Conservation ecology, morphology and reproduction

of the nocturnal

northern giant mouse lemur Mirza zaza

in Sahamalaza National Park, northwestern Madagascar

Dissertation Course Name

MSc Primate Conservation

Title

Conservation ecology, morphology and reproduction of the nocturnal northern giant mouse

lemur Mirza zaza in Sahamalaza National Park, northwestern Madagascar

Student Number Surname

09082861 Rode

Other Names

Eva Johanna

Course for which acceptable:

MSc Primate Conservation

Date of Submission

17th September, 2010

This dissertation is submitted in part fulfilment of the regulations for an MSc degree.

Oxford Brookes University Statement of originality Except for those parts in which it is explicitly stated to the contrary, this project is my own work. It has not been submitted for any degree at this or any other academic or professional institution. 17th September, 2010 ……………………………………… ……. ………………… Signature Date Regulations Governing the Deposit and Use of Oxford Brookes University Projects/ Dissertations

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be available for reading and photocopying at the discretion of the Dean of School in accordance with 3 and 4 below.

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4. Permission for any one other then the author to reproduce or photocopy

any part of the dissertation must be obtained from the Head of School who will give his/her permission for such reproduction on to an extent which he/she considers to be fair and reasonable.

I agree that this dissertation may be available for reading and photocopying at the discretion of my Dean of School in accordance with regulations 3 and 4 above.* 17th September, 2010 ……………………………………… ……. ………………… Signature Date

*The underlined words may be deleted by the author if he/she so wishes.

i

Abstract

Madagascar, a primate conservation hotspot, has by far the highest percentage of

primate species Red-Listed as Data Deficient. The underlying gaps in conservation-relevant

knowledge make it difficult to design effective conservation measures. The northern giant

mouse lemur (Mirza zaza) was only described in 2005 (Kappeler et al, 2005) and is listed as

Data Deficient on the IUCN Red List. This study was conducted as the first comprehensive

ecological study of the species and aimed at gathering necessary information for the design of

effective conservation measures. In Ankarafa Forest in Sahamalaza National Park,

northwestern Madagascar, we radio-tracked 8 individuals of M. zaza over 2.5 months in the

dry season. During its nocturnal activity the species was found to have extensively

overlapping home ranges.Group home ranges varied between 0.52 and 2.34 ha. M. zaza

favoured large trees in dense microhabitats and preferred certain tree species. Up to 4 animals

including several males with fully developed testes shared a group-exclusive nest which

suggests multi-male/multi-female or extended families nest groups. The nests were changed

maximum three times during the study time which could indicate a scarcity in suitable nest

sites. Nest sites were characterised by large and tall trees with many lianas. Morphology data

and behaviour observations suggest that M. zaza reproduces aseasonally and exhibits a

promiscuous mating system. We found significant morphological differences to another M.

zaza population in the region of Ambato which is divided from Sahamalaza by the large

Sambirano River. Genetic analyses should clarify whether the Sahamalaza population

represents another sub-species or species. Based on these finding we recommend protecting

the remaining habitat of M. zaza in Ankarafa Forest, focussing on dense forest areas and large

trees while limiting selective logging. Reforestation measures should include preferred tree

species and target a high density of trees.

ii

Acknowledgements

The people I want to thank here cannot be ranked according to importance as the help of

each person was highly appreciated and necessary to complete this project as it appears here.

First, I would like to thank my academic supervisor Dr. Anna Nekaris who encouraged

me to do this project and assisted me in its development and finalisation. Her passion for

nocturnal primates and enthusiasm for Mirza zaza (which she has never seen) was infectious.

The advices of the MSc Primate Conservation staff Prof. Simon Bearder and Dr. Vincent

Nijman were highly appreciated.

My sincere thanks go to Dr. Christoph Schwitzer who made it possible for me to travel

to Madagascar and realise this project. He offered me constant assistence in England and

during the field time. Whenever I had a problem I could count on his help. This thank is

extended to Bristol Conservation and Science Foundation, Bristol Zoo Gardens and AEECL

for supporting and facilitating the conservation work in Sahamalaza. AEECL programme

director Guy H. Randriatahina and his wife Sylviane Volampeno helped me to organise my

project in Madagascar. I am grateful to the MICET staff that assisted with the paperwork and

MNP that allowed me to conduct research in Sahamalaza – Iles Ramada National Park.

Special thanks goes to my fabulous research counterpart „Fara“ Faratiana

Rafianinantsoa (University of Mahajanga) and my two excellent guides „Popol“ Rakotonirina

Jean Paul and „Patrice“ (anonymous). Thanks also to all the other guides and researchers at

Ankarafa Research Station, and the staff of Tsimbazaza Zoo for their initial help to capture

the animals.

Many other people helped me to access information about Mirza zaza and assisted me

in the project: Sarah Zehr and David Haring from the Duke Lemur Center, US, provided me

with interesting life history data about Mirza zaza, Mathias Markolf from the German Primate

Center, Germany, gave me numerous advice for the practical implementation of the project,

and Chris Birkinshaw helped me to translate Malagasy names of tree species.

The help of numerous people, who read my dissertation, assisted in understanding

methods and gave helpful tips for improvement, was highly appreciated.

The project would not have been feasible without the financial support of Primate

Conservation Inc. and Conservation International Primate Action Fund.

Last but not least, I want to thank my family and my partner Christoph Reiß for their

never ending support, encouragement and love throughout the whole project.

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Table of contents

Abstract …………………………………………………………………………………….... i

Acknowledgements …………………………………………………………………………. ii

Table of contents …………………………………………………………………...…...…. iii

List of tables ……………………………………………………………………………..….. v

List of figures ………………………………………………………………………........…. vi

List of acronyms ……………………………………………………………………......…. vii

1. General Introduction ........................................................................................................ 1

1.1. Madagascar: The home of the lemurs ........................................................................ 1

1.2. Main threats to biodiversity in Madagascar ............................................................... 2

1.3. Sahamalaza- Iles Ramada National Park, northwestern Madagascar ........................ 2

1.4. Goal and aims of the project ...................................................................................... 3

1.5. Structure of dissertation ............................................................................................. 4

2. General methods ............................................................................................................... 5

2.1. Taxonomy of Mirza zaza ............................................................................................ 5

2.2. Study site .................................................................................................................... 5

2.3. Data collection ............................................................................................................ 8

2.3.1 Capturing Mirza zaza ................................................................................................. 8

2.3.2 Morphology ................................................................................................................ 8

2.3.3 Radio-tracking and home ranges................................................................................ 9

2.3.4 Habitat and nest .......................................................................................................... 9

2.3.6 Analysis .................................................................................................................... 10

Plate 1: Study site Ankarafa Forest, Sahamalaza, northwestern Madagascar

Plate 2: Lemur community in Ankarafa Forest, Sahamalaza

Plate 3: Procedure of capturing and processing Mirza zaza

Plate 4: Morphology and reproduction of Mirza zaza

Plate 5: Food of Mirza zaza

Plate 6: Injuries of Mirza zaza

iv

3. Morphology and reproduction of the northern giant mouse lemur Mirza zaza in Sahamalaza National Park, northwestern Madagascar ..................................................... 11

3.1. Introduction .............................................................................................................. 11

3.2. Methods .................................................................................................................... 12

3.3. Results ...................................................................................................................... 13

3.4. Discussion ................................................................................................................ 17

3.5. Conclusions .............................................................................................................. 20

4. Conservation implications of home range and habitat use of the northern giant mouse lemur Mirza zaza, in Sahamalaza, northwestern Madagascar ............................... 21

4.1. Introduction .............................................................................................................. 21

4.2. Methods .................................................................................................................... 23

4.3. Results ...................................................................................................................... 24

4.4. Discussion ................................................................................................................ 32

4.5. Conclusions and conservation recommendations .................................................... 34

5. Characteristics and use of nests and nest sites of the northern giant mouse lemur Mirza zaza, in Sahamalaza, northwestern Madagascar ...................................................... 35

5.1. Introduction .............................................................................................................. 35

5.2. Methods .................................................................................................................... 37

5.3. Results ...................................................................................................................... 38

5.4. Discussion ................................................................................................................ 42

5.5. Conclusions and recommendations .......................................................................... 47

6. Synopsis ............................................................................................................................ 48

6.1. Conclusions .............................................................................................................. 48

6.2. Future research ......................................................................................................... 48

7. References ........................................................................................................................ 49

Appendix 1: Oestrus cycle of Mirza zaza………………………………..…………………..58

Appendix 2: Incremental area analysis of group and individual home rages of Mirza zaza...59

Appendix 3: Variables used to study Mirza zaza… ……………………………………..65

(Word count: 16,125)

v

List of tables

Table 1: Identification codes, sex and age of all individuals captured at the given dates in Ankarafa forest research station in May and July 2010. ........................................... 14

Table 2: Descriptive statistics (mean and SD) for 18 morphometric variables of adult male and female Mirza zaza from Sahamalaza National Park. .......................................... 15

Table 3: Weight, absolute and relative testes volume (testes volume divided by body mass) at the first and the second capture of 5 male individuals of Mirza zaza ....................... 16

Table 4: Summary of suspected birth and mating season of Mirza zaza. ............................... 18

Table 5: Summary of morphological and behavioural characteristics of Mirza zaza that give an indication of the mating system. ........................................................................... 19

Table 6: Mirza zaza captured in May and July 2010. ............................................................. 24

Table 7: Individual home ranges for 8 animals of Mirza zaza, as calculated using MCP and 95 % kernel method. .................................................................................................. 26

Table 8: Home range overlap between individuals of group 1 and 3 respectively, as calculated with MCP and 95 % kernel method ........................................................................... 27

Table 9: Medians for 5 variables of used and random trees in two forests A and B. .............. 29

Table 10: Medians for 7 variables of used and random microhabitat in two forests A and B. 30

Table 11: Tree species, families and Malagasy names of large and small trees used most often by Mirza zaza during their nightly activity. .............................................................. 31

Table 12: Height, distance from top of the tree and number of lianas of 6 Mirza zaza nests . 39

Table 13: Medians for 5 nest tree variables and comparison to used trees and random trees in two forests A and B. .................................................................................................. 40

Table 14: Medians for 7 variables of microhabitat and comparison to used microhabitat and random microhabitat in two different forests. ........................................................... 40

Table 15: Nest group composition of three groups of Mirza zaza. ......................................... 41

Table 16: Oestrus cycle of Mirza zaza in captivity and vaginal appearance of each cycle. ... 58

Table 17: Variables of habitat and habitat use, and ethogram of Mirza zaza as used for this project ........................................................................................................................ 65

List of figures

Figure 1: Ankarafa Forest with the two study sites forest A and forest B and the location of the camp ..................................................................................................................................... 7

Figure 2: Home range overlap between nest group 1 and individual F2, using MCP method. .................................................................................................................................................. 25

Figure 3: Individual home ranges for groups 1, 2 and 3 in two forests A and B, and overlap, using MCP method. .................................................................................................................. 26

Figure 4: Individual home ranges for groups 1, 2 and 3 in two forests A and B, and overlap, using 95 % kernel method ........................................................................................................ 27

Figure 5: Percentage (%) of height classes used by 8 individuals Mirza zaza in forest A and B during nocturnal activity .......................................................................................................... 28

Figure 6: Percentage of tree types used by Mirza zaza compared to random trees. ............... 29

List of acronyms

AEECL: Association Européenne pour L’Etude et la Conservation des

Lémuriens (European Association for the Study and Conservation of

Lemurs)

DBH: Diameter at Breast Height

IUCN: World Conservation Union

MICET: Madagascar Institut pour la Conservation des Environnements

Tropicaux (Malagasy Institute for the Conservation of Tropical

Environments)

MNP: Madagascar National Parks

UN: United Nations

UNESCO: United Nations Educational, Scientific and Cultural Organization

WCS: Wildlife Conservation Society

1

1. General Introduction

1.1. Madagascar: The home of the lemurs

The “great red island” Madagascar has separated from Afrika 180 million years ago and

since then its biodiversity has evolved in isolation and at very high rates [Ratsimbazafy et al.,

2008]. The divergence of Lemuriformes and Lorisiformes (galagos and lorises in mainland

Africa and Asia) is estimated at 75 Million years and thus happened after the separation of

Madagascar from Africa [Horvath et al., 2008]. Their arrival on Madagascar could be

explained by early lemuriformes ancestors crossing the Mozambique Channel drifting on

large vegetation rafts [Horvath et al., 2008; Krause, 2010; Yoder and Yang, 2004].

Madagascar is one of the most important biodiversity hotspots in the world,

underpinned by its high proportion of endemic species and rates of deforestation [Myers et al.,

2000; Mittermeier et al., in press]. The island is among the main priorities for primate

conservation [Harcourt and Thornback, 1990] and is home to over 100 primate species

[Mittermeier et al., in press]. This makes it the country with the second highest primate

species diversity in the world, despite it being only 7 % the size of Brazil, which ranks first

(103 species). Furthermore, it harbours the highest number of threatened primate taxa in any

one country [Mittermeier et al., in press]. Of the 94 taxa that have been assessed for the IUCN

Red List, 41 % are listed as threatened (14 Vulnerable, 17 Endangered, 8 Critically

Endangered) [IUCN, 2009]. In the last decades there have been major taxonomic revisions

within the lemurs of Madagascar, particularly within the nocturnal families Cheirogaleidae

and Lepilemuridae. Between 2000 and 2008, 39 species were newly described and nine other

taxa resurrected [Mittermeier et al., 2008]. This has resulted in the unusual situation that 45 %

of all Malagasy primate species are now Red-Listed as Data Deficient by the IUCN [2009],

by far the highest such figure for any primate habitat country (by comparison, 13 % of all

primates and 15 % of all mammals are Red-Listed as Data Deficient). This situation has led to

increased concern among ecologists and conservationists [Tattersall, 2007]. Many of the

recently described species are only known from single locations. Especially for many of the

small nocturnal Lepilemur and Microcebus species few data are available about distribution,

population densities, habitat requirements or conservation status. The lack of species specific

knowledge makes it impossible to determine the IUCN Red List status and design effective

conservation measures. Since Data Deficient species could well be threatened, they represent

an immediate priority for conservation ecology research [Vié et al., 2009].

2

1.2. Main threats to biodiversity in Madagascar

Madagascar’s biodiversity is very threatened. Less than 10 % of its primary vegetation

is left [Kaufmann, 2006]. Since the 1970s 33 % of the primary vegetation vanished and

1500 km2 are lost every year [Moat and Smith, 2007]. Some vegetation types disappear faster

than others. Western dry forest makes up 5.4 % of Madagascar’s vegetation and decreased by

40 % from 1975 to 2000 [Moat and Smith, 2007]. Anthropogenic pressure includes fires,

slash and burn agriculture (tavy), farming and logging activities [Wells and Andriamihaja,

1997]. Madagascar’s former president Marc Ravalomanana tripled the protected areas in

Madagascar but in 2009 his government was brought down by city major and former DJ Andy

Rajoelina. The violent coup has led to a very instable situation and low enforcement and has

allowed armed loggers and hunters to intensify environmental destruction [Smith, 2009]. The

disappearance of vegetation also negatively affects the generally poor but rapidly growing

human population: Rain water is not absorbed and floods wash away land, infrastructure and

resources [Vérin, 2003; Wright and Rakotoarisoa, 1997]. To say it with the words of Alison

Jolly: Madagascar is “committing environmental suicide” [Jolly, 2004, p. 196].

1.3. Sahamalaza- Iles Ramada National Park, northwestern Madagascar

In collaboration with the Wildlife Conservation Society (WCS) and Madagascar

National Parks (MNP), the Lemur Conservation Association (Association Européenne pour

l'Etude et la Conservation des Lémuriens, AEECL) was instrumental in establishing a

UNESCO biosphere reserve and a national protected area in the Sahamalaza region

[Schwitzer et al., 2006]. As part of their "Programme Sahamalaza", a community-based

natural resource management and conservation ecology research programme, in 2004

scientists of AEECL and the universities of Antananarivo and Mahajanga established a field

station in the Ankarafa Forest [Schwitzer et al., 2006], situated on the Sahamalaza Peninsula

within the boundaries of the national park. In order to support habitat protection measures,

several studies have since been conducted on the flagship species of the project, the critically

endangered blue-eyed black lemur (Eulemur flavifrons) [Schwitzer et al., 2007a, 2007b].

The Sahamalaza Peninsula can be reached in 2 to 3 days via local bus, local ferry and

pirogue (local boat). In the rainy season it is often inaccessible.

Extreme hunting pressure on wildlife is observed outside the park but inside it seems to

be almost none due to the presence of researchers [Schwitzer, pers. comm.]. However, during

3

May and August 2010 two loggers were found to have killed and roasted a Lepilemur

sahamalazensis (personal observation). Illegal small scale logging activities and fires (either

accidentally or to express disagreement with National Park) are a constant threat to the

habitat.

The lemur community at the study site Ankarafa Forest comprises Eulemur flavifrons,

Lepilemur sahamalazensis, Mirza zaza and an unidentified Cheirogaleus species [Schwitzer,

pers. comm.].

1.4. Goal and aims of the project

The nocturnal species Mirza zaza (Primates: Lemuridea: Cheirogaleidae) is a Data

Deficient nocturnal lemur species. It occurs in northwestern Madagascar and apart from basic

biological and genetic information collected for the description of the species [Kappeler et al.,

2005], a distribution survey [Markolf et al., 2008] and a first estimation of the conservation

status [Roos and Kappeler, 2006] no data are available about the species’ ecology.

Sahamalaza National Park is the only protected area where M. zaza occurs [Markolf et al.,

2008]. Basic ecological data on M. zaza is needed in order to ensure that ongoing and future

conservation measures in Sahamalaza and elsewhere in the species' distribution range actually

benefit its long-term survival. Furthermore, data about home range size and overlap can

indicate the species space requirements and may assist the Red-Listing of this Data Deficient

lemur species.

Accordingly, the main goal of this dissertation will be to determine features of habitat

and nest sites used by Mirza zaza in order to enable ongoing and future conservation efforts in

Sahamalaza and elsewhere to effectively target the species and to provide information

necessary for the IUCN Red-Listing of the species. Specific aims will be:

1. To determine home range size, overlap and ranging patterns of Mirza zaza in order to

draw conclusions about space requirements and social organization

2. To investigate preferences of M. zaza towards microhabitat characteristics

3. To describe nest characteristics and determine preferences of M. zaza towards

characteristics of nest trees and nest microhabitat

4. To provide information about the general morphology of M. zaza in Ankarafa Forest in

order to compare them to other populations, and to reveal details about their

reproduction

4

5. To make recommendations for the conservation of M. zaza, that can be used by various

local, national and international organizations like AEECL, MNP or IUCN

1.5. Structure of dissertation

I have chosen to write this dissertation in an “article-style” which includes that the

different, self-contained chapters follow the guidelines of certain journals. Morphology and

reproduction is the topic of the first chapter (section 3) as the information presented gives the

reader a better impression of the species. It is written for submission to Folia Primatologica as

a primate-specific journal. The second chapter (section 4) deals with home range and habitat

use of Mirza zaza and is formatted for submission to Endangered Species Research as a

journal including all wildlife taxa but focusing on conservation. The third chapter (section 5)

investigates the nest, nest sites and nest site utilization and is written for Lemur News which

is freely distributed. However, chapters are not exactly formatted as the required manuscript:

no line numbers and acknowledgements will be added, and tables and figures will be

integrated in the text and numbered throughout the whole dissertation to improve readability.

Only one Abstract is given at the beginning of the whole dissertation which can be adapted

for publication of single chapters. An overall reference list is provided at the end. To avoid

repetition, a general methods section (section 2) is added and single chapters might refer back

to this. Finally, a synopsis with conclusions and future research is given. Recommendations

are outlined at the end of each paper chapter. UK English was chosen for the whole

dissertation even though journal requirements may differ.

5

2. General methods

As methods were applied for all of the chapters, most will be described in this section to

avoid repetition.

2.1. Taxonomy of Mirza zaza

The genus Mirza GRAY, 1870, has been widely recognized as Microcebus (species

name M. coquereli) until Tattersall resurrected it as a separate genus in 1982 [Kappeler et al.,

2005]. Until recently Mirza comprised only one species M. coquereli. In 2005 the second

species northern giant mouse lemur (M. zaza) was described in Kappeler et al. [2005]. Lately,

the presence of a third species was proposed [Gardner and Jasper, 2009] but has not been

confirmed yet.

2.2. Study site

The study took place at Ankarafa Forest, Sahamalaza, northwestern Madagascar, during

the dry season for 10 weeks from the beginning of May until mid of July. Ankarafa Forest is

situated on the Sahamalaza Peninsula, province Mahajanga, within the boundaries of the UN

Biosphere Reserve and Aire Protégée Marine et Côtière Sahamalaza – Iles Radama (Fig 1).

The national park extends between 13°52'S and 14°27'S, and 45°38'E and 47°46'E [Schwitzer

et al., 2007b]. It covers an area of 26,035 ha and includes marine, coastal and terrestrial zones

[Madagascar National Parks, no date]. Sahamalaza is biogeographically located in a transition

zone between the Sambirano evergreen rainforest domain in the north and the western dry

deciduous forest region in the south [Schwitzer and Lork, 2004; Schwitzer, 2005]. The strict

seasonal climate of this zone is represented by a dry and cool season from May to September

and a rainy and hot season from October to April [Schwitzer et al., 2007b]. Mean annual

rainfall is 1600 mm, mean annual temperature 28.0 °C and monthly temperatures range from

20.6 °C in August to 32.0 °C in November [Schwitzer et al., 2007b].

In general the vegetation is not consistent but shows characteristics of the two very

different domains that meet here. Due to traditional slash and burn agriculture and clearance

for cattle herds, only fragments of primary and secondary forest are left that are connected by

savannah areas (Fig. 1) [Schwitzer and Lork, 2004; Schwitzer et al., 2007b].

6

A primary and a secondary forest patch were selected as study sites as the animals were

believed to be present there. The primary forest “forest A” has been degraded by a forest fire

a few years ago, but is in progress of regeneration [Schwitzer, Seiler, pers. comm.].

“Forest B” does mainly represent “mature” secondary forest with a small part of primary

forest. Due to this rather unclear division into primary and secondary forest, I will continue

using the terms “forest A” and “forest B”.

7

Figure 1: Ankarafa Forest (above) with the two study sites forest A and forest B and the location of the camp. The research site is located on the Sahamalaza peninsula (below left) in northwestern Madagascar (below right).

A B

Camp

8

2.3. Data collection

Two teams were built until 21/06/2010 when the field assistant had to leave. The

principal researcher and one local guide made up one team while the field assistant and the

other field guide were another team. We conducted training to ensure observer reliability

[Martin and Bateson 1993], and the first week of radio-tracking and habitat sampling we

worked all together.

Two weeks at the end of June a very strong wind (called Varatraza, Schwitzer et al.,

2007b) caused many tree falls of trees up to 1.5 m DBH. Due to the associated danger,

especially at night when vision is limited, we had to stop working for several days.

2.3.1 Capturing Mirza zaza

We captured Mirza zaza using 24 to 30 live traps (Tomahawk Live Traps size 12).

Following the advice of experienced guides the traps were placed systematically in two

forests fragments. We baited the traps with banana in the evening and checked in the early

morning [Kappeler et al., 2005]. Because of the winter season nights can get cold. To avoid

too much energy loss of the animals in traps we sometimes controlled traps as early as 9 pm.

The first week we did not capture, hear or encounter any animal. After that, the animals

seemed to learn about the new “food source” and entered the traps relatively quickly. This

was especially the case during recapture when we caught 12 animals in one week. While

radio-tracking the animals we observed one female always visiting the traps first after

emerging from the nest and finding ways to reach the banana without entering traps (set for

Microcebus). Animals caught first got caught again for up to 5 times. Rats were released

immediately while Mirza zaza was carried to the camp for further procedure. We captured 8

animals in May. All of these could be recaptured in July. Another 4 animals were captured.

2.3.2 Morphology

We pushed the animals in a corner of a trap using clothes to restrain the animals and

anesthetized them briefly with Ketamine (0.01 ml/100 g body mass, 100 mg/ml) [Lahann,

2008]. First we weighed the animal with a standard kitchen scale (precise to 1 g) and sexed it.

Then, small ear biopsies (small cuts of 2 x 2 mm in the outer pinna) were taken with a special

Ear Punch (Kent Scientific Corporation, US) at different parts of the ear pinna for subsequent

identification. Tissue samples are currently analyzed at Hannover University to identify the

9

species, estimate genetic distance and determine relatedness of individuals. Teats and external

opening of the vagina were investigated to determine reproductive status of females

[following Stanger et al., 1995, Appendix 1]. Details about morphometric measurements can

be found in section 3. In preparation of the radio-tracking, an individual ring was cut into in

the fur of the tail for subsequent identification during the night [Kappeler, 1997a].

2.3.3 Radio-tracking and home ranges

Nocturnal species are not easy to study [Eberle and Kappeler, 2004]. Mittermeier et al.,

[2006] described Mirza as being highly active, which makes their identification and

observation difficult in the field. Thus, radio-tracking was used to receive a sufficient amount

of reliable data. Eight animals were fitted with TW3 rubber-coated cable tie radio-collars

(Biotrack Ltd., UK, 3-4 g, max. 2 % of body weight]. All collars were removed at the end of

the study. We used a TR-4 receiver (Telonics Inc., USA; frequency range 150.545–

150.969 MHz) and flexible Yagi antenna (Biotrack Ltd., UK) to locate the animals during the

night. Home ranges were determined by nightly follows of focal animals [Pimley et al., 2005].

Two teams followed the animals 6 days per week during two night shifts (18:00-0:00 and

00:00 to 05:00). Before 18:00 and after 5:00 nests were observed. We changed the focal

animal after approximately 2 hours of observation in order to receive a representative sample

of each animal over the whole field period. Methods for investigating home ranges are

outlines in section 4. Incremental area analyses for the all home ranges can be found in

Appendix 2.

2.3.4 Habitat and nest

During nightly follows, trees used by Mirza zaza were marked with a laminated number

and a thumbtack every 15 minutes, unless the animal stayed in the same tree.

Trees were described the next day by the variables tree species, tree height, diameter at

breast height (DBH), canopy size, number of lianas and number of connected trees

[Ruperti 2007; Schwitzer et al., 2007b]. The microhabitat was assessed using the point-

centred quarter method [Ganzhorn, 2003]. A used tree served as the centre point. The four

compass directions joining at the centre tree divided the microhabitat into four quadrants. The

distance to the nearest tree in each of the quadrant as well as the above-mentioned variables of

the four trees were measured. We always distinguished between large (10 cm DBH) and

small tree species (5 – 9.9 cm DBH) (Ruperti, 2007), except for section 3 where only large

10

trees were considered. Additionally, the canopy cover was measured by walking 2.5 m away

from the centre into northwest and vertically taking a photo of the canopy applying the same

zoom for each photo. I used Adobe Photoshop to calculate the percentage cover [Ganzhorn,

2003; Ruperti, 2007]. A 5 x 5 m plot was laid into the northwest quadrant adjacent to the tree.

Presence of cattle faeces, evidence of fire and tree stumps cut by humans was collected in this

plot to assess human disturbance [Ruperti, 2007; Schwitzer et al., 2007b]. Details about the

variables can be found in Appendix 3. The same variables were collected for random trees

and their microhabitat with a random tree as the centre point. Random trees were selected by

taking the minimum and maximum latitude and longitude of the group’s respective home

range and randomly computing locations within that area. We walked to the point using a

GPS device (Garmin GPS 60) and identified the nearest tree (bamboo > 3 cm DBH or tree

> 5 cm DBH) to that point which consequently served as a random tree.

Every 5 minutes we recorded the height of the animal, if it used a large (10 cm

diameter) or small tree (<10 cm) or a bamboo, and the support type (trunk, branch, leaves,

fork, liana) [Crompton and Andau, 1987; Martin and Bateson, 1993; Ganzhorn, 1995]. The

behaviour (moving, resting, feeding/foraging, grooming, playing, other) was noted and

feeding events were observed ad libitum [Martin and Bateson, 1993; Biebouw, 2009].

Descriptions of variables can be found in Appendix 3. If the animal was lost for longer than

15 minutes, we collected data the next time it was encountered. All height-related variables

were estimated by the researcher and the guide, and the mean of the estimates was taken

[Ruperti, 2007]. In retroperspective, the intensity of light was received by looking at moon

phases stored by the GPS device. The variable is described in Appendix 3. Details about nest

variables are given in section 5.

2.3.6 Analysis

Analysis and statistical tests performed are described separately in the following

chapters. Comparisons of morphology between different Mirza zaza populations and M.

coquereli in Kirindy have been performed using a one-way t-test and means from Kappeler et

al. [2005]. Prof. Kappeler kindly promised to send original data so that a parametric t-test can

be applied.

11

For submission as a manuscript of original research as required by the journal

FOLIA PRIMATOLOGICA

3. Morphology and reproduction of the northern giant mouse lemur Mirza zaza in Sahamalaza National Park, northwestern Madagascar

Johanna Rode Nocturnal Primate Research Group, Oxford Brookes University, Oxford, UK

Key words

Mirza zaza, Madagascar, seasonal reproduction, testes size, promiscuous

3.1. Introduction

If direct observations are difficult to obtain as it is the case for many nocturnal primate

species, size dimorphism, testes size, post copulative mechanisms and spatial distribution of

the different sexes are often used as indirect indicators of primate mating systems [Schwab,

2000]. While monogamous species are morphologically characterised by a lack of sexual

dimorphism and small testes size in males, physically competing males of polygynous species

are bigger than females but also have relatively small testes [Schwab, 2000; Harcourt et al.,

1981; Kenagy and Trombulak, 1986]. In contrast, species with a promiscuous mating system

(each sex mates with several individuals of the other sex, Bearder, 1999] do not show

intensive sexual dimorphism but have relatively large testes and males make use of

postcopulatory sperm plugs that seal the female vagina after mating [Schwab, 2000]. Large

testes and accordingly more sperm [Moller, 1998] are related to intensive sperm competition

and mating with several females [Kappeler, 1997a]. Body mass and testes size of promiscuous

species increase towards the onset of the mating season [Kappeler, 1997a; Schmid and

Kappeler, 1998].

In comparison to haplorrhini primate species, most strepsirrhines do not show marked

sexual dimorphism despite the existence of various mating system [Kappeler, 1990; Pochron

and Wright, 2002]. Furthermore, the harsh environment and seasonality of food in

Madagascar [Wright 1999] constrain most species to a short mating season that does not

allow males to monopolise receptive females [Ridley, 1986; Richard and Dewar, 1991;

Kappeler, 1991; Young et al., 1990; Harcourt et al., 1981].

12

The nocturnal strepsirrhini species Mirza zaza, Family Cheirogaleidae, was

distinguished from M. coquereli as a unique species in 2005 [Kappeler et al., 2005; taxonomy

see section 2.1]. M. zaza is a squirrel-sized nocturnal lemur that lives in the dry deciduous

forests of northwestern Madagascar. Several morphological variables differ between M. zaza

and M. coquereli, including a smaller overall size, but slightly larger testes [Kappeler et al.,

2005]. The geographical distribution of M. zaza seems to be limited by two large rivers, the

Maeverano River in the south and the Mahavavy in the north [Markolf et al., 2008]. Large

rivers are suggested to serve as species boundaries and the Sambirano River, crossing the

currently assumed distribution of M. zaza, could be another boundary [Craul et al., 2007].

Although an individual from Sahamalaza in the south of Sambirano was genetically tested as

M. zaza it could have morphological differences from the reference population of Ambato, in

the north of Sambirano. Due to large testes and loud oestrus calls M. zaza is suggested to have

a highly promiscuous mating system [Kappeler et al., 2005]. Their mating season is believed

to fall into July and August [Kappeler et al., 2005]. However, animals kept at the Duke

University Primate Centre, on which several behavioural and physiological studies were

conducted, cycled throughout the year and reproduced aseasonally [Stanger et al., 1995].

The aim of this study is to describe and compare the morphology of Mirza zaza from

Sahamalaza peninsula to M. zaza from Ambato and to test predictions about their

reproduction. Assuming that their mating season is restricted to July and August, testes size

and body mass of males should increase towards the end of the study that was conducted from

May to July. We should observe animals mating and capture females in oestrus in July. We

expect to only capture sub-adults with weights typical for animals born in October the

previous year but no smaller animals.

3.2. Methods

Details about the study site can be found in section 2.2. General proceedings of

capturing, anesthetizing, and material used are described in section 2.3. Animals were

captured in May and July in order to collect data before and during the mating season.

Standard morphometric measurements taken of adult Mirza zaza included body mass,

body length, tail length, head length and width, canine height, ear length and width, hind foot,

hand, upper and lower hind- and forelimb, testes length and width and state of the external

opening of the vagina [following Schmid and Kappeler, 1994; Stanger et al., 1995, details see

Appendix 1]. A standard tape measure and electronic calliper were used. Testes volume was

13

calculated with the formula for a regular ellipsoid V = 1/6 * (W2L) where W was the average

width of both testes and L was the length of the longest testis [Kappeler, 1997b]. Relative

testes size was calculated as the mean testes volume divided by mean body mass [Schwab,

2000]. Using the data set of 18 strepsirrhines in Kappeler [1997b] I calculated the regression

line y = 1.7x + 80.5, whereas y is the testes volume (mm3) and x is the body mass (g). I used

this equation to calculate the expected testes volume for M. zaza. It should be noted that

Stanger et al. [1995] calculated testes volume as one ellipsoid of both testes, while Kappeler

[1997b] calculated the volume for each testis and added both. Age was classified according to

body weight with 150-200 g juvenile, 200-250 g sub-adult and above 250 g adult [Kappeler et

al., 2005]. Mean of the measurements of both captures were compared to means from

Kappeler et al. [2005] for M. zaza animals from Ambato peninsula north of Sahamalaza

[13°25'S, 48°29'E] and M. coquereli animals from Kirindy national park in the south

[20°40'S, 44°39'E]. If not indicated differently all measurements are in mm. As mating was

predicted at the end of the study period, body weight, relative testes volume and the state of

the vagina of adult animals were compared between the first capture in May and the recapture

mid of July [Stanger et al., 1995; Schwab, 2000]. External injuries as a result of fighting were

checked for males [Kappeler, 1997a].

Statistical analyses were performed with SPSS 17.0. All body measurements were

normally distributed (One Sample Kolmogorov-Smirnov Goodness-of-Fit Test; Dytham,

2003). Since there was no difference in variables found between sexes using t-tests, animals

were combined and one-way t-tests computed to compare variables to means of animals from

Ambato and Kirindy [Dytham, 2003]. Repeated measures ANOVA was used for the

difference in weight, testes volume and relative testes volume between the first and second

capture [Dytham, 2003]. Significance level was set to P = 0.05.

3.3. Results

We captured eight animals in May and fitted them with radio collars. We recaptured

them in July. Four additional individuals were trapped at the end of the study (Table1).

14

Table 1: Identification codes, sex and age of all individuals captured at the given dates in Ankarafa forest research station in May and July 2010.

ID Sex Age 1. capture 2. capture M1 male adult 16/05/2010 11/07/2010 M2 male adult 18/05/2010 09/07/2010 F1 female adult 19/05/2010 09/07/2010 M3 male sub-adult 19/05/2010 10/07/2010 F2 female adult 22/05/2010 11/07/2010 M4 male adult 27/05/2010 18/07/2010 M5 male adult 28/05/2010 11/07/2010 F3 female sub-adult 29/05/2010 10/07/2010 M6 male adult 10/07/2010 F4 female juvenile 10/07/2010 M7 male sub-adult 13/07/2010 F5 female adult 17/07/2010

No difference in sex was found between weight or any morphometric measurements of

adult animals (Table 2). Compared to measurements of Mirza zaza from Ambato and M.

coquereli from Kirindy [Kappeler et al., 2005], we found several differences in morphometric

measurements (Fig. 2).

Figure 2: Proportional differences (in %) between the Sahamalaza population and Mirza zaza from Ambato and M. coquereli from Kirindy, respectively. The Sahamalaza population served as a reference and thus corresponds to 0 %. Significant differences of one-way t-tests are indicated by an asterisk.

body mass body length tail length head length head width canine height ear length hind foot femur tibia humerus radius testes

* * *

*

*

*

*

*

*

*

*

* *

*

15

Table 2: Descriptive statistics (mean and SD) for 18 morphometric variables of adult male (M) and female (F) Mirza zaza from Sahamalaza National Park.

Combined sex Males Females

Median Mean SD N Median Mean SD N Median Mean SD N

Weight [g] 284 283.13 17.65 8 290.3 283.92 20.81 6 280.8 280.75 0.35 2 HeadBody [cm] 22 22.31 0.75 8 22.3 22.5 0.77 6 21.8 21.75 0.35 2 Tail [cm] 30 30.28 0.54 8 30.1 30.17 0.54 6 30.6 30.63 0.53 2 Head L 56.8 56.23 1.34 7 56.2 55.92 1.49 5 57.0 57.03 0.28 2 Head W 32.8 33.10 2.17 7 32.9 33.44 2.14 5 32.3 32.26 2.8 2 Canine L 4.3 4.01 0.67 7 3.9 3.86 0.76 5 4.4 4.38 0.11 2 Canine W 2.5 2.34 a 0.69 4 2.6 2.34 0.84 3 2.3 2.34 . 1 EarL 27.1 27.08 1.38 8 27.1 26.98 1.46 6 27.4 27.37 1.57 2 EarW 16.0 16.08 a 0.77 8 15.9 15.91 0.82 6 16.6 16.56 0.48 2 Foot 57.6 57.11 2 8 57.2 56.69 2.1 6 58.4 58.37 1.35 2 Hand 33.6 33.09 a 2.87 8 33.6 32.61 3.17 6 34.5 34.53 1.38 2 Femur 60.9 60.71 4.49 8 60.9 61.24 4.57 6 59.1 59.11 5.44 2 Tibia 70.9 71.27 3.35 8 71.6 71.84 3.62 6 69.6 69.55 2.26 2 Humerus 47.5 47.37 2.43 8 48.0 47.82 2.38 6 46.0 46.04 2.88 2 Radius 44.1 44.85 2.99 8 44.1 44.38 2.46 6 46.3 46.27 5.2 2 Testes L 29.0 27.31 4.16 6 Testes W 31.7 30.33 a 6.05 6

Testes V [mm3] 11791.9 3545.02a 1840.63 6

Asterisks mark significant differences to means of animals from Ambato [Kappeler et al. 2005]. L = length, W = width, V = volume. SD = standard deviation of the mean.

a = not tested against Kappeler et al. [2005]

16

We observed Mirza zaza mating three times mid-June. F5 captured in July showed a

swollen, pink and wrinkled vagina which is typical for met-oestrus [Stanger et al., 1995]. The

average weight of the two sub-adult females F1 and F3 were 207.5 g (sd 7.78, n = 2 captures)

and 214 g (sd 8.49, n = 2 captures) while the sub-adult M7 weighed 231 g and the juvenile F4

144 g. F2 and F4 shared a nest and were believed to be mother and daughter. Although F4

seemed to roam independently from the mother, enlarged teats of F4 suggest ongoing

lactating. Compared to data from Duke University Primate Centre the two female sub-adults

should be between 165 and 179 days (F1) and between 186 and 221 days (F2) old at their

capture in May. M7 should be around 242 days in July. Calculating back, birth should have

taken place between mid of November and end of December the previous year. The juvenile

F4 should be around 80 days at her capture and thus born in April. Even though the juvenile

was very small and the mother was still lactating, it seemed to forage independently. The

mother was observed alone as well as in company of the juvenile during the night.

There was no difference found in the weight, absolute or relative testes volume between

the first capture in May and the second capture in July (weight: F = 1.103, P = 0.29; absolute

testes volume: F = 3.072, P = 0.16; relative testes volume: F = 3.014, P = 0.16). In all males

but one the relative testes volume was higher in July (Table 3). Testes volume in general

varied greatly between individuals. Mean relative testes volume of all male adults in July was

29.77 mm3/g [sd 9.67, n = 6]. Compared to the expected value of 987 mm3 average testes

volume of all adult Mirza zaza in July was 8336.23 mm2, more than 8 times higher.

Table 3: Weight, absolute and relative testes volume (testes volume divided by body mass) at the first and the second capture of 5 male individuals of Mirza zaza. Median, mean and standard deviation of the mean are given.

ID Weight 1 [g]

Weight 2 [g]

Testes Volume 1

[mm3]

Testes Volume 2

[mm3]

Rel. testes volume 1 [mm3/g]

Rel. testes volume 2 [mm3/g]

M1 294 318 990.57 3428.95 3.37 10.78 M2 256 247 9747.99 7309.94 38.08 29.59 M3 295 280 2714.95 9310.51 9.20 33.25 M4 264 269 6120.91 9225.01 23.19 34.29 M5 299 287 6475.69 9433.81 21.66 32.87 Median 294 280 6120.91 9225.01 21.66 32.87 Mean 281.60 280.20 5210.02 7741.64 19.10 28.16 sd 20.01 25.99 3429.79 2564.70 13.50 9.87

17

3.4. Discussion

Mirza zaza was described as being different from M. coquereli in 2005. Except for body

length M. zaza showed significantly smaller means for all test variables. The larger testes size

was not significant [Kappeler et al., 2005]. One animal from Sahamalaza Peninsula was

captured and genetically tested to be M. zaza [Schwitzer, pers. comm.]. In this study animals

from Sahamalaza were compared to means from animals in Kirindy [Kappeler et al., 2005],

and all significant results suggest smaller body measurements but bigger testes. This conforms

to previous differences found between M. zaza and M. coquereli [Kappeler et al., 2005].

However, the animals captured in Sahamalaza for this study also showed significant

differences in several variables to the population of M. zaza in Ambato. They had a smaller

body and smaller extremities, while the tail was longer and head and testes were larger than in

Ambato. Although differences can stem from inter-observer differences between the studies

or small sample size, differences found in several variables lead us to conclude that the

Sahamalaza population differs morphologically from Ambato population.

Several authors emphasised the importance of large rivers as geographic boundaries in

Madagascar [Craul et al., 2007; Olivieri et al., 2007]. Craul et al. [2007], who examined

phylogenetic relationships within Lepilemur, suggested an “eight Inter-River-System” that

separates the regions north and south from Sambirano river. This would split the areas of

Sahamalaza and Ambato. In respect to Lepilemur this border acts like a barrier, with L.

dorsalis in the north and L. sahamalazaensis and L. mittermeieri in the south accepted as full

species [Craul et al., 2007; Andriaholinirina et al., 2006; Rabarivola et al., 2006]. Yoder et al.

[2000] stress that only a combination of physical, historical, and biological differences

between populations should lead to a species classification. Additionally, several authors are

concerned about the steep increase of lemur species in the last decades, which makes it hard

for conservationists to define priorities and target their efforts [e.g. Tattersall, 2007]. Genetic

samples of the Sahamalaza animals are currently analysed and may clarify matters. However,

we suggest undertaking further surveys to avoid spotty sampling.

In order to prepare for high activity and sperm competition during the short mating

season promiscuous lemur species like Microcebus murinus [Schmid and Kappeler, 1998],

Mirza coquereli [Kappeler, 1997b] or Galago moholi [Pullen et al., 2000] show an increase of

male body weight and testes volume. In M. zaza no significant increase in weight, relative or

absolute testes volume could be found towards the onset of the presumed mating season. One

explanation could be unfortunate sampling timing if mating already took place in June, the

18

middle of the study. Combination of data available from literature and this study rather

suggests that mating is not restricted to a discrete season but can take place all year round

(Table 4). Interbirth intervals between successfully raised litters in captivity ranged between 7

and 15 months [Stanger et al., 1995]. In lemurs, seasonal reproduction may be promoted by

seasonal variations in food availability. M. zaza was observed to feed on the sugary secretions

of the larvae of Homopteran Flatidae in the dry season [Rode, 2010]. This and the geographic

situation of Sahamalaza between the dry western forests and more humid Sambirano region,

resulting in less trees shedding leaves, might allow a more flexible timing of reproduction in

M. zaza. The juvenile F4 found in this study clearly grew up during the dry season but seemed

to be in a very good health.

Table 4: Summary of suspected birth and mating season of Mirza zaza. If only birth or only mating time was known, the missing variable was calculated using the gestation time of approximately 3 months. Methods are mentioned to clarify how conclusions about mating season were drawn.

Birth Mating Method Source

December to February September to November

Estimated from weights of sub-adults

Pages, 1980

September Early June Pregnancy of wild-captured female

Stanger et al., 1995

March, September December, June Observations of captive animals under Madagascar time

Stanger et al., 1995

September June Observation of mating This study

October July Capture of female in met-oestrus

This study

November/December and April

August/September and January

Estimated from weights of sub-adults (n=3) and a juvenile (n=1)

This studya

a Weights from captivity for comparison in this study stem from only two sets of twins. Although twins might be lighter than singletons, food supply in captivity might be better and primates are often overweight [Schwitzer and Kaumanns, 2003]. Accordingly, estimated birth months should be treated with caution.

As nocturnal predators mainly rely on sound for hunting, living in groups is not

advantageous for prey species and thus, many nocturnal primates are solitary during their

nightly activity [Kappeler, 1997c]. However, a variety of social systems exist in nocturnal

strepsirrhini, e.g. dispersed pairs [e.g. Cheirogaleus medius, Fietz, 1999b] or dispersed

promiscuous groups [e.g. Microcebus ravelobensis, Weidt et al., 2004] that forage solitarily

19

but reunite during the day. Information presented in Table 5 indicates a promiscuous mating

system in Mirza zaza except for the lack of sexual dimorphism.

Table 5: Summary of morphological and behavioural characteristics of Mirza zaza that give an indication of the mating system. Examples of other species exhibiting the respective characteristics are given.

Characteristic of M. zaza Source Mating system Similar species source

No sexual dimorphism

This study; Stanger et al., 1995

Monogamous, polyandrous; but most strepsirrhines regardless of mating system

Aotus spp. Cheirogaleus major

Kappeler, 1997c Fietz, 1999a

Estrous call Stanger-Hall, unpublished data

Promiscuous Mirza, microcebus Daubentonia

Stanger, 1993 Sterling, 1993; Stanger and Macedonia 1994

Large relative testes

This study; Stanger et al., 1995; Kappeler 1997a

Promiscuous, polygynous with sperm competition

Microcebus cf myoxinus Mirza coquereli Microcebus murinus

Schwab, 2000 Kappeler, 1997b Fietz, 1999a

Copulatory plug

Stanger et al., 1995

Promiscuous, polygynous with sperm competition

Microcebus cf myoxinus Microcebus murinus

Schwab 2000 Eberle and Kappeler, 2004

Kappeler [1990] suggested that lemurs of Madagascar may be more selected for speed

and agility than strength and body size, which is mostly used for indicating sexual

dimorphism [Leutenegger, 1978]. However, information about spatial distribution of the sexes

does not necessarily support a promiscuous mating system in Mirza zaza [Rode, 2010].

Details can be found in section 3. Compared to M. coquereli, where injuries are more

common in males compared to females in the mating season [Schwab, 2000; Kappeler,

1997a], sperm plugs, oestrus calls and lack in injuries in M. zaza emphasise a higher

importance of sperm competition and higher promiscuity. Especially striking is the enormous

testes volume of M. zaza. Using the width of both testes at their broadest point to calculate

volume, mean testes volume for this study of 15.483 cm3 was very similar to testes volume of

13.63 cm3 in captivity [Stanger et al., 1995]. This corresponds to 8 times the volume normally

expected for strepsirrhines [Kappeler, 1997a]. Compared from available data for other primate

species [Harcourt et al., 1981; Kenagy and Trombulak, 1986; Kappeler 1997b; Schwab, 2000]

20

M. zaza has the largest testes among primates and values rather range among typical values

for some rodent species [Kenagy and Trombulak, 1986].

3.5. Conclusions

1. If genetic analyses point to a difference between Mirza zaza in Sahamalaza and M.

zaza north from the Sambirano River additional to the data presented here, we

recommend further surveys and the inclusion of several methods to describe a new

taxon on species or subspecies level.

2. Mirza zaza in the wild is not restricted to a short mating season but reproduces

throughout the year.

3. Morphological and behavioural data, especially large testes size, suggests that Mirza

zaza shows a highly promiscuous mating system.

4. Mirza zaza has the relatively largest testes among primates.

21

For submission as a manuscript of original research as required by the journal

ENDANGERED SPECIES RESEARCH

4. Conservation implications of home range and habitat use of the northern giant mouse lemur Mirza zaza, in Sahamalaza, northwestern

Madagascar

Johanna Rode Nocturnal Primate Research Group, Oxford Brookes University, Oxford, UK

KEY WORDS: Mirza zaza, Madagascar, home range, microhabitat use, reforestation,

conservation

4.1. Introduction

Madagascar is one of the most important biodiversity hotspots in the world,

underpinned by its high proportion of endemic species and high rates of deforestation (Myers

et al. 2000, Mittermeier et al. in press). The last years have been characterized by an

enormous increase of lemur species diversity. Between 2000 and 2008, 39 species were newly

described and 9 other taxa resurrected (Mittermeier et al. 2008). The lack of species-specific

knowledge makes it impossible to determine IUCN Red List status, resulting in 45 % of all

Malagasy primate species being Red-Listed as Data Deficient (IUCN 2009). More than 85 %

of the Data Deficient lemur species are nocturnal (IUCN 2009), which might partly be due to

difficulties inherent in studying them (Eberle & Kappeler 2004). The situation has led to

increased concern among ecologists and conservationists (Tattersall 2007) since a thorough

understanding of the biology and ecology of species is needed to design effective

conservation measures (Schwab & Ganzhorn 2004, Merker et al. 2005, Schwitzer et al.

2007b).

This study provides information about home range size, home range overlap and

microhabitat use of a least known nocturnal lemur, the northern giant mouse lemur Mirza

zaza. A home range is generally defined as the “area repeatedly traversed by an animal”

(Kenward 2001, p. 208). Home range patterns have been used to define the rather elusive

social organisation of primate species (e.g. Harcourt & Nash 1986, Müller 1998) while

22

microhabitat use has widely been applied to investigate competition between sympatric

species, e.g. in different lemur communities (Rendings et al. 2003, Lahann 2008) or desert

rodents (Price 1978). Information about home range use and habitat requirements however is

also crucial for conservation activities (Merker et al. 2005, Neilson et al. 2006, Schwitzer et

al. 2007b). Home range sizes give an indication about the species’ space requirement which

should be incorporated in habitat management plans (Crompton & Andau 1986). For different

species like Dian’s tarsier (Tarsius dianae, Merker et al. 2005) or the Hawaiian bird 'Elepaio

(Chasiempis sandwichensis, VanderWerf 1993) it was found that home range size increases in

lower quality habitat e.g. in secondary forests due to the animal’s need to find sufficient

resources. Microhabitat preferences can be used to model the species distribution and

abundance (Rendings et al. 2003, Chouteau 2004) and help to give recommendations for

effective conservation measures as knowledge about importance of certain microhabitat

variables can help to manage endangered populations more effectively (Crompton & Andau

1986, Rendings et al. 2003, Chouteau 2004). Preferences are assumed if use intensity of

certain microhabitat variables differs from that of generally available microhabitat

(Adrianasolo et al. 2006, Neilson et al. 2006), or if used variables do not co-vary with

variations between different habitat types (Schwitzer et al. 2007b, Adrianasolo et al. 2006).

The northern giant mouse lemur Mirza zaza, Family Cheirogeleidae, is one of the

nocturnal lemur species for which detailed ecological data are lacking. It lives in the

northwestern deciduous lowland forests of Madagascar up to the transition zone to the

Sambirano evergreen rainforest domain in the north (Kappeler et al. 2005, Markolf et al.

2008). Due to a highly fragmented range of 15,000 km2 (IUCN 2009) the species is very

likely to be “threatened” (Markolf et al. 2008). The only population estimates so far yielded

the highest encounter rates in degraded forests with a high number of mango trees (Mangifera

indica, Family Anacardiaceae), the fruits of which may be beneficial to Mirza zaza (Markolf

et al. 2008, Mittermeier pers. comm.). Apart from this, nothing is known about the ecological

requirements of M. zaza. Western dry forest is one of the forest types declining the most

quickly in Madagascar and due to ongoing threats to remaining and already heavily

fragmented forests where M. zaza occurs (Schwitzer and Lork 2004, Schwitzer et al. 2007b)

information on its ecological needs are required to design effective conservation plans.

In order to facilitate the planning of conservation measures and provide information that

could help to clarify the uncertain status of Mirza zaza I address three main questions. First,

what are group and individual home range size and overlap of M. zaza? Such data can be used

to estimate the total population size in Sahamalaza and the species’ entire range. Second, how

23

does M. zaza use its habitat in terms of height and position in trees? Third, what are

microhabitat requirements of M. zaza?

4.2. Methods

Study site and capturing. Please refer to section 2 for details and a map of the study

site, for capturing and handling of the animals.

Data collection. Data collection of light variables and tree and microhabitat variables is

described in section 2.3. Radio-tracking was used to follow the animals during the night (see

section 2.3.3). We aimed for 15 minutes interval between GPS location of the focal animal

(Harris et al. 1990) but due to erratic encounters and regular loss of the animal we also

collected data after shorter intervals (Schwitzer, Nekaris pers. comm.). Close triangulation

was applied in some cases. We used a Garmin GPS 60. We did not use locations with a lower

precision than 15 m and mean precision was 8 m. Home ranges were calculated as 100 %

Minimum Convex Polygon (MCP) and 95 % fixed kernel with smoothing multiplier = 1 and

matrix set to the number of cells (n = 40). MCP draws a line around the outmost locations of

an area to build a polygon (Kenward 2001). Even though this method is known to include

areas which might have never been visited by the animal and thus might overestimate the

home range (Kenward 2001, Pimley et al. 2005), it was chosen for better comparability as it is

used in many ecological studies (Harris et al. 1990). 95% kernel method depends on the use

intensity of different areas. Different centres of activity are possible, excursions of the animal

are excluded and thus, home range estimates are more accurate (Kenward 2001, Pimley et al.

2005). Each nest site used by the animals was included only once as we controlled the nest

sites every day and wanted to avoid an overrepresentation of these areas. Group home ranges

referrs to home ranges of one nest group. Home range size and overlap were analysed with

RANGES 8.5 (Anatrack Ltd., UK). The home range size for several animals did not

asymptote. This can be the case if animals shift their home ranges or simply when not enough

locations have been sampled (Harris et al. 1990).

Data analysis. Differences in height classes used by the animals between forests and

between the first and second half of the night (before and after midnight respectively) were

calculated with a Pearson’s chi-square test while influence on light intensity was calculated

using a Kruskal Wallis test. Preferences towards habitat were investigated by comparing used

and random trees as well as used and random microhabitat (Adrianasolo et al. 2006, Neilson

et al. 2006). Random trees and microhabitats were additionally compared between forests. If

24

differences were found I investigated if used habitat fluctuated as well. If not, this was taken

as an indication that the animals have preferences in respect to this variable as only generalists

are expected to co-vary with the habitat structure and to use the available resources

indiscriminately (Adrianasolo et al. 2006, Schwitzer et al. 2007b). As none of the habitat

variables were normally distributed, differences between used and random trees as well as

between used and random microhabitat were calculated with non-parametric Kruskal Wallis

tests. Four Mann-Whitney U tests (two-tailed) were used as post hoc tests. According to

Bonferroni correction significance level was set to P = 0.0125 (Cabin & Mitchell 2000).

Species preferences were investigated by computing Pearson’s chi-square tests. For this test

the most frequently used trees species were selected (between 4 and 11 species) in order to

avoid more than 20 % of the expected counts being lower than 5 (Dytham 2003). Species

preferences could not be investigated for small used and random trees because of low sample

size. All statistical tests were performed with SPSS 17.0 and followed Dytham (2003).

4.3. Results

We captured 12 animals and radio-collared 8 of them (Table 6). These 8 individuals

stemmed from three nest groups. In two groups all individuals were radio-collared while only

one individual was radio-collared in group 2, which consisted of this animal, a juvenile and

occasionally an unidentified adult. Details about the other four individuals can be found in

Rode (2010).

Table 6: Mirza zaza captured in May and July 2010. Identification code, stable nest group the animal was belonging to and total number of waypoints (GPS locations taken during nightly follows) are given. Total numbers of waypoints include nest waypoints while nest waypoints were listed separately.

Nest group

Focal individual Sex Reproductive

age Radio-tracked Total waypoints

Nest waypoints

From To 1 M1 male adult 20/05/2010 08/07/2010 19 1 1 M2 male adult 26/05/2010 09/07/2010 12 1 1 F1 female sub-adult 25/05/2010 09/07/2010 80 1 1 M3 male adult 27/05/2010 10/07/2010 19 1 2 F2 female adult 26/05/2010 11/07/2010 14 3 3 M4 male adult 27/05/2010 13/07/2010 83 3 3 M5 male adult 28/05/2010 12/07/2010 49 3 3 F3 female sub-adult 28/05/2010 13/07/2010 90 3

25

Group home ranges

The MCP method yielded group home range sizes of 0.97 ha and 2.34 ha for group 1

and 3 respectively, whereas the 95 % kernel method yielded 0.52 ha and 1.59 ha respectively.

Since these groups lived in different forests there was no overlap. The home range of F2 (the

single collared individual of group 2 and thus regarded as a separate nest group here), as

calculated using the MCP method, overlapped with 14 % of nest group 1’s home range, while

the home range of nest group 1 overlapped with 7 % of F2’s home range (Fig. 2). Using the

95% kernel method there was no overlap between nest group 1 and F2.

Figure 2: Home range overlap between nest group 1 and individual F2, using MCP method.

Individual home ranges

The MCP method gave individual home range sizes of 1.28 ha while the 95% kernel

method gave 1.02 ha (Table 7). Mean individual home ranges increased when ranges that did

not asymptote were excluded. There were differences between individuals but no consistent

differences between sexes. Individual home ranges calculated with MCP overlapped to a high

extent (Fig. 3) but less when calculated with 95 % kernel (Table 8, Fig. 4).

26

Table 7: Individual home ranges for 8 animals of Mirza zaza, as calculated using MCP and 95 % kernel method. a = home range size of animal did not asymptote and thus may be not representative. To account for this, a mean without these animals was calculated as well.

Home range (ha) ID 100 % MCP 95 % kernel

M1 0.58a 0.44a M2 0.51a 0.28a F1 0.84 0.31 M3 0.63a 0.57a F2 1.99a 1.58a M4 1.92 1.82 M5 2.21a 2.20 F3 1.55 0.95 Mean ± SD 1.28 ±0.71 1.02 ± 0.75 Mean ± SD (excluding a) 1.44 ± 0.55 1.32 ± 0.85 Male mean ± SD 1.17 ± 0,82 0.95 ± 0.63 Female mean ± SD 1.46 ± 0,58 1.06 ± 0.88

Figure 3: Individual home ranges for groups 1, 2 and 3 in two forests A and B, and overlap, using MCP method. Nest sites are indicated.

27

Figure 4: Individual home ranges for groups 1, 2 and 3 in two forests A and B, and overlap, using 95 % kernel method. Nest sites are indicated.

Table 8: Home range overlap between individuals of group 1 and 3 respectively, as calculated with MCP and 95 % kernel method. Percentages show how much the individuals in the table rows overlap with the individuals of the table columns.

Group 1 Group 3 Percentage overlap between MCP home ranges M1 M2 F1 M3 M4 M5 F3

M1 58 90 75 M4 95 72 M2 65 98 74 M5 82 65 F1 62 60 67 F3 89 92 M3 69 60 90

Percentage overlap between kernel home ranges M1 M2 F1 M3 M4 M5 F3

M1 37 49 44 M4 91 51 M2 59 46 69 M5 75 43 F1 70 41 42 F3 100 99 M3 35 34 23

28

Support type and strata used

The animals were found on median height of 7 m (range 0-25 m, n = 326) (Fig. 5). They

were observed at heights of 1 m or lower on several occasions. There was no difference in

used height classes between forests (Z = -1.721, P = 0.085) and between the first and the

second part of the night (Z = -0.311, P = 0.756), and also no influence of light intensity on use

of height classes (Kruskal Wallis test = 1.255, P = 0.869). On most occasions we saw Mirza

zaza on branches (45.3 %) or tree trunks (28.4 %). They were seen less often in the leaves

(12.7 %). The rest of the time we observed them on lianas and forks.

Figure 5: Percentage (%) of height classes used by 8 individuals Mirza zaza in forest A and B during nocturnal activity. N = 326.

Comparison between used and random trees, and used and random microhabitat

During their nocturnal activity Mirza zaza used more big trees and fewer small trees and

bamboo in both forests compared to the composition of random points in the forest (Fig. 6).

There were significantly fewer big trees and more small trees among random trees compared

to trees used by the animals (2 = 19.38, P < 0.001).

29

Figure 6: Percentage of tree types used by Mirza zaza compared to random trees.

Used large trees in forest B had significantly higher DBH, larger canopy diameter and

higher connectivity than random trees (Table 9). Large trees in Forest A and small trees in

both forests showed no difference between variables. In respect to the microhabitat, used

microhabitat (large trees) was significantly more interconnected in forest B and used small

trees had a smaller canopy diameter compared to random microhabitat (Table 10). In forest A,

both large trees and small trees showed a smaller distance to the centre tree in used

microhabitat compared to random microhabitat.

Table 9: Medians for 5 variables of used and random trees in two forests A and B. Empty cells indicate where no data were available. Significance level was set to P < 0.0125 and indicated by p < 0.05 (*), p < 0.01 **, p < 0.001 ***.

Median

Used A Random A Used B Random B

Height of large trees (m) 12.00 12.00 12.00 13.00 Height of small trees (m) 6.00 7.25 9.00 8.00 DBH of large trees (cm) 17.63 16.62 18.78(*) 15.28 DBH of small trees (cm) 7.32 6.89 7.00 6.90 Canopy diameter of large trees (m) 6.00 5.88 6.00** 5.00 Canopy diameter of small trees (m) 3.00 3.00 2.50 2.50 Lianas of large trees (no.) 2 2 2 Lianas of small trees (no.) 1 2 1 Connectivity of large trees (m) 3 4*** 2 Connectivity of small trees (m) 2 2 1 N large trees

55 DBH: n = 164

Height and canopy diameter:

n = 65 45 228

N small trees 15

DBH: n = 150 Height and

canopy diameter: n = 63

11 232

Used n = 73

Random n = 52

30

Table 10: Medians for 7 variables of used and random microhabitat in two forests A and B. Empty cells indicate where no data were available. Significance level was set to P < 0.0125 and indicated by p < 0.05 (*), p < 0.01 **, p < 0.001 ***.

Median

Used A Random A Used B Random B

Height of large trees (m) 12.50 12.00 12.50 Height of small trees (m) 7.25 8.00 8.00 DBH of large trees (cm) 14.00** 16.30 14.00 15.40 DBH of small trees (cm) 6.70 6.80 6.70 6.70 Canopy diameter of large trees (m) 5.90 4.50 5.00 Canopy diameter of small trees (m) 3.00 2.00*** 2.50 Lianas of large trees (no.) 2 2 Lianas of small trees (no.) 1 1 Connectivity of large trees (no.) 3** 2 Connectivity of small trees (no.) 2(*) 1 Distance of large trees (m) 3.98** 4.69 3.90 3.85 Distance of small trees (m) 2.98*** 4.07 2.96 3.25

N of large trees 204 DBH: n = 196

Height and canopy diameter

n = 60 212 208

N of small trees 204 DBH: n = 182

Height and canopy diameter

n = 60 212 208

Canopy cover (%) 84 85 N of canopy cover 47 50

Difference between forests

Random large trees in forest A had a significantly larger canopy diameter than in forest

B (Z = -3.796, P < 0.001). This difference was not found in used large trees between forests.

In respect to small trees, canopy diameter (Z = -3.763, P< 0.001) and height (Z = -2.524,

P < 0.05) differed significantly between forests in random microhabitat, but not in used

microhabitat.

In respect to microhabitat (large trees) there was a significant difference found between

forests in canopy size (Z = -3.952, P < 0.001, n = 268) and distance to the centre (Z = -4.008,

P < 0.001, n = 403). Canopy diameter could not be compared. Small trees also differed

significantly in canopy size (Z = -3.4, P < 0.01) and distance between forests (Z = -4.266,

P < 0.001). No such difference was found between the used microhabitat (large and small

trees) between the forests in distance.

31

Disturbance

There was no significant difference in number of stumps and evidence of fire between

used and random microhabitat but cattle faeces were significantly more found in used

microhabitats (Z = -7.713, P < 0.01, n =105).

Tree species

Tree species used most often during nightly activity of Mirza zaza in both forests are

listed in Table 11. In forest A animals used Albizia gummifera, Family Fabaceae, more often

than expected while in forest B it was Mangifera indica, Family Anacardiaceae (2= 16.894;

P < 0.01). In respect to microhabitat (large trees) Mirza zaza used Mascarenhasia

arborescens, Family Apocynaceae, and Petalodiscus platyrachis, Family Euphorbiaceae

(Malagasy name Kiropoka), in large trees more than expected (2 = 30.11; P < 0.001) but

there was no preference for species found in small trees.

Table 11: Tree species, families and Malagasy names of large and small trees used most often by Mirza zaza during their nightly activity. Total count and percentage of all trees collected are given. Trees n = 99, microhabitat n = 234.

Species Family Malagasy name Count %

Trees

Mangifera indica Anacardiaceae Manga 19 19.2

Macarisia lauciolata Rhizophoraceae Kirontsana 14 14.1

Albizia gummifera Fabaceae Sambalahy 12 12.1

Grangeria porosa Chrysobalanaceae Morasiro 8 8.1

Garcinia pauciflora Clusiaceae Taranta 8 8.1

Microhabitat

Macarisia lauciolata Rhizophoraceae Kirontsana 46 19.7

Mangifera indica Anacardiaceae Manga 30 12.8

Garcinia pauciflora Clusiaceae Taranta 21 9.0

Mascarenhasia arborescens Apocynaceae Gidroa 15 6.4

Grewia boinensis Malvaceae Selivato 10 4.3

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4.4. Discussion

Analysing home range overlap of Mirza zaza using the MCP method revealed only

slight overlap of the two neighbouring home ranges, whereas using 95 % kernel method, there

was no overlap at all. The relative exclusiveness of group home ranges was supported by the

fact that we saw only one uncollared animal (together with M5 at the periphery of its

individual home range) while following focal animals during the whole study period. There

was no obvious difference between male and female individual home range size. Individual

home ranges overlapped extensively between 60 and 98 % (MCP), which is expected for

animals living in dispersed pairs like in Phaner furcifer (Schülke & Kappeler 2003) or family

groups like Cheirogaleus major and C. medius (Lahann 2008). Promiscuous mating system

was suggested for Mirza zaza due to its large testes (Kappeler et al. 2005, Rode 2010). Males

of promiscuous M. coquereli increased their home range to 25 ha in the mating season

(Kappeler 1997a). July was the proposed mating season of M. zaza (Kappeler et al. 2005) but

males do not seem to increase their home range. Possibly, groups use the same core home

range while males search the periphery for other females in addition to the mating female in

the group. Genetic analysis should reveal whether groups are close relatives or breeding

groups. Another explanation is that group living may be an artefact of small fragment size that

forces animals to share habitat. Due to affiliative social behaviour observed we do not think

that the social organisation is unusual in these groups. F3 for instance spent 20% of the

observations in close proximity (< 5 m) with one of the males. Quiet “Hn”- calls were noticed

very frequently. Mirza and Cheirogaleus emit these calls during locomotion and meetings

with familiar individuals suggest that animals stay in close contact during the night (Pages

1980, Stanger 1993).

Compared to Mirza coquereli with a mean individual home range size of 4 ha,

individual and group home ranges of M. zaza were relatively small (max. 2.34 ha for group

home ranges and max. 2.21 ha for individual home ranges, calculated as MCP). Because dry

season is less severe in the range of M. zaza (Schwitzer 2005) animals may not require as

much space. In contrast home ranges could be limited by suitable forest available. The home

range of group 1 for instance was limited on three sides by another animal’s range, savannah

and bamboo forest (Fig. 3). It was also difficult to follow animals as no systematic paths were

established in order not to destroy remaining forest, and many areas were impenetrable due to

thick understorey and erosion holes (personal observation).

33

Pages (1978) observed Mirza coquereli in heights of on average 4.5 m (range 1 – 8 m).

M. zaza ranged on heights between 0 and 25 m. The apparent flexibility in height use seems to

be an advantage as vertical stratification is suggested to mitigate interspecific competition in

lemurs (Lahann 2008).

In respect to the composition of small, large trees and bamboos, Mirza zaza preferred

large trees. High connectivity of used trees and small distances to other trees are favoured.

Canopy diameter was preferred to be higher in forest B but lower in forest A. This

contradiction can be explained by a possible negative relation between distance between trees

and canopy diameter. Forest A was much degraded, distances between trees were large and

accordingly canopy had more space to develop. If denser areas are preferred this would then

relate to smaller canopy diameter. The preference towards small canopy diameter thus would

not show up in the denser forest B. Even though Ganzhorn (1995) found that M. coquereli

benefits from selective logging and small disturbances increase forest productivity (Ganzhorn

et al. 1997) we suggest that selective logging would only be acceptable if it does not decrease

the density of trees under a critical value. Distances preferred were approximately 4 m

between large trees and 3 m between small trees in both forests. This corresponds to 625 large

and 1111 small trees per hectare. Selective logging should only take place if densities are

higher. If reforestation is planned, these values should be taken into account. Although no

preference for trees with many lianas was apparent in this study, M. coquereli was found to

spent 60 % of their feeding time and 50 % of the feeding observations licking at branches of

the vines Hippocratea or Elachyptera minimiflora colonised by aggregations of homopteran

Flatidae larva and cochineals (Petter 1978, Hladik et al. 1980, Pages 1980).They also take up

the liquid directly from the adults and distribution of M. coquereli seemed to depend more on

the insects than on larva colonies (Pages 1980). The feeding preference was suggested to

allow the relatively small-bodied M. coquereli to stay active during dry season (Hladik et al.

1980). We observed M. zaza feeding on this larva two times but only on one occasion on a

liana. However, it would be interesting to determine in which microhabitat Flatidae is found

and if this coincides with preferences of M. zaza.

Disturbance measured as tree stumps and evidence offire seemed not to be important for

microhabitat selection of Mirza zaza. In contrast, more faeces were found in used

microhabitat than in random. Janzen (1988) states that in tropical dry forests cattle grazing is

a possibility to restore old pastures because animals feed on grass which competes with

saplings and burns very quickly. However, it is not clear if this would be also the case in

Madagascar.

34

Several tree species were favoured by Mirza zaza. Preference of Manga trees

(Mangifera indica) was expected because encounter rates were highest in forests with many

of these fruit trees (Markolf et al. 2008, Mittermeier, pers. comm.). This could be confirmed.

Manga trees are regarded as useful trees by the human population and are often the last trees

remaining in deforested areas (Schwitzer pers. comm., personal observation). The home range

of group 3 coincided with the only primary forest Manga tree patch in the respective forest.

Another tree preferred by Mirza zaza was Petalodiscus platyrachis. Interestingly the

Malagasy name Kiropoka translates into „Lemur tree“ which emphasises the local knowledge

of the ecosystem. The sympatric Lepilemur sahamalazensis was found to feed on Mangifera

indica and Albizia gummifera (Ruperti 2007). As lepilemur is folivorous it is probably not

competing with Mirza zaza.

4.5. Conclusions and conservation recommendations

Based on our results and the fact that much of the habitat in Sahamalaza is already

highly fragmented we recommend protecting the remaining habitat, especially large tree and

intact dense forest areas. Selective logging should only occur in areas with more than

approximately 625 large and 1100 small trees per hectare. Recovery of degraded forests

should be allowed. When reforestation programmes are planned preferred tree species of

Mirza zaza and target density of trees should be taken into account. The space requirements of

Mirza zaza could assist in the clarification of its Red List status.

35

For submission as a manuscript of original research as required by the journal

LEMUR NEWS

5. Characteristics and use of nests and nest sites of the northern giant mouse lemur Mirza zaza, in Sahamalaza, northwestern Madagascar

Johanna Rode

Nocturnal Primate Research Group, Oxford Brookes University, Oxford, UK

Key words

Mirza zaza, Madagascar, nest use, social organisation, conservation

5.1. Introduction Security offered by shelters is an important aspect in the survival and reproduction of

many small mammals including strepsirrhines that are generally nocturnal to avoid predation

(Terborgh and Janson 1986, Anderson 1998, Kappeler 1998). Different types of shelters

include tree holes or cavities, dense vegetation tangles and self-constructed or abandoned leaf

nests (Bearder et al. 2003). Shelters provide protection against predators, especially when

raising young, maintain good health through thermoregulation, protect against environmental

conditions and facilitate social relations (Anderson 1998; Schmid 1998; Thorén et al. 2010;

Perret 1998; Aquino and Encarnación 1986; Kappeler 1998). Although tree holes are

generally regarded as higher quality shelters (Schmid 1998; Radespiel et al. 1998),

constructing leaf nests has a high adaptive potential due to independence from pre-formed tree

cavities and possible immediate and flexible responses to environmental changes (Thorén et

al. 2010). While some taxa like Varecia variegata only use nests in the breeding season to

hide their altricial infants (Kappeler 1998), many nocturnal lemurs also spend the days in leaf

nests as adults. Detailed information on regular leaf nest use is only available for some

strepsirrhini species, for example Galagoides, Galago and Otolemur (Bearder and Doyle

1974; Bearder et al. 2003), several mouse lemurs like Microcebus ravelobensis (Weidt et al.

2004; Thorén et al. 2010) or M. murinus (Radespiel et al. 1998), Mirza coquereli (Sarikaya

and Kappeler 1997), Cheirogaleus major (Wright and Martin 1995) and Daubentonia

madagascariensis (Ancrenaz et al. 1994; Sterling 1993). Type and location of nests as well as

structural characteristics probably have a crucial impact on the survival and reproduction for

36

nest-using species (Wells et al. 2006) and respective information about this important

resource will be essential in conservation planning.

Mirza zaza, distinguished from M. coquereli as a separate species in 2005 (Kappeler et

al. 2005), is one of the nocturnal lemur species in Madagascar that uses arboreal leaf nests as

shelters during the day (Kappeler et al. 2005). The species is Red-Listed as Data Deficient but

its restricted and highly fragmented distribution of as little as 2000 km2 (calculated using

distribution data of Markolf et al. 2008 and vegetation data of Moat and Smith 2007) suggests

that it is very likely to be Endangered (Markolf et al. 2008). Due to ongoing threats to

remaining and already heavily fragmented forests where M. zaza occurs (Schwitzer and Lork

2004; Schwitzer et al. 2007b) information on its ecological needs is urgently required to

design effective conservation measures.

The size of nests limits the number and body size of animals seeking shelter during the

day. In stark contrast to its sister species Mirza coquereli, that has never been observed to

share nests (Kappeler 1997a), M. zaza sleeps in nests with 2-8 individuals (Kappeler et al.

2005). In captivity the large spherical nests of M. zaza are 50 cm in diameter and all

individuals, males, females and young, contribute to their construction (Pages 1980). Large

nests might become unstable and disintegrate with time, as exhibited in possums

(Lindenmeyer et al. 2008), which might set an upper limit for nest size. Support and location

seem to be important conditions for a good nest. Structure, stability and texture of branches

must be appropriate and materials for construction available (Wells et al. 2006). The height

and position of nests may have an impact on thermoregulation including exposure to sun and

rain or humidity (Bearder et al. 2003). The self-constructed nests of M. coquereli in Kirindy

were built a few meters below the top of Securinega (Family Euphorbiaceae) trees (Sarikaya

and Kappeler 1997) while Pages (1980) suggests heights of 2-10 m in trees that do not shed

their leaves (e.g. Euphorbiaceae) and are covered in lianas.

Sleeping in nests in groups might have energetic advantages but social constraints will

limit the maximum number of animals sleeping together. In Microcebus murinus 2 - 4 animals

seem to be a compromise between energetic advantages and social constraints (Perret 1998).

Nest associations can give an indication about the social organization and mating system of

the species (Kappeler and Van Schaik 2002). Morphological and behavioural data suggest a

highly promiscuous mating system for Mirza zaza (Kappeler et al. 2005; Rode 2010), but

information about nest use could further sharpen the picture.

To make information about nests and nest sites available for the design of effective

conservation measures I address three questions. First, what do nests of Mirza zaza look like?

37

Second, what are nest site characteristics preferred by M. zaza? Third, how does the species

use nests in terms of nest fidelity and composition and stability of groups sharing the nest?

This can give insight to the mating system.

5.2. Methods

The study site is described in section 2.2. After capturing Mirza zaza in life traps we

fitted them with radio collars to be able to follow them throughout the night. Details about the

capture process and radio-tracking can be found in section 2.3.

During the day animals were located in their nests and nest locations verified by

observing the animals emerge from or return to the nests. Nest characteristics were measured

as nest height in the tree, distance from the top of the tree (using trigonometry), position in

tree (trunk, branch or leaves), number of lianas connected to the nest and number of routes

used by the animals (Garcia and Braza 1993).

Nest trees were marked and subsequently described by tree species, tree height,

diameter at breast height (DBH), canopy size, number of lianas and number of connected

trees. The same variables were measured for trees used by individuals during the night when

they were active, and random trees. Nest microhabitat, used and random microhabitat

variables were measured using the point-centred quarter method (Ganzhorn 2003, see section

2.3). All nest trees variables were included for microhabitat as well as distance to nest tree

and canopy cover. Appendix 3 describes how variables were measured. For the analysis only

trees larger than 10 cm diameter were used since only large trees were used as sleeping sites.

Data of nest trees were compared to data of used and random trees while data of nest

microhabitat was compared to data of used and random microhabitat. In order to find out if

the nest tree species were more common among large and tall trees we compared species of

big trees (>10 cm DBH) to small trees (5 – 10 cm diameter) and species of tall trees (>10 m)

to low trees (< 10 m).

Nest sites were monitored via radio-tracking during the day and observations in the

evening and morning. Number of animals sleeping in one nest as well as sex and age

composition were investigated. Age classes were established as described in section 3. Return

and emergence times from the nests were noted down for each animal and behaviour observed

ad libitum right before returning and after emergence to the nest site. Even though the exact

location of one nest could only be estimated, its emergence and return times were included in

the analysis. The number of different sleeping sites per individual and return rate (number of

38

returns to a nest divided by the total of possible returns, Radespiel et al. 1998) was

determined.

Data analysis

Nest tree characteristics were compared between forests with Mann-Whitney U tests.

Since no difference in nest trees was found between forests the data were lumped. Due to non-

normal distribution of the data a non-parametric Kruskal-Wallis test was applied to compare

the nest, used and random trees, used and random microhabitat. Subsequently four Mann-

Whitney U tests (two-tailed) each were applied as post hoc tests to find out if the nest differed

from the other datasets. I applied a Bonferroni correction and set the significance level to

0.0125 for these tests (Cabin and Mitchell 2000). In order to test if nest tree species are more

present in larger or taller trees, 2 tests were computed. Emergence and return time was

normally distributed and subsequently one-way ANOVA was used to detect differences

between groups. All tests were performed according to Dytham (2003) and computed using

the software SPSS 17.0.

5.3. Results

Nests and nest sites

From May to July 2010 we captured 8 individuals and found seven nest trees

exclusively used by 3 stable groups. Four nests were located in Forest A and three in Forest B

(Fig. 7). Except for two nest sites the trees of a nest group were only 10-20 m apart.

Due to dense foliage, only one nest could be directly seen. The spherical nest was

approximately 50 to 80 cm in diameter. Due to rustling noises during observation we suspect

the nest material to be small branches and foliage. For one nest we could not determine the

exact location in the tree. There were no significant differences in nest variables between the

two forests. The attributes of all six nests are described in table 12. When excluding one nest

that was on a very high Canarium madagascariensis, mean distance from the top decreased to

1.60 m (±1.07, n = 5). Five of the nests were located maximum 0.5 m next to or on the trunk,

while one was located on a branch of 1 m diameter. All locations were well covered under the

canopy. For three nests the animals used two different routes to leave or return to the nest, for

one nest three routes were used and for two nests only one route.

39

Table 12: Height, distance from top of the tree and number of lianas of 6 Mirza zaza nests

We found that nest trees are significantly higher and have a higher number of lianas

than used trees in both forests (Table 13). Differences between nests and random trees were

only found in forest B: nest trees are significantly higher, larger, have a higher canopy

diameter and more lianas. No differences were found in the microhabitat (Table 14).

Nest Group Height of nest (m) Distance from top (m) Lianas (no.) 1 1 14.30 2.18 5 2 2 11.90 3.17 20 3 2 17.74 1.05 10 4 2 22.19 11.06 50 5 3 11.96 0.51 13 6 3 10.65 1.06 5 Mean 14.79 3.17 17 Sd 4.41 3.98 17 Median 13.13 1.62 12 Min 10.65 0.51 5 Max 22.19 11.06 50

Figure 7: Locations of 7 nest trees within the observed home ranges of nest groups 1, 2 and 3 in two different forests (forest A and forest B). White areas contain no forest but savannah. Home ranges were calculated using 100 % Minimum Convex Polygon (MCP).

40

Table 13: Medians for 5 nest tree variables and comparison to used trees and random trees in two forests A and B.

Median

Nest Used trees Forest A

Used trees Forest B

Random trees forest A

Random trees forest B

Height (m) 16.00 12.00** 12.00** 12.00(*) 13.00** DBH (cm) 29.92 17.63 18.78 16.62(*) 15.28** Canopy diameter (m) 8.50 6.00 6.00 5.88 5.00* Lianas (no.) 15 2*** 2*** 2*** Connectivity (no.) 3 3 4 2 N 7 45 55 DBH: n = 164

Height and canopy

diameter: n = 65

228

Empty cells indicate where no data were available. Significance level was set to P < 0.0125 and indicated by p < 0.05 (*), p < 0.01 **, p < 0.001 *** Table 14: Medians for 7 variables of microhabitat and comparison to used microhabitat and random microhabitat in two forests A and B.

Median

Nest habitat Used habitat

Forest A Used habitat

Forest B

Random habitat forest

A

Random habitat forest

B Height (m) 12.00 12.00 12.50 12.50 DBH (cm) 16.60 14.00(*) 14.00 16.30 15.40 Canopy diameter (m) 4.50 4.50 5.90(*) 5.00 Lianas (no.) 1 2 2 Connectivity (no.) 2 3 2 Distance (m) 4.45 3.98 3.90 4.69 3.85 N 28 204 212 DBH: n = 196

Height and canopy diameter: n = 61

208

Empty cells indicate where no data were available. Significance level was set to P < 0.0125 and indicated by p < 0.05 (*), p < 0.01 **, p < 0.001 ***

Nest tree species were Macarisia lauciolata, Family Rhizophoraceae (3x), Garcinia

pauciflora, Family Clusiaceae (2x), Sorindeia madagascariensis, Family Anacardiaceae (1x)

and Canarium madagascariensis, Family Burseraceae (1x). Only Macarisia lauciolata was

more present among big trees (>10 cm DBH) than small trees (5 – 10 cm diameter) (2 =

77.085; P < 0.001). Nest tree species were not more common among trees higher than 10 m,

compared to trees lower than 10 m.

41

Nest utilisation

Animals were located in their nests on 33 days. Focal observations were carried out

during emergence from the nest on 26 evenings between 05:15 pm and 6:00 pm and return to

the nest on 24 mornings between 05:00 am and 06:00 am. The total time of nest behaviour

observation added up to 41.5 hours.

In total three nest groups could be observed (Table 15). Group size was 2 to 4

individuals (mean 3.3, sd 0.47, n = 3 nests). Nests of group 1 and 3 contained only one female

but several adult males with fully developed testes. The second nest group consisted of an

adult female and her young. We observed a third adult individual of unknown sex in their nest

on three days.

Table 15: Nest group composition of three groups of Mirza zaza. F2 and N1 were not collared but were observed sharing a nest with the collared female F2 in group 2.

Group Forest ID sex age Group 1 A M1 male adult M2 male adult F1 female sub-adult M3 male adult Group 2 A F2 female adult F4 female juvenile N1 ? adult Group 3 B M4 male adult M5 male adult F3 female sub-adult

There was no difference in the return time between the different nest groups. The

animals returned between 4:12 am and 5:47 am (mean 5:28 am, sd 17:14, n = 42 mornings).

In the evening we found a significant difference in emergence time between the nest group 1

and nest group 3 (One way ANOVA F = 5.275, P = 0.08). Group 1 left their nests on average

at 17:39 (sd 5:37, range 17:23 - 17:49; n = 25 evenings) while group 3 emerged at 17:34 (sd

4:51, range 17:22 - 17:45; n = 21 evenings). Group 2 emerged between 17:30 and 17:49

(mean 17:37, sd 6:10, n = 15). When emerging from nests the individuals left the nest site

immediately. At their return they often entered the area early and showed grooming and social

behaviour like playing. One time we could observe one individual of group 1 improving the

nest by biting off a leafy branch and carrying it to the nest.

Group 1 stayed in the same nest during 24 control days over a 44-day period. Group 2

was located in the nests during 16 days in a 35-day period. This group swapped between two

42

close nest trees during some days but after a storm lasting several days they were found

changing their nest to another area. The third group was detected on 31 days during a 50 day

period and were found to use three close nests during this time. The change of one nest to the

other took several days in which different single individuals were swapping back and forth

between the new and the old nest tree during c. 17 days. Return rate was high with an average

of 91.9 % (sd 11.3, n = 8 individuals).

5.4. Discussion

Nests and nest sites

It is not always clear if nests of small mammals are self-constructed or abandoned by

other species (Thorén et al. 2010). Wright and Martin (1995) observed a female of

Microcebus rufus constructing a nest of 28 large leaves. They also witnessed Cheirogaleus

major improving existing leaf nests by integrating new leaves. A female of Microcebus

ravelobensis needed approximately an hour to build a leaf nest (Thorén et al. 2010). Although

we suggest the observed nest to be self-constructed due to an animal taking in a leaved branch

and due to rustling noise of dead leaves, it is possible that natural vegetation tangles or old

nests of other species are modified into nests by Mirza zaza. In a pilot study near Maromandia

one M. zaza was found occupying a nest that was built by Daubentonia madagascariensis

according to local guides, but may also have been built by M. zaza (personal observation).

Since we observed animals using very near trees as new nest locations we suggest that they

construct own nests since it is unlikely that old nests become available that frequently. Nests

of M. coquereli seem to be self-constructed (Sarikaya and Kappeler 1997) and in captivity M.

zaza built their own nests with individuals of all sex and age contributing to the construction

(Stanger et al. 1995).

The size of the observed spherical nest resembled nests described for captivity that were

about 50 cm in diameter (Pages 1980; Stanger et al. 1995) and could be confirmed for the nest

observed in this study. As Mirza zaza might sleep in groups of up to 8 individuals (Kappeler

et al. 2005) this size seems adequate for housing the high number of animals.

Often predation is suggested to be of the highest importance in the selection of sleeping

sites (Hamilton 1982; Fan and Jiang 2008). Due to very dense foliage only one nest was

visible to the observer. In the sub-humid forests of Sahamalaza National Park most of the

trees keep their foliage despite the dry season of 6 months (Schwitzer 2005). Additionally,

selecting nest places with dense vegetation and good camouflage improves concealment

43

(Bearder et al. 2003). Hediger (1977) suggests that it is more important for nocturnal prey

species to be hidden from the view of predators during the day compared to diurnal primates

that sleep during the night. This might explain why except for great apes none of the diurnal

primates build nests (Kappeler 1998).

In our study the nests was situated on average 3 meters below the top of tall trees. If the

outlier, a very tall Canarium madagascariensis, was excluded the average distance from the

top decreases to 1.5 m. Sarikaya and Kappeler (1997) confirm that Mirza coquereli builds

nests 1-2 m under the top of the tree while Pages (1980) suggests nest height of 2-10 m for M.

coquereli. As the branch where one of the nests was located functionally resembled a trunk

due to its enormous diameter, all nests were placed near the trunk and not the periphery of the

tree. The hidden and high position suggests a good protection against predators (Rasoloarison

et al. 1995). Goodman et al. (1993) report an individual of the equally sized M. coquereli

caught by a Madagascar Buzzard (Buteo brachypterus) and several individuals found with

scars indicating an attack by the raptor. Since Buteo as well as other raptors like the

Madagascar harrier hawk (Polyboroides radiates) are diurnal he suggests that the lemurs were

caught from their nests. Nests near the trunk with much foliage above thus seem to increase

protection.

Mirza zaza used one to three different routes to leave or access the nests. This was

especially evident for the single used tree of group 1 where three of four animals always used

exactly the same branches of nest and neighbouring tree to leave the site. Similar behaviour

was observed for owl monkeys (Garcia and Braza 1993). Knowing escape routes in case of a

predator attack should be of advantage (Aquino and Encarnación 1986; Wells et al. 2006).

Nest tree characteristics differed from other used trees as well as from random trees.

Mirza zaza favours high and large trees with many lianas. High trees might be more difficult

for terrestrial predators to reach. Due to its bigger size M. zaza might not be as vulnerable to

smaller predators as for instance Microcebus (Goodman et al. 1993; Rasoloarison et al. 1995)

but remains of it have been found in scats of Cryptoprocta ferox (Rasoloarison et al. 1995),

which hunts during the day and the night (Karpanty and Wright 2007). Smaller diurnal

viverrids might be less dangerous for the medium-sized Mirza but may be for their young.

Schülke (2001) confirmed that the Madagascar tree boa Sanzinia madagascariensis preyed on

M. coquereli. However, the preference for high and large trees can not be explained by

predation pressures of snakes since the climbing ability of snakes is not affected by the height

or diameter of trees (Ancrenaz et al. 2004). Environmental forces are suggested to influence

the choice of sleeping sites (Aquino and Encarnación 1986). As tree fall was very common in

44

Sahamalaza, especially during windy periods (personal observation), animals may select more

robust trees in order to sleep in a secure place. This was suspected for Orang-utans (Ancrenaz

et al. 2004). The location of nests near the trunk supports the importance of solid support. The

high number of lianas covering the sleeping trees might serve as dilution from predators

(Rendings et al. 2003; Garcia and Braza 1993). Suitable structure of surrounding vegetation

and lianas may be useful as support for the nests (Wells et al. 2006). Pages (1980) reports that

nest trees of M. coquereli were usually covered in lianas. In respect to microhabitat of the nest

there were no differences in variables found. This emphasises the relative uniqueness of the

nest trees.

In Kirindy, Mirza coquereli used Euphorbiaceae as nest tree species probably because

this family does not shed leaves during dry season (Sarikaya and Kappeler 1997, Pages 1980).

The different climate with less trees shedding foliage during dry season might allow M. zaza

in Sahamalaza to be less specific about tree species. We found only for one species

(Macarisia lauciolata) being more present among trees with a higher DBH and might be

favoured by Mirza zaza due to its large diameter instead of the species itself. There was no

such association found for the other species, although Canarium madagascariensis is known

to be a very big and tall tree. In the studied forests not many of these charismatic trees were

left and thus occurrence of the species was low. Tree species might be favoured for other

reasons, e.g. of different species-specific structure (Wells et al. 2006).

There seems to be much interspecific competition for pre-structured shelters.

Microcebus cf myoxinus competed for holes with M. murinus, Cheirogaleus medius, rodents

and reptiles (Schwab 2000). Interspecific competition but also cohabitation of sites was also

found between Aotus and other nocturnal mammals. Allocebus trichotis was observed to share

holes with the white-tailed tree rat without aggression (Brachytarsomys albicauda) (Biebouw

et al. 2009). Group 2 once changed their sleeping site to a nearby tree but went back to the old

tree on the following day. That evening a Lepilemur sahamalazensis was seen emerging from

the new nest tree. Although Ruperti (2007) reported that sympatric L. sahamalazensis use

different tree species as found for Mirza zaza, this might be an indication that good nesting

trees are rare in general and there is interspecific competition for them.

Nest utilisation

Mirza zaza differs from its sister species M. coquereli in its diurnal gregarious nesting

behaviour. While M. coquereli sleeps in nests alone, M. zaza was found to share nests

between 2-8 individuals (Kappeler et al. 2005). In this study we could observe nest groups

45

from 2 to 4 individuals. During the dry season Microcebus murinus can build sleeping groups

of up to 15 animals but average sleeping group size is usually much smaller for Malagasy

nocturnal primates (Eberle and Kappeler 2006). Bearder et al. (2003) report that galagines

may sleep in groups of up to 10 individuals, whereas the Myosore Slender Loris (Loris

lydekkerianus lydekkerianus) can sleep in groups of up to 7 (Nekaris 2003). Nocturnal

primate species were traditionally regarded as solitary but revealed to show different social

systems (Müller and Thalman 2000). The existing variability is underlined by the unusual

composition of Mirza zaza nest groups. Most nocturnal strepsirrhines sleep in small groups

including female kin and offspring but not several males (Radespiel et al. 1998; Nash and

Harcourt 1986; Pimley 2003; but see Nekaris 2003). Interestingly, two groups observed for

this study contained one sub-adult female and several adult males with fully developed testes.

Kappeler et al. (2005) found on average 0.77 adult females and 1.06 adult males with fully

developed testes in a nest. The high number of adult males was only reported for a few other

species. Weidt et al. (2004) report that some sleeping associations of Microcebus ravelobensis

contained several adult males. One of the explanations was that this presents a mating strategy

where males have direct control and access to the females in their group instead of having to

search for them (Weidt et al. 2004). Several adult males have been observed to sleep in the

same group including females and young in Lori lydekkerianus lydekkerianus (Nekaris 2003).

The nest composition found in Mirza zaza may indicate a multi-male multi-female system but

genetic analysis may have to confirm this conclusion. High variability in testes size within

Mirza zaza groups (Rode 2010) might also suggest that reproductive suppression takes place

(Kappeler 1997b), like assumed for Eulemur fulvus rufus (Glander et al. 1992). In M. zaza

groups could also be extended families as it is the case for Cheirogaleus where an adult pair

formed a sleeping group with sub-adults and the recent year’s infants (Müller 1998).

Nest groups of Mirza zaza were stable and did not change during the whole study

period. A third adult individual of group 2 was occasionally observed but may have joined the

group for only a few days. In other species sleeping groups were not only also stable in

dispersed pairs or families (e.g. Lepilemur edwardsi, Rasoloharijaona et al. 2003;

Cheirogaleus medius, Müller 1999), but also in mixed-sex groups of Microcebus ravelobensis

(Weidt et al. 2004).

Nest were group-exclusive and groups stayed in the same nest during long time periods

of up to at least 44 days (group1). Only up to three nests were used. Return rates thus were

very high. In contrast, Kappeler et al. (2005) found individuals of Mirza zaza using 2-5

different nests on the 3-7 days they could be located. Lepilemur edwardsi showed a similar

46

high nest site fidelity than M. zaza with only 2-3 close nest sites (Rasoloharijaona et al. 2003)

while some mouse lemurs used as few sites as for instance 3 to 7 in female Microcebus

murinus (Radespiel et al. 1998). Weidt et al. (2004) reports M. raveobensis staying in one

nest for maximum 16 successive days. There may be two non-exclusive explanations for a

small number of exclusive nest sites. If suitable trees become less available in degraded or

logged forests the continuous use and reuse of certain trees may increase (Ancrenaz et al.

2004). Less frequent change of nest sites may be a function of low habitat quality. Second,

males of Microcebus murinus changed their sleeping site frequently in order to decrease

predation risk (Radespiel et al. 1998). Observed nest sites of Mirza zaza may be very high in

quality, which would decrease the necessity for changing the site (Radespiel et al. 1998). Both

explanations would lead to intensive intraspecific competition between groups for this

resource and animals trying to monopolize high quality nest sites like it was suggested for

Lepilemur edwardsi (Rasoloharijaona et al. 2003), Microcebus ravelobensis (Braune et al.

2005) or M. murinus (Radespiel et al. 1998). M. ravelobensis marked their sleeping sites

when animals dispersed in the evening. This was interpreted as facilitation of relocation and

claiming of the sleeping site (Braune et al. 2005). Aotus showed a delay in leaving the nest

which was associated with marking the nest (Garcia and Braza 1993). Mirza zaza was not

observed to mark their nest but due to dense foliage this behaviour might have been missed.

However, as M. zaza only used a few nests in close vicinity this might have not been

necessary. In terms of relocation, groups returned to the nest with time lag between the first

and the last individual. Individuals took their time before permanently entering the nest. They

were often seen on the nest tree or neighbouring trees grooming or engaging in social

activities. This was also observed for Lori lydekkerianus lydekkerianus (Nekaris 2003). Pages

(1978) confirms that M. coquereli shows more social activities during the second half of the

night compared to the first half where behaviour focuses more on feeding.

The difference in emergence time can be explained by the western-facing location of the

nest of group 1. Due to later sunset the animals probably emerged later in order to decrease

predation risk.

If the nest was changed, in all cases except one a very near tree was chosen as a new

nest site. This suggests that the terrestrial predator risk might be low and changing trees not a

function of predator risk. Mirza zaza have a strong body odour (personal observation) and

changing the nest site might not be very effective against predator with good olfactory senses.

Changing nests might be more a function of environmental conditions, disintegration of the

nest over time or accumulation of parasites (Aquino and Encarnación 1986; Roper et al.

47

2002). The observation of group 2 changing the nest after or during a heavy storm suggests

this.

When group 3 changed their nest they did it gradually with single animals sleeping first

in the new tree. This was also observed for Lori lydekkerianus lydekkerianus (Nekaris 2003).

In Mirza zaza all individuals slept in the new tree at least once and thus probably all

individuals helped preparing a new nest like observed in captivity (Stanger et al. 1995).

Finally they moved as a whole group like in Microcebus ravelobensis (Weidt et al. 2004) or

Aotus (Aquino and Encarnación 1986). The previously used nest disintegrated very quickly

during a storm.

5.5. Conclusions and recommendations

This study showed a preference of Mirza zaza for large and tall nest trees with a high

amount of lianas. The animals did not use many different nest trees, which may be a sign of

scarcity in suitable trees within the respective home ranges. Nest sites are not only important

for security against predators or environmental conditions, but also for social activity.

Accordingly, we recommend the protection of forest fragments with big trees and discourage

selective logging of big and tall trees. Reforestation in respect to the provision of suitable nest

sites should focus on tree species growing fast to become high and big trees. Nest

composition suggests M. zaza living as dispersed groups with cohesive multi-male/multi-

female or extended families nest groups.

48

6. Synopsis

6.1. Conclusions

This first comprehensive ecological study about Mirza zaza gave an insight into the

requirements and preferences of the species and showed that species research can lead to

precise recommendations for conservation. Several preferences were found towards trees and

microhabitat used during the animals‘ nightly activity as well as for their daily nest sites.

These preferences were translated into recommendations for the strategic design of

conservation action plans. Although the study period seemed too short to gather accurate

information about home range sizes a first estimate was done which as the best available

information should guide first assessments of the species’ conservation status. Interesting

findings about the mating system and social organisation bring up new questions as

morphology points to a promiscuous mating system but ranging and sleeping patterns indicate

a close family or group bond. In summary, M. zaza is a very interesting (and cute) species.

Many aspects of its life are remaining unsolved but are worth investigating because M. zaza

might be unique in its life style.

6.2. Future research

In this project I was able to collect many data and due to time restrictions not all data

could be included here. I plan to prepare two other publications, one about general behaviour

and feeding, and another about genetic distance of the Ankarafa Forest population and

relatedness of nest group members. Genetic analysis may further indicate possible genetic

differences to other populations. I suggest that research about Mirza zaza goes on, for instance

in order to verify home range sizes and overlap or investigate the relation between M. zaza

and abundance of Flatidae.

49

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Appendix 1: Oestrus cycle of Mirza zaza

Table 16: Oestrus cycle of Mirza zaza in captivity and vaginal appearance of each cycle. Data adapted from Stanger et al., 1995.

Vaginal appearance Phase Duration (days) Colour Swelling Opening Comments Pro-oestrus 0-2 Pink Swollen Wide open Oestrus 1 Pink-red Very swollen Wide open Skin smooth Met-oestrus 1-2 Pink-red Very swollen Open Skin wrinkled Di-oestrus 14-24 White Not swollen Sealed or closed

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Appendix 2: Incremental area analysis of group and individual home ranges of Mirza zaza

I. Method: 100 % MCP

Figure A1: Incremental area analysis of home ranges of group 1 (left) and group 3 (right) (100% MCP)

Figure A2: Incremental area analysis of home ranges of M1 (left) and M2 (right) (100% MCP)

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F1

Figure A3: Incremental area analysis of home ranges of F1 (left) and M3 (right) (100% MCP)

Figure A4: Incremental area analysis of home ranges of F2 (left) and M4 (right) (100% MCP)

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Figure A5: Incremental area analysis of home ranges of M5 (left) and F3 (right) (100% MCP)

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II. Method: 95 % kernel

Figure A6: Incremental area analysis of home ranges of group 1 (left) and group 3 (right) (95% kernel)

Figure A7: Incremental area analysis of home ranges of M1 (left) and M2 (right) (95 % kernel)

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Figure A8: Incremental area analysis of home ranges of F1 (left) and M3 (right) (95 % kernel)

Figure A9: Incremental area analysis of home ranges of F2 (left) and M4 (right) (95 % kernel)

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Figure A5: Incremental area analysis of home ranges of M5 (left) and F3 (right) (95 % kernel)

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Appendix 3: Variables used to study Mirza zaza

Table 17: Variables of habitat and habitat use, and ethogram of Mirza zaza as used for this project

Tree and microhabitat variables for large tree (10 cm DBH), small tree ( between 5.1 and10 cm DBH) Height (m) Height of tree top, mean of two estimates DBH (cm) Diameter at breast height, taken with measurement tape Canopy diameter (m) Largest horizontal width of the tree crown, mean of two estimates Lianas (no.) Count of all lianas with >1 cm DBH Connectivity (no.) Number of connections to other trees with > 5 cm DBH Distance (m) Distance from centre tree to nearest tree in the respective quadrant, precise

to 1 cm Canopy cover (%) Percentage of canopy cover, as analysed from a photo taken 2.5 m to the

northwest from the centre tree Tree species Malagasy name, translated into scientific name (if possible) Disturbance variables Tree stumps (no.) Number of tree stumps, cut by humans Evidence of fire (no.) Number of black spots or wood clearly indicating the occurrence of fire in

the past Cattle faeces (no.) Number of cattle faeces that can be still distinguished from soil Position of animal Type of tree Type of tree used by animal, measured as large tree (10 cm DBH), small

tree (<10 cm DBH) or bamboo (>3 cm DBH) Height of the animal Estimated height of the animal when first seen or after a time interval of 5

minutes, mean of two estimates Support type Support type includes trunk, branch, leaves (including branches < 1 cm),

fork and liana Ethogram Behaviour category Resting Animal is non-mobile with eyes closed or no apparent voluntary activity for

at least 3 seconds Moving Non-stationary activity which involved the act of moving from one location

to the other without any apparent engagement in searching for food Grooming Picking at another individual with fingers and/or teeth (Allogrooming) or

picking at one’s own body with teeth and fingers (Autogrooming) Playing Engagement in rough and tumble activity with one another or alone that

clearly has no aggressive component, such as touching, tugging, chasing or swinging

Feeding, foraging Involvement in the process of actively taking in food, including eating, chewing, examining or holding food (feeding) or active involvement in the process of locating food, e.g. manipulating support surface while staring intently at the surface in search of food (foraging)

Other Behaviour different from the categories above Light Light intensity Light intensity as inferred from GPS, measured as (1) no light, (2) up to ¼

moon, (3) between ¼ and half moon, (4) between half moon and ¾ moon, and (5) between ¾ moon and full moon.

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