performed1100lu.com

AsianHerpetologicalResearch2020,11(2):155–160DOI:10.
16373/j.
cnki.
ahr.
190043ORIGINALARTICLE1.
IntroductionThedigestivetheorypredictsthatanimalsforaginghighcontentsofdigestiblematerialsleadtodecreasegutdimensions(PenryandJumars,1987).
Inparticular,animalschangetheirdigestivemorphologytraitstomeetfoodavailabilityvariationinordertomaximizeoverallenergyreturn(Sibly,1981).
Thereareevidencesthattheconsumptionofflavorousfoodcanpromotelargergutsthantheconsumptionofgranivorousfoodinrodents(Hansson,1985;HanssonandJaarola,1989).
Forspeciesoffrogs,individualsforagingindigestiblematerialspossesslongerdigestivetractsthanindividualspreyingondigestiblematerials(Nǔnezetal.
,1982;Nayaetal.
,2009;Louetal.
,2013;Maetal.
,2016).
Environmentaldifferencescanshapevariationinmorphology,physiologyandbehaviorinorganisms(Nǔnezetal.
,1982;Jinetal.
,2016;Lüpoldetal.
,2017;ShultzandBurns,2017;Altonetal.
,2017;Huangetal.
,2018;WangandLiao,2018;Rodriguesetal.
2018;Yuetal.
,2018;Samuketal.
,2018;Zhongetal.
,2018;Inostroza-Michaeletal.
,2018;McCulloughetal.
,2018;MaiandLiao,2019;Caietal.
,2019;Wangetal.
2019;Hussainetal.
2019).
Ithasbeenshownthatlengthofdigestivetractvarieswithaltitudeacrosspopulationsinanimals(Hammondetal.
,1999;Nayaetal.
,2009;Maetal.
,2016;Wangetal.
,2017).
Forinstance,lowabundanceofpreyitemsandhighindigestiblematerialsfromofstomachcontentsfromlowtemperatureandshortactiveperiodathighaltituderesultinproducinglongerdigestivetractinfrogs(Wangetal.
,2017).
Bycontrast,anincreaseingutlengthisaccompaniedbytheincreasedTheEffectsofPreyItemsDiversityandDigestibleMaterialsinStomachonDigestiveTractLengthinHylaranaguentheriLinCAI1,JianpingYU2,3,4,ChunlanMAI2,3,4andWenboLIAO2,3,4*Keywordsaltitude,digestivetract,digestiblematerials,diversityofpreyitems,Hylaranaguentheri1ClinicalMedicineDepartmentofTCMandWesternMedicine,NorthSichuanMedicalCollege,Nanchong637000,Sichuan,China2KeyLaboratoryofSouthwestChinaWildlifeResourcesConservation(MinistryofEducation),ChinaWestNormalUniversity,Nanchong637009,Sichuan,China3KeyLaboratoryofArtificialPropagationandUtilizationinAnuransofNanchongCity,ChinaWestNormalUniversity,Nanchong637009,Sichuan,China4InstituteofEco-adaptationinAmphibiansandReptiles,ChinaWestNormalUniversity,Nanchong637009,Sichuan,China*Correspondingauthor:Prof.
WenboLIAO,fromChinaWestNormalUniversity,Nanchong,Sichuan,China,withhisresearchfocusingonevolutionaryecologyinanurans.
E-mail:liaobo_0_0@126.
comReceived:21August2019Accepted:4December2019AbstractDifferenceinenvironmentalconditionshapesvariationindigestivetractlengthinevolutionaryprocess.
Inparticular,environmentaldifferenceresultsinvariationinfoodresourceamongdifferenthabitats,andtherebyaffectingenergyintakeandenergyallocation.
Thedigestivetheorypredictsthatanimalsforaginghighindigestiblematerialsofstomachcontentscanpromotetheincreasedgutdimensions.
Here,westudiedvariationindigestivetractandgutlengthacrosssixHylaranaguentheripopulationsatdifferentaltitudesandlatitudestotestthepredictionofthedigestivetheory.
Wefoundthataltitudeandlatitudedidnotaffectvariationinrelativesizeofdigestivetractandgutamongpopulations.
Wealsofoundthatrelativesizeofdigestivetractandgutdidnotbecorrelatedwithdiversityofpreyitems,butnegativelycorrelatedwithproportionofdigestiblematerials.
Ourfindingssuggestthatindividualsforaginglessdigestiblematerialsdisplayrelativelylongerdigestivetractthanindividualsforagingmoredigestiblematerials.
Vol.
11156temperatureamongBufoandrewsipopulations(Maetal.
,2016).
Hence,morestudiesevaluatingdigestivetractvariationassociatedwithdiversityofpreyitemsanddigestiblematerialsofstomachcontentsacrosspopulationsatdifferentaltitudesandlatitudesinfrogsareneeded.
TheGünther'sfrog,Hylaranaguentheri(Anuar:Ranidae)iswidelydistributedinChinaanditsdistributionrangesfrom0to1100ma.
s.
l.
Previousstudieshaveinvestigatedadvertisementcalls(Feietal.
,2010;Lietal.
,2010),testissizeasymmetry(Liuetal.
,2011)andbrainsizevariationamongpopulations(Guetal.
,2017).
Sofar,littleinformationonvariationindigestivetractlengthassociatedwithdiversityofpreydietsanddigestiblematerialsofstomachcontentsacrosspopulationsinH.
guentheriisavailable.
Here,weexploredvariationindigestivetractlengthamongsixpopulationsalongageographicalgradient.
Wealsotestedthepredictionofthedigestiontheorywhetherlengthofdigestivetractdisplaysanegativecorrelationwiththeproportionofdigestiblematerials,andapositivecorrelationwithdiversityofpreyitemsacrosspopulations.
2.
MaterialsandMethodsWecapturedatotalof68malesfromsixpopulationsinpaddyfields,poolsandneighboringgreenswardbyhandatnightduringthebreedingseasonatdifferentsitesacrossHunan,HubeiandSichuanprovincesinChinabetweenJuneandAugustin2016(Figure1).
Weconfirmedallindividualstobeadultsandthesexesweredeterminedbydirectobservationofsecondarysexualcharacteristics(theblackthroatthatispresentonlyinadultmalesandontheinflatedbody,whichischaracteristicofadultfemalescarryingtheeggs)(LiaoandLu,2010).
Eachindividualimmediatelywaskeptatarefrigeratorwithtemperatureof-20℃andtakentothelaboratory.
Subsequentlywesacrificedallindividualsusingsingle-pithingandpreservedthemin4%bufferedformalininaphosphatebuffer(Zhaoetal.
,2018).
Aftertwomonths,bodysize(snout-ventlength,SVL)ofeachindividualwasmeasuredtothenearest0.
01mmusingacalliperanddigestivetractwasremovedforfurthermeasurements.
Thelengthofdigestivetract(i.
e.
,thebeginningoftheesophagustoventlength)andgutofthespecimenwasmeasuredtothenearest0.
01mmusingaverniercalliperforthreetimes.
Wecalculatedthefinalvalueasmeanofthesemeasurementsintheanalyses.
Therewasahighcorrelationbetweenrepeatedmeasuresforlengthofdigestivetractsandguts(bothR>0.
94).
Thepreservationtimedonotaffectlengthofdigestivetracts(seedetailsinLouetal.
,2013).
Alldissectionsandmeasurementswereperformedbyoneperson(YuJP).
Figure1LocationsofsampledpopulationsofsixHylaranaguentheripopulationsinChina.
LinCAIetal.
DigestiveTractVariationinaFrogNo.
2157ThestomachcontentsofeachindividualwerecollectedinOctoberin2016.
PreyitemsweresubsequentlyplacedinaPetridishandidentifiedunderastereoscopicmicroscope,andreferenceslideswerefromwings,antennaandlegs(Khatiwadaetal.
,2016).
Allpreyitemswerethenidentifiedtothelowestpossibletaxonomiclevel.
Weconsideredallpreyitems(e.
g.
,riceplantweevil,rootweevil,riceborer,stemborer,grasshoppers,crickets,insectlarvae,leafhoppers,aphids,andmolecrickets,ricethrips,ants,ladybirdbeetles,anddragonflies)asOrdertocalculatediversityofpreyitemsandproportionofdigestiblematerials.
Wefirstdeterminednumberofpreyitemsandpresenceofparticularpreycategoriesinstomachcontentswithineachindividual.
Wethencalculatedpreycompositionforeachfrogindividual,expressedasrelativefrequency(%)(PRF=observedoccurrenceofitem/observedoccurrenceofallitems;Wangetal.
,2017).
Finally,wecalculatedaverageperpreycategorywithineachpopulationandusedtheShannon-Wiener'diversityindextoestimatethediversityofpreyitemsofstomachcontents.
Thediversityofpreyitems(H)wasobtainedusinganellipsoidmodel:H=[(PRF)*(㏑PRF)].
Speciesrichness(s)isbasedonthenumberofspeciespresentinthestomach(Magguran,2004).
Wedeterminedtheproportionofdigestiblematerialsbasedonoccurrenceofspiders,insectlarvaeandangleworminstomachcontents.
Theproportionofdigestiblematerialsindex(D)wasusedasfollows:D=occurrenceofspiders,insectlarvaeandangleworm/occurrenceofallpreyitems.
AllanalyseswereperformedusingSPSS22.
0(StatisticalProductandServiceSolutionsCompany,Chicago,USA).
Bodysize,digestivetractandgutlengthwerelog10-transformedtoimprovehomogeneityofvariances.
Relativedigestivetractandgutlengthwereestimatedfromdigestivetractandgutlengthdividedbybodysize.
Weusedone-wayANOVAtotestdifferencesinbodysize,digestivetractandgutlengthamongpopulations.
Totesttheeffectsoflatitudeandaltitudeonvariationinrelativesizeofdigestivetractandgutacrosspopulations,weperformedLinearMixedModels(LMMs)treatingdigestivetractorgutlengthasadependentvariable,populationasarandomfactor,latitudeandlatitudeasfixedfactors,andbodysizeasacovariate.
Wealsoanalyzedtherelationshipsbetweenrelativesizeofdigestivetractorgutandbothdiversityofpreyitemsandproportionofdigestiblematerialsamongpopulationsusingaregressionanalysis.
3.
ResultsBodysize,digestivetractandgutlengthsignificantlydifferedamongsixpopulations(Table1;bodysize:F5,62=10.
059,P<0.
001;digestivetract:F5,62=3.
870,P=0.
004;gut:F5,62=2.
258,P=0.
06).
TheLMMsrevealedthataltitudeandlatitudedidnotaffectvariationinrelativesizeofdigestivetract(altitude:F1,64=1.
862,P=0.
177;latitude:F1,64=0.
846,P=0.
361)andrelativesizeofgut(altitude:F1,64=0.
627,P=0.
432;latitude:F1,64=0.
980,P=0.
326).
Thelengthofdigestivetractandgutwaspositivelycorrelatedwithbodysize(Figure2;digestivetract,F1,64=17.
846,P<0.
001;gut:F1,64=13.
234,P=0.
001).
Theindicesofdiversityofpreyitemsandproportionofdigestiblematerialsacrosssixpopulationsrangedfrom1.
67to2.
15and11.
76%to55.
56%,respectively.
ThediversityofpreyitemsdidnotbecorrelatedwithrelativesizeofdigestivetractFigure2TherelationshipbetweenlengthofgutordigestivetractandbodysizeamongsixHylaranaguentheripopulationsinChina.
Vol.
11158(Figure3;relativesizeofdigestivetract=0.
295diversityofpreyitems+1.
023,t=1.
490,F=2.
219,P=0.
211)andrelativegutsize(relativegutsize=1.
130diversityofpreyitems+0.
620,t=0.
936,F=0.
876,P=0.
402).
Wealsofoundanegativecorrelationbetweenproportionofdigestiblematerialsandrelativesizeofdigestivetract(Figure4;relativedigestivetractsize=-0.
005proportionofdigestiblematerials+1.
739,t=-2.
898,F=8.
398,P=0.
044),buttendedtocorrelatenegativelywithrelativegutsize(relativegutsize=-0.
003proportionofdigestiblematerials+1.
247,t=-2.
374,F=5.
637,P=0.
076).
4.
DiscussionOurstudydemonstratesthataltitudeandlatitudedonotaffectvariationsinrelativesizeofdigestivetractandgutamongH.
guentheripopulations.
Consistentwiththepredictionofthedigestivetheory,therelativesizeofdigestivetractisnegativelywithproportionofdigestiblematerials,suggestingthatindigestiblefoodcanpromotelongdigestivetractforthisfrog.
Todealwithenvironmentalchanges,variationinorganmorphologyandsizeinanimalsarebasisoflocalfoodresourceavailabilityanddiversity(Hammondetal.
,1999;Liaoetal.
,2013;Liaoetal.
,2015;Jiangetal.
,2015;Maietal.
,2017;Liuetal.
,2018).
Inparticular,abioticenvironmentsassociatedwithaltitude(e.
g.
,temperature,wateravailability)canchangebioticconditions(e.
g.
,vegetationcover,preyavailability)andaffectforagingbehaviorofindividuals(e.
g.
,widthandcompositionoftrophicniche),andultimatelychangingindividuals'digestivefeatures(e.
g.
,gutmorphology)(Hammondetal.
,1999).
Forinstance,individualsfrompopulationsconsuminggreaterplantmaterials(e.
g.
,folivorousfood)exhibitlongergutsthanindividualsfrompopulationspredatingongranivorousfoodinthebankvoles(Clethrionomysglareolus)(Hansson,1985).
Forspeciesofanurans(Bufospinulosus,P.
pleuraden,F.
limnocharis),individualslivinginloweraltitudeswithhigherenvironmentaltemperatureandhigherpreyavailabilityhaveshortergutsthanthoselivinginhigheraltitudeswithlowerenvironmentaltemperatureandlowerpreyavailability(Nayaetal.
,2009;Louetal.
,2013;Wangetal.
,2017).
Inthisstudy,wedidnotfindthatrelativesizeofdigestivetractandgutwasaffectedbyaltitudeandlatitude.
Actually,allindividualswerecollectedfromsixpopulationsalonga420-kmlatitudinaland341-maltitudinaltransectwheresmallgeographicalrangesmadethemtoexperiencesimilarenvironmentaltemperature(rangingfrom16.
9to18.
0℃)andpreyavailability,andthusleadingtothenon-significanteffectsofaltitudeandlatitudeonlengthofdigestivetractandgut.
Infuture,weusedmoresamplingsandpopulationstostudydigestivetractvariationalonggeographicalrangesinthisspecies.
Thereareevidencesthatanincreaseinrelativesizeofdigestivetractincreaseswithbodysizeinmostspeciesofanuransduetogrowth(Nayaetal.
,2009;Louetal.
,2013;Wangetal.
,2017).
Meanwhile,energyrequirementsmayresultinvariationsindigestivetractperunitbodymassamongindividuals(Pulliainen,1976).
Largerindividualsneedmoreenergythansmallerindividuals,andrelativelylongerdigestivetractsinlargerfrogscanprobablybeexplainedbymoreenergyrequirements(Louetal.
,2013).
Inthisstudy,therewasapositivecorrelationbetweenbodysizeanddigestivetractlength,suggestingthatgrowth,ratherthanecologicalorevolutionaryselection,canexplaindifferenceinlengthofdigestivetract.
.
Previousstudieshavesuggestedthatlessdigestiblematerialsand/ordiversedietsleadtorelativelyshorterdigestivetractinanimals(Nǔnezetal.
,1982;Nayaetal.
,2009;Louetal.
,2013).
ForSitesAltitudeLatitudeTemperature(℃)Meanbodysize(mm)Gutlength(mm)Digestivetractlength(mm)Proportionofdigestiblematerials(%)DiversityindexofpreyitemsYidu8430.
391769.
47±5.
2489.
6±21.
39124.
13±24.
8211.
761.
83n=13n=13n=13Washi34829.
311865.
45±4.
1368.
75±10.
8196.
13±12.
8751.
281.
69n=8n=8n=8Liujia32929.
171865.
88±3.
6575.
6±26.
14102.
79±29.
8628.
571.
23n=12n=12n=12Xiyan37626.
6216.
668.
58±3.
6874.
79±8.
01103.
37±8.
8655.
561.
67n=11n=11n=11Yuanlin11328.
4416.
975.
99±3.
8784.
03±11.
28121.
21±14.
25182.
15n=14n=14n=14Taoyuan4028.
91767.
16±3.
678.
34±12.
34107.
98±13.
3617.
241.
68n=10n=10n=10Table1Altitude,latitude,temperature,meanbodysize,gut,digestivetractlength,proportionofdigestiblematerials,anddiversityofpreyitemsforsixHylaranaguentheripopulations.
LinCAIetal.
DigestiveTractVariationinaFrogNo.
2159instance,individualsincreaseareaandlengthofdigestivetracttodigestandabsorbmorenutrientsviaforgingmorediversedietsandindigestiblefood(PenryandJumars,1987).
ForF.
limnocharis,individualsforagingmorediversepreydietspossessrelativelylongerdigestivetractsthanindividualsforaginglessdiversepreydiets(Wangetal.
,2017).
Here,wedidnotfindapositivecorrelationbetweenrelativesizeofdigestivetractanddiversityofpreyitems,suggestingthatdiversepreydietscanexplainvariationinlengthofdigestivetract.
Consistentwiththepredictionofthedigestivetheory,wefoundthatproportionofdigestiblefoodwasnegativelycorrelatedwithdigestivetractlengthamongpopulations,whichsuggestedthatindividualsforgingmoredigestiblematerialspossessedrelativelyshorterdigestivetract.
Inconclusion,becauseoursamplingsarecollectedonthelowaltitudinalrange,andsmallsamplesizeineachpopulation,high-altitudeand/or-latitudeindividualsdonotdisplayrelativelylongerdigestivetractthanlow-altitudeand/or-latitudeindividuals.
Moreover,individualsforaginghigherproportionofdigestiblefooddisplayrelativelyshorterdigestivetracts,whichsupportthedigestivetheory.
AcknowledgmentsWethankMaojunZHONGandTaoTANGforassistancewithfiledwork.
FinancialsupportwasprovidedbytheNationalNaturalSciencesFoundationofChina(31772451;31970393),theScienceandTechnologyYouthInnovationTeamofSichuanProvince(19CXTD0022),theKeyCultivationFoundationofChinaWestNormalUniversity(17A006)andTalentProjectofChinaWestNormalUniversity(17YC335).
AllexperimentsinvolvingthesacrificeofliveanimalswereapprovedbytheAnimalEthicsCommitteeofChinaWestNormalUniversity(17003).
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