Mammalian Collection on Noah's Ark

12 Pages·2013·0.71 MB·English

Mammalian Collection on Noah’s Ark: The Effects of
Beauty, Brain and Body Size
Daniel Frynta*, Olga Sˇimkova´, Silvie Lisˇkova´, Eva Landova´
DepartmentofZoology,FacultyofSciences,CharlesUniversityinPrague,Prague,CzechRepublic
Abstract
Theimportanceoftoday’s zoologicalgardensastheso-called‘‘Noah’sArk’’ growsasthenatural habitatofmanyspecies
quicklydiminishes.Theirpotentialtoshelteralargeamountofindividualsfrommanyspeciesgivesustheopportunityto
reintroduceaspeciesthatdisappearedinnature.However,theselectionofanimalstobekeptinzoosworldwideishighly
selectiveanddependsonhumandecisionsdrivenbybothecologicalcriteriasuchaspopulationsizeorvulnerabilityand
audience-driven criteria such asaesthetic preferences. Thus we focused our study onthe most commonly keptand bred
animal class, the mammals, and we asked which factors affect various aspects of the mammalian collection of zoos. We
analyzedthepresence/absence,populationsize,andfrequencyperspeciesofeachofthe123mammalianfamilieskeptin
theworldwidezoocollection.Ouraimwastoexplainthesedatausingthehuman-perceivedattractivenessofmammalian
families,theirbodyweight,relativebrainsizeandspeciesrichnessofthefamily.Inagreementwithvariouspreviousstudies,
we found that the body size and the attractiveness of mammals significantly affect all studied components of the
mammaliancollectionofzoos.Thereisahigherprobabilityofthelargeandattractivefamiliestobekept.Oncekept,these
animalsarepresentedinlargernumbersinmorezoos.Onthecontrary,therelativemeanbrainsizeonlyaffectstheprimary
selectionwhethertokeepthefamilyornot.Itdoesnotaffectthezoopopulationsizeorthenumberofzoosthatkeepthe
family.
Citation:FryntaD,Sˇimkova´ O,Lisˇkova´S,Landova´ E(2013)MammalianCollectiononNoah’sArk:TheEffectsofBeauty,BrainandBodySize.PLoSONE8(5):
e63110.doi:10.1371/journal.pone.0063110
Editor:DavidL.Roberts,UniversityofKent,UnitedKingdom
ReceivedDecember10,2012;AcceptedMarch28,2013;PublishedMay15,2013
Copyright: (cid:2) 2013 Frynta et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalauthorandsourcearecredited.
Funding:TheprojectwassupportedbytheGrantAgencyoftheCzechAcademyofSciences(projectnumberIAA601410803).PersonalcostsofOSˇandSLwere
partiallysupportedbytheprojectnumberSVV-2013-267201.Thefundershadnoroleinstudydesign,datacollectionandanalysis,decisiontopublish,or
preparationofthemanuscript.
CompetingInterests:Theauthorshavedeclaredthatnocompetinginterestsexist.
*E-mail:[email protected]
Introduction ofzoosduringtheConventiononBiologicalDiversity(CBD),and
obliged the zoos to manage theex-situ and in-situ conservational
Nowadays, mankind covers about 83% of the Earth’s land role under the CBD’s requirements [7], regardless of the lack of
surface [1], causing global biodiversity to decline due to a quick thegovernment’ssystematicfinancialorothersupport[8].EAZA
loss of natural habitats of many species [2]. The proportion of (American Association of Zoos and Aquariums) and AZA
potentially threatened species is rapidly increasing, leaving only (American Association of Zoos and Aquariums) supervise many
veryfewspeciessafefromapossibleextinction[3].Itistherefore specific ex-situ conservation programs such as Species Survival
important not to miss any potential chance for animal conserva- PlansandEuropeanEndangeredSpeciesProgrammes.Moreover,
tion,includingbothin-situandex-situconservationalefforts.The theycooperatewithCBSG,TAGs(TaxonAdvisoryGroups)and
world’s zoos,aquaria,botanicalgardens,andgenebanksprovide use various studbooks and data management systems, notably
insurance for species and genetic diversity [4]. According to the ISIS, to maintain the breeding of a variety of species which may
ISIS (International Species Information System) online database, also raise the effectiveness and possibility of species survival
more than 7 million individual animals are kept in 872 zoos and through captive breeding [9–11].
aquariums (as recorded by the date of 12th January 2011). The However, although the space to accommodate wild animals in
highpotential ofzoostoserve aswildlifereservoirs, coupledwith zoos worldwide altogether is large, it is still very limited when
therapiddestruction ofnaturethat wehavefacedinthelastfew comparedtothelistofallextantspecies.Onlyasmallfractionof
decades,led[5]toframethelandmarkArkHypothesis.Therole the world’s animal population can board the Ark. In the year
of zoos as an ark proved viable in the case of amphibians (the 2009, the Ark provided space for about 152 thousand individual
‘‘AmphibianArk’’)thatsufferedarapidpopulationdeclinedueto mammalsbelongingto990species(18.5%ofextantspecies)within
thechytridiomycosisdisease.Inresponsetothisthreat,TheWorld a median worldwide zoo population size of 34.5 individuals.
Association of Zoos and Aquariums (WAZA), the IUCN/SSC Empirical studies suggest that the minimum population size
(The International Union for Conservation of Nature/Species necessary for short-time captive maintenance of animal species/
Survival Commission) Amphibian Specialist Group, and the breeds under controlled conditions is about 50 [12], and
IUCN/SSC Conservation Breeding Specialist Group (CBSG) populations over about 500 individuals are usually not affected
worked together to collect a large number of species [6]. byinbreedingdepression[13].Althoughthesethresholdsareonly
Moreover,in1993theEUrecognizedthisconservationpotential rough estimates because the effect depends on both effective
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population size and frequency of deleterious recessive mutations Similarly, imagine a well-educated surgeon with no experience
(cf. [14–16]). The zoos worldwide maintain 416 mammalian with realpatients toperformoperations onliving humans.
speciesrepresentedbymorethan50individuals,whichis7.8%of The situation is complicated due to the fact that conservation
all extant species. For the threshold of 500 individuals, the activitiesarenottheonlypurposeofthezoos.Infact,itisanissue
numberscountonly79mammalianspecies,representing1.5%of discussed more intensively during the last several decades [38].
the extant mammalian diversity [17]. Similar numbers were Zoosarevitallydependantonthefundsgainedfromvisitors[39].
confirmedinanindependentstudyfromApril2010[18],finding Guestscometozoosmainlyforrecreationalactivities,expectingto
thatoutofall142threatenedmammalianspeciesbelongingtothe see large, attractive, and active animals [40–42]. This may
IUCNcategoriesEndangered,CriticallyEndangered,andExtinct seeminglyleadtotheconclusionthatthereisatrade-offofwhich
in the wild, 68 species are being kept in zoos in more than 50 animalstokeepinzoostosatisfybothconservationalpurposesand
individuals, out of which 30 species are kept in more than 250 thevisitors’recreationaldesires.Thespecies’conservationalstatus
individuals. accordingtotheIUCNwasnotthekeyfactorfortheselectionof
Such small numbers point out that, even theoretically, if zoos speciestobeincludedintheworldwidezoocollection(see[17,18]
tried to keep and breed endangered species, the space would be forterrestrialvertebrates;[43]forparrots,[44]forboidsnakes).A
limited to hold only a tiny fraction of needful species at question thus arises: is it the attractiveness and/or factors
populations large enough tosustain a long-term captive breeding connected with the attractiveness of the animals that determines
program of animals while avoiding an inbreeding depression. thecompositionofthecollectionofzooanimalsaroundtheworld?
However,thepresenceofjustafewunrelatedindividualsinzoos Balmfordetal.[45]hypothesizedthatitisthesizeoftheanimal
may occasionally save the species if the captive population is that determines its presence in a zoo and we confirmed this
immediately expanded when necessary, e.g., after an unexpected relationshipinalmostallexaminedtaxaofterrestrialvertebratesin
crisis of the wild populations (but see [19] for negative effects of our previous papers [17,43,44]. Additionally, we found that
bottlenecking).Thissuggeststhatcooperativeex-situconservation attractivenessoftheanimalstohumanrespondentsalsoaffectsthe
can help restore animal populations once the threat has world’s zoo population numbers in some clades, namely snakes
diminished. Although many authors have questioned this [44], parrots [43], terrestrial birds (grouping followed [46],
assumption ever since (i.e., [20–24]), many researchers find the excludingAccipitriformes,Strigiformes,TrogonidaeandColiidae;
theoreticalroleofzoosinreintroductionprogramsasfeasible(fora Psittaciformes, Opisthocomus and Cuculiformes were added),
review of the limitations and solutions of availability of captive basal mammals (Monotremata, Marsupialia, Xenarthra and
populations in reintroduction, see [25]; e.g., disease risk, behav- Afrotheria), and mammals of the carnivore-ungulate clade
ioral competence of captive-reared individuals such as reduced (Laurasiatheria, [17]).
abilitytoavoidpredatorsorfindfoodresourcesandattachmentto On principle, larger animals are more conspicuous and visible
humans; changes in genetic compositions, etc.), and a notable topotentialzoovisitors.Thisleadstotheassumptionthatsizecan
contribution of zoos to animals ex-situ breeding can be demon- bedifficulttoseparatefromattractiveness,yetstillthereismoreto
stratedbysuccessfulreintroductionswhichreducedthethreatlevel beautythansizeitself.Inthispaper,wemeasuredseparatedataof
of particular species. Species such as the Przewalski horse (Equus attractiveness perceived by human respondents for a nearly
ferus przewalskii; [26]), the American bison (Bison bison; [27]), the complete set of mammalian families. We hypothesized that both
European wisent (Bison bonasus; [28–30]), Pe´re David’s deer sizeandattractivenessofmammalsaregoodpredictorsofthesize
(Elaphurus davidianus; [31]), or Arabian oryx [32] may serve as of their captive zoo populations (World Zoo Collection; further
examples of successfully maintained zoo animal populations referred toas WZC).
releasedbackintothewild.Othernotablysuccessfulreintroduced Moreovertotheabove-mentionedphysicalproperties,thebrain
animalsweretheAsiaticwildass(Equushemionus;[33]),thegolden size may modulate the attractiveness of animals to zoo curators
liontamarin(Leontopithecusrosalia;[34]),andtheblack-footedferret andvisitors.AdolfPortmann,thewell-knownSwissbiologistofthe
(Mustelanigripes).Thelatterrecoveredfromaverysmallpopulation 20th century, hypothesized that humans categorize animals into
of onlyeighteen remaining individuals([35]). the‘‘higher’’and‘‘lower’’rankedanimalgroups[47],andthatthis
Moreover to the ex-situ breeding role of captive zoo popula- categorization, reflecting the brain size of the animal, affects the
tions, these groups might contribute to conservation purposes in perceived attractiveness. Accordingly, we hypothesized that the
otherwaysthatdonotnecessarilydemandhighcaptivepopulation brain size is a good predictor of behavioral attractiveness of
densities. A very important role of today’s zoological gardens mammalian species.
presents education, especially promotion of increased public and Inthispaper,weaimedtoanalyzetheeffectofbodysize,brain
political awareness oftheneed forin-situconservation [36]. size, and attractiveness of mammalian species from almost all
Asinglepopularanimal(orasmallgroupofthese)mightserve recent families to several variables explaining the WZC. We
asaflagshipspeciesandhelpitsendangeredrelativesinthewild, elaborate the previously-questioned number of individuals in the
or their natural habitat and its residents, to gain the necessary WZCinseparateanalysestoaskwhichfactorsdeterminewhether
financialsupportfromthepublic[37].Anothersignificantroleof theanimalispresentinanyzooornot,andtoaskhowmanyzoos
zoosresidesintrainingspecialistswiththerightknowledgeabout actually keep those selected ones, and in how large or small
thebreedingandcareoftheanimals[38].Internationalstudbooks numbers.Thereisapossibilitythatratherthanspeciesrecognized
running under the World Association of Zoos and Aquariums bycurrenttaxonomists,taxaclosertogeneraorfamiliesrepresent
(WAZA) and collaboration with the ISIS database include the primary units of human spontaneous categorization [48].
husbandryandveterinaryguidanceforasmanyspeciesaspossible Thus,thespecieswithinafamilymaycompetewitheachotherfor
(www.waza.org). However, keeping a few individuals of a rare the space available on the Ark (e.g., a zoo might select just one
species,ortheirrelatives,mayhelptoretaintherightspecialistsfor ‘‘mouse’’or‘‘rat’’tokeepinitscollectioninsteadofall715species
futureneeds.Theexperienceofstaffandresearchersworkingwith of the family Muridae). Because of that, we included the species
living animals is irreplaceable by studbook information and richness of the family as another factor to explain the analyzed
guidelines, and their presence may help to save the species. WZC variables.
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Materials and Methods choice process from the list of extant genera and species ([49];
domestic forms were excluded). Thus, duplicated presence of
The dataset used for statistical analyses (see Appendix S1) identical genera and species was avoided whenever possible. In
includes123rowsreferredtoasfamilies.Therewere119families monotypic families, the species was represented by different
recognized by [49] and four infraorders (i.e., Microchiroptera, pictures.SetscodedasA,BandCconsistedofillustrationswhile
Megachiroptera, Mysticeti, Odontoceti). Cetaceans and chirop- Dconsistedofphotographs.Themainsourcesofthepictureswere
teranswerepooledintoinfraordersbecausethesespecializedaerial [55–58]. In order to avoid possible effects of body size and
andmarinetaxadeviateconsiderablyfromthetypicalmammalian background on rating, we adjusted the pictures with a white
body plan and theirrepresentation in zoosisratherpoor. background and we resized them so that the pictured mammals
were of asimilar relative size (forillustration, see Figure 2).
Dependent variables The aesthetic attractiveness of the families was examined by
Information about the numbers of mammalian species and presenting pictures of mammalian species to human volunteers
individuals kept in zoos worldwide was obtained from the ISIS (following [44]). The respondents were Czech citizens, mostly
(International Species Information System) online database universitystudentswithintheagerangeof19–29years.Onecan
(http://www.isis.org)coveringmorethan800zoosandaquariums arguethatasfarasage,sex,andethniccompositionisconcerned,
from 76 countries. We excluded hybrids, ambiguous genera, and our respondents did not properly represent the full scope of zoo
domestic species/forms (see Appendix S2) from the dataset. We visitors. The Czech Republic belongs among the least socially
analyzed the following four variables derived from this dataset stratifiedcountriesintheworldasdemonstratedbytheGiniindex
(accessed on 12th January2011): (GI) measuring the extent to which the distribution of income
among individuals within an economy deviates from a perfectly
(1) Proportionofzoospecies.Thenumberofspecieskeptin
equal distribution (0 corresponds to perfect equality while 100 to
the WZC scaled to the total number of extant species of a
perfect inequality). The GI of the Czech Republic is 31 which
given family. This binomial variable reflects the mean
corresponds to the 110 rank of 137 countries included in a
probability that a speciesiskept at least inonezoo.
comparisonprovidedbytheWorldBank([59];compare,e.g.,with
(2) Mean population size. The world zoo population size GI=45fortheUSAwhichplacesthemtothe41stpositioninthe
(square-roottransformed)perspeciespresentintheWZC(the ranking;thehighertherank,thehigheristheequalityinsociety).
families not represented intheWZC were excluded). Thus, we expected the Czech students to possess aesthetic
(3) Number of zoos. The natural log-transformed mean preferences for animals comparable to the rest of the society,
number of zoos keeping the species (species and families not including zoo visitors (but see [60,61] who found socio-economic
represented intheWZC were excluded). and educational differences in preferences, but their method did
(4) Number of conspecifics per zoo. The mean number of notfocuspurelyonaesthetics).Sincewepreferredahomogenous
conspecifics per zoo keeping the species (the families not exampleofrespondentswellmotivatedtoperformingthetask,in
represented intheWZC were excluded). whichwecouldfocusonthevariablesrelatedtothetestedstimuli
rather than respondent characteristics, the students presented a
good testing sample for the experiments evaluating human-
Explanatory variables perceived animal attractiveness.
Species richness. The number of extant species of each Moreover, our previous studies revealed that the aesthetic
familywaslog-transformed.Inthecaseofinfraorders,thenumber ranking of animal species is highly stable with the factors of age,
ofextantspecieswasdividedbythenumberoffamiliesbelonging sex and ethnic composition having only a marginal effect ([43]).
totheinfraorder. This is especially surprising in the case of cross-cultural
Body size. We gathered body weight records (in grams) for comparisons,e.g.,insuchdifferentculturesasarethoseinEurope
representatives of most mammalian genera from literary sources and Papua New Guinea ([62,63] and new unpublished data; see
(mostly from [50]). These values were naturally log-transformed alsotheagreementinphysicalattractivenessratingsoffemalefaces
and usedforcomputation offamily means. across cultures [64], but see [65]). Note that the sample of
Brain size. The relative brain size was substituted by an respondents from non-European countries differed greatly in age
encephalization quotient. This variable, introduced by [51–53] and/orsocioeconomicrankbuttheirpreferencesfortheexamined
and then repeatedly used as a measure of relative brain size (e.g. animals still highly correspondedtothose of theCzechstudents.
[54]), is a natural log-transformed ratio between observed brain Duringtheexperiment,eachrespondentwasexposedtooneset
weight and theoretical brain weight predicted by an allometric of 123 pictures that were placed on a table in a random
equation for mammalian species of the given body size. We assemblage. Their objective was to ‘‘pack the photographs in an
performed an ordinary least square regression to calculate the ordercorrespondingtothebeautyofthedepictedspeciesfromthe
allometricrelationshipbetweenbrainandbodysize.Wegathered mostbeautifultotheleastbeautifulone’’,asweaskedthem.The
theprimarydataonbrainandbodyweightsfor1309mammalian orderofthepicturesinthepackwasthencodedbynumeralsfrom
species from various literary sources (see Appendix S3). Because 1 (the most beautiful one) to 123, further referred to as ranks.
the individual families were unequally represented in the dataset, Although no explicit time limit was given, all the respondents
weemployedaweightingbythevariableinverselyproportionalto performedthetaskinabout30minutes.Eachsetofpictures was
thenumberofincludedspeciesbelongingtotheparticularfamily evaluated by a comparable number of respondents: 77 (25 men),
(Figure 1). The resulting empirical allometric equation 85 (31), 77 (27) and 75 (25) for sets A, B, C and D, respectively.
(lnB=20.6601*lnM-2.4100; B=brain mass, M=body mass) Altogether,wegathereddatafrom314respondents;206ofwhich
was usedfora calculation of theencephalization quotients. were womenand108were men.
Attractiveness. For the purpose of data collection, we Allrespondentsagreedtoparticipateintheprojectvoluntarily.
defined four sets of 123 pictures depicting species from each Eachsubject provideda writteninformed consent andadditional
family. Speciesrepresenting individualfamiliesineachpartialset informationaboutgender,ageandtheiraffinitytomammals.The
were selected by a two-step (first genus then species) random age and gender had no effect on the preferences (MANOVA, all
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Figure 1. The allometric relationship between the brain and body sizes in 1309 mammalian species. Because the families were
represented by an unequal number of data points (species), each family was given an equal weight when calculating the ordinary least-square
regression.Thiscorrectionforbiasedrepresentationofthefamiliesresultedinalineseeminglyunfittingthedatapoints(representingspeciesand
notfamilies).ThisadjustedregressionlineisconsiderablymorereliableforfurtherGLManalysesperformedbetweenfamilylevel,though.Allometric
equation:ln(brainmass)=20.6601*ln(bodymass)22.4100.
doi:10.1371/journal.pone.0063110.g001
Ps.0.05), which allowed us to pool the data. The affinity to In order to quantify and test congruence in species ranking
mammals exhibited too low of a variance (91.85% respondents provided by different respondents and/or to compare sets
reported positive affinity to mammals, 8.15% neutral and 0 composed of different species, we adopted Kendall’s Coefficient
negative) to allow reliable testing. The experiments were of Concordance (W) as implemented in SPSS v.16.0 [66]. There
performed in accordance with the European law and were was considerable congruence among the respondents in all four
approved by The Institutional Review Board of Charles Univer- setsofpictures;Wcoefficientswere0.206,0.264,0.224and0.334
sity,Faculty of Science(No. 2009/2). forsets A,B, CandD, respectively (allp,0.001).
Prior to further analyses, the raw ranks were transformed as
follows: each value was divided by the number of evaluated
families (123) and square-root arcsine transformed to improve its
statistical distribution. Next, we computed the mean transformed
rank for each set and family. Mean transformed ranks computed
for individual sets were mutually significantly correlated
(r2=0.334, 0.450, 0.401, 0.324, 0.449 and 0.420 for A vs. B, A
vs. C, A vs. D, B vs. C, B vs. D and C vs. D, respectively; all
p,0.0001). This allowed us to compute family means from the
meanpreferenceranksobtainedforpartialsetsofpicturesandto
further use this variable as a simplified measure of aesthetic
attractivenessofthefamilyforhumans.Thenumericvaluesofthis
variable were positivized (multiplied by 21) to make the
explanation of theresultsmoreintuitive.
We included another explanatory variable in preliminary
analyses: whether the family is mainly diurnal or nocturnal/
fossorial. However, this variable correlates with the body size
(r=20.51), and when the influence of body size is removed, the
factor itself explains neither of the analyzed dependant variables.
Figure 2. The pictures of the representatives of the family
As such,weremoved itfromfurther analyses.
Felidae(thesecondmostpreferredfamilyoutof123examined
ones).Itillustratesthevariationofbodypositionsamongfourtested
setsofpictures(fordetailsseeunderMaterialsandMethods):clouded Statistical treatment
leopardNeofelisnebulosa(topleft),servalLeptailurusserval(topright), In order to examine the effects of species richness, body size,
jaguar Panthera onca (bottom left; pictures painted by Silvie Lisˇkova´)
attractiveness, and brain size on dependent variables, we
andcaracalCaracalcaracal(bottomright;photofromthearchiveofthe
generated General Linear Models (GLMs) in R 2.8.0 [67]. In
ZooPrague).
doi:10.1371/journal.pone.0063110.g002 thecaseoftheproportionofzoospecies,weadoptedthebinomial
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modelwithlogitlinkfunctionandChi–squaretests.Weusedthe (P=0.0045andP=0.0002,respectively)oftheanimal(Table1c,
Gaussiandistributionwithidentitylinkinremaininganalyses.AIC Figure 4c,d).
criterion was used to reduce the original full models. The
simplified model was also compared to the previous model by Number of conspecifics per zoo
theANOVAtesttoverifythatthechangeinresidualdeviancewas GLM revealed negative effect of body size (P=0.0016) on the
not significant (P.0.05). mean number of conspecifics kept in a zoo. This effect was
Because species data are not independent as a result of shared confirmed by multiple regression of independent contrasts
phylogeny among more closely related taxa [68], we also carried (P=0.0002). The latter analysis also revealed negative effect of
out a phylogenetically controlled analysis using the independent species richness (P=0.0318;Table 1d,Figure 4e,f).
contrast method[69].For thepurposeof thisanalysis, weuseda
phylogenetictreeoffamiliescompiledfromrecentstudiesdealing
Discussion
with molecular phylogenies. The main branching was adopted
from Bininda-Emonds [70] and Arnason et al. [71], while We analyzed the representation of mammalian species in the
specialized studies were used to improve the branching of partial WZC in the year 2011 and we found that it was very poor and
crown taxa: Marsupialia [72], Xenarthra [73], Cetartiodactyla highly selective, comparable to its state in 2009. [18] The list of
[74],Carnivora[75],Madagascarcarnivores[76],Rodentia[77], currently recognized mammalian species [49] contains 5334
Hystricognathi [78], Platacanthomyidae [79], Muridae [80], and extantspecies,butonly1048ofthem(16%)wereactuallypresent
Primates[81].Whenphylogeneticinformationwasequivocal,we intheWZC.Thereweretwentyfamiliesthatwereentirelyabsent
resolved the tree in accordance with the conventional taxonomy. in the WZC. Such selectivity may not only affect the putative
The independent contrasts of the arcsine-transformed mean conservation value of zoo populations, but it may also warn us
preference rank, log-transformed WZPS, species number and about the existence of a large bias in species selection for
body mass were computed using COMPARE, version 4.6b [82]. conservation in general.
All branch lengths were set to 1 because the corresponding The selection of species into the WZC is determined by
estimationswerenotavailable.Thus,forthecontrastsanalysis,we decisions made by humans, and although the selection criteria
assumedtheapplicabilityofthepunctuationalmodelofevolution. might be different, we may still assume that the psychological
Thediagnosticproposedby[83]revealedthatthecontrastswere drivesbehindsuchselectionarethesameorsimilartothoseforthe
appropriately standardized. The multiple regression analyses selection of species for conservation and reintroduction. Such
basedonindependentcontrastscoreswereperformedinStatistica conclusionissupportedbythefactthat,betweentheyears1992–
6.0.[84] andconstrained topassthrough theorigin [83]. 2009, out of the 12 evaluated reintroduced mammalian families,
11 of them are in the top-half when taking brain size (EQ) or
Results attractiveness into account (for the list of reintroduced families
with detailed published results, see Appendix S4). The ‘‘intelli-
The analyzed zoos kept 179868 mammals belonging to 1048
gent’’ and ‘‘beautiful’’ animals seem to be favored in human
species and103families.Themostrepresentedfamiliesbelonged
decision-makings.Moreover,manyconservationprogramsstrong-
predominantly to the carnivore-ungulates, primates and Xenar-
ly depend on financial support by the public, and it is most
thra-Afrotheria clades(Appendix S1).
appropriatetoassumethattheirdecisionswhichspeciestosupport
Thehighestaestheticattractivenesswasfoundinthelargesized
andwhichnottoisdrivenbysimilarfactors.Therefore,adeeper
mammals (families Ailuridae, Felidae, Phascolarctidae, Ursidae,
understandingofthefactorsthataffectvariousaspectsoftheWZC
Giraffidae, Elephantidae, Equidae, Macropodidae, Mephitidae,
isvery important.
and Cervidae). In contrast, the least preferred mammals (families
It was previously demonstrated that large species selectively
Notoryctidae,Bathyergidae,Chrysochloridae,Spalacidae,Caeno-
attract human attention and conservation efforts [85,86]. We
lestidae, Solenodontidae, Talpidae, Ctenomyidae, Geomyidae,
confirmedthatthebodysizeaffectsfundamentallyallcomponents
andDasypodidae) were predominantly smallsubterranean (fosso-
of mammalian representation in the WZC. Mammalian species
rial) creatures with reduced eyes.
characterizedbyalargebodysizehaveahigherprobabilitytobe
includedinWZC.Theytendtoberepresentedbymorenumerous
Proportion of zoo species
populations and they are also kept by more zoos. Because the
GLM revealed that the proportion of zoo species is associated materialcostofkeepinganimalsincreaseswiththebodysizeofthe
positively with body size, attractiveness, and brain size, and animal (Balmford 1996), the preferential representation of large
negatively with species richness (all Ps,0.0001). This result was mammals in the WZC is an interesting phenomenon. The
confirmed when the original variables were replaced by their
metabolism (and thus the amounts of food and feces) and the
independent contrasts and treated by a multiple regression
required area of enclosure exponentially increase with the body
through theorigin (Table1a, Figure 3). size to about L (0.72; [87,88]; for review see [89]) and 2/3 (i.e.,
thelengthofthesuggestedenclosureisroughlyproportionaltothe
Mean population size body length of the animal in breeder’s guidelines, e.g., [90]),
Mean population size of zoo species was associated positively respectively.Thefactthatkeepingalargespeciesisconstrainedby
with body size (P=0.0001) and attractiveness (P=0.0008). Only theavailablespaceandexpensesisfurtherillustratedbyourresults
the effect of attractiveness was confirmed by the independent suggesting that the number of conspecifics per zoo tends to be
contrast analysis (P,0.0001;Table 1b, Figure4a,b). smallerinspeciesofalargerbodysize.However,itseemsthatthe
zoos are able to overcome these constraints and selectively keep
Number of zoos large animals because these attract more visitors and thus secure
Both GLM of original data and multiple regression of countervailing income([91]).
independent contrasts agreed that the mean proportion of zoos In our previous study, we performed a separate analysis of the
keeping the species was significantly predicted by the body size WZC of selected mammalian clades and we demonstrated that
(P,0.0001 and P=0.0104, respectively) and attractiveness human preferences affect the WZC positively in basal mammals
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Figure 3. The proportion of zoo species as predicted by GLM. The effects of species richness (a), brain size (b), body size (c), and
attractiveness(d).ThedependentvariableisthenumberofspecieskeptinWZCscaledtothetotalnumberofextantspeciesofagivenfamily.This
binomialvariablereflectsthemeanprobabilitythataspeciesiskeptinatleastonezoo.Forthedefinitionandtransformationoftheexplanatory
variablesseeundertheMaterialandmethodssection.
doi:10.1371/journal.pone.0063110.g003
and Laurasiatheria [17]. The results of this study first show this ofaparticularspeciesE deviatesfromtheexpectedbrainsizeE,
a e
relationship across all mammalian families; the species belonging andare,tosomeextent,goodpredictorsofso-called‘‘intelligence’’
to aesthetically attractive families have a higher probability to be of a mammal(fora review,see [95]).
included in the WZC, and they tend to be represented by more However, the exact definition of the term ‘‘intelligence’’, or
numerous populations as well asbeing kept by morezoos. higher cognitive abilities, is ambiguous. There are two main
The positive effect of the encephalization index on the conflicting views: the adaptive specializations theory [96], saying
representation of mammalian species in the WZC predicted by that ‘‘intelligence’’ includes various learning and memory
[47] was only confirmed in the case of the proportion of zoo processes, which lead to adaptations for specific ecological task
species. Apparently species of small-brained clades have a higher resolutions; and the general process view of ‘‘intelligence’’,
probability to be entirely omitted by the world zoos and their describedbytheexistenceofgeneralassociative-learningabilities,
managers and curators. In agreement with Portman, the overall whichdifferquantitativelyamongspecies[97].Anew,consensual
brain size (non-human primates: [92]), relative brain size theory describes ‘‘intelligence’’ as a behavioral flexibility [95]
(executive brain size: [93]; residuals: [94]) or the encephalization manifestedinquickproblem-solvingtaskornumberofinnovations
quotient, EQ=E /E,indicate theextent towhichthebrainsize [94].Fagen[98]assumedthatthenumberofinnovationsandplay
a e
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FactorsDeterminingMammalianCollectioninZoos
g d
reflectin Materialan
s e
ariable p-level 0.0001 ,0.0000 0.0221 0.0020 p-level ,0.0000 p-level 0.0104 0.0002 p-level 0.0318 0.0002 underth
v e
nt se
depende B 20.063 0.059 0.165 0.582 B 16.375 B 0.145 3.416 B 20.152 20.193 hevariables
nesson ontrasts ontrasts ontrasts ontrasts mationoft
sizeandattractive Independentc Beta 20.309 0.363 0.176 0.242 Independentc Beta 0.389 Independentc Beta 0.237 0.350 Independentc Beta 20.209 20.370 definitionandtransfor
bodysize,brain Coefficients Estimate 20.447 20.199 0.257 0.861 3.178 Coefficients Estimate 11.152 0.468 12.499 Coefficients Estimate 2.336 0.188 2.366 Coefficients Estimate 3.663 20.129 20.001 alsoincluded.Forthe
s, e
es ar
n n)
h gi
ric ori
ofspecies P ,0.0000 ,0.0000 ,0.0000 ,0.0000 P 0.0001 0.0008 P ,0.0000 0.0045 P 0.0016 0.1525 throughthe
d
cts me
effe erfor
ningthe Resid.Dev 1522.18 751.42 669.69 598.36 Fvalue 16.9380 12.0210 Fvalue 38.2475 8.4308 Fvalue 10.5723 2.0789 contrastsp
mi nt
e
a d
ex pen
s e
del Df Sq Sq Sq ind
earmo Resid. 121 120 119 118 Mean 383.31 272.03 22.63 Mean 44.23 9.75 1.16 Mean 11.02 2.17 1.04 essionof
TheparametersofthereducedgenerallinTable1.therepresentationofmammalianspeciesinWZC. AnovaA. DfDeviance NULL1221855.22 (Intercept) Taxonomicuniqueness1333.04 Bodysize1770.76 Brainsize181.73 Attractiveness171.33 AnovaB. DfSumSq (Intercept) Bodysize1383.31 Attractiveness1272.03 Residuals1002263 AnovaC. DfSumSq (Intercept) Bodysize144.23 Attractiveness19.75 Residuals100115.65 AnovaD. DfSumSq (Intercept) Taxonomicuniqueness Bodysize111.02 Attractiveness12.17 Residuals100104.20 a)ProportionofextantspecieskeptinWZC.b)WorldzoopopulationsizeperspeciesinWZC.c)Proportionofzooskeepingthespecies.d)IndividualsperZooKeepingthespecies.Theresultsofthephylogeneticallyadjustedanalyses(multipleregrmethodssection.doi:10.1371/journal.pone.0063110.t001
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FactorsDeterminingMammalianCollectioninZoos
Figure4.Theeffectsofbodysizeandattractiveness.Theeffectsofbodysizeandattractivenessonthemeanpopulationsize(a,b),numberof
zoos(c,d)andnumberofconspecificsperzoo(e,f).Themeanpopulationsize:Theworldzoopopulationsize(square-roottransformed)perspecies
presentinWZC.Thenumberofzoos:Thenaturallog-transformedmeannumberofzooskeepingthespecies.Thenumberofconspecificsperzoo:
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FactorsDeterminingMammalianCollectioninZoos
The mean number of conspecifics per zoo keeping the species. The families not represented in WZC were excluded from the analyses. For the
definitionandtransformationoftheexplanatoryvariablesseeundertheMaterialandmethodssection.
doi:10.1371/journal.pone.0063110.g004
has close or causal relationship. In mammals, the large-brained zoo’s popularity among visitors, but also to use such species in
taxa aremorelikelytocontainspecies thatplaymoreoften[99], educational programs, or present them as flagship species for
and playful and active animals are more attractive tozoo visitors further in-situ protection of wildlife. A reasonable definition of
(e.g.,Felidae:[100]).Theattractivenessofanimalswithinteresting flagship species was proposed by Verissimo et al. [105] (page 2):
behavior was also confirmed in [60], which reported higher ‘‘Aspeciesusedasthefocusofabroaderconservationmarketing
willingnesstosupportbirdswithspecialbehavioralcharacteristics, campaignbasedonitspossessionofoneormoretraitsthatappeal
e.g., courtship rituals. tothetargetaudience’’.Smithetal.[106]foundthatlargebodied
Species richness of a family has a negative effect on the mammalian species with forward-facing eyes are most frequently
proportion of zoo species, the mean population size, and the usedasflagshipsbynon-governmentconservationalorganizations
number of conspecifics per zoo. Thus, the zoo curators tend to (NGO) and, based on these characteristics, they suggested five
avoid simultaneous keeping of species belonging to the same critically endangered species with a strong potential to serve as
family. This can be explained by human tendency to categorize good flagship species: the African wild ass, tamarau (dwarf
mammals into primary cognitive categories frequently joining buffalo), pygmy raccoon, Talaud bear cuscus and Pennant’s red
multiple scientific species into a single unit. Ethnobiologists colobus. When compared with our results, four of these animals
repeatedly demonstrated that the primary units of human belongtoattractivemammalianfamiliespositionedinthetop-half
categorizationofanimalscorrespondtoso-called‘‘genericnames’’ rank of the attractiveness (up to the fifth position; Equidae 7,
(for a review see [48]). These are one-word terms describing a Bovidae 20, Procyonidae 38 and Phalangeridae 50). The high
typicalspeciesofa‘‘genus’’;additionalspeciesnamesarederived attractivenessofthreatenedspeciespersemayfurtherincreasethe
by adding theadjectives. potentialoftheseorsimilarlyselectedspeciestoserveasflagships.
The knowledge of the factors affecting the selection of animals In contrast, the Pennant’s red colobus belongs to the family
in the WZC might be applicable to a broad array of efforts Cercopithecidaewhichappearedtoberatherunattractive(placing
influenced by human-induced selection of species. Once we the 94th rank position). However, this family contains a large
becomeawareofit,wemayadjustfutureplanningofconservation number of species the attractiveness of which may vary. A more
projects to lead them into a better success, saving both time and detailed analysis on a species level could help to determine the
financesalongtheway.Zoocuratorsmayintentionallytrytoselect actualattractivenessoftheredcolobus,orhelpfindaspecieswith
unattractive, but needful, endangered species along with the similarattributesbuthigherattractivenesstobeusedasaflagship
attractiveonestobeincludedintheircollectiontofulfillboththe instead.
advisable ex-situ conservation role and the expectation of zoo Aproperlyselectedflagshipspeciesmayconvincethepublicto
visitors.Forexample,theleastattractivemammalianfamilyofthe donate more money for conservation, just as demonstrated by
marsupial moles (Notoryctidae) includes only two species, both [107].Intheirstudy,therespondentswerewillingtopaymorefor
endangered according to the IUCN status. They are not kept in the conservation of an otter than that of a water vole. This is in
any zoo at present, and their future is very insecure unless accordwithourfindingthatottersfromthefamilyMustelidaeare
selectively focused on, going against the unwanted bias. Another moreattractivetohumans,placing34thinthepreferenceranking,
waytofulfillbothoftherolesistoselectthemostattractivespecies thanwatervolesfromthefamilyMuridae,whichplacedasfaras
out of a list of species with a similar threat status. For example, 73rd (See Appendix S1). Also, when lumped together into one
there are both attractive and unattractive species within some conservation program, these two animals received less support
animalfamilies,asshownbyFryntaetal.[43],onall367parrots thanottersalone[107].Thismaybeexplainedeitherbythesole
of the family Psittacidae. From within such families, endangered presenceoftheunattractiveanimalintheprogram,whichpushes
yet attractiveanimals could be includedin theWZC. the respondents back, or by the rising complexity of the message
Whatever the conservation priorities are ([101]), if there is an that was presented to the respondents. Either way, if conserva-
existing tendency to prefer the conservation of some species over tionists select a single highly attractive animal to be presented to
the others, the factors affecting this tendency should be known. the public as a messengerfor conservation planning, it mayraise
Nowadays, the preservation of biodiversity is a widely accepted thesuccessoftheproject.Thismaybecausedbothbyraisingthe
priorityforspeciesconservation(e.g.,[102,103]).Thispriorityisin financialsupportoftheprojectbypeoplelivingfarawayfromthe
conflict with human tendency to pay the proper attention placeofquestion,orbylocalpeoplewhomayre-thinktheirview
selectivelytolargeandattractiveanimals.However,theawareness of the natural riches surrounding them [37]. Furthermore, we
of this selectivity may help the conservationists to improve their found that the attractiveness of snakes as perceived by humans is
strategies.There aremanysmalland/orunattractivespeciesthat shared among such different cultures as Europeans and villagers
are phylogenetically significant and thus key for biodiversity from Papua New Guinea [62]. Another study confirmed these
preservation.Withonlylittleornosupportreceived,thesespecies resultsonpeople fromthefivemaininhabited continents[63].If
could be lost forever. A good example of possible application of applicabletootheranimaltaxa,themessagefromasingleflagship
speciesattractivenessassessmentisinthecaseoftheEDGEspecies speciescouldtouchpeopleworldwideaswellaspeoplelocaltothe
(Evolutionarily Distinct and Globally Endangered [104]) – a conservation project. Although local communities face various
selection ofthreatenedspecieswithhighbiodiversityvalue.Once problemswithpotentialflagshipsthattriggerconflictsaspredatory
known, the unattractive species putatively lacking public aware- animals, competitors or pests ([108,109]), the attractiveness may
ness and support could receive special attention by conservation play its role when the flagship is selected from harmless, non-
specialists. conflicting species. In case of highly attractive animals, the
Moreover, knowing that the attractiveness of an animal itself attractivenessmayevenoutweighthepossibleconflict.Thefamily
playsamajorroleinahuman’sdecision-making,theymaybeable Equidae placed 7th rank of attractiveness in our study and the
tointentionallyselectthe‘‘beautiful‘‘speciesnotonlytoraisethe reintroduction of the Przewalski horse was well-accepted by local
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FactorsDeterminingMammalianCollectioninZoos
peopleinMongolia(HustainNuru;Ku˚sE.,ZooPrague,personal AppendixS2 TheformsandspecieslistedintheISISdatabase
communication)despiteitbeingacompetitorfordomestichorses that were excluded from(or added to) theanalysis.
([26]). (PDF)
In conclusion, this study shows that the predictors associated
AppendixS3 Theliterary sources of brainsize data.
with human attention, especially body size and aesthetic attrac-
(PDF)
tiveness,haveasubstantialeffectonthecompositionoftheWZC.
Inthe21stcentury,itisofanutmostimportancetopayattention AppendixS4 Reviewofmammalsreintroducedduringtheyears
to the biodiversity preservation, and it might be up to the 1992–2009. We collected journals and book sources of mamma-
worldwidezoologicalgardenstoplayasignificantroleinthistask. lian reintroductions within the years 1992–2009 with detailed
Thisisespeciallybecausezooshavethecapacitytoholdnumerous information aboutthereintroduction events.
species,acapacitylargerthananyotherinstitution,togetherwith (PDF)
theknowledgeaboutthebreedingofvariousspeciesandproperly
managedstudbooks.Whethertheyutilizethispotentialisavision Acknowledgments
of the future. However, for the zoos and conservationists whose
We thank Michaela Zelenkova´ for help with the data collection, Pavel
intentions are to conserve biodiversity, our study reveals one of
NeˇmecandZuzanaKra´lova´ forprovidingalargeportionofmammalian
manyfactors–thehumanfactor–thatmayfundamentallyaffect brain size data, Ludmila Konecˇna´ and Marke´ta Janovcova´ for the
the conservation efforts. Thus, conservation biologists should collectionofpapersdealingwithreintroducedspecies,JanaMareˇsova´and
considerthesepsychologicalfactorsforpropermanagementofthe Barbora Elia´sˇova´ for critical reading of the manuscript, Emily from
‘‘Ark’’. AustraliaandCoreyStringerfromNorthCarolina,USA,foralinguistic
revisionandDr.FranciscoCeaceroHerradorforarevisionofthescientific
styling of the manuscript, and all of the respondents for their kind
Supporting Information
participationinthisproject.
AppendixS1 Thedatasetusedforstatisticalanalyses,sortedby
attractivenessfromthemostattractivefamilytotheleastattractive Author Contributions
one. (See under the Materials and methods section for the
Conceived and designed the experiments: DF EL. Performed the
definition of thevariables.) experiments: DF OS SL EL. Analyzed the data: DF OS SL EL. Wrote
(XLS) thepaper:DFOSSLEL.
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