©EntomologicaFennica.11October2006 Effects of varying sampling effort on the observed diversity of carabid (Coleoptera: Carabidae) assemblages in the Danglobe Project, Denmark MariaSapia,GáborL.Lövei*&ZoltánElek Sapia,M.,Lövei,G.L.&Elek,Z.2006:Effectsofvaryingsamplingeffortonthe observeddiversityofcarabid(Coleoptera:Carabidae)assemblagesintheDan- globeProject,Denmark.—Entomol.Fennica17:345–350. Diversityrelationsamongthreestagesofanurbanisationgradientwerestudied, usingtheRényiscalablediversityindexfamilyandtheRightTailSum(RTS)di- versity.Theruralareaswerelessdiversethaneithertheurbanorthesuburban ones.Theurbanareasweremorediverseconsideringthedominantspecies,while thesuburbanareasweremorediverseconsideringtherarespecies.Next,weex- aminedtheimpactofdifferentsamplingregimesonthesediversityrelations.A pulsatingsamplingmethod(samplingfor2weekseverymonth)gavethesame diversityorderingascontinuoussampling.Furtherreductioninsamplingperiod alteredthediversityrelations. M.Sapia,DepartmentofIntegratedPestManagement,DanishInstituteofAgri- culturalSciences,FlakkebjergResearchCentre,DK-4200Slagelse,Denmark& DepartmentofEcology,UniversityofCalabria,87036Rende(CS),Italy G.L.Lövei,DepartmentofIntegratedPestManagement,DanishInstituteofAg- riculturalSciences,FlakkebjergResearchCentre,DK-4200Slagelse,Denmark; *correspondingauthor’se-mail:[email protected] Z.Elek,DepartmentofIntegratedPestManagement,DanishInstituteofAgricul- turalSciences,FlakkebjergResearchCentre,DK-4200Slagelse,Denmark.Per- manentaddress:DepartmentofEcology,Szt.IstvánUniversity,H-1400Buda- pest,P.O.Box4,Hungary Received31December2005,accepted25March2006 1.Introduction (Ishitanietal.2003),Belgium(Gaublommeetal. 2005),andHungary(Maguraetal.2004,2005) Globenet,aninternationalresearchproject,aims indicateaconsiderableeffectofurbanisationon at assessing changes in biodiversity caused by forest carabids, although this effect is not uni- anthropogenicmodificationoflandscapesindif- form.FirstresultsfromDenmark(Elek&Lövei ferent countries, using a common sampling 2005)indicatethattheeffectsinthiscountryare method(pitfalltrapping)andreferencegroup(ca- closertothoseinCentralthanNorthernEurope rabidbeetles,Coleoptera:Carabidae)(Niemeläet (Maguraetal.2004vs.Vennetal.2003). al.2000).ResultsfromFinland(Alaruikkaetal. OneoftheaimsoftheGlobenetProjectisto 2002;Vennetal.2003),Canada(Niemeläetal. monitor the effects of urbanisation on ground 2002), Bulgaria (Niemelä et al. 2002), Japan beetles.Theoriginalset-upcallsforseason-long, 346 Sapiaetal. (cid:127) ENTOMOL.FENNICAVol.17 continuoussampling(Niemelaetal.2000).How- ofAprilandmid-October,2004.Forfurtherde- ever,inanymonitoringscheme,thereisacontin- tails,seeElekandLövei(2005). uousdrive(oftenbytheendusers)tosimplifythe We compared the diversity extracted from methodsandevaluation. Thisisalegitimatere- continuous trapping material from 2004 with quirement, given the frequent lack of logistical threeother“imaginarysamplingregimes”asfol- supportandtrainedpersonnel. lows: (1) considering only every second fort- In this respect, the standard literature on nightly sample (= pulsating sampling), (2) con- groundbeetleshaslittletooffer.Publishedstud- sideringthecatchforthree,equallyspacedfort- ieshaveexaminedtheimpactofthetrapmaterial nightly intervals during the sampling period (at and size (Work et al. 2002), trap arrangement the beginning, middle and end of the growing (Wardetal.2001,Hansen&New2005)andpre- season),and(3)evaluatingonlymaterialtrapped servative(Thiele1977)onthecatch,butthestan- during two fortnights, during the peak of the dard recommendation is still the use of season- carabidactivityperiod.Thesedatawerethussub- longsampling(Woodcock2005).Acomparison setsofthedatafromcontinuoustrapping. between continuous pitfall trapping and combi- Weanalysedthediversityofthegroundbeetle nationsofearlyandlateseasonsamplingperiods assemblages using the Renyi diversity profiles. (Niemelä et al. 1990) established that the latter The Renyi diversity index provides a non-point canbeanadequatesamplingmethodtoaddress description of diversity, overcoming the prob- severaltypesofecologicalproblems, especially lems with single index descriptions (Magurran thosethatfocusonindividualspeciesorgroupsof 2003). The samples were analysed by using locallyabundantspecies. DivOrd 1.70, a computer program for diversity Tofulfilthisknowledgegap,wehaveexam- ordering (Tóthmérész 1993) which calculates inedtheeffectofreducedoralteredsamplingef- anddisplaystheRényidiversityprofilesofcom- fort on the diversity relationships among three munitiesandseveralotherdiversitymeasures. stages of the urbanisation process: rural, subur- DivOrdisbasedonparametricfamiliesofdi- ban,andurbanareas. versity indices, and this method involves more We found that the usual recommendation of calculationsthanasimplediversityindex[forde- continuous, season-long sampling (e.g., Wood- tails,seeTóthmérész&Magura(2005)].Fordata cock 2005) was not necessary to arrive at the analysistwoindexfamilieswereused,theRényi same conclusions as by continuous sampling diversityandtheRightTailSum(RST)diversity considering diversity relationships among these (Patil&Taillie1979). threehabitattypes. 3.Results 2.Materialandmethods 3.1.Thediversityrelations To assess the impact of different sampling ar- ofwhole-seasonsamples rangements on diversity, we used the material collectedintheDanglobeProject,inandaround The comparison of the Rényi diversity profiles the town of Sorø, Denmark, in 2004 (Elek & (Fig. 1) ofthethreecarabid assemblages (rural, Lövei2005).TheDanglobeProjectfollowedthe suburbanandurban)indicatedthattheruralareas Globenetprotocol(Niemeläetal.2000).Weused werelessdiversethaneithertheurbanorthesub- pitfalltraps(plasticcupsof10cmdiameter,with urban areas. The urban and suburban diversity 200ml70%ethyleneglycol+adropofdetergent, profilesintersected,whichmeansthatthediver- withagalvanisedironcover)ineachofthefour sityrelationshipbetweenthesuburbanandurban separate(distancebetweenadjacentpatcheswas area was not unequivocal. The urban area was aminimumof100m)forestedpatchesineachof more diverse considering the dominant species, thethree(rural,suburbanandurban)areas.The whilethesuburbanareawasmorediverseconsid- traps (distance between traps within each patch ering the rare species. Using the RTS-diversity 10m)werecheckedfortnightlybetweentheend profiles(Fig.2),thischangeinthediversityor- ENTOMOL.FENNICAVol.17 (cid:127) Samplingregimeeffectsonobservedcarabiddiversity 347 Fig.2.RightTailSum(RTS)diversityprofilesofthe Fig.1.Rényidiversityprofilesforcarabidassem- carabidassemblagesatthesuburbanandurbanar- blagesinrural,suburbanandurbanareasatSorø, easatSorø,Denmark,in2004. Denmark,in2004. samplingregimes(Fig.3a).Atthesuburbanar- deringbetweenurbanandsuburbanareascanbe eas,thedifferencewaslesspronounced,andthe located(Tóthmérész1995).Theurbanandsubur- profileranveryclosetothoseofthecontinuous banprofilescrossedeachother betweenthe4th samplingabove(cid:1)>1.3(Fig.3b).Asimilarcourse and5thmostfrequentspecies(Fig.2).TheRTS wasseenintheurbanarea(Fig.3c),butherethe diversitycurvesshowedthatthesuburbanareas couldbeconsideredmorediversethantheurban areasonlyifthefirstfourmostabundantspecies wereincludedintheevaluation. 3.2.Diversityrelations ofreducedsamplingmethods Thepulsatingsamplingmethod,i.e.samplingfor twoweekseverymonth,gavethesamediversity ordering results as continuous sampling. The Rényidiversityprofilesofrural,suburbanandur- banareas,whenapplyingthepulsatingsampling method (weeks 1, 3, 5, 7, 9 and 11), coincided withthediversityprofilesofthecontinuoussam- plingmethod(Fig.3).Therewereonlyminordif- ferencesbetweenthetwoprocedures,usuallyat thebeginningoftheprofile,indicatingthatsome rare species were present only in the data from continuoustrapping.Thisisadirectconsequence of reduced trapping effort, and does not greatly changethediversityoftheassemblage. Afurther reduction in the time of sampling, i.e. three 2-week periods over the growing sea- son,hadclearerimpactonthediversityprofilesin thethreehabitattypes,comparedtothetwometh- odsabove.Inallthreeurbanisationstages,itde- Fig.3.Rényidiversityprofilesofthecarabidassem- tectedfewerspecies(Fig.3a–c).Intheruralarea, blagessampledusingvarioussamplingregimesinru- theprofileindicated amorediverseassemblage ral(a),suburban(b)andurban(c)areasatSorø, overmostofthescaleparameterthanthefirsttwo Denmark,in2004. 348 Sapiaetal. (cid:127) ENTOMOL.FENNICAVol.17 Fig.4.Rényidiversityprofilesofcarabidassemblages Fig.5.Rényidiversityprofilesofcarabidassemblages ofrural,suburbanandurbanareas,sampledover ofrural,suburbanandurbanareas,sampledovertwo threefortnightlyintervalsatSorø,Denmark,duringthe fortnightlyintervalsatpeakcarabidactivityatSorø, growingseasonin2004. Denmark,duringthegrowingseasonin2004.. twocurvesranclosetoeachotheratonly(cid:1)>1.5. 4.Discussion Thethreefortnightlyperiodsofsamplingin- dicated a different relationship among the three In comparative diversity studies, the frequent urbanisationstages,too(Fig.4).Theforestarea questionis:“whichassemblageismorediverse?” wasorderedin-betweentheurbanandsuburban (Tóthmérész1995).Theansweroftendependson atlowvaluesofthescaleparameter,anditslow the choice of the diversity index, which leads diversity became apparent only at (cid:1) >1.5. The someecologiststodeclarethequestforananswer suburbanassemblageseemedtobemorediverse futile and the methods nearly useless (Hurlbert than theurban oneat theinterval 0.7 < (cid:1) < 4.0 1971).Theuseofone-parametricindexfamilies (Fig.4).Bothoftheseindicationsweredifferent can resolve this paradox (Tóthmérész 1995, fromtheresultsobtainedfromthefullaswellas Southwood&Henderson2003). thepulsatingsamplingregimes. Analysingthediversityalonganurbanisation Restricting the trapping further to two fort- gradientusingRényiscalablediversityindex,we nights during the peak carabid activity substan- verifiedthatinDenmarkthediversitybetweena tially alteredthediversity profiles, andallthree rural, forested and urban forest patches area in- profilesranconsistentlybelowtheothercurves, creased along the urbanisation gradient. This thusunderestimatingthediversityoftheassem- trend contrasts with findings in several other blagevirtuallythroughoutthewholerangeofthe countries, for example in Finland (Alaruikka et scaleparameteralpha(Figs.3a–c). al. 2002), but is similar to the trends found in Comparingtherelationshipofthedetecteddi- CentralEurope(Maguraetal.2005)andmerits versity trends among the urbanisation stages, furtherstudy. samplingonlyduringthetwopeakactivityperi- Our results also showed that it is not neces- odsalsodistortsthediversity relationships.Un- sarytofollowtheseason-long,continuouspitfall der this sampling regime, the suburban area trappingrecommendedbyseveralauthors,most seemed to support the most diverse carabid as- recently by Woodcock (2005), at least for the semblageformostoftheprofile(Fig.5),except evaluationofdiversity.Withrespecttodiversity, under the scale parameter values of (cid:1) <0.4, i.e. thedataresultingfromthepulsatingmethodpro- whentherarespecieshadhighinfluenceonthe duced the same results as did continuous trap- diversity measure. This sampling method cor- ping,suggestingthatthenumberofthesampling rectlyindicatedtheurbanareaasbeingthemost occasions can be somewhat reduced. These re- diverseone,butnotbetween(cid:1)valuesof0.5and sults are encouraging for the development of 2.1 (Fig. 5). The relationship between the rural morebenignandlessarduousmonitoringmeth- andsuburbanareaswascorrectlyrepresented,ex- ods for carabids. Reducing the sampling effort cept for very small values of the scale para- withoutsignificantlynegativelyaffectingthede- meter,(cid:1). tecteddiversityrelationshipsmaybedesirednot ENTOMOL.FENNICAVol.17 (cid:127) Samplingregimeeffectsonobservedcarabiddiversity 349 only for logistic reasons, but also for biomoni- editorialresponsibilitiesforthispaper.Thisispublication toringofprotectedorotherareaswheree.g.en- no.5oftheDanglobeProject. dangered species occur. However, compared to thepulsatingmethod,theothersamplingregimes References withevenshorterdurationdidnotgivethesame results as the continuous sampling. These re- Alaruikka,D.,Kotze,D.J.,Matveinen,K.&Niemelä,J. gimes should therefore be used with caution at 2002:Carabidbeetleandspiderassemblagesalonga leastiftheywouldbeconsideredabasisforcom- forestedurban-ruralgradientinSouthernFinland.— parativediversitystudies. JournalofInsectConservation6:195–206. Our method of generating sub-samples in Elek,Z.&Lövei,G.L.2005:Groundbeetle(Coleoptera, time was simple, and assumed that the catch in Carabidae)assemblagesalonganurbanisationgradi- entnearSorø,Zealand,Denmark.—Entomologiske fortnightxdidnotinfluencethecatchinthesub- Meddelelser73:115–121. sequentintervals.Thisisnotnecessarilytrue,and Gaublomme,E.,Dhuywetter,H.,Verdyck,P&Desender, thustheresultsobtainedshouldbeviewedwith K.2005:Effectsofurbanisationoncarabidbeetlesin caution. The overlap in diversity between the oldbeechforests.—DIASReport114:111–123. continuous and the pulsating sampling regimes, Hansen,J.E.&New,T.R.2005:Useofbarrierpitfalltraps toenhanceinventorysurveysofepigaeicColeoptera. however,indicatesthatourassumptionmaynot —JournalofInsectConservation9:131–136. begrosslyincorrect. HurlbertS.H.1971:Thenon-conceptofspeciesdiversity We note that the use of pitfall trapping may –critiqueandalternativeparameters.—Ecology52: generaterelativeabundancepatternsthatarebi- 577–586. ased.Largespeciescanbemoremobileandless Ishitani,M.,Kotze,D.J.&Niemelä,J.2003:Changesin carabidbeetleassemblagesacrossanurban-ruralgra- abletoescapeoncefallenintothetrap,somaybe dientinJapan.—Ecography26:481–489. more“catchable”.Thisisaperennialproblemof Magura,T.,Tóthmérész,B.&Molnár,T.2004:Changesin anytrappingmethodthatreliesontheactivityof carabidassemblagesalonganurbanisationgradient. thestudysubjecttogeneratesamples.Forcom- —LandscapeEcology19:747–759. parativepurposesandforspeciesinventory,these Magurran,A.E.2003:Measuringbiologicaldiversity.— Blackwell,Oxford.256pp. methodsareuseful.Theabovelimitationsshould Niemelä,J.,Halme,E.&Haila,Y.1990:Balancingsam- be kept in mind when drawing conclusions on plingeffortinpitfalltrappingofcarabidbeetles.— generaldiversitytrends,comparing,forexample, EntomologicaFennica1:233–238. forestedvs.othertypesofhabitats. 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