational Park and Buhanga eco-park Endemic and migra-tory birdswere also found inMusanze cityOneAlbertine Riftendemic bird species the Ruwenzori Double-collared Sun-bird was observed in Musanze during this study which hasnot been previously recorded Similarly threemigratory birdswere found inMusanze region for the first time the Common

Sandpiper the Spotted Flycatcher and theWillowWarbler Inaddition two bird species were observed that have not beenpreviously reported in Rwanda the Garden Warbler (Sylviaborin) and the Lesser Spotted Eagle (Aquila pomarina) Theeffect of landscape types on bird species richness and relativeabundance was also illustrated Residential neighborhoodsinstitutional grounds and informal settlements had thehighest species diversity indices and rankabundance relativeto the rest of the microlandscapes in this study Riversidelandscapes emerged with the most specialized bird faunaincluding species that are restricted to wetland environmentsand water bodies This study confirmed that scavengers inMusanze city contribute more to biomass recycling than anyother bird feeding groups Our study provides a current anduseful reference for urban decision makers and confirms theexistence of a great diversity of wildlife within cities Wesuggest that the development and implementation of cityland-use plans should consider this biodiversity especiallywhen villages and cities are in close proximity of protectedareas or natural reserves Finally it may be important thatbotanical gardens and public parks are included in themasterplan of the city as our study indicates that their designrequires an understanding of biodiversity in particular ofavian populations

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors acknowledge technical support from staffat DFGFI-Karisoke Research Center namely Dr WinnieEckardt Mr Deogratias Tuyisingize Mr Emmanuel Faidaand Mrs Keiko Mori

References

[1] S R Loss M O Ruiz and J D Brawn ldquoRelationships betweenavian diversity neighborhood age income and environmentalcharacteristics of an urban landscaperdquo Biological Conservationvol 142 no 11 pp 2578ndash2585 2009

[2] K L Evans D E Chamberlain B J Hatchwell R D Gregoryand K J Gaston ldquoWhat makes an urban birdrdquo Global ChangeBiology vol 17 no 1 pp 32ndash44 2011

[3] S Bolwig D Pomeroy H Tushabe and D Mushabe ldquoCropstrees and birds biodiversity change under agricultural inten-sification in Ugandas farmed landscapesrdquo Danish Journal ofGeography vol 106 no 2 pp 115ndash130 2006

[4] J Hitchmough and N Dunnett ldquoIntroduction to naturalisticplanting in urban landscapesrdquo in The Dynamic LandscapeJ Hitchmough and N Dunnatt Eds pp 1ndash32 Spon PressLondon UK 2004

[5] G T Austin and E L Smith ldquoWinter foraging ecology of mixedinsectivorous bird flocks in oakwoodland in southernArizonardquoThe Condor vol 74 pp 17ndash24 1972

[6] B R Coppedge D M Engle R E Masters and M S GregoryldquoAvian response to landscape change in fragmented southern

12 The Scientific World Journal

great plains grasslandsrdquo Ecological Applications vol 11 no 1 pp47ndash59 2001

[7] K L Evans S E Newson and K J Gaston ldquoHabitat influenceson urban avian assemblagesrdquo Ibis vol 151 no 1 pp 19ndash39 2009

[8] MW Strohbach D Haase and N Kabisch ldquoBirds and the cityUrban biodiversity land use and socioeconomicsrdquo Ecology andSociety vol 14 no 2 pp 31ndash45 2009

[9] T Stevenson and J Fanshawe Field Guide to the Birds of EastAfrica Kenya Tanzania Uganda Rwanda Burundi T amp A DPoyser London UK 2002

[10] J Mistry A Berardi and M Simpson ldquoBirds as indicators ofwetland status and change in the North Rupununi GuyanardquoBiodiversity and Conservation vol 17 no 10 pp 2383ndash24092008

[11] H Slabbekoorn and E A P Ripmeester ldquoBirdsong and anthro-pogenic noise implications and applications for conservationrdquoMolecular Ecology vol 17 no 1 pp 72ndash83 2008

[12] W S Judd C S Campbell E A Kellogg P F Stevens andM JDonoghue Plant Systematics A Phylogenetic Approach SinauerAssociates Sunderland Mass USA 3rd edition 2008

[13] W Weber ldquoRuhengeri and its resources an environmentalprofile of the Ruhengeri prefecturerdquo ETMAUSAID KigaliRwanda

[14] E Sabuhoro and G Bush ldquoThe Dian Fossey Gorilla FundInternationalPADGEF Assessing the Benefit Stream fromIllegal Activities in the Parc National des Volcansrdquo TargetingCommunity Conservation Interventions Musanze Rwanda2008

[15] J C Sano Urban Environmental Infrastructure in Kigali CityRwanda Challenges and Opportunities for Modernized Decen-tralized Sanitation Systems in Poor Neighborhoods WageningenUniversity Wageningen The Netherlands 2007

[16] R J Staniforth ldquoEffects of urbanization on bird populations inthe Canadian Central Arcticrdquo Arctic vol 55 no 1 pp 87ndash932002

[17] DWGibbons andRD Gregory ldquoBirdsrdquo in Ecological CensusesTechniques W L Sutherland Ed pp 308ndash350 CambridgeUniversity 2nd edition 2006

[18] D H Johnson ldquoPoint counts of birds what are we estimatingrdquoTech Rep PSW-GTR-149 USDA Forest Service 1995

[19] A Haslem and A F Bennett ldquoBirds in agricultural mosaics theinfluence of landscape pattern and countryside heterogeneityrdquoEcological Applications vol 18 no 1 pp 185ndash196 2008

[20] M L Rurangwa Feeding Ecology of Albertine Rift Endemic Birdsin the Volcanoes National Park Regal Sunbird Rwenzori Double-Collared Sunbird and Rwenzori Turako National University ofRwanda 2011

[21] R B Arellano-Valle H Bolfarine and V H Lachos ldquoSkew-normal linear mixedmodelsrdquo Journal of Data Science vol 3 pp415ndash438 2005

[22] D Bates Fitting LinearMixedModels in RTheNewsletter of theR Project Volume 51 University of Wisconsin Madison WisUSA 2005

[23] A E Magurran Measuring Biological Diversity Blackwell Sci-ence Malden Mass USA 2004

[24] D Tuyisingize and K Fawcett ldquoThe common bird distributionin the Parc National des Volcans and its surrounding patternsconservation and future challengesrdquo DFGF Technical Report2011

[25] A T Peterson and N A Slade ldquoExtrapolating inventory resultsinto biodiversity estimates and the importance of stoppingrulesrdquoDiversity and Distributions vol 4 no 3 pp 95ndash105 1998

[26] M Salek J Svobodova and P Zasadil ldquoEdge effect of low-trafficforest roads on bird communities in secondary productionforests in central Europerdquo Landscape Ecology vol 25 no 7 pp1113ndash1124 2010

[27] S Murererehe ldquoCollecte et analyse de donnees pourlrsquoamenagement durable des forets -Joindre les efforts nationauxet internationaux Etat des ressources forestieres au RwandardquoTech Rep FAO Rome Italy 2000

[28] S J Nsengimana M Ndimukaga L Gakwerere et al ldquoBiodi-versity surveyrdquo Tech Rep Rufford Small Grant FoundationLondon UK 2009

[29] C Nsabagasani ldquoA Migratory Species African Pitta ldquoPittaangolensisrdquo passed Buhanga relict forestrdquo Backbone vol 17 pp6ndash8 2008

[30] J Jokimaki and M Kaisanlahti-Jokimaki ldquoThe role of residen-tial habitat type on the temporal variation of wintering birdassemblages in northern Finlandrdquo Ornis Fennica vol 88 2011

[31] T M Bergin L B Best K E Freemark and K J KoehlerldquoEffects of landscape structure on nest predation in roadsides ofa midwestern agroecosystem a multiscale analysisrdquo LandscapeEcology vol 15 no 2 pp 131ndash143 2000

[32] T Koellner AMHersperger andTWohlgemuth ldquoRarefactionmethod for assessing plant species diversity on a regional scalerdquoEcography vol 27 no 4 pp 532ndash544 2004

[33] S H Faeth P S Warren E Shochat and W A MarussichldquoTrophic dynamics in urban communitiesrdquo BioScience vol 55no 5 pp 399ndash407 2005

[34] R J Fuller and J D Wilson ldquoThe ecology of seed-eating birdsin relation to agricultural practices current research and futuredirectionsrdquo British Trust for Ornithology Research Report no149 1995

[35] J N Holland andD L DeAngelis ldquoEcological and evolutionaryconditions for fruit abortion to regulate pollinating seed-eaters and increase plant reproductionrdquo Theoretical PopulationBiology vol 61 no 3 pp 251ndash263 2002

[36] C J Whelan D G Wenny and R J Marquis ldquoEcosystemservices provided by birdsrdquo Annals of the New York Academyof Sciences vol 1134 pp 25ndash60 2008

[37] O Gilbert The Ecology of Urban Habitats Chapman amp HallLondon UK 1989

[38] A Millard ldquoSemi-natural vegetation and its relationship todesignated urban green space at the landscape scale in LeedsUKrdquo Landscape Ecology vol 23 no 10 pp 1231ndash1241 2008

[39] I Kowarik ldquoOn the role of alien species in urban flora andvegetationrdquo in Plant Invasions General Aspects and SpecialProblems P Pysek K Prach M Rejmanek and M WadeEds pp 85ndash103 SPB Academic Publishing Amsterdam TheNetherlands 1995

[40] G W Luck ldquoA review of the relationships between humanpopulation density and biodiversityrdquo Biological Reviews vol 82no 4 pp 607ndash645 2007

[41] Victorian Government Department of Sustainability and Envi-ronment (VGDSE) Managing Native Vegetation in VictorianCemeteries Victorian Government Department of Sustainabil-ity and Environment Melbourne Australia 2009

[42] C Dowd ldquoEffect of development on bird species compositionof two urban forested wetlands in Staten Island New YorkrdquoJournal of Field Ornithology vol 63 no 4 pp 455ndash461 1992

Page 12: Bird Diversity and Distribution in relation to Urban Landscape Types in Northern Rwanda · 2016. 1. 26. · ResearchArticle Bird Diversity and Distribution in relation to Urban Landscape

12 The Scientific World Journal

great plains grasslandsrdquo Ecological Applications vol 11 no 1 pp47ndash59 2001

[7] K L Evans S E Newson and K J Gaston ldquoHabitat influenceson urban avian assemblagesrdquo Ibis vol 151 no 1 pp 19ndash39 2009

[8] MW Strohbach D Haase and N Kabisch ldquoBirds and the cityUrban biodiversity land use and socioeconomicsrdquo Ecology andSociety vol 14 no 2 pp 31ndash45 2009

[9] T Stevenson and J Fanshawe Field Guide to the Birds of EastAfrica Kenya Tanzania Uganda Rwanda Burundi T amp A DPoyser London UK 2002

[10] J Mistry A Berardi and M Simpson ldquoBirds as indicators ofwetland status and change in the North Rupununi GuyanardquoBiodiversity and Conservation vol 17 no 10 pp 2383ndash24092008

[11] H Slabbekoorn and E A P Ripmeester ldquoBirdsong and anthro-pogenic noise implications and applications for conservationrdquoMolecular Ecology vol 17 no 1 pp 72ndash83 2008

[12] W S Judd C S Campbell E A Kellogg P F Stevens andM JDonoghue Plant Systematics A Phylogenetic Approach SinauerAssociates Sunderland Mass USA 3rd edition 2008

[13] W Weber ldquoRuhengeri and its resources an environmentalprofile of the Ruhengeri prefecturerdquo ETMAUSAID KigaliRwanda

[14] E Sabuhoro and G Bush ldquoThe Dian Fossey Gorilla FundInternationalPADGEF Assessing the Benefit Stream fromIllegal Activities in the Parc National des Volcansrdquo TargetingCommunity Conservation Interventions Musanze Rwanda2008

[15] J C Sano Urban Environmental Infrastructure in Kigali CityRwanda Challenges and Opportunities for Modernized Decen-tralized Sanitation Systems in Poor Neighborhoods WageningenUniversity Wageningen The Netherlands 2007

[16] R J Staniforth ldquoEffects of urbanization on bird populations inthe Canadian Central Arcticrdquo Arctic vol 55 no 1 pp 87ndash932002

[17] DWGibbons andRD Gregory ldquoBirdsrdquo in Ecological CensusesTechniques W L Sutherland Ed pp 308ndash350 CambridgeUniversity 2nd edition 2006

[18] D H Johnson ldquoPoint counts of birds what are we estimatingrdquoTech Rep PSW-GTR-149 USDA Forest Service 1995

[19] A Haslem and A F Bennett ldquoBirds in agricultural mosaics theinfluence of landscape pattern and countryside heterogeneityrdquoEcological Applications vol 18 no 1 pp 185ndash196 2008

[20] M L Rurangwa Feeding Ecology of Albertine Rift Endemic Birdsin the Volcanoes National Park Regal Sunbird Rwenzori Double-Collared Sunbird and Rwenzori Turako National University ofRwanda 2011

[21] R B Arellano-Valle H Bolfarine and V H Lachos ldquoSkew-normal linear mixedmodelsrdquo Journal of Data Science vol 3 pp415ndash438 2005

[22] D Bates Fitting LinearMixedModels in RTheNewsletter of theR Project Volume 51 University of Wisconsin Madison WisUSA 2005

[23] A E Magurran Measuring Biological Diversity Blackwell Sci-ence Malden Mass USA 2004

[24] D Tuyisingize and K Fawcett ldquoThe common bird distributionin the Parc National des Volcans and its surrounding patternsconservation and future challengesrdquo DFGF Technical Report2011

[25] A T Peterson and N A Slade ldquoExtrapolating inventory resultsinto biodiversity estimates and the importance of stoppingrulesrdquoDiversity and Distributions vol 4 no 3 pp 95ndash105 1998

[26] M Salek J Svobodova and P Zasadil ldquoEdge effect of low-trafficforest roads on bird communities in secondary productionforests in central Europerdquo Landscape Ecology vol 25 no 7 pp1113ndash1124 2010

[27] S Murererehe ldquoCollecte et analyse de donnees pourlrsquoamenagement durable des forets -Joindre les efforts nationauxet internationaux Etat des ressources forestieres au RwandardquoTech Rep FAO Rome Italy 2000

[28] S J Nsengimana M Ndimukaga L Gakwerere et al ldquoBiodi-versity surveyrdquo Tech Rep Rufford Small Grant FoundationLondon UK 2009

[29] C Nsabagasani ldquoA Migratory Species African Pitta ldquoPittaangolensisrdquo passed Buhanga relict forestrdquo Backbone vol 17 pp6ndash8 2008

[30] J Jokimaki and M Kaisanlahti-Jokimaki ldquoThe role of residen-tial habitat type on the temporal variation of wintering birdassemblages in northern Finlandrdquo Ornis Fennica vol 88 2011

[31] T M Bergin L B Best K E Freemark and K J KoehlerldquoEffects of landscape structure on nest predation in roadsides ofa midwestern agroecosystem a multiscale analysisrdquo LandscapeEcology vol 15 no 2 pp 131ndash143 2000

[32] T Koellner AMHersperger andTWohlgemuth ldquoRarefactionmethod for assessing plant species diversity on a regional scalerdquoEcography vol 27 no 4 pp 532ndash544 2004

[33] S H Faeth P S Warren E Shochat and W A MarussichldquoTrophic dynamics in urban communitiesrdquo BioScience vol 55no 5 pp 399ndash407 2005

[34] R J Fuller and J D Wilson ldquoThe ecology of seed-eating birdsin relation to agricultural practices current research and futuredirectionsrdquo British Trust for Ornithology Research Report no149 1995

[35] J N Holland andD L DeAngelis ldquoEcological and evolutionaryconditions for fruit abortion to regulate pollinating seed-eaters and increase plant reproductionrdquo Theoretical PopulationBiology vol 61 no 3 pp 251ndash263 2002

[36] C J Whelan D G Wenny and R J Marquis ldquoEcosystemservices provided by birdsrdquo Annals of the New York Academyof Sciences vol 1134 pp 25ndash60 2008

[37] O Gilbert The Ecology of Urban Habitats Chapman amp HallLondon UK 1989

[38] A Millard ldquoSemi-natural vegetation and its relationship todesignated urban green space at the landscape scale in LeedsUKrdquo Landscape Ecology vol 23 no 10 pp 1231ndash1241 2008

[39] I Kowarik ldquoOn the role of alien species in urban flora andvegetationrdquo in Plant Invasions General Aspects and SpecialProblems P Pysek K Prach M Rejmanek and M WadeEds pp 85ndash103 SPB Academic Publishing Amsterdam TheNetherlands 1995

[40] G W Luck ldquoA review of the relationships between humanpopulation density and biodiversityrdquo Biological Reviews vol 82no 4 pp 607ndash645 2007

[41] Victorian Government Department of Sustainability and Envi-ronment (VGDSE) Managing Native Vegetation in VictorianCemeteries Victorian Government Department of Sustainabil-ity and Environment Melbourne Australia 2009

[42] C Dowd ldquoEffect of development on bird species compositionof two urban forested wetlands in Staten Island New YorkrdquoJournal of Field Ornithology vol 63 no 4 pp 455ndash461 1992