Differential utilization of surface and arboreal water bodies by birds and mammals in a seasonally dry Neotropical forest in southern Mexico

Abstract

Water availability significantly influences bird and mammal ecology in terrestrial ecosystems. However, our understanding of the role of water as a limiting resource for birds and mammals remains partial because most of the studies have focused on surface water bodies in desert and semi-desert ecosystems. This study assessed the use of two types of surface water bodies (waterholes and epikarst rock pools) and one arboreal (water-filled tree holes) by birds and mammals in the seasonally dry tropical forests of the Calakmul Biosphere Reserve in southern Mexico. We deployed camera traps in 23 waterholes, 22 rock pools, and 19 water-filled tree holes in this karstic region to record visits by small, medium, and large-bodied birds and mammals during the dry and rainy seasons. These cameras were set up for recording videos documenting when animals were making use of water for drinking, bathing, or both. We compared the species diversity and composition of bird and mammal assemblages using the different types of water bodies by calculating Hill numbers and conducting nonmetric multidimensional scaling (NMDS), indicator species, and contingency table analyses. There was a greater species richness of birds and mammals using surface water bodies than tree holes during both seasons. There were significant differences in species composition among bird assemblages using the different water bodies, but dominant species and diversity remained the same. Terrestrial and larger mammalian species preferentially used surface water bodies, whereas arboreal and scansorial small and medium mammals were more common in arboreal water bodies. These findings suggest that differences in water body characteristics might favor segregation in mammal activity. The different water bodies may act as alternative water sources for birds and complementary sources for mammals, potentially favoring species coexistence and increasing community resilience to environmental variation (e.g., fluctuations in water availability). Understanding how differences in water bodies favor species coexistence and community resilience is of great relevance from a basic ecological perspective but is also crucial for anticipating the effects that the increased demand for water by humans and climate change can have on wildlife viability.

Full text

Ecology and Evolution. 2023;13:e10781.  
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https://doi.org/10.1002/ece3.10781
www.ecolevol.org
Received:26August2023
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Revised:26October2023
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Accepted:15November2023
DOI:10.1002/ece3.10781
RESEARCH ARTICLE
Differential utilization of surface and arboreal water bodies by
birds and mammals in a seasonally dry Neotropical forest in
southern Mexico
Carlos M. Delgado-Martínez1,2,3 | Melanie Kolb2 | Fermín Pascual-Ramírez4 |
Eduardo Mendoza3
ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicense,whichpermitsuse,distributionandreproductioninanymedium,
providedtheoriginalworkisproperlycited.
© 2023 The Au thors . Ecology and EvolutionpublishedbyJohnWiley&SonsLtd.
1Posgrad o en Cien cias Biológica s,
UniversidadNacionalAutónomade
México,UnidaddePosgrado,EdificioD,
1erPiso,CiudaddeMéxico,Coyoacán,
Mexico
2InstitutodeGeografía,Universidad
NacionalAutónomadeMéxico,Circuito
exterior s/n, Ciud ad Unive rsita ria, Ciudad
deMéxico,Coyoacán,Mexico
3InstitutodeInvestigacionessobre
losRecursosNaturales,Universidad
MichoacanadeSanNicolásdeHidalgo,
Morelia,Michoacán,Mexico
4InstitutodeInvestigacionesen
EcosistemasySustentabilidad,
UniversidadNacionalAutónomade
México,Morelia,Michoacán,Mexico
Correspondence
CarlosM.Delgado-Martínez,Posgrado
en Ciencias Biológicas , Univer sidad
NacionalAutónomadeMéxico,Unidadde
Posgrado,EdificioD,1erPiso,Circuitode
Posgrados, Ciu dad Universit aria, Ciudad
deMéxico,Coyoacán,04510,Mexico.
Email:pistache06@ciencias.unam.mx
EduardoMendoza,Institutode
InvestigacionessobrelosRecursos
Naturales,UniversidadMichoacanade
SanNicolásdeHidalgo,Av.SanJuanito
Itzícuaros/n,Col.NuevaEsperanza,
Morelia,Michoacán,58337,Mexico.
Email:eduardo.mendoza@umich.mx
Funding information
AmericanSocietyofMammalogists,
Grant/AwardNumber:LatinAmerican
StudentFieldResearchAward2022;
AssociationforTropicalBiologyand
Conservation,Grant/AwardNumber:Seed
ResearchGrant2022;RuffordFoundation,
Grant/AwardNumber:34365-2
Abstract
Water availabilit y significantly influ ences bird and mammal ecol ogy in terrestria l
ecosystems.However,ourunderstandingoftheroleofwaterasalimitingresource
forbirds andmammalsremains partialbecause mostofthe studies havefocused
onsurfacewaterbodiesindesertandsemi-desertecosystems.Thisstudyassessed
theuseoftwotypesofsurfacewaterbodies(waterholesandepikarstrockpools)
andone arboreal (water-filledtree holes)by birdsand mammalsin theseasonally
drytropicalforestsoftheCalakmulBiosphereReserveinsouthernMexico.Wede-
ployedcameratrapsin23waterholes,22rockpools,and19water-filledtreeholes
inthiskarstic regiontorecordvisitsbysmall,medium,andlarge-bodiedbirdsand
mammalsduringthedryandrainyseasons.Thesecamerasweresetupforrecording
videosdocumentingwhenanimalsweremakinguseofwaterfordrinking,bathing,
orboth.Wecomparedthespeciesdiversityandcompositionofbirdandmammalas-
semblagesusingthedifferenttypesofwaterbodiesbycalculatingHillnumbersand
conductingnonmetricmultidimensionalscaling(NMDS),indicatorspecies,andcon-
tingencytableanalyses.Therewasagreaterspeciesrichnessofbirdsandmammals
usingsurfacewaterbodiesthantreeholesduringbothseasons.Thereweresignifi-
cantdifferencesinspeciescompositionamongbirdassemblagesusingthedifferent
water bodies , but dominant specie s and diversity rem ained the same. Terrestr ial
and larger ma mmalian species prefe rentially used sur face water bodies, w hereas
arborealandscansorialsmallandmediummammalsweremorecommoninarboreal
waterbodies.Thesefindingssuggestthatdifferencesinwaterbodycharacteristics
mightfavorsegregationinmammalactivity.Thedifferentwaterbodiesmayactas
alternative watersourcesforbirds andcomplementary sourcesfor mammals, po-
tentially favoring species coexistence and increasingcommunity resilienceto en-
vironmentalvariation(e.g.,fluctuations in wateravailability).Understanding how
differencesinwaterbodiesfavorspeciescoexistenceandcommunityresilienceisof
greatrelevancefromabasicecologicalperspectivebutisalsocrucialforanticipating

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1 | INTRODUC TION
The supply of essential resources strongly affects the distribu-
tion and abundance of animal species (Hamilton & Murphy,2018;
Messier, 1991). These effects can escalate to affect the structure
anddynamicsofanimalcommunities.Examplesoflimitingresources
affecting bird and mammal communities include shared prey (Gilg
et al., 2003), nect ar-producing flower s (Guevara et a l., 2023), and
cavitiesfornestingbirds(Jiménez-Francoetal.,2018).
Wateravailability isa clearexample of a limiting factor having
asignificant impact onthe ecology ofbirds and mammals in most
terrestrialecosystems.Animalsdependonwatersourcesfordrink-
ing, bathing, cooling, and preying, among other things (Clayton
et al., 2010; Go ssner et al., 2020; Hafe z, 1964; Lee et al., 2017).
Variation in w ater availabilit y is linked to fluctu ations in mammal
populations(Gandiwaetal.,2016),movementpatterns(Chamaillé-
Jammesetal.,2016),andhabitatconnectivity(O'Farrilletal.,20 14).
Severalstudieshaveincorporatedwaterbodyfeaturesascovariates
toanalyzeecologicalparameterssuchasmammaloccupancy (e.g.,
Di Bitetti et al., 2020),butlessresearchhasfocuseddirectlyonana-
lyzingthecharacteristicsoftheuseofwaterbodiesbyvertebrates.
Furthermore,mostofthesestudiesareconcentratedinaridregions
(e.g.,Amorosoetal.,2020; Edwards et al., 2016;Harrisetal.,2015),
limitingourunderstandingoftheroleofwaterasalimitingfactorfor
vertebratesinotherecosystems.
Resource partitioning has been proposed as a mechanism for
animal species to reduce antagonistic interactions (e.g., competi-
tion and predation) occurring when exploiting limited resources
(Schoener,1974;Walter,1991).Thi sada ptiveme chan ism allowsi nte r-
actingspeciestocoexistbyspecializingindifferentresourcesources
orbyutilizingthematdifferenttimesorplaces(Learetal.,2021).
Tropicalbirdsandmammalshaveevolveddifferentstrategiesto
exploit watersources. Theycanusewaterinriversandpools(e.g.,
Stommel et al.,2 016)or tankepiphytesandwater-filled treeholes
inthecanopy(e.g.,Sharmaetal.,2016).Somespecies,suchasscan-
sorialmammalsandbirds,likelyhavemoreflexibilitytousesurface
and canopy water sources, but for other animals, access might be
more limited. Theinterplaybetween thevariation in water source
characteristics and typesofanimal locomotionopens thepossibil-
ityforresourcepartitioningtooccur.Previousstudieshavefocused
on analy zing the tempora l partitionin g of water use by mammals
(Adams&Thibault,2006; Edwards et al., 2017; Valeix et al., 2007),
butuntilnow,thedynamicsoftheuseofsurfaceandarborealwater
bodies at t he community l evel are unknown . A better know ledge
ofthestrategiesinvolvedintheuseofwater sourcesbybirds and
mammals isessential to improve our understandingof species co-
existencemechanismsandtopredicttheimpactsofanthropogenic
disturbances such as thoseassociatedwith climatechange (Galetti
et al., 2016; Votto et al., 2020).
Seasona lly dry tropic al forests are w ater-stress ed ecosystems
richinvertebratespecies,offeringanidealopportunitytostudyre-
source par titionin g (Allen et al. , 2017; Mooney e t al., 1995; O cón
et al., 2021).Seasonalforestsgrowingonkarsticsoils,suchasthose
occurringintheCalakmulregioninsouthernMexico,undergoapar-
ticularlymarkedlimitation in wateravailability due to theabsence
ofpermanent,extensivesurfacewaterbodiescausedbyfastwater
infiltration(García-Giletal.,2002).Thereissomeevidenceshowing
thesignificant impact variationinwater availabilityhas on wildlife
distributionandsurvivalintheCalakmulregion.Forinstance,white-
lippedpeccariesconcentratetheiractivityaroundwaterholesduring
the dry season, and adocumented peak in tapir deaths coincided
withamarkeddroughtintheyear2019(Reyna-Hurtadoetal.,2012,
2019).The congregationofspeciesinwaterholes mightresult ina
greaterriskofattacks,suchassuggestedbythedocumentedkillof
anocelotbyajaguarinthenearbyGuatemalaMayaforest(Perera-
Romeroetal.,2021).InCalakmul,wildlifecanobtainwaternotonly
fromwaterholes but alsofromepikarst rockpoolsand water-filled
treeholes.Eachofthesewaterbodieshasfeaturesthatcanattract
differ ent species (see f ull description i n Section 2). Som e studies
have individually documented the extensive use of these water
sourcesbybirdsandmammals,butacomparativeapproachismiss-
ing (Delgado-Mar tínez, Alvarado, et al., 2022; Delgado-Martínez,
Cudney-Valenzuela,&Mendoza,2022;Reyna-Hurtadoetal.,2012).
TheCalakmulregionstandsoutgloballyduetoitshighbiodiver-
sity (Myers et al., 2000).However, it iscurrently facing escalating
pressureduetoanthropogenically-drivenfactorssuchasdeforesta-
tion and climate change (Mardero et al., 2020; Ramírez-Delgado
et al., 2014). Thissituationposes a significantrisktowater quality
andavailability,whichcanhavefar-reaching consequencesforver-
tebrate populations.Thisresearchevaluatesifthere exists a parti-
tioningintheuseofwaterbodiesbysmall,medium,andlarge-bodied
birdsandmammalsintheseasonallydrytropicalforestoccurringin
theCalakmulregion.Specifically,weassessedthespeciesdiversity
andcompositionofbirdandmammalassemblagesusingtwo types
ofsurfacewaterbodies(waterholesandepikarstrockpools)andone
typeofarborealwaterbody(water-filledtreeholes). Moreover,we
theeffectsthattheincreaseddemandforwaterbyhumansandclimatechangecan
haveonwildlifeviability.
KEY WORDS
Calakmul,dendrotelmata,resourcepartitioning,SelvaMaya
TAXONOMY CLASSIFICATION
Communityecology
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DELGADO-MARTÍNEZ et al.
analyze d how differen ces in water sourc e use between b irds and
mammals arerelated to contrastsinfunctional traitssuchas loco-
motion an d body size. We hypothe size that there will b e distinct
patternsofwatersource usebetweenbirdsandmammalsandthat
differ ences among sp ecies within th ese groups will b e associated
with variation in their functional traits. We expect to find more
pronounced differencesinwater useamongspecieswithin animal
groupsduringtherainyseason,whenwaterismorewidelyavailable
and,therefore,animalshaveagreateropportunitytoselect.
2 | METHODS
2.1 | Study area
Fieldworkwascarriedoutinthesouthernportionofthebufferzone
oftheCalakmul Biosphere Reserve (CBR, 89°43′26″–89°49′23″ W,
18°16′01″–18°8′49″ N),inthestateofCampeche,southernMexico
(Figure 1). The CBR was created in 1989 and has an extent of
723,185 ha,constitutingthelargesttropicalprotectedareainMexico
(Galindo-Leal,1999;Gómez-Pompa& Dirzo,1995).Thestudy area
has an appr oximate extent of 6 3,000 h a and suppor ts continuou s
vegetation, except for anarrowroad (ca. 4 m wide) leading to the
CalakmulArcheologicalsite.Duringthisstudy,onlyecotourismand
researchwereallowedinthe studyarea,andno primary activities
haveoccurredtheresincetheestablishmentoftheCBR(INE,1999).
TheCBRiscriticallyimportantfortheconservationof biodiversity
inLatinAmericaduetothefactthatitsupportssomeofthelargest
populationsoficonicspeciesofMesoamerica,suchasTapirus bairdii
and Panthera onca(Ceballos et al., 2021;Naranjo, 2018). Together
with the M aya Biosphere Rese rve in Guatemal a, the CBR consti-
tutes the largest tract of tropical forest in Mesoamerica (Potapov
et al., 20 17). However,likemostofthetropics,thisregionisunder
increasing human pressure du e to activities such as illegal selec-
tivelogging,hunting,deforestationforfarmingandcattleranching,
and more recently, infrastructure development (Ramírez-Delgado
et al., 2014;Špirićetal.,2022).
The CBR has a tropical wet and dry climate with a dry winter
(Köppen-Geigerclassification:Aw;Becketal.,2018).Theregionhas
amarkedprecipitationseasonalitywitharainyseasonoccurringfrom
MaytoOctoberandadryseasonfromNovembertoApril(monthly
precipitation is <60 mm)(Marderoetal.,2020; Vidal-Zepeda, 2005)
with a mea n annual precipit ation of 1076 mm (CONAGUA , 2023;
Martínez & Galindo-Leal, 2002). The aver age annual temp erature
is 25.7°C, whereas the average annual minimum and maximum
temperature are18.7and 32.8°C, respectively (CONAGUA, 2023;
Figure S1).Accordingtothestandardizedprecipitationindexcalcu-
lated forthe region, the amount ofprecipitation during ourstudy
periodwaswithintherangeofnormalvariation(CONAGUA,2023).
2.1.1 | GeologyandhydrologyintheCBR
The CBRis located on thekarstic landscape of the Petén Plateau
which is primarily composed of limestone, shaped by chemical
weathering and erosion (Ensley et al., 2021; Torrescano-Valle &
Folan,2015).Waterbodieswithinthestudysitedependonprecipi-
tation astheir main sourceofwater due to theabsenceofperen-
nial streams. The following are themost common water bodies in
the stud y site and are the fo cus of this study. Waterholes. Thes e
FIGURE 1 Studyareaanddistribution
ofsampledwaterbodiesintheCalakmul
BiosphereReserve,Campeche,Mexico.
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DELGADO-MARTÍNEZ et al.
water bodi es, locally k nown as aguadas, are dolines resulting from
the disso lution of limesto ne that, togethe r with clay accumul ation,
reduceswaterpercolationandpromotestheaccumulationofrainfall
(Figure 2a;Back&Lesser,1981;García-Giletal.,2002;Kranjc,2013).
Waterholeshaveanapproximatedensityof oneper10.5 km2 in the
CBRandvaryinsizefrom10to40,000 m2buttypicallytheydonot
exceed 50 00 m2 (Reyna-Hur tado et al., 2012). Usu ally, a high pro-
portionofthewaterholesdries upduringthedry season,remaining
onlythelargest.Duringextremedroughtevents,eventhelargestwa-
terholescanbegone(O’Farrilletal.,2014).
Epikarstrock pools.Thesewater bodies, locally knownassart-
enejas,areclassifiedaskamenitzasinge olo gic a ltermsan dar enatur al
depressions in landformedbythe dissolutionof exposed bedrock
(Lundberg,2013). Rockpools usuallyoccur on elevated ground or
hilltopsinthestudyarea(Figure 2b;Flores,1983).Thereisapproxi-
matelyonerockpoolper0.1 km2,usuallycoveringlessthanasquare
meter(C.M.Delgado-Martínez,unpublisheddata).Rockpools col-
lectwaterevenduringmoderateprecipitationeventsandcanstore
itforseveralweeks(C.M.Delgado-Martínez,personalobservation;
Reyna-Hurtadoetal.,2012).
Water-filledtree holes.These waterbodiesareformed in cavi-
tiesordepressionsintrees,whererainwateraccumulates(Figure 2c;
Kitching,2000).Thedensityandaveragevolumeofwater-filledtree
holesintheCalakmulregionareunknown.Asrockpools,mosttree
holes have e phemeral hydr operiods, b ut some of them c an retain
water during the whole year (C. M. Delgado-Martínez, personal
observation).
2.2 | Searching and sampling of water bodies
Wecompiledinformationonthelocationof24waterholes,37rock
pools, a nd 73 tree holes b ased on exist ing informatio n for water-
holes (García-Gil et al.,2002),previousstudies(Delgado-Martínez,
Alvarado, et al., 2022; Delgado-Martínez, Cudney-Valenzuela, &
Mendoza,2022),andfieldworkconductedforthisstudy(ca.150 km
ofsearchbyfoot).Fromthesewaterbodies,weselected23water-
holes,22rockpools,and19treeholes.Theselectionofwaterholes
wasbasedonwhethertheyhadwaterduringourinitialvisit,which
occurredin July–August 2021 (these months corresponded to the
FIGURE 2 TargetwaterbodiesintheCalakmulBiosphereReserve,Campeche,Mexico:(a)waterhole,(b)rockpool,and(c)water-filled
tree hole.
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DELGADO-MARTÍNEZ et al.
startoftherainyseason).Ontheotherhand,weonlyselectedrock
pools with an estimated volume >10 L. For the selection of tree
holes,weappliedthefollowingcriteria:(1)tohavetheirentranceat
least1 mabovetheground;(2)tohaveaminoraxisoftheentrance
>10 cm;and(3)tohaveadepth>20 cm.Thesecriteriawereaimedat
increasingtheprobabilityofthedifferentwaterbodiesmaintaining
waterthroughoutthestudyperiod.Topreventspatialautocorrela-
tion,weavoidedmonitoringwaterbodiesofthesametype,<500 m
apart,atthesametime.
Duetologisticlimitations,wewerenotabletosampleall the
water bodies simultaneously. Therefore, we divided them into
three groups, including 7–8 water bodies of each type. These
groupsweremonitoredsequentially,withonecameratrapaimed
ateach waterbody forat least45 days. After thecompletion of
thisperiod,cameratrapsweremovedtothenextgroupofwater
bodies . Were peated this pr ocedure to comp lete one rainy se a-
sonandonedryseasonforeachgroupofwaterbodies(fromJuly
2021 to Septem ber 2022). Came ra traps in the w aterholes and
rockpoolswereinstalledatheightsrangingfrom40to70 cmand
atdistances of 2–4 mfrom the water edges. We usedtrailcam-
era hold ers (HME-TCH-SO) to set the camer a traps focused o n
thetreeholes.Inmostcases,theseholderswerefastenedtothe
same tre e where the tree hol e was located, app roximately 2 m
fromtheentrancetothetreehole,to secureadirect view of its
entrance.When itwas not possible to fasten thecamera holder
tothesametreewherethetreeholewaslocated,wefastenedit
toanearbytree.Asinglecamerawasenoughtofullymonitorthe
entirerockp oolsa ndtre ehole s,b utnotth ewaterhole s.Toreduce
theprob abilit yofmissings omeanimalspeciesvisitingwaterhole s,
wefollowedtwo strategies: (a) we aimed the cameras preferen-
tiallyatareaswithevidence ofanimalactivity,suchasfootprints
orpeccarywallows,and(b)wemadesuretohaveaclearviewof
the areaswithin thewaterholes thatmaintain waterevenin the
dryseason.WeusedcameratrapmodelsBrowningSpecOpsElite
HP4,BrowningStrikeForceEliteBTC5HDE,andBushnellTrophy
CamHDAggressor119876Cprogrammedtotake20-s longvid-
eoseachtimetheywereactivatedandtohavea5-sdelaybefore
reactivation.
2.3 | Data processing
Wetagged videos withthe identityofthe species recorded and
madeadatabaseaddinginformationabouttheirlocomotion(i.e.,
arboreal, scansorial, and terrestrial) and body mass (González-
Salazar, 2013). We classified the species into three categories
basedontheir bodymass:small,medium,andlarge. Birdswitha
body mass lowerthan 0.5 kg were classifiedassmall, thosewith
a body mas s higher than 0. 5 kg but lower th an 2 kg as mediu m,
and birds with a body mass higher than 2 kg as large. Mammals
withabodymasslower than4 kg were classifiedassmall, those
withabodymasshigherthan4 kgbutlowerthan13 kgasmedium,
and mamma ls with a body ma ss higher than 13 k g as large. The
categoriesweredefinedtohavean approximatelyequal number
ofspeciesineachgroup.
To reduce sources of bias during the statistical analysis, we
discard ed records of aquati c birds and specie s with a body mass
<220 g(which can be missed bycameratrapsmore frequently) or
foundinlessthanfoursites.Wegroupedvideosofthesamespecies
recorde d consecutively an d with the same cam era, following th e
methodologydescribed inCamargo-SanabriaandMendoza(2016).
These grouped videoswere classified as visitations.Wecalculated
thefrequencyofvisitationforeachanimalspeciesusingthefollow-
ing equat ion: (number of visi ts/sampling ef fort) × 100 c amera tra p
days (O'Br ien et al., 2003). Th e sampling effo rt was equal to t he
totalnumber ofdaysacameratrapwasactive. Toensurerecorded
visitsusedforanalyseswereprimarilydrivenbyanimals'attraction
towater,weonlyconsideredthoseinwhichitwas cleartheywere
drinking,bathing,orboth.Duringthereviewofvideos,weidentified
somecommonbehaviors,suchasscent-markinginthecaseofcarni-
vores,diggingintotheorganicmaterialfoundinrockpoolsandtree
holes,groomingamongpeccaries,andevenfrogandturtlehunting
byocelots.
2.4 | Data analysis
2.4.1 | Comparisonofbirdandmammalspecies
richnessanddiversityamongwaterbodies
Weuseda samplecoverage analysis(Chao &Jost,2012)to esti-
matethecompletenessofbirdandmammal surveysineachtype
of water bod y (i.e., waterho les, rock pool s, and tree hole s). For
eachtypeofwaterbody,wegeneratedsample-basedrarefaction
andext rapol at ioncurvesofHillnu mbers(q = 0,1,and2)withtheir
corresponding 95%confidence intervals (Chao et al., 2014). We
comparedthecurvesofthedifferenttypesofwatersourcesand
their corresponding 95% confidence intervals within the same
season.TheseanalyseswereperformedusingtheiNEXT R pack-
age(Hsiehetal.,2022).
2.4.2 | Comparisonofbirdandmammalspecies
compositionamongwaterbodies
Weconductedanon-metricmultidimensionalscaling(NMDS)analy-
sis to test for differences in thespecies compositionof groups of
birdsandmammalsvisitingeachtypeofwaterbody.Wecalculated
the Bray-Curtisindex, basedon thespecies'frequenciesofvisita-
tion,touseitasameasureofdistanceintheNMDS.Totestforthe
statistical significance of species clusters indicated by the NMDS,
we analyzed similarities (ANOSIM) using 10,000 permutations.
Weusedthevegan Rpackageto conduct theseanalyses(Oksanen
et al., 2022).
Toassessif therewere animal species associated with specific
water bodies, we conducted an indicator species analysis using
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10,000permutations withthe R package indicspecies (De Caceres
& Legendre, 2009). By comparing observed data to randomized
permut ations, this a nalysis deter mines which spe cies have a non-
random a ssociation with a pa rticular type of water bo dy. Finally,
toassessif capture frequencies of the different locomotion types
and body mass categories differed among the species visiting the
three water bodies, weaggregated the frequenciesandconducted
acontingencytableanalysis(Frankeetal.,2012).Incaseswherethe
resulting p-valuewasbelow.05,wecalculatedtheadjustedresiduals
tomeasurethestandardizeddifferencesbetweentheobservedand
expectedfrequencies.
3 | RESULTS
We totalized a sampling effort of 6713 camera trap days, with
2203 days in the waterholes, 2828 days in the rock pools, and
1682 days in the tree holes (Table S1).We recorded 43 species in
total(18birdsand25 mammals;Figure 3 and Table S2)visitingthe
three water sources: 15bird and20mammalspeciesinthewater-
holes, 8bird and 11mammalspeciesinthetreeholes,and13bird
and19mammalspecies in the rockpools.Crax rubrawasthemost
observedbirdspeciesthroughoutboththedryandrainyseasonsin
the three types ofwater bodies. During thedryseason, Philander
opossumwasthemostcommonmammalspeciesinthewaterholes,
while Sciurus deppeiwa s the most commo n in the tree hole s and
Pecari tajacuintherockpools.Incontrast,duringtherainyseason,
Odocoileus virginianuswasthemostcommonmammalspeciesinthe
waterholes,followedbyUrocyon cinereoargenteus in the tree holes,
and Cuniculus pacaintherockpools(Figure S2).
3.1 | Differences in animal species richness and
diversity among water bodies
The sample coverageof bird speciesin the different water bodies
was very high (above 99%)duringboth the dry andrainy seasons
(Table S3);onlythe treeholes hadaslightlylowercoverageinthe
rainy season (95.2%).Duringthe dry season, birdspecies richness
(q0) was highest in the waterholes and lowest in the tree holes
(Figure 4).Likewise,Shannondiversity (q1) was highest inthe wa-
terholes, while the tree holes androck pools had similar levels of
diversity(Figure S3).Finally,Simpsondiversity(q2)washigherinthe
waterho les than in the ro ck pools but ind istinguisha ble from tree
holes(Figure S4). In compari son, in the rai ny season, bird spe cies
richness(q0) was higher in the rockpoolsthan in the waterholes,
whereas tree holes were indistinguishable from the other water
bodies (i.e., their 95% confidence intervals overlapped). Similarly,
theconfidenceintervalsofthetreeholecurveoverlappedwiththe
curvesofotherwaterbodieswhenexaminingShannonandSimpson
diversity.
Sample coverageofmammal species was alsovery high (above
99%) durin g both seasons (Table S4). In the dry se ason, mammal
species richness(q0)andShannondiversity(q1)weresimilarinthe
waterho les and rock pools b ut lower in the tree ho les (Figure 4;
Figure S3).Simpsondiversity (q2)washigher in the rockpoolsand
lower in thewaterholes; diversityin thesetwo water sourceswas
indisti nguishable fr om that found in tr ee holes (Figure S4). In the
rainyseason,speciesrichness(q0)andShannon(q1)diversityhada
similarpattern,withwaterholesandrockpoolshavinggreaterdiver-
sityandtreeholeslower.Simpsondiversitywaslowestintreeholes
and highest in the rock pools.
3.2 | Differences in bird and mammal species
composition
During boththe dry (ANOSIM; R = .22, p < .001)and rainyseasons
(R = .28, p < .001),the birdassemblages visitingthe differentwater
sources displayed a moderate yet statistically significant dissimi-
larit y. In the dr y season, C. rubra, Coragyps atratus, and Meleagris
ocellata were associated with waterholes, while Crypturellus cin-
namomeuswasassociatedwithrockpools(Figure 5). I n the rainy
season, C. rubra and M. ocellata were associated with waterholes,
whereas Pteroglossus torquatus was associated with tree holes, and
bothC. cinnamomeus and Rupornis magnirostris were associated with
rock pools.
Weidentified asignificant association between the locomotion
categoriesofbirdsandtheiroccurrenceinthedifferentwaterbody
types (Figure S5). In the dr y season (χ2 = 1113.2, d f = 4, p < .001),
terrestrial birds exhibited a higher frequency in waterholes,while
scansorial species visited them less frequently. Moreover, arbo-
real and sc ansorial birds sh owed a greater freque ncy in the tree
holes, whereas terrestrial species displayeda lower visitationrate.
Interes tingly, rock pools rece ived fewer visits f rom both arborea l
andt err estrialbi rds .Inco ntr ast ,du rin gth era inyse aso n(χ2 = 2514.4,
df = 4,p < .001), scansorialbirdshadahigher frequencyof visitsto
waterholes, while arboreal species visited them less frequently.
Additionally, arboreal birds exhibited ahigher preference for tree
holes, while scansorial and terrestrial species showed lower visita-
tionrates.Therewasnotabirdgroupshowingaspecificassociation
with rock pools.
Wealsoobservedarelationshipbetweenthebodymasscatego-
riesofbirdsandtheiroccurrenceinthedifferentwaterbodytypes
(Figure S6). In the dr y season (χ2 = 83 6.96, df = 4, p < .001), medi-
um-sized birdsweremore frequentlyrecordedin treeholes, while
small and large species showed lower frequencies. Rock pools re-
ceivedmorevisitsfromsmallbirdsandfewerfrommediumspecies.
Onlywaterholeswerenotvisited byanybirdgroup atafrequency
greater than expected bychance.In the rainy season (χ2 = 1310.5,
df = 4,p < .001),waterholeswerefrequentedmorebylargebirdsand
lessbysmallandmedium-sizedbirds.Bothtreeholesandrockpools
werevisitedmorebysmallandmedium-sizedbirdsandlessbylarge
species.
Differences in mammal composition among the water bod-
ies were more pronounced than those observed among bird
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assemblages,bothduringthedryseason(ANOSIM;R = .43,p < .001)
and the rainy season (R = .50, p < .001). During the dry season,
Dasyprocta punctata, Puma concolor, and T. bairdii were associated
with waterholes, while Sciurus spp. and Eira barbara were associated
with tree holes, and P. taja cu and U. cinereoargenteus with rock pools
(Figure 5).Intherainyseason,O. virginianus, P. opossum, and T. bair-
dii were associated with waterholes; Didelphis virginiana and Sciurus
spp. with tree holes and C. paca; E. barbara, and P. tajacu with rock
pools.
Wef oun dasig nif ican tassoc iationbet weenthelo com oti onc ate -
goriesofmammalsandtheiroccurrenceinthedifferentwaterbody
types(Figure S5).Inthedryseason( χ2 = 10,378,df = 4,p < .001),wa-
terholeswere more frequented byscansorial and terrestrialmam-
mals, whi le arboreal m ammals visited t hem less freq uently. In the
rainy season(χ2 = 5901.7,df = 4, p < .001),waterholes wereprimar-
ily visitedby terrestrial mammals. Across bothseasons, treeholes
werepreferredbyarborealandscansorialmammals,whileterrestrial
speciesshowedlowervisitationrates.Similarly,rockpoolsattracted
moreterrestrialmammalsandwerelessfrequentlyvisitedbyarbo-
realandscansorialspecies,regardlessoftheseason.
Likewise, we f ound signific ant associations b etween the bo dy
massofmammalsandwaterbodytypes(Figure S6).Duringthedry
season (χ2 = 5373.7, df = 4, p < .001), water holes had a higher f re-
quencyof visits by largemammals andalowerfrequency by small
and mediu m species. Tree holes we re more frequent ly visited by
smallandmediummammals,whilelargemammalsshowedareduced
tendencytovisitthem.Rockpoolshadhighervisitationbymedium
mammals andlowervisitationbysmallspecies.Intherainy season
(χ2 = 4296.3, df = 4, p < .001), waterholes werefrequented moreby
small and l arge mammals, w hile medium sp ecies had a lower visi-
tation r ate. Tree holes were more f requently vi sited by small and
mediummammalsandlessfrequentlybylargemammals.Rockpools
FIGURE 3 AsampleofthebirdsandmammalsusingdifferentwaterbodiesintheCalakmulBiosphereReserve.(a)Crax rubraand(b)
Tapirus bairdiirecordedatwaterholes;(c)Penelope purpurascensand(d)Panthera oncarecordedatarockpool;(e)Ramphastos sulfuratusand(f)
Urocyon cinereoargenteusobservedinwater-filledtreeholes.
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were more frequently visited by medium mammals and less fre-
quentlybysmallandlargemammals.
4 | DISCUSSION
Thisstudyshowsnovelinformationabouttheutilizationofsurface
andar bor ealwat erb odi esbyadiv erseco mmunityofbirdsa ndm am-
malsinaseasonallydrytropicalforest.Oursamplingeffortmadeit
possibletorecordadiversecommunityofbirdsandmammalsinboth
seasons,showingthatthethreetypesofwaterbodiesarecentersof
highwildlifeactivity.Notably,ourrecordsdocumentedthepresence
of elusive sp ecies of signif icant conser vation inte rest, incl uding T.
pecari and Mazama pandorainbothwaterholesandrockpools.
Ourfindings providedsupport for ourinitial hypothesis,show-
ingcontrasting responsesbetweenbirds andmammals,with more
pronounceddifferences inwater partitioningamong speciesinthe
lattergroup.Weconsistentlyobservedhigherspeciesrichnessand
diversit y of mammals in s urface wate r bodies, wit h larger speci es
con ce nt ratingtheiracti vityinthewaterholesandarb oreala ndscan-
sorialspeciesinthetreeholes;albeitinfrequently,werecordedlarge
species, such as P. onca, Leopardus pardalis, and U. cinereoargenteus,
climbing to u se tree holes. Th ese differenc es were more marked
duringtherainyseason,aswepredicted.
Inecosystemswithlimitedwater sources,speciesoftencongre-
gatearoundthefewavailablewaterbodies,particularlyduringthedry
season,leadingtopotentialnegativeinteractionswithdominantspe-
cies(Ferryetal., 2016).Nevertheless,whenmultiplewatersources
areavailableindifferentlocations withvaryingaccessibility,suchas
groundversuscanopy,resourcepartitioningcanoccur,enablingdif-
ferentialresourceuse.Resourcepartitioningiswidelyrecognizedas
akeymechanismforpromotingspeciescoexistenceandmaintaining
biodiversity by reducing interspecific competition (Chesson, 2000;
Schoener,1974 ). This mechanism has been documented in tropical
FIGURE 4 Speciesrichnessofbirdsandmammalsvisitingthewaterholes,treeholes,androckpoolsduringthe(a)dryand(b)rainy
seasonsintheCalakmulBiosphereReserve,Campeche,Mexico.
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bi rdan dmam m alsp e cies ,incl udingver ti c alstr a tific ation (e. g .,A k k awi
et al., 2020;Ferreguettietal.,2018;Mohd-Azlanetal.,2014;Sushma
& Singh, 2006). Both water holes and rock pools exhibited similar
mammalspeciesrichnessanddiversityinboththedryandrainysea-
sons, which were greater than for the tree holes. The presence of
comparablediversityinthesesurfacewatersourceshighlightstheir
importanceinsupportingadiversemammalcommunitythroughout
the year (Delgado-Martínez,Alvarado, etal., 2022; Reyna-Hurtado
et al., 2010). Yet, ouranalyses also showed theexistence of differ-
encesinspeciescompositionoftheanimalassemblages visitingthe
three waterbody types. These findings suggest thatthe analyzed
waterbodieshaveecologicalfeaturesthatincreasetheirprobability
ofbeing visitedbyspecific mammalian species. Thus, for themam-
malcommunity,the waterbodiesmaybe acting as complementary
sources (Mallingeretal., 2016; Maurer et al., 2022).This couldpo-
tentially enable a greater number of mammal species to coexist
withinthiswater-stressedecosystem(Martinsetal.,2018;Thomsen
et al., 2022),asresourcesinacommunityareconsideredco mplemen-
tarywhendifferentspeciesusetheminawaythatavoidsdirectcom-
petition(Cleland,2011;Tilman,1982).
FIGURE 5 Speciescompositionofbirdsandmammalsthatvisitedthetargetwaterbodiesduringthe(a)dryand(b)rainyseasons.Bird
species codes: Coat, Coragyps atratus; Crru, Crax rubra; Crci, Crypturellus cinnamomeus; Meoc, Meleagris ocellata; Ptto, Pteroglossus torquatus;
and Ruma, Rupornis magnirostris.Mammalspeciescodes:Cupa, Cuniculus paca; Dapu, Dasyprocta punctata; Divi, Didelphis virginiana; Eiba,
Eira barbara; Odvi, Odocoileus virginianus; Peta, Pecari tajacu; Phop, Philander opossum; Puco, Puma concolor; Scde, Sciurus deppei; Scyu, Sciurus
yucatanensis; Taba, Tapirus bairdii; Urci, Urocyon cinereoargenteus.
20457758, 2023, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ece3.10781 by Cochrane Mexico, Wiley Online Library on [28/11/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License

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Incontrast, inthe case of bird assemblages,we foundthat a
substantialproportion ofspeciesweresharedandtheidentityof
thedominantspecieswasmaintained,despitetherebeingsignifi-
cantdifferencesinspeciescomposition.Althoughwefoundanas-
sociationbetweenpredominantly terrestrialbird species(e.g., M.
ocellata)andsurfacewaterbodies,noneoftherecordedbirdspe-
ciesiscompletelyflightless(Greenwood,2001).The irabili tyt ou ti-
lizethecanopyprovidesthemwithgreatermobilityandpotential
accesstoalternativeresources(Partasasmitaetal.,2017;Winkler
&Preleuthner,2001).Therefore,therelativelylessmarkeddiffer-
entialwaterusebybirdscanbeattributedtotheircapacitytoex-
ploitverticalspace,reducingtheirdependenceonspecificwater
sources. Consequently, these results suggest that the different
waterbodiesmaybeacting,tosome degree,asalternativewater
sourcesforbirds(Tilman,1982),leadingtosimilaritiesinthe spe-
ciescompositionoftheassemblagesrecordedineachofthem.
Alternatively,themoderate dissimilarities inbird species com-
positionobser vedacrossdifferentwaterbodiescouldbeexplained
bythe fact thatspeciesin thisgroup mayadopt distinct temporal
pat ternsofuseofthisresourceasastr ategytominimizedirectcom-
petitionandpredationrisk(Harmangeetal.,2021;Oleaetal.,2022).
However,nostudies have focused on thetemporal partitioning of
watersourcesbybirds.Suchtemporalsegregationcouldpotentially
allowbirdstoaccesswatersourceswithoutengaginginantagonistic
interactions,butthispossibilitywarrantsfurtherresearch.
An additional factor influencing the differential use of water
sources can be the perceived predation risk associated with the
visitationtoeach type of waterbody (Periquet et al.,2010 ; Valeix
et al., 2009).Largeterrestrialpredatorspecies,suchasP. onca and
P. concolor,wereassociatedwithwaterholesduring thedryseason
and with wa terholes and r ock pools duri ng the rainy seas on. The
presence of these predators can contribute to the creation of a
landsc ape of fear due to t he potential for l ethal intera ctions wit h
preyspecies(Bleicher,2017; Laundre et al., 2010 ; Perera-Romero
et al., 2021).Tomitigatethisrisk,preyspeciesmayactivelyseekout
alternativewatersources,suchastreeholes,wheretheprobabil-
ity of encounters withpredators is lower(Doody etal., 20 07;Hall
et al., 2013).ThiscouldbethecaseforP. ta jacu and N. narica,twoof
theirmainpreyspecies(Núñezetal.,2000),whichweremorecom-
monlyrecordedinrockpoolsandtreeholes,respectively,duringthe
dry season.Thus,predatoravoidance behaviormight interact with
resourcepartitioningtocontributetotheobserveddifferentialpat-
ternofuseofwatersources.
Theabsenceofdetailedinformation regarding thepresenceor
absenceofwaterinrockpoolsandtreeholescouldpotentiallylead
toan underestimationofvisitationfrequenciesforsomespeciesin
thesewaterbodies.Forexample,insomecases,wewereunableto
confirm whether ananimal hadindeeddrunkwater or hadmerely
inspectedthe site.Nevertheless,thesecases werenot included in
theanalyses,andwethink thatthisprobability ofunderestimation
wasconsistentacrossdifferentwaterbodies.
Althoughourstudyprimarilyfocusedonthetypeofwatersource
as the main explanato ry variable, it is impor tant to acknowledge
thatseveralotherfactorscaninfluencetheselectionandutilization
ofwater sources by birds and mammals.Some potential variables,
whichwerenotincludedinourstudybut are knownto impactthe
use of waterbodies, encompass thecharacteristics ofthe vegeta-
tiongrowingwithinwaterbodiesandtheirsurroundingareas(Eakin
et al., 2018; Votto et al., 2022),waterbodyand landscape features
suchaswaterdepth,terrainslope,distancetoroads,andproximity
tootherwatersources(Najafietal.,2019; Pin et al., 2018),andfood
availabilitywithinandaroundthewaterbodies(Chavesetal.,2021;
Eakin et al., 2018). Fur thermore, in t he case of tree hol es, varia-
tions in hei ght and connec tivity of t ree holes (e.g. , through liana s
andneighboringtrees)may influencethe utilization of thesewater
sources(Cudney-Valenzuelaetal.,2021).Exploringtheroleofthese
factorswouldlikelyhelptogainamorecomprehensiveunderstand-
ingofwatersourceselectionbywildlife.
4.1 | Implications for conservation
TheCalakmul region,like otherpartsofthe world,isexperiencing
anincreaseindroughtfrequencyanddisruptionsinrainfallpatterns
due to global climate change, resulting in more uneven distribu-
tionofrainfallthroughouttheyearandmoreintenserainfallevents
(Mardero etal., 2020).These changes havethe potential to affect
water availability for wildlife byaltering the hydrological cycles of
waterbodies.Waterholesseemtobe experiencinglongerperiods
ofdrying, whichcan makethemless available aswater sources in
thefuture (Reyna-Hurtadoetal.,2019).Incontrast,treeholesand
rockpoolsseemtobeabletofillevenwithmoderaterainfalls(C.M.
Delgad o-Martínez, unpublished data). T herefore, specie s strongly
associated with waterholes, such as T. bairdii,seemtobemoreprone
tobeaffectedbychangesinrainfallpatterns.Furthermore,arecent
studyintheregionhasdocumentedthatintimesofscarcity,wildlife
seekswaterinhuman-madeplaces,suchascattletroughsandapiar-
ies,whichsometimesleadstohuman-wildlifeconflicts(Pérez-Flores
et al., 2021).Thissituationmaybecomemorecommonsoondueto
changesinwateravailabilityintheregion.
Moreover,theCalakmulregionisfacinggreaterpressuredueto
increasinginfrastructuredevelopmentandhumanactivity.Inpartic-
ular,theconstructionoftheMayaTrain,oneofthemostimportant
infrastructureprojectsofthecurrentfederaladministration,hasthe
potential toimpactregional biodiversity.Theprojectaimstoboost
transportation and tourism, potentially benefiting local communi-
tiesbutincreasingresourcedemands,particularlywater(Camargo
&Vázquez-Maguirre,2021; García et al. , 2022). Some waterho les
areacommonattractioninthe reserve;thus, anuncontrolled rise
in tourist activity at waterholes has the potential to disrupt the
behavior of sensitive species, causing their displacement to low-
er-qualitysitesandpotentiallyintensifyinginterspecificcompetition
and predation risk (Crosmary et al., 2012; Zukerman et al., 2021).
Additionally,theselectiveloggingandclear-cuttingpracticesprev-
alentinthe regioncan further reducethe availabilityoftreeholes
(Armenta-Monteroetal.,2020;Blakely&Didham,20 08),whichare
20457758, 2023, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/ece3.10781 by Cochrane Mexico, Wiley Online Library on [28/11/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License

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essentialforarborealandscansorialspecies.Thescarcityofsuitable
treeholesmayforcethesespeciestorelyonsurfacewatersources,
consequentlyincreasingtheir vulnerabilitytoterrestrialpredators.
Therefore,ove rall,thecombinedimp act sofhumanac tivitiesandcli-
matechangeseemtohaveagreatpotentialtoaffectthespatio-tem-
poral water distribution patterns, altering the patterns of water
usebybirdsandmammals,whichinturnmightgenerateincreased
competition among species, greater predation risk, and potential
human–wildlifeconflicts.
Seasonally dry tropical forests are extensively distributed
through out the tropi cs and face sim ilar threat s to those affe cting
theCalakmulBiosphereReserve(Siyum,2020).However,significant
knowledgegapsstill existconcerningtheecologyoftheseecosys-
temsand theeffects of human activityon theirfunctioning (Allen
et al., 20 17). O ur findings help to increase o ur understanding of
the rolewater source characteristics have onwildlife ecology and
shedsomelightonthepotentialimpactsanthropogenicactivitycan
bringaboutonthefaunabythealterationsofthepatternsofwater
availability.
AUTHOR CONTRIBUTIONS
Carlos M. Delgado-Martínez: Conceptualization (lead);dat acur a-
tion (lead); formal analysis (lead); funding acquisition (lead);inves-
tigatio n( lead); methodo logy (lead); pro ject administ ration (equal);
soft ware (lead); visua lization (lead); w riting – original d raft (lead);
writing–reviewandediting(equal).Melanie Kolb:Conceptualization
(supporting); methodology (supporting); project administration
(equal);supervision(equal);validation(equal);writing–reviewand
editing (equal). Fermín Pascual-Ramírez: Conceptualization (sup-
porting); methodology(supporting); supervision (equal); validation
(equal); writing – review and editing (equal). Eduardo Mendoza:
Conceptualization (supporting); funding acquisition (supporting);
methodology(supporting);projectadministration(equal);supervi-
sion(equal);validation(equal);writing–reviewandediting(equal).
ACKNOWLEDGMENTS
This contribution constitutes a requirement for CMD-M to obtain
his Ph.D. de gree at the Posgrad o en Ciencias Biológ icas, UNAM.
ThisworkwassupportedbytheRuffordFoundation(grantnumber
34365-2); the Association for Tropical Biology and Conservation
(Seed Research Grant 2022); and the American Society of
Mammalogists(LatinAmericanStudentFieldResearchAward2022).
WearedeeplygratefultothepeopleofNuevoConhuas,especially
Andrés Barrientos' family,for theirhospitalityandinvaluableassis-
tanceduringourfieldwork.Wewouldalsoliketoextendourthanks
tothestaffoftheregionalofficeoftheCONANPfortheirsupport,
aswellastoV.Chanan dL .Carmo nafortheirassis tan ceduringf ield-
workanddataprocessing.CMD-Mwassupportedbyascholarship
fromtheConahcyt.
CONFLICT OF INTEREST STATEMENT
Theauthorsdeclarenoconflictofinterest.
DATA AVA ILAB ILITY STATE MEN T
Thedatasupportingthefindingsofthisstudy,alongwiththecode
toconduct the analyses, are openly availablein the Dryad Digital
Repository:h t t p s : / / d o i . o r g / 1 0 . 5 0 6 1 / d r y a d . 1 j w s t q k 2 2 .
ORCID
Carlos M. Delgado-Martínez https://orcid.
org/0000-0002-0913-932X
Melanie Kolb https://orcid.org/0000-0002-3329-3861
Fermín Pascual-Ramírez https://orcid.org/0000-0002-1005-9597
Eduardo Mendoza https://orcid.org/0000-0001-6292-0900
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SUPPORTING INFORMATION
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How to cite this article: Delgado-Martínez,C.M.,Kolb,M.,
Pascual-Ramírez,F.,&Mendoza,E.(2023).Differential
utilizationofsurfaceandarborealwaterbodiesbybirdsand
mammalsinaseasonallydryNeotropicalforestinsouthern
Mexico. Ecology and Evolution, 13, e10781. h t t p s :// do i .
org /10.10 02/ece3.10781
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