Research Article Body Size Mediated Coexistence in...

Research ArticleBody Size Mediated Coexistence in Swans

Katharina A M Engelhardt1 Mark E Ritchie2 and James A Powell3

1 Appalachian Laboratory University of Maryland Center for Environmental Science Frostburg MD 21532-2307 USA2Department of Biology Syracuse University Syracuse NY 13244-1270 USA3Department of Mathematics and Statistics Utah State University Logan UT 84322-3900 USA

Correspondence should be addressed to Katharina A M Engelhardt kengelhardtumcesedu

Received 28 August 2013 Accepted 24 October 2013 Published 4 February 2014

Academic Editors R Julliard and S Rossi

Copyright copy 2014 Katharina A M Engelhardt et al This is an open access article distributed under the Creative CommonsAttribution License which permits unrestricted use distribution and reproduction in any medium provided the original work isproperly cited

Differences in body sizes may create a trade-off between foraging efficiency (foraging gainscosts) and access to resources Such atrade-off provides a potential mechanism for ecologically similar species to coexist on one resource We explored this hypothesisfor tundra (Cygnus columbianus) and trumpeter swans (Cygnus buccinator) a federally protected species feeding solely on sagopondweed (Stuckenia pectinata) tubers during fall staging and wintering in northern Utah Foraging efficiency was higher fortundra swans because this species experienced lower foraging and metabolic costs relative to foraging gains however trumpeterswans (a) had longer necks and therefore had access to exclusive resources buried deep in wetland sediments and (b) were moreaggressive and could therefore displace tundra swans from lucrative foraging locations We conclude that body size differentiationis an important feature of coexistence among ecologically similar species feeding on one resource In situations where resourcesare limiting and competition for resources is strong conservation managers will need to consider the trade-off between foragingefficiency and access to resources to ensure ecologically similar species can coexist on a shared resource

1 Introduction

Ecological theory predicts that the number of coexistingspecies within a community should be finite and that speciesdiffer in their morphological traits more than what would beexpected by chance [1ndash4] Patterns of size differentiation havebeen observed among various guilds and communities [5ndash7]and across ecosystems [3 8] leading to the hypothesis thatsize differences drive functional differences among species[9] and therefore resource partitioning in space [5 10 11]Resource partitioning occurs by eating different types offoods or different size classes of the same food [2 12ndash15]where coexistence is possible when species are limited by theresources they can exploit best [16ndash18] Much less is knownabout how body size differentiation may lead to coexistencein the absence of resource partitioning [14] We illustratethis idea by examining a system featuring ecologically similarswan species feeding on the same resource in space andtime One species the tundra swan (Cygnus columbianus)is common whereas the other species the trumpeter swan(Cygnus buccinator) is rare and federally protected in the

United States Understanding whether and how the twospecies can coexist on a shared resource is important to themanagement and conservation of this group of species whenfood resources are limited

Two species can coexist on a shared resource when abody size mediated trade-off between foraging efficiency andaccess to resources exists (1) Foraging efficiency is definedhere as the ratio between foraging gains and foraging costs[19] Larger-bodied animals incur greater foraging costswhenthey require more energy for metabolism and locomotionthan their smaller-bodied counterparts [3 20 21] Howeverlarger animals gain more energy per unit foraging timebecause they are more effective in searching handling andprocessing their prey [20 22ndash24] Thus how foraging effi-ciency is related to body size depends on body size mediatedforaging gains relative to foraging costs (2) Similarly accessto resources can be mediated by body size through physicalor behavioral mechanisms Longer necks and bodies allowlarger-bodied animals physical access to exclusive resourcessuch that smaller species are included entirely within theniche of the larger species [3 14 25] Likewise larger

Hindawi Publishing Corporatione Scientific World JournalVolume 2014 Article ID 643694 12 pageshttpdxdoiorg1011552014643694

2 The Scientific World Journal

animals are generally more likely to displace smaller-bodiedindividuals through aggressive behavior [21 26ndash31]

If larger species indeed have greater access to resourcesthen species coexistence may be mediated by body sizedifferentiation if smaller species are more efficient foragersFor example the niche of one speciesmay be entirely includedwithin the niche of a second species For species to coexistunder these conditions [32 33] the species with the narrowerincluded niche must be more efficient in exploiting theshared resources and the species with the broader nichemust not achieve sufficient density on exclusive resourcesto numerically outcompete the included niche species forthe shared resources (ldquoincluded nicherdquo hypothesis) [34ndash36]Similar to the included niche scenario two species can coexistwhen the larger species can displace the smaller species fromlucrative foraging locations through aggressive behavior butthe smaller species is more efficient in exploiting the sharedresources (ldquoshared preferencerdquo hypothesis) [37ndash39]

Tundra and trumpeter swans are often observed sharingthe same habitats in space and time [40] and feed on the sameresource sago pondweed (Potamogeton pectinatus) tuberswhile staging and wintering in Utah because the tubers arethe only available food source during that time [41ndash43] Weexplored the hypothesis that differences between swan bodysizes allow the two species to coexist on one resource viaan included niche For the included niche hypothesis not tobe rejected tundra swans would have to be more efficientforagers but trumpeter swans would have to have access totuber resources buried deep in wetland sediments We alsotested the shared preference hypothesis that trumpeter swansare superior competitors for the food resources throughinterspecific aggression If so the two species can coexisteven without access to exclusive resources if a trade-off existsbetween superior foraging efficiency of tundra swans andaggressive behavior by trumpeter swans

2 Methods

To assess the potential for tundra and trumpeter swancoexistence via body size mediated trade-offs we sought toestimate foraging efficiency of the two species versus eitherniche breadth (amount of shared and exclusive resourcesavailable to the swans included niche hypothesis) or aggres-sive behavior (shared preference hypothesis) Because assess-ment of energy gains and costs associated with body sizeis inherently difficult and would have required extensivehandling and undue stress on a federally protected species weestimated foraging efficiency using a mechanical estimationapproach By measuring the quantity and distribution offood resources in wetland sediments we could calculate theamount of shared and exclusive tuber resources availablein wetland sediments Behavioral observations documentedinterspecific aggression and displacement of individuals fromforaging locations

21 Species and StudyArea Westudied tundra and trumpeterswans and their food resources at the Bear River MigratoryBird Refuge (BRMBR divided into 3 separate wetland units

Unit 1 Unit 2 and Unit 4) and the Bear River Club Company(BRC) in northern Utah (41∘271015840N 112∘181015840W) Trumpeterswans are rare inUtah hence 57 trumpeter swans from Idahowere released by state (Utah Division of Wildlife ResourcesIdaho Department of Fish and Game) and federal (US Fishand Wildlife Service) agencies into BRC in November andDecember 1996 to expand their wintering range [43 44]Tundra swans are abundant throughout the study area duringthe fall winter and spring months (as estimated by the UtahDivision of Wildlife Resources every two weeks in Octoberevery week in November and December and once in Januaryand March with surveys of low-flying aircraft)

22 Tuber Resources We quantified biomass of sagopondweed tubers before swans migrated through orwintered on the study areas in the four study wetlands Weresampled the same areas in March after the swans had leftto migrate north to their breeding grounds We placed 64transects in the 4 wetlands using a two-stage systematic-random sampling design where each transect was randomlyplaced within a 1 km2 area and each 1 km2 area was part ofa grid covering the 4 study wetlands Transects were 200mlong with one core taken every 20m Cores (52 cm diameter)were between 15 cm and 45 cm long depending on the depthof the Calcium hardpan that delineates the depth to whichsago pondweed tubers are produced We divided cores into5 cm sections to explore the 3-dimensional distribution oftuber biomass in wetland sediments which allowed us tocalculate the shared and exclusive portions of the tuberresource We washed all samples through a sieve with 1mmopenings to extract all tubers which we subsequently driedand weighed

To test the hypothesis that swans have access to biggertubers found in deeper sediments [45 46] and preferentiallyfeed on bigger tubers we first determined the relation-ship between tuber length and depth in Utah sedimentsand then compared tuber length distributions in wetlandsediments to tuber length distributions in swan esophagiWe determined the diets of tundra swans by extracting thegizzards and esophagi of 50 swans killed by swan huntersWe then measured the length and mass of all tubers foundin the gizzards and esophagi Trumpeter swan diets couldnot be determined because this species is protected fromhuntingWe supplemented the diet information by observingfeeding trumpeter and tundra swans during the day (wedyed trumpeter swans pink under their left wing to enhanceidentification without drawing undue attention to the swans)and locating them by radiotelemetry (Holohill Canada) atnight

23 Swan Morphology and Behavior We reviewed morpho-logical measurements in the literature [47 48] and measuredneck length to estimate the maximum depth each speciescan potentially forage to by stretching its neck down throughthe water and sediment Swans also ldquotip uprdquo to reach deeperresources the legs latter part of the body and tail are the onlybody parts remaining above the water surface [49] Thus weestimated the maximum reach of a swan as 15 times the neck

The Scientific World Journal 3

length corresponding to conservative estimates derived fromOwen and Cadbury [50]

We observed mixed tundra and trumpeter swan flockswhile they were feeding to test for interactions that resultin displacement of a swan from a feeding ldquoholerdquo Mixedflocks were observed for 235 h across five consecutive daysObservations were made between dawn and dusk when wecould locate mixed flocks foraging close to shore (lt100m)in areas that were not frozen shut Because trumpeter swanswere almost exclusively foraging in BRC our observationswere all made in that wetland unit at 4 different locationsincluding a spillway and fringe or interior marsh areas Weobserved 7 trumpeter swans (5 adults and 2 juveniles) and7 tundra swans (6 adults and 1 juvenile) Social class couldnot be determined for either species however the trumpeterswans were generally lone adults and juveniles Tundra swanswere generally present as intact family groups Less than 5of all individuals in a foraging area were trumpeter swansTwo juvenile trumpeter swans feeding together with onelone adult tundra swan were the only exception Becausedensity of trumpeter swans was low we observed trumpeterswans for 75 of the observation time to increase the chancewe would observe interspecific interactions Sampling wasrandomized among individuals when sample size allowedUsing focal-individual sampling we recorded the directionand outcome of the interaction and the type of interaction(bite chase threat by extending neck passive displacementvia occupation of space and hiss) We took care not todisturb the swans while they were foraging and observedthe swans from behind cover and through binoculars andspotting scopes

Likewise we explored whether the two swan speciesdiffered in the effort they put into foraging and in the timethey spent foraging for tubers We observed the two specieswhile they were actively feeding on tubers and timed (a)how long they were paddling and (b) how long their headswere submersed when searching under water for tubers Weobserved 19 swans (12 trumpeter swans and 7 tundra swans)that were adults (11 swans) or juveniles (8 swans) andwatchedeach swan from when it started foraging until it stoppedforaging and either deliberately swam or flew to a new areaObservation times ranged from 10min to 150min (762mintotal) and were made in BRC Unit 2 and Unit 4

24 Foraging Gains Nolet et al [49] estimate tuber harvestrates (119877tub) for tundra swans to be between 001 and 004 gdry mass sminus1 We adopt 119877tub = 002 g s

minus1 as the averageharvest rate in our calculations which corresponds to atuber biomass between 20 and 40 gm2 supported by a clayeysubstrate [49] similar to our estimates of tuber biomass inthe study wetlands (Figure 1) If we assume that the digestiveprocesses are not constrained by differences in gizzard sizethen foraging gains may be in direct proportion to bill sizeObservations on geese show that bite size scales to bill lengthto power 1424 and to body mass to power 299 [51] Largerbills of swans may increase encounter rate owing to a largersurface area but larger bills may not be as adroit in extractingtubers from sediments Because bill length of a trumpeter

Study areaUnit 1 Unit 2 Unit 4 BRC

0

10

20

30

40

50

SeptemberMarch

a

b

b

b

A

B BB

Tube

r bio

mas

s (g m

minus2

)

Figure 1 Tuber biomass in sediments of the four study wetlands inSeptember (before swans started foraging) and inMarch (after swansstopped foraging tomigrate to breeding grounds)Multiple Analysisof Variance tested for differences among wetlands and datesSame letters indicate no significant differences among wetlandsCapitalization emphasizes which observations are compared Errorbars = 1SE

swan is approximately 12 the size of tundra swans [47 48]we estimate that

119877Trumpetertub = 12 sdot 119877

Tundratub (1)

realizing that this may be a liberal estimate and that foraginggains of trumpeter swans relative to Tundra swans may needto be decreased We keep this uncertainty in estimatingresource gain in mind when calculating and interpretingforaging efficiency

25 Foraging Cost All foraging costs were estimated in Jsecto allow comparisons among estimates We calculated basalmetabolic rate for adult swans using the standard metabolicrate (SMR) equation for homeotherms by Hemmingsen [52](in Peters [9] page 29)

SMR = 411198820751 (2)

where SMR is measured in Jsec and 119882 = mass of anindividual (109 kg for trumpeter swans and 68 kg for tundraswans [47 48]) Kendeigh et al [53] suggested that theaverage daily metabolic rate (ADMR) for birds is 16 to 2times SMR in the thermal neutral zone We use the upperrange value to account for extra costs for thermoregulationin the winter The ADMR estimate includes measurementsof existence metabolism (rate of metabolizable energy intakein caged animals maintaining constant body mass outdoors)and estimates of additional metabolic costs of free livingSimilarly Nagy [54] developed allometric equations formammals and birds to calculate field metabolic rate (FMR)FMR for birds [54] is

FMR = 109 times 119882064 (3)


FMR similar to ADMR estimates the costs of free existenceADMR and FMR were developed for birds during the breed-ing season and therefore underestimates food requirementsand consumption when birds are hyperphagic [54] Never-theless we use ADMR and FMR for both species to obtainan estimate of tundra and trumpeter swan average metabolicenergy requirements during one day of free existence keepingin mind that swans may exceed their metabolic requirementduring staging or wintering The estimates of metabolic costallowed us to calculate the number of swans that the tuberbiomass in the study areas could support during staging andwintering

We identified three foraging costs that could differ sub-stantially among species (1) cost of flying between foraginglocations (2) cost of swimming between foraging locationsand (3) cost of paddling in one location to stir up top sedimentlayers [49 55] Cost of digging deeper in the sediment layer bybill stabbing and cost of tipping the body vertically to reachfurther into the sediment are also associated with energeticcosts [49] however we assumed these costs to be relativelysmall compared to flying swimming and paddling costs andto be similar among the two swan species Other costs offree existence such as alertness posture reproduction andgrowth were also assumed to be either nonexistent at thetime of the year negligible or similar among the two speciesCosts for flying swimming and paddling were quantifiedusing mechanistic models because direct measurements onswans were logistically not feasible to obtain However wewere primarily interested in the ratio of costs between thetwo species Potential inaccuracies which should be similarbetween the two species cancel in the ratio

251 Costs of Flying Swans would typically fly from a restinglocation to a foraging location at dawn and from a foraginglocation to a resting location at dusk Swans were alsoobserved flying between foraging locations however theseforaging flights were relatively infrequent and differencesamong species could not be observed readily We predictedshort-distance flights to be energetically costly and energyconsumption during lift-off and flight to be dependent onbody mass and morphology We calculated costs of shorthop flights for tundra and trumpeter swans [56] using amodel for the aerodynamics of bird flight [57] We estimatedparasite power (power required to overcome the drag of thebody) induced power (power required to generate lift) andprofile power (the power required to overcome the drag of thewings) The total power required for horizontal flight is thesum of parasite induced and profile powers plus an over-head for respiration and metabolism Parameter estimatesand calculations can be found in Powell and Engelhardt [56]

252 Costs of Swimming We calculated the power requiredfor a swan to swim (119875swim) at an average velocity of 025msecA swimming swan is treated as a tugboat [58]

119875swim = 0011119872H2OV

swimave (4)

where119872H2O is the mass of the water displaced by the swan

approximately 12 of a swanrsquos body mass and Vswimave is thevelocity at 025msec during foraging

253 Costs of Paddling Wemeasured the surface area of thewebbed feet and leg length for tundra and trumpeter swansand determined the energy consumed by pressing the areasvertically down a column of water using a fluid mechanicsmodel [59]

119865paddle = 119888119863120588water119860

2

(Vpaddleave )2

(5)

where 119865paddle is the force required to move a swan footthrough the water column 120588water is 1000 kgm

3 at 0ndash5∘C 119860 isthe area of foot (14103 cm2 for tundra swans and 16772 cm2for trumpeter swans) Vpaddleave is the average velocity of aswan foot traveling vertically through the water columnestimated below 119888

119863is a function of the Reynolds number

when assuming that swan feet are circular [59] whereRe = 120588waterV

paddleave 119871120583H2O 119888

119863is constant at 101 for Re gt 3 times

103 which is the case here (Re = 302 times 104 for tundra swans

and Re = 325 times 104 for trumpeter swans) 119871 is the travellength of a swan foot (146 cm for tundra swans and 157 cmfor trumpeter swans traveling at a 30∘ angle through thewatercolumn) 120583H

2O = 1518 times 10

minus3The average power requirements for paddling are119875paddle = 119865paddleV

paddleave To determine average velocity of

paddling we assumed that the power requirement forpaddling vigorously to stir up sediments is the same asthat for vigorous swimming as when swans swim awayto avoid observers This speed is approximately 1mseca comfortable walking pace over rough ground We basethis estimate on observations of how rapidly we could walktoward swans before they would choose to take flight asopposed to continue swimming away To determine Vpaddleave we calculated

119888119863

120593water119860

2

(Vpaddleave )3

= 119875paddle = 119875swim

= 0011 sdot 119872H2O sdot 1msec

(6)

We solved this equation for Vpaddleave and subsequently deter-mined 119875paddle for each species

26 Comparative Efficiencies We define efficiency of eachspecies as the ratio of energy gains to energy expendituresWecalculate a ratio rather than a difference to obtain an efficiencyestimate that is dimensionless In Utah where the swans donot reproduce and life is reduced to the basics of flying to andfrom foraging sites swimming between foraging locations


and foraging for tubers the daily energy gains and losses canbe summarized as

efficiency =foraging gainsenergy costs

=

120578 (119891forage119877tub119873sec)

2sdot119864flight+119873sec(119875met+119891swim119875swim+119891paddle119875paddle)

(7)

where 120578 is the energy content (joulesgram) of tubers per drymass [60] 119891forage is the fraction of day spent foraging 119877tubis the rate of tuber intake [49] (gramssecond) 119873sec is thenumber of seconds in one day (seconds) 119864flight is the energyrequired for one-way flight between resting and foraging sites(joules) 119875met is the standard metabolic rate (joulessecond)119891swim is the fraction of day spent swimming 119875swim is thepower requirement for swimming (joulessecond) 119891paddle isthe fraction of time spent paddling to uncover tubers 119875paddleis the power requirement for paddling (joulessecond)

The standard metabolic rate 119875met does not include anycosts of free existence such as costs of swimming (119875swim)costs of paddling (119875paddle) and costs of flight (119864flight)The costsare calculated separately for those activities that we believemay differ substantially among the two species owing to dif-ferences in body size Other costs such as costs of posture andstaying alert are assumed not to be substantially influencedby body size and are therefore excluded when calculatingefficiency This means that costs are underestimated but tothe same extent for both species As a comparison we usedFMR as our 119875met estimate to calculate costs that incorporateall costs of free existence

27 Statistical Analysis To estimate shared and exclusivetuber resources we needed to know the quantity and spatialdistribution of tuber biomass in each sampled wetlandWe estimated tuber biomass (gm2) for each of the 64transects sampled and extrapolated the results to the scaleof the four wetlands using geostatistical analysis [43] Wequantified exclusive resources by calculating the maximumsediment depth at each transect to which an adult tundraand trumpeter swan might forage after accounting for waterdepth We then summed tuber biomass at depths greaterthan the maximum tundra swan reach but less than themaximum trumpeter swan reach for every wetland Likewisewe calculated shared resources by subtracting exclusive tuberbiomass and tuber biomass not accessible to either speciesfrom total tuber biomass

Swan days are the number of tundra and trumpeter swansthat could be supported on a resource for one day (or howmany days one swan could be supported) We estimatedtundra and trumpeter swan days for each wetland by dividingtuber biomass of each wetland by the tuber biomass requiredper individual per day The daily tuber biomass requirement(DTR) was calculated using two approaches (1) ADMR (orFMR) for the two species was divided by the metabolizableenergy content (dietary energy content of the food minus

energy voided in fecal and urinary excretions) of sagopondweed tubers (120578 = 117 kJg [60])

DTR = ADMR120578

(8)

(2) An allometric equation for birds [54] is

DTR = 0648 times1198820651 (9)

We assumed that 25 of tuber biomass was unavailablefor consumption owing to decomposition [61] To understandhow limiting tuber resources were we compared theseestimates to estimates of the number of swans frequentingthe wetlands between October and March using countsfrom the 12 aerial flyovers and extrapolating over the entirestudy period by assuming each count represented the week(November and December) two weeks (October) or themonth (January and February) the flyover was conductedWe also compared tuber biomass before swans arrived inSeptember to biomass after swans left in March using Mul-tiple Analysis of Variance (MANOVA) with the two datesand the four wetlands as factors to further explore howmuchthe swans had exploited the tuber resource over the fall andwinter period

We used MANOVA to test the hypothesis that tuberbiomass and length increased with sediment depth (5 cmincrements corresponding to the 5 cm sediment core sec-tions) and that the relationship would be similar among allsampled wetlands To test whether swans were preferentiallyfeeding on larger tubers we developed frequency distribu-tions of tuber lengths collected from swan esophagi andfrom sediments of the 4 wetlands and then used ANOVA totest for statistical differences in mean tuber length of tuberingested by swans or found in wetland sediments Likewisewe compared frequency distributions of tubers collected inSeptember and in March to test whether certain sizes weredepleted to a greater extent

We used a two-population 119905-test to test for differencesin neck lengths between the two swan species To exploredifferences in foraging behavior we used MANOVA to testwhether species and age influenced the percent time spentpaddling while foraging and the time spent foraging fortubers (heads and necks submersed)

All biomass measurements are recorded as 100 drymatter (mean dry mass = 3334 wet mass) We used SASsoftware [62] for all statistical tests and S+ for geostatisticalinterpolation between samples [63] Unless otherwise notedwe evaluated statistical significance at 119875 lt 005 and we reportvalues as means plusmn SE

3 Results

31 Tuber Resources In September 1996 Unit 1 supportedthe least average tuber biomassm2 (5 plusmn 27 gm2) followedby Unit 4 (27 plusmn 44 gm2) Unit 2 (35 plusmn 59 gm2) and BRC(41 plusmn 50 gm2) Biomass was significantly different amongwetlands (ANOVA 119865

360= 786 119875 lt 0001) but only

because Unit 1 supported significantly lower tuber biomass


Table 1 Amount of total and exclusive tuber resources and the amount of tuber biomass ingested for each wetland between September andMarch Exclusive resources are only available to trumpeter swans All values reported as 103

Site Shared kg before Exclusive kg before Shared kg after Exclusive kg after Shared kg ingesteda Exclusive kg ingesteda

Unit 1 65 0 33 0 16 0Unit 2 571 0 311 0 117 0Unit 4 243 0 172 0 10 0BRC 892 80 340 61 329 0aAccounts for 25 tuber biomass lost to decomposition [59]

Table 2 Comparison of tundra and trumpeter swan days that the tuber resource (Table 1) could potentially support and the number of tundraand trumpeter swans actually observed foraging in the four study wetlands We assume tundra swans require 2585 g tubersday (twice basalmetabolic rate) and trumpeter swans require 3618 g tubersday Swans are likely to ingest more tuber biomass per day during staging tomaximize energy intake

Site Calculated tundra swandays on shared resourcesa

Actual tundraswan daysb

Calculated trumpeter swandays on exclusive resourcesa

Actual trumpeterswan daysb

Unit 1 189000 90000 0 0Unit 2 1657000 418000 0 0Unit 4 705000 127000 0 0BRC 2588000 821000 166000 600Total 5138000 1456000 165000 600aCalculation of swan days does not take into account that swans will not completely deplete the tuber resources in the sediments Calculations account for25 tubers lost to decomposition during dormancybCalculation of actual swan days takes into account days that the wetlands were frozen shut and swans were not foraging

(Figure 1) In March 1997 50 of the tuber resources weredepleted in Unit 1 (25 plusmn 23 gm2) 29 in Unit 4 (20 plusmn54 gm2) 43 in Unit 2 (20 plusmn 46 gm2) and 59 in BRC(17 plusmn 43 gm2) Comparison of wetlands and dates showedthat biomass differed significantly (MANOVA119865

4123= 1173

119875 lt 0001) because Unit 1 produced significantly less tuberbiomass than the other wetlands in September and March(Table 1) Tuber depletion in the 4 wetlands reflects swan useduring the study period as observed during flyovers whereswans frequented BRC themost (4549 swans per day betweenOctober 15 and March 15) Unit 2 supported on average 2821swansday and Unit 4 supported 1854 swansday Unit 1 wasused almost exclusively as a resting area during the dayhence counts are inflated andwere not used in our analysis ascounts of foraging swans From these counts and accountingfor days when the wetlands were frozen and swans could notforage the wetlands supported 15 times 106 swan days betweenSeptember and March (Table 2) The tuber resources on theother hand could potentially support 51 times 106 swan days(Table 2) This estimate is calculated by dividing total tuberresources in each wetland after accounting for 25 tuberbiomass loss to decomposition [61] by estimates of dailytuber requirements of both species (see calculations for tuberbiomass requirements under Comparative Efficiency) Theestimate does not account for swans giving up a foraging areaat a tuber biomass or density that is no longer lucrative formaximizing energy intake [64 65] It also does not take intoaccount that swans are hyperphagic during staging and willconsume more than their daily requirement to gain weight

BRC was the only wetland that supported exclusiveresources during the study period (Table 1) Exclusive

tuber resources accounted for 8 of total tuber biomassin BRC or 4 of total biomass in all four wetlands Weestimate that exclusive resources could support 17 times 105trumpeter swan days (Table 2) however we found noevidence that these resources were actually exploited bytrumpeter swans (Table 1)Nevertheless groundobservationsand radiotelemetry data suggest that trumpeter swans fedalmost exclusively in BRC corresponding to areas supportingthe highest tuber biomass and providing exclusive tuberresources to trumpeter swans

Tuber length and total biomass increased with sedimentdepth in all sampled wetlands (Figure 2 MANOVA 119865

22732=

689 119875 lt 0001 for biomass 119865221122= 2380 119875 lt 0001

for size) Wetlands differed in their mean tuber length andbiomass (119875 lt 001 in both cases) We found a significantinteraction (119875 lt 001) between wetland and sediment depthfor tuber length only which was driven by one of the fourwetlands Unit 1 which supported the least tuber biomass

Ground and aerial observations indicated that bothspecies exclusively fed in sediment beneath submersedaquatic plant beds which in November and Decemberonly provide sago pondweed tubers as a food resource forswans Of 50 tundra swan gizzards and esophagi collected7 contained 100 sago pondweed tubers and no other plantmaterials The rest of the esophagi and gizzards were emptyTuber lengths extracted from tundra swan esophagi were sig-nificantly longer than tuber lengths extracted from wetlandsoils (Figure 3(a) ANOVA 119865

42299= 6552 119875 lt 0001)

Frequency distributions of tuber lengths in swan esophagicompared to wetland soils show a mode of 7mm for swansversus 5mm for wetland soils (Figure 3(a)) Lengths of tubers


5 10 15 20 25 30 35 40 45

Tube

r siz

e (m

m)

3

4

5

6

7

8

9

10

11

Sediment depth (cm)

(a)

Unit 1 Unit 2

Unit 4 BRC

Sediment depth (cm)5 10 15 20 25 30 35 40 45

0

20

40

60

80

100

120

Tube

r dry

wei

ght (

g mminus2

)

(b)

Figure 2 Tuber length (a mean plusmn 1SE) and tuber dry mass (b mean plusmn 1SE) per 5 cm depth increments (eg values at 5 cm depth representtubers found in 0ndash5 cm sediment depth) for the four study wetlands Maximum sediment to a calcium hardpan differed among wetlandswith BRC being the wetland with the deepest sediments

Tuber size (mm)1 2 3 4 5 6 7 8 9 10 11 12 13

Num

ber o

f tub

ers

0

50

100

150

200

(a)

Tuber size (mm)1 2 3 4 5 6 7 8 9 10 11 12 13

Num

ber o

f tub

ers

0

50

100

150

200

Unit 1Unit 2Unit 4

BRCSwan esophagus

(b)

Figure 3 Number of tubers for each tuber length (mm) in a representative swan esophagus (a) and collected from sediment cores of thefour studied wetlands in September (a) and March (b) Note that absolute number of tubers is presented to show differences in tuber densityamong wetlands and seasons Mean plusmn 1SE of tuber length for swans 757 plusmn 064mm Unit 1 557 plusmn 022mm Unit 2 614 plusmn 013mm Unit 4606 plusmn 014mm BRC 625 plusmn 007mm

sampled from March sediments (Figure 3(b)) show thattubers in Unit 2 (ANOVA 119865

1528= 628 119875 = 001) and BRC

(ANOVA11986511207= 1836119875 lt 0001) are significantly smaller

than tubers collected in September (667 plusmn 013mm in Unit 2and 566 plusmn 012mm in BRC) Average tuber length for Unit 1and Unit 4 did not differ between September and March

32 Body Size and Behavioral Observations Body morphol-ogy measurements found in the literature [47 48] and field

measurements show that size ratios range from 11 to 12 forlinear estimates (eg bill length and neck length) and 16 formass measurements with trumpeter swans being the biggerof the two species Trumpeter swans had longer necks (5104plusmn070 cm) than tundra swans (4705 plusmn 037 cm) (ANOVA1198651134= 3112 119875 lt 0001)

Behavioral observations showed that swans differed in thepercent time they spent paddling while foraging (MANOVA119865216= 471 119875 = 002) and the time spent foraging under


Table 3 Inter- and intraspecific aggression between and among tundra and trumpeter swans while feeding on sago pondweed tubers Swanswere observed feeding in mixed flocks for 235 h Interactions always resulted in the target individual moving away Swans actively displacedeach other through bites and chases and often threatened with outstretched necks or a hiss Occasionally they would passively displace eachother by passively occupying the space of a foraging swan (ldquospatialrdquo) A gt B denotes that A wins in an aggressive encounter

Interaction Tundra gt tundra Tundra gt trumpeter Trumpeter gt tundra Trumpeter gt trumpeterBite 3 0 16 3Chase 5 0 0 1Neck 2 0 2 0Hiss 2 0 7 0Spatial 0 1 1 0

water (MANOVA 119865216= 924 119875 = 0002) We did not

detect significant differences among species Rather adultsand juveniles exhibited different foraging behaviors withjuveniles spending more time paddling (119875 = 007) and lesstime submersed under water (119875 = 0001)

Observations on intra- and interspecific interactionsamong swans showed that out of 43 interactions observedtrumpeter swans displaced tundra swan 26 times whereasone adult tundra swans displaced one juvenile trumpeterswan once during the observation period (Table 3) Weobserved one juvenile trumpeter swan displacing one adulttundra swan Field notes suggest that trumpeter swans wereclearly the dominant species even when few individuals wereforaging in the midst of a large tundra swan flock

33 Comparative Efficiency The calculated standardmetabolic rates are 17 Jsec for a 675 kg adult tundra swanand 25 Jsec for a 1086 kg trumpeter swan Average dailymetabolic rate (ADMR) and field metabolic rate (FMR)were both calculated as 35 Jsec for a tundra swan and49 Jsec for a trumpeter swan Dividing field metaboliccost by the true metabolizable energy content of sagopondweed tubers (117 kJg [60]) a tundra swan requires2585 g tubers per day (Beekman et al [61] estimated 283 gper day for tundra swans in the Netherlands) whereasa trumpeter swan requires approximately 3618 g tubersper day Using the allometric equation for birds proposedby Nagy [54] the tuber requirement for tundra swans is2016 gday and 274 gday for trumpeter swans Becausethe allometric equation underestimates food consumptionduring staging [54] and our estimates incorporate the actualenergy content of tubers we used our estimates of the dailytuber biomass requirements while swans stage or winter inUtah to calculate how many swans can be supported on theshared and exclusive portions of tuber resources (see above)

Tundra swans consume approximately 1700 Jsec whenflying whereas trumpeter swans consume approximately3500 Jsec [56] that is flight costs are 21 times higher fortrumpeter swans Tundra swans consume 00375 Jsec whileswimming and trumpeter swans consume 006 Jsec that isswimming costs are 16 times greater for trumpeter swansLikewise trumpeter swans consume 048 Jsec when pad-dling while tundra swans consume 030 Jsec Thus paddlingis also 16 times more costly for trumpeter swans as it is fortundra swans

Table 4 Calculation of efficiency indices for tundra and trumpeterswans The index is defined as the ratio between foraging gains andtotal energy requirements in one day including costs of free livingand mechanical costs of foraging flights swimming and paddlingIntake rate for tundra swans (119877tub) was derived fromNolet et al [49]for clayey substrate Fraction of each day spent foraging (119891forage)swimming (119891swim) and paddling (119891paddle) is based on observationsof foraging swans Powell and Engelhardt [56] reported 119864flight fora 5 kilometer foraging flight Mechanical costs are not adjusted byaerobic efficiency

Tundra swan Trumpeter swan119891forage 042 042119877tub (gsec) 0020 0024119873sec (sec) 86400 86400Eflight (kJ) 80 120Pmet (Jsec) 3460 4931f swim 0094 0094Pswim (Jsec) 00375 00600f paddle 0019 0030Ppaddle (Jsec) 030 048Gain (kJ) 8424 10109Cost (kJ) 3102 4432Efficiency 272 228

Field observations on swans foraging in the BRMBR andBRC wetland units suggest that time spent foraging approxi-mately 10 h per day (similar to Squires [60]) is roughly equalfor each species Exact foraging time over a 24 h period couldnot be determined because swans would frequently forageduring the night when observations could not be madeHowever inaccuracies of foraging time cancel out because weassume that both species forage for approximately the sameamount of time Detailed observations on foraging swansshow that on average swans spent 10 of their foragingtime paddling to uncover tubers and 15 of their foragingtime swimming between and searching for lucrative tuberpatches Hence using values summarized in Table 4 and theenergy content of sago pondweed tubers (120578 = 117 kJg)the efficiency (kJ gainkJ cost) for tundra swans is 52 and42 for trumpeter swans Gains here greatly exceed costsbecause not all costs of free existence are accounted for andmechanical costs are not adjusted by an aerobic efficiency IfADMRor FMR is used rather than SMR for the119875met estimate


then efficiency decreases to 27 for tundra swans and 23 fortrumpeter swans

4 Discussion

In this study we explore whether body size differentiationcan lead to coexistence even in the absence of resourcepartitioning when one species incurs lower foraging costsbut the other species can gain access to exclusive resourcesby (a) exploiting the portion of the resource that the otherspecies cannot physically reach (included niche hypothesis)or by (b) displacing the other species from the shared resourcethrough aggressive behavior (shared preference hypothesis)While resources were probably not limiting during the studyperiod we show that the smaller tundra swan ismore efficientin exploiting tuber resources because it incurs lower foragingcosts per unit energy gained than the bigger trumpeter swanhowever trumpeter swans have access to exclusive tuberresources that are available to them through their longernecks and bodies (the included niche hypothesis) Even inthe absence of exclusive resources a trade-off exists betweenlower foraging costs of tundra swans and the aggressivebehavior by trumpeter swans that allows them access tolucrative resource locations (the shared preference hypothe-sis) Thus in situations where resources are limiting such assmall wetlands with large swan populations the trade-offs wereport may be important in enhancing the coexistence of thetwo swan species during staging and wintering

Smaller species are often more efficient foragers [66]where foraging efficiency is defined as the energetic gainper unit cost of foraging [19 22] In our case the smallertundra swan incurred lower costs associated with flying shortdistances between foraging and resting areas [56] swimmingbetween tuber patches and paddling to stir up the watercolumn and sediments Standard and field metabolic ratesare also lower for tundra swans Thus extra resource gainsto overcome costs need to be at least 15 times higher fortrumpeter swans However trumpeter swans are at most 12times more effective in foraging for tubers if larger bill sizeallows trumpeter swans to encounter and capturemore tubersper unit effort If not trumpeter swans are at an even greaterdisadvantage when comparing energetic gains to energeticcosts related to body size Trumpeter swans have to overcometheir greater foraging costs relative to foraging gains byinterfering more andor by feeding longer in one areaIndeed we found that trumpeter swans were more aggressive(Table 4) and should be less inclined to take off because flightsare approximately twice as expensive for trumpeter swansas tundra swans [56] We did not observe any interspecificdifferences in time spent foraging in an area Differences inforaging behaviors need not be large to overcome differencesin foraging costs however high variance in foraging behavioramong individuals of the same species especially betweenadults and juveniles would require the sample size to beunrealistically large to detect differences among species

Mass intake rate is a function of tuber density tuberlength and burial depth where larger tubers buried deeper inthe sediments may not necessarily yield higher mass intake

rates [67 68] Mass intake rates are hard to predict withoutdirect experiments Nevertheless tuber lengths found intundra swan esophagi were on average bigger than tubersfound in wetland sediments (Figure 3(a)) and longer tuberswere depleted to a greater extent in the two study wetlandsthat most swans foraged in (Unit 2 and BRC Figure 3(b))Thus we can conclude that tundra swans selected biggertubers that are found deeper in the sediments (Figure 2)where tuber density is lower (compare Figure 2(a) andFigure 3(a)) We have no reason to believe that trumpeterswans would select tubers differently

Swans left the study area in the spring when the threemost productive wetlands reached a surprisingly constanttuber biomass of 17ndash20 gm2 and a tuber density of 634ndash672 tubersm2 Wetlands with the highest tuber biomass anddensity were depleted to a greater extent than less lucrativewetlands (Figure 1) indicating that the swans maximizedtheir energy intake by foraging in the most lucrative areasAerial and ground observations that monitored presenceand density of tundra and trumpeter swans through timecorroborate this conclusion From the tuber depletion mea-surements and the interaction observations we can concludethat swans were competing for access to the most lucrativetuber patches even though total food resources may not havebeen limitingWe also conclude that trumpeter swans cannotachieve sufficient density on exclusive tubers alone (Table 2)to outcompete tundra swans for the shared tubers hence anincluded niche scenario is a plausible explanation for speciescoexistence in our model system

Even when exclusive resources are absent or cannot beused profitably (no depletion of exclusive resources wasdetected Table 1) trumpeter swans through their aggressivebehavior could gain easy access to shared resources Thisscenario is similar to the shared preferenceinterferencesystem developed and tested by Pimm et al [37] In thissystem hummingbirds share a preference for a habitat butat a high enough density of the dominant species thesubdominant switches to the less preferable habitat Habitatsin our swan system are dominated by the same food item butdensity and biomass of the tuber resource differ within andamongwetlands Hence we predict that trumpeter swans willdisplace tundra swans from lucrative areas when trumpeterswan densities and harassment pressures are large enoughfor tundra swans to move away A trade-off then betweenaggressive behavior of the bigger species and the lowerforaging costs of the smaller species may lead to coexistenceof the two species [24] At what trumpeter swan abundancethis switch will occur is unknown during the study only 57translocated trumpeter swans were present in the study areaand we observed both species foraging in mixed flocks

In summary we show that the larger body size of trum-peter swans may indeed allow this species greater access toexclusive and shared tuber resources because of their greaterniche breadth and aggressive behavior however we foundthat the larger body size is associated with higher energeticcosts Tundra swans on the other hand are able to exploitthe shared resources more efficiently These observationssuggest that the two species can coexist even in the absenceof resource partitioning when resources are limiting owing


to a body size mediated trade-off between greater foragingefficiency by the smaller-bodied tundra swan and greateraccess to resources by the bigger trumpeter swan

5 Conservation Implications

Our findings suggest that competition with tundra swansmost likely cannot account for the absence of trumpeterswans in Utah even when tuber resources are limitingbecause neither species exerts a strong enough negativeeffect on the other that would lead to a population declineThus other factors such as differential mortality and nestingsuccess have to account for the absence of trumpeter swansin Utah wetlands The findings may be applied to othersystems such as the Chesapeake Bay where managers areconcerned about the direct and indirect effects of nonnativemute swans (Cygnus olor) on the survival of native swansIn the Chesapeake Bay wetlands unlike the Utah wetlandslimiting food resources owing to habitat degradation overlyaggressive behavior of mute swans and a large and non-migratory population of mute swans may exert a strongnegative effect on native swans that may ultimately lead totheir decline

Conflict of Interests

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

Acknowledgments

Funding was provided by the Utah Division of WildlifeResourcesUnited States Fish andWildlife Service andDucksUnlimited The Bear River Migratory Bird Refuge and BearRiver Club Company generously provided access to studysites and facilitiesThe authors thank JohnKadlec Renee ChiGregory Wattley and the staff of the Bear River MigratoryBird Refuge for their help in many aspects of the project

References

[1] D Lack Darwinrsquos Finches Cambridge University Press Cam-bridge UK 1947

[2] G E Hutchinson ldquoHomage to Santa Rosalia or why are theresomany kinds of animalsrdquoAmericanNaturalist vol 93 pp 145ndash159 1959

[3] J H Brown Macroecology University of Chicago PressChicago Ill USA 1995

[4] J B Wilson and W J Stubbs ldquoEvidence for assembly ruleslimiting similarity within a saltmarshrdquo Journal of Ecology vol100 no 1 pp 210ndash221 2012

[5] F A Hopf T J Valone and J H Brown ldquoCompetition theoryand the structure of ecological communitiesrdquo EvolutionaryEcology vol 7 no 2 pp 142ndash154 1993

[6] M R Winston ldquoCo-occurrence of morphologically similarspecies of stream fishesrdquoAmerican Naturalist vol 145 no 4 pp527ndash545 1995

[7] S Rocha D Posada and D J Harris ldquoPhylogeography anddiversification history of the day-gecko genus Phelsuma in the

Seychelles islandsrdquo BMC Evolutionary Biology vol 13 article 32013

[8] C S Rolling ldquoCross-scale morphology geometry and dynam-ics of ecosystemsrdquo Ecological Monographs vol 62 no 4 pp447ndash502 1992

[9] RH PetersTheEcological Implications of Body Size CambridgeUniversity Press Cambridge UK 1983

[10] E E Werner ldquoSpecies packing and niche complementarity inthree sunfishesrdquoAmerican Naturalist vol 111 pp 553ndash578 1977

[11] D Schluter ldquoAdaptive radiation in sticklebacks size shape andhabitat use efficiencyrdquo Ecology vol 74 no 3 pp 699ndash709 1993

[12] J A Wiens and J T Rotenberry ldquoMorphological size ratios andcompetition in ecological communitiesrdquo American Naturalistvol 117 pp 592ndash599 1981

[13] D Schluter and P R Grant ldquoDeterminants of morphologicalpatterns in communities of Darwinrsquos finchesrdquo American Natu-ralist vol 123 no 2 pp 175ndash196 1984

[14] A Basset ldquoBody size-related coexistence an approach throughallometric constraints on home-range userdquo Ecology vol 76 no4 pp 1027ndash1035 1995

[15] S H Choi and H Y Suk ldquoThe mechanisms leading to onto-genetic diet shift in a microcarnivore Pterogobius elapoides(Gobiidae)rdquo Animal Cells and Systems vol 16 pp 343ndash3492012

[16] D Tilman ldquoResource competition between planktonic algaean experimental and theoretical approachrdquo Ecology vol 58 pp338ndash348 1977

[17] D Tilman Resource Competition and Community StructurePrinceton University Press Princeton NJ USA 1982

[18] M V Price and K M Heinz ldquoEffects of body size seed densityand soil characteristics on rates of seed harvest by heteromyidrodentsrdquo Oecologia vol 61 no 3 pp 420ndash425 1984

[19] E E Werner and D J Hall ldquoCompetition and habitat shifts intwo sunfishes (Centrarchidae)rdquo Ecology vol 58 pp 869ndash8761977

[20] K RMorgan andM V Price ldquoForaging in heteromyid rodentsthe energy cost of scratch-diggingrdquo Ecology vol 73 no 6 pp2260ndash2272 1992

[21] L T Ballance R L Pitman and S B Reilly ldquoSeabird communitystructure along a productivity gradient importance of compe-tition and energetic constraintrdquo Ecology vol 78 no 5 pp 1502ndash1518 1997

[22] G G Mittelbach ldquoForaging efficiency and body size a study ofoptimal diet and habitat use by bluegillsrdquo Ecology vol 62 pp1370ndash1386 1981

[23] M V Price ldquoEcological consequences of body size a model forpatch choice in desert rodentsrdquo Oecologia vol 59 no 2-3 pp384ndash392 1983

[24] J S Brown ldquoDesert rodent community structure a test of fourmechanisms of coexistencerdquo Ecological Monographs vol 59 no1 pp 1ndash20 1989

[25] G E Belovsky ldquoOptimal foraging and community structurethe allometry of herbivore food selection and competitionrdquoEvolutionary Ecology vol 11 no 6 pp 641ndash672 1997

[26] T W Schoener ldquoField experiments on interspecific competi-tionrdquo American Naturalist vol 122 no 2 pp 240ndash285 1983

[27] L Persson ldquoAsymmetric competition are larger animals com-petitively superiorrdquo American Naturalist vol 126 pp 261ndash2661985


[28] C R Dickman ldquoBody size prey size and community structurein insectivorous mammalsrdquo Ecology vol 69 no 3 pp 569ndash5801988

[29] S Downes andD Bauwens ldquoAn experimental demonstration ofdirect behavioural interference in two Mediterranean lacertidlizard speciesrdquo Animal Behaviour vol 63 no 6 pp 1037ndash10462002

[30] J Melville ldquoCompetition and character displacement in twospecies of scincid lizardsrdquo Ecology Letters vol 5 no 3 pp 386ndash393 2002

[31] S I Robinson-Wolrath and I P F Owens ldquoLarge size in anisland-dwelling bird intraspecific competition and the Domi-nance Hypothesisrdquo Journal of Evolutionary Biology vol 16 no6 pp 1106ndash1114 2003

[32] R S Miller ldquoPattern and process in competitionrdquo Advances inEcological Research vol 4 pp 1ndash74 1967

[33] T W Schoener ldquoCompetition and the form of habitat shiftrdquoTheoretical Population Biology vol 6 no 3 pp 265ndash307 1974

[34] J M Chase and G E Belovsky ldquoExperimental evidence for theincluded nicherdquoAmericanNaturalist vol 143 no 3 pp 514ndash5271994

[35] J M Chase ldquoDifferential competitive interactions and theincluded niche an experimental analysis with grasshoppersrdquoOikos vol 76 no 1 pp 103ndash112 1996

[36] J M Chase ldquoVarying resource abundances and competitivedynamicsrdquo American Naturalist vol 147 no 4 pp 649ndash6541996

[37] S L PimM L Rosenzweig andWMitchell ldquoCompetition andfood selection field tests of a theoryrdquo Ecology vol 66 no 3 pp798ndash807 1985

[38] M L Rosenzweig ldquoHabitat selection and population interac-tions the search for mechanismrdquo American Naturalist vol 137pp S5ndashS28 1991

[39] Y Ziv B P Kotler Z Abramsky and M L RosenzweigldquoForaging efficiencies of competing rodents why do gerbilsexhibit shared-preference habitat selectionrdquo Oikos vol 73 no2 pp 260ndash268 1995

[40] R E Shea The ecology of Trumpeter swans in YellowstoneNational Park and vicinity [MS thesis] University of MontanaMissoula Mont USA 1979

[41] R L Craner Production and waterfowl utilization of sagopondweed on the Bear River Migratory Bird Refuge [MS thesis]Utah State University Logan Utah USA 1964

[42] M R Sterling Seasonal utilization of sago pondweed by water-fowl at Bear River Migratory Bird Refuge Utah [MS thesis]Utah State University Logan Utah USA 1970

[43] K A M Engelhardt Evaluation of translocation criteria fortrumpeter swans reintroduced to northern Utah habitat qualityand interactions with tundra swans [MS thesis] Utah StateUniversity Logan Utah USA 1997

[44] K A M Engelhardt J A Kadlec V L Roy and J A PowellldquoEvaluation of translocation criteria case study with trumpeterswans (Cygnus buccinator)rdquo Biological Conservation vol 94 no2 pp 173ndash181 2000

[45] D F Spencer ldquoTuber size and planting depth influence growthof Potamogeton pectinatus LrdquoAmericanMidland Naturalist vol118 no 1 pp 77ndash84 1987

[46] D F Spencer and G G Ksander ldquoInfluence of planting depthon Potamogeton gramineus Lrdquo Aquatic Botany vol 36 no 4pp 343ndash350 1990

[47] R J Limpert and S L Earnst ldquoTundra swan (Cygnuscolumbianus)rdquo in The Birds of North America A Poole andF Gill Eds No 89 The Academy of Natural Sciences TheAmerican OrnithologistsrsquoUnion Philadelphia Pa USA 1994

[48] C D Mitchell ldquoTrumpeter swan (Cygnus buccinator)rdquo in TheBirds of North America A Poole and F Gill Eds No 89The Academy of Natural Sciences The American Ornitholo-gistsrsquoUnion Philadelphia Pa USA 1994

[49] B A Nolet O Langevoord RM Bevan et al ldquoSpatial variationin tuber depletion by swans explained by differences in netintake ratesrdquo Ecology vol 82 no 6 pp 1655ndash1667 2001

[50] M Owen and C J Cadbury ldquoThe ecology and mortality ofswans at the Ouse Washes Englandrdquo Wildfowl vol 26 pp 31ndash42 1975

[51] D R CopeM J J E Loonen J M Rowcliffe and R A PettiforldquoLarger barnacle geese (Branta leucopsis) are more efficientfeeders a possible mechanism for observed body size-fitnessrelationshipsrdquo Journal of Zoology vol 265 no 1 pp 37ndash42 2005

[52] A M Hemmingsen Energy Metabolism as Related to Body SizeandRespiratory Surfaces and Its Evolution vol 9 Reports on theSteno Memorial Hospital and Nordink Insulin Laboratorium1960

[53] S C Kendeigh V R Dolrsquonik and V M Govrilov ldquoAvianenergeticsrdquo in Granivorous Birds in Ecosystems J Pinowski andS C Kendeigh Eds pp 127ndash204 Cambridge University PressCambridge UK 1977

[54] K A Nagy ldquoField metabolic rate and food requirement scalingin mammals and birdsrdquo Ecological Monographs vol 57 no 2pp 111ndash128 1987

[55] W E Banko The Trumpeter Swan North American Fauna 63US Fish and Wildlife Service Washington DC USA 1960

[56] J A Powell and K A M Engelhardt ldquoOptimal trajectoriesfor the short-distance foraging flights of swansrdquo Journal ofTheoretical Biology vol 204 no 3 pp 415ndash430 2000

[57] C J Pennycuick Bird Flight Performance A Practical Calcula-tion Manual Oxford University Press Oxford UK 1989

[58] E A Avallone and T Baumeister III Eds Marksrsquo StandardHandbook for Mechanical Engineers McGraw-Hill New YorkNY USA 10th edition 1996

[59] G H Flammer R W Jeppson and H F Keedy FundamentalPrinciples and Applications of Fluid Mechanics Utah StateUniversity Logan Utah USA 1986

[60] J R Squires Trumpeter swan food habits forage processingactivities and habitat use [PhD thesis] University ofWyomingLaramie Wyo USA 1991

[61] J H Beekman M R Van Eerden and S Dirksen ldquoBewickrsquosswans Cygnus columbianus bewickii utilising the changingresource of Potamogeton pectinatus during autumn in theNetherlandsrdquoWildfowl no 1 pp 238ndash248 1991

[62] SAS Institute Inc SASSTAT Userrsquos Guide Version 8 01 SASInstitute Cary NC USA 1999

[63] S P Kaluzny S C Vego T P Cardoso and A ShellyS+apatialatata Uaerrsquoa Manual for Windows and Unix Springer1998

[64] J S Brown ldquoPatch use as an indicator of habitat preferencepredation risk and competitionrdquo Behavioral Ecology and Socio-biology vol 22 no 1 pp 37ndash47 1988

[65] J S Brown Y Arel Z Abramsky and B P Kotler ldquoPatch use bygerbils (Gerbillus allenbyi) in sandy and rocky habitatsrdquo Journalof Mammalogy vol 73 no 4 pp 821ndash829 1992


[66] M L Rosenzweig and P W Sterner ldquoPopulation ecology ofdesert rodent communities body size and seed-husking as basisfor heteromyid coexistencerdquo Ecology vol 51 pp 217ndash224 1970

[67] S E Richman and J R Lovvorn ldquoEffects of clam speciesdominance on nutrient and energy acquisition by spectacledeiders in the Bering Seardquo Marine Ecology Progress Series vol261 pp 283ndash297 2003

[68] S E Richman and J R Lovvorn ldquoRelative foraging value tolesser scaupducks of native and exotic clams fromSanFranciscoBayrdquo Ecological Applications vol 14 no 4 pp 1217ndash1231 2004

Submit your manuscripts athttpwwwhindawicom

Forestry ResearchInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Environmental and Public Health

Journal of



EcosystemsJournal of


MeteorologyAdvances in

EcologyInternational Journal of


Marine BiologyJournal of


Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Advances in


Environmental Chemistry

Atmospheric SciencesInternational Journal of



Waste ManagementJournal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics


Geological ResearchJournal of

EarthquakesJournal of


BiodiversityInternational Journal of


ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

OceanographyInternational Journal of


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Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014


ClimatologyJournal of


animals are generally more likely to displace smaller-bodiedindividuals through aggressive behavior [21 26ndash31]

If larger species indeed have greater access to resourcesthen species coexistence may be mediated by body sizedifferentiation if smaller species are more efficient foragersFor example the niche of one speciesmay be entirely includedwithin the niche of a second species For species to coexistunder these conditions [32 33] the species with the narrowerincluded niche must be more efficient in exploiting theshared resources and the species with the broader nichemust not achieve sufficient density on exclusive resourcesto numerically outcompete the included niche species forthe shared resources (ldquoincluded nicherdquo hypothesis) [34ndash36]Similar to the included niche scenario two species can coexistwhen the larger species can displace the smaller species fromlucrative foraging locations through aggressive behavior butthe smaller species is more efficient in exploiting the sharedresources (ldquoshared preferencerdquo hypothesis) [37ndash39]

Tundra and trumpeter swans are often observed sharingthe same habitats in space and time [40] and feed on the sameresource sago pondweed (Potamogeton pectinatus) tuberswhile staging and wintering in Utah because the tubers arethe only available food source during that time [41ndash43] Weexplored the hypothesis that differences between swan bodysizes allow the two species to coexist on one resource viaan included niche For the included niche hypothesis not tobe rejected tundra swans would have to be more efficientforagers but trumpeter swans would have to have access totuber resources buried deep in wetland sediments We alsotested the shared preference hypothesis that trumpeter swansare superior competitors for the food resources throughinterspecific aggression If so the two species can coexisteven without access to exclusive resources if a trade-off existsbetween superior foraging efficiency of tundra swans andaggressive behavior by trumpeter swans

2 Methods

To assess the potential for tundra and trumpeter swancoexistence via body size mediated trade-offs we sought toestimate foraging efficiency of the two species versus eitherniche breadth (amount of shared and exclusive resourcesavailable to the swans included niche hypothesis) or aggres-sive behavior (shared preference hypothesis) Because assess-ment of energy gains and costs associated with body sizeis inherently difficult and would have required extensivehandling and undue stress on a federally protected species weestimated foraging efficiency using a mechanical estimationapproach By measuring the quantity and distribution offood resources in wetland sediments we could calculate theamount of shared and exclusive tuber resources availablein wetland sediments Behavioral observations documentedinterspecific aggression and displacement of individuals fromforaging locations

21 Species and StudyArea Westudied tundra and trumpeterswans and their food resources at the Bear River MigratoryBird Refuge (BRMBR divided into 3 separate wetland units

Unit 1 Unit 2 and Unit 4) and the Bear River Club Company(BRC) in northern Utah (41∘271015840N 112∘181015840W) Trumpeterswans are rare inUtah hence 57 trumpeter swans from Idahowere released by state (Utah Division of Wildlife ResourcesIdaho Department of Fish and Game) and federal (US Fishand Wildlife Service) agencies into BRC in November andDecember 1996 to expand their wintering range [43 44]Tundra swans are abundant throughout the study area duringthe fall winter and spring months (as estimated by the UtahDivision of Wildlife Resources every two weeks in Octoberevery week in November and December and once in Januaryand March with surveys of low-flying aircraft)

22 Tuber Resources We quantified biomass of sagopondweed tubers before swans migrated through orwintered on the study areas in the four study wetlands Weresampled the same areas in March after the swans had leftto migrate north to their breeding grounds We placed 64transects in the 4 wetlands using a two-stage systematic-random sampling design where each transect was randomlyplaced within a 1 km2 area and each 1 km2 area was part ofa grid covering the 4 study wetlands Transects were 200mlong with one core taken every 20m Cores (52 cm diameter)were between 15 cm and 45 cm long depending on the depthof the Calcium hardpan that delineates the depth to whichsago pondweed tubers are produced We divided cores into5 cm sections to explore the 3-dimensional distribution oftuber biomass in wetland sediments which allowed us tocalculate the shared and exclusive portions of the tuberresource We washed all samples through a sieve with 1mmopenings to extract all tubers which we subsequently driedand weighed

To test the hypothesis that swans have access to biggertubers found in deeper sediments [45 46] and preferentiallyfeed on bigger tubers we first determined the relation-ship between tuber length and depth in Utah sedimentsand then compared tuber length distributions in wetlandsediments to tuber length distributions in swan esophagiWe determined the diets of tundra swans by extracting thegizzards and esophagi of 50 swans killed by swan huntersWe then measured the length and mass of all tubers foundin the gizzards and esophagi Trumpeter swan diets couldnot be determined because this species is protected fromhuntingWe supplemented the diet information by observingfeeding trumpeter and tundra swans during the day (wedyed trumpeter swans pink under their left wing to enhanceidentification without drawing undue attention to the swans)and locating them by radiotelemetry (Holohill Canada) atnight

23 Swan Morphology and Behavior We reviewed morpho-logical measurements in the literature [47 48] and measuredneck length to estimate the maximum depth each speciescan potentially forage to by stretching its neck down throughthe water and sediment Swans also ldquotip uprdquo to reach deeperresources the legs latter part of the body and tail are the onlybody parts remaining above the water surface [49] Thus weestimated the maximum reach of a swan as 15 times the neck








0

10

20

30

40

50

SeptemberMarch

a

b

b

b

A

B BB

Tube

r bio

mas

s (g m

minus2

)




Tundratub (1)



SMR = 411198820751 (2)


FMR = 109 times 119882064 (3)






119875swim = 0011119872H2OV

swimave (4)




119865paddle = 119888119863120588water119860

2

(Vpaddleave )2

(5)





paddleave 119871120583H2O 119888




2O = 1518 times 10




119888119863

120593water119860

2

(Vpaddleave )3

= 119875paddle = 119875swim


(6)






=

120578 (119891forage119877tub119873sec)


(7)






DTR = ADMR120578

(8)


DTR = 0648 times1198820651 (9)





3 Results


360= 786 119875 lt 0001) but only













4123= 1173





22732=

689 119875 lt 0001 for biomass 119865221122= 2380 119875 lt 0001



42299= 6552 119875 lt 0001)



5 10 15 20 25 30 35 40 45

Tube

r siz

e (m

m)

3

4

5

6

7

8

9

10

11

Sediment depth (cm)

(a)

Unit 1 Unit 2

Unit 4 BRC


0

20

40

60

80

100

120

Tube

r dry

wei

ght (

g mminus2

)

(b)


Tuber size (mm)1 2 3 4 5 6 7 8 9 10 11 12 13

Num

ber o

f tub

ers

0

50

100

150

200

(a)

Tuber size (mm)1 2 3 4 5 6 7 8 9 10 11 12 13

Num

ber o

f tub

ers

0

50

100

150

200

Unit 1Unit 2Unit 4

BRCSwan esophagus

(b)



1528= 628 119875 = 001) and BRC



















4 Discussion














Acknowledgments


References












































































Journal of












Volume 2014

Advances in









Geophysics





















0

10

20

30

40

50

SeptemberMarch

a

b

b

b

A

B BB

Tube

r bio

mas

s (g m

minus2

)




Tundratub (1)



SMR = 411198820751 (2)


FMR = 109 times 119882064 (3)






119875swim = 0011119872H2OV

swimave (4)




119865paddle = 119888119863120588water119860

2

(Vpaddleave )2

(5)





paddleave 119871120583H2O 119888




2O = 1518 times 10




119888119863

120593water119860

2

(Vpaddleave )3

= 119875paddle = 119875swim


(6)






=

120578 (119891forage119877tub119873sec)


(7)






DTR = ADMR120578

(8)


DTR = 0648 times1198820651 (9)





3 Results


360= 786 119875 lt 0001) but only













4123= 1173





22732=

689 119875 lt 0001 for biomass 119865221122= 2380 119875 lt 0001



42299= 6552 119875 lt 0001)



5 10 15 20 25 30 35 40 45

Tube

r siz

e (m

m)

3

4

5

6

7

8

9

10

11

Sediment depth (cm)

(a)

Unit 1 Unit 2

Unit 4 BRC


0

20

40

60

80

100

120

Tube

r dry

wei

ght (

g mminus2

)

(b)


Tuber size (mm)1 2 3 4 5 6 7 8 9 10 11 12 13

Num

ber o

f tub

ers

0

50

100

150

200

(a)

Tuber size (mm)1 2 3 4 5 6 7 8 9 10 11 12 13

Num

ber o

f tub

ers

0

50

100

150

200

Unit 1Unit 2Unit 4

BRCSwan esophagus

(b)



1528= 628 119875 = 001) and BRC



















4 Discussion














Acknowledgments


References












































































Journal of












Volume 2014

Advances in









Geophysics



















119875swim = 0011119872H2OV

swimave (4)




119865paddle = 119888119863120588water119860

2

(Vpaddleave )2

(5)





paddleave 119871120583H2O 119888




2O = 1518 times 10




119888119863

120593water119860

2

(Vpaddleave )3

= 119875paddle = 119875swim


(6)






=

120578 (119891forage119877tub119873sec)


(7)






DTR = ADMR120578

(8)


DTR = 0648 times1198820651 (9)





3 Results


360= 786 119875 lt 0001) but only













4123= 1173





22732=

689 119875 lt 0001 for biomass 119865221122= 2380 119875 lt 0001



42299= 6552 119875 lt 0001)



5 10 15 20 25 30 35 40 45

Tube

r siz

e (m

m)

3

4

5

6

7

8

9

10

11

Sediment depth (cm)

(a)

Unit 1 Unit 2

Unit 4 BRC


0

20

40

60

80

100

120

Tube

r dry

wei

ght (

g mminus2

)

(b)


Tuber size (mm)1 2 3 4 5 6 7 8 9 10 11 12 13

Num

ber o

f tub

ers

0

50

100

150

200

(a)

Tuber size (mm)1 2 3 4 5 6 7 8 9 10 11 12 13

Num

ber o

f tub

ers

0

50

100

150

200

Unit 1Unit 2Unit 4

BRCSwan esophagus

(b)



1528= 628 119875 = 001) and BRC



















4 Discussion














Acknowledgments


References












































































Journal of












Volume 2014

Advances in









Geophysics

















=

120578 (119891forage119877tub119873sec)


(7)






DTR = ADMR120578

(8)


DTR = 0648 times1198820651 (9)





3 Results


360= 786 119875 lt 0001) but only













4123= 1173





22732=

689 119875 lt 0001 for biomass 119865221122= 2380 119875 lt 0001



42299= 6552 119875 lt 0001)



5 10 15 20 25 30 35 40 45

Tube

r siz

e (m

m)

3

4

5

6

7

8

9

10

11

Sediment depth (cm)

(a)

Unit 1 Unit 2

Unit 4 BRC


0

20

40

60

80

100

120

Tube

r dry

wei

ght (

g mminus2

)

(b)


Tuber size (mm)1 2 3 4 5 6 7 8 9 10 11 12 13

Num

ber o

f tub

ers

0

50

100

150

200

(a)

Tuber size (mm)1 2 3 4 5 6 7 8 9 10 11 12 13

Num

ber o

f tub

ers

0

50

100

150

200

Unit 1Unit 2Unit 4

BRCSwan esophagus

(b)



1528= 628 119875 = 001) and BRC



















4 Discussion














Acknowledgments


References












































































Journal of












Volume 2014

Advances in









Geophysics

























4123= 1173





22732=

689 119875 lt 0001 for biomass 119865221122= 2380 119875 lt 0001



42299= 6552 119875 lt 0001)



5 10 15 20 25 30 35 40 45

Tube

r siz

e (m

m)

3

4

5

6

7

8

9

10

11

Sediment depth (cm)

(a)

Unit 1 Unit 2

Unit 4 BRC


0

20

40

60

80

100

120

Tube

r dry

wei

ght (

g mminus2

)

(b)


Tuber size (mm)1 2 3 4 5 6 7 8 9 10 11 12 13

Num

ber o

f tub

ers

0

50

100

150

200

(a)

Tuber size (mm)1 2 3 4 5 6 7 8 9 10 11 12 13

Num

ber o

f tub

ers

0

50

100

150

200

Unit 1Unit 2Unit 4

BRCSwan esophagus

(b)



1528= 628 119875 = 001) and BRC



















4 Discussion














Acknowledgments


References












































































Journal of












Volume 2014

Advances in









Geophysics















5 10 15 20 25 30 35 40 45

Tube

r siz

e (m

m)

3

4

5

6

7

8

9

10

11

Sediment depth (cm)

(a)

Unit 1 Unit 2

Unit 4 BRC


0

20

40

60

80

100

120

Tube

r dry

wei

ght (

g mminus2

)

(b)


Tuber size (mm)1 2 3 4 5 6 7 8 9 10 11 12 13

Num

ber o

f tub

ers

0

50

100

150

200

(a)

Tuber size (mm)1 2 3 4 5 6 7 8 9 10 11 12 13

Num

ber o

f tub

ers

0

50

100

150

200

Unit 1Unit 2Unit 4

BRCSwan esophagus

(b)



1528= 628 119875 = 001) and BRC



















4 Discussion














Acknowledgments


References












































































Journal of












Volume 2014

Advances in









Geophysics



























4 Discussion














Acknowledgments


References












































































Journal of












Volume 2014

Advances in









Geophysics




















Acknowledgments


References












































































Journal of












Volume 2014

Advances in









Geophysics





























































Journal of












Volume 2014

Advances in









Geophysics














Research Article Body Size Mediated Coexistence in...

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