Bioindication using trap-nesting bees and wasps and their natural enemies: community structure and interactions

Journal ofApplied Ecology0887\ 24\697Ð608

Þ 0887 BritishEcological Society

697

Bioindication using trap!nesting bees and wasps and their

natural enemies] community structure and interactions

TEJA TSCHARNTKE\ ACHIM GATHMANN and INGOLF STEFFAN!DEWENTERAgroecology\ University\ Waldweg 15\ D!26962 Go�ttingen\ Germany

Summary

0[ Results from four _eld studies show that communities of trap!nesting bees andwasps and their natural enemies are promising bioindicators for ecological change orhabitat quality[ These small and easy!to!handle communities can be analysed withrespect to "i# species richness and related parameters\ and "ii# ecological functions orinteractions[ The communities comprise Hymenoptera "Apidae\ Sphecidae\ Eumen!idae\ Pompilidae# and natural enemies belonging to many insect taxa[ Traps consistedof 049Ð199\ 04Ð19!cm long\ reed internodes\ put into tins or plastic tubes of 02Ð04 cmdiameter^ wooden posts with 1Ð09 of such reed!_lled tins were exposed in the targethabitat[1[ Species richness and abundance of bees "but not wasps# were closely related toplant species richness of the habitat\ a measure of the bees| food resource[ However\availability of nest sites of above!ground nesting species was equally important]meadows with old trees supported greater populations than meadows without trees[A threefold increase in exposed traps resulted in a twofold increase in species[2[ The sensitivity of this bioindicator system pro_ts from the fact that evaluationsrely not only on presence:absence data\ descriptive population attributes or diversityindices\ but also on interactions or ecological functions[ Monitoring ecologicalresponses or multitrophic interactions\ and their relationship to species diversity\ israrely done but much needed[ Ecological functions include "i# the percentage mortalityof trap!nesting bees and wasps due to parasitoids and predators\ which was correlatedwith the species richness of these natural enemies^ "ii# seed set of allogamous plantsdue to successful pollination by trap!nesting bees^ and "iii# biological control by thepredacious wasps[3[ With increasing isolation of fragmented habitats "when traps were exposed in acleared agricultural landscape#\ both species richness of natural enemies and per!centage mortality "parasitism and predation# declined signi_cantly[ In a comparisonof habitat types "grasslands and _eld margins#\ species richness of the trap!nestcommunity correlated with plant diversity\ but percentage mortality\ due to parasitismand predation\ with _eld age only[ The threshold distance to the nearest habitat was095Ð429m for a 09Ð49) decrease in mean mortality\ and the mortality increasedgreatly in habitats that were older than 4 years[ Accordingly\ these studies emphasizethe signi_cance of a continuum of old habitat patches for the augmentation of naturalenemies[4[ Exposure of standardized traps is an experimental approach with a small\ inter!acting and reproducing community that can be easily characterized by simple par!ameters[ Taxonomy and biology are well known\ and quick evaluations can be doneusing the close correlation between the number of occupied traps and species richness[Species richness of trap!nesting bees and wasps was closely correlated with thatsampled by sweep nets[ Further criteria of indicator taxa that apply to this system arediscussed in the text[

Key!words] Apidae\ diversity\ fragmented habitats\ Hymenoptera\ parasitism[

Journal of Applied Ecology "0887# 24\ 697Ð608

Correspondence] Teja Tscharntke "fax] 38 440287795^ e!mail] ttscharÝgwdg[de#[

698

T[ Tscharntke\A[ Gathmann +I[ Steffan!Dewenter

Þ 0887 BritishEcological Society\Journal of AppliedEcology\ 24\697Ð608

Introduction

There has been much detailed research on the use ofbiological indicators for the detection of pollution\and the issue of bioindication is therefore largelybiased towards the e}ects of pollutants on targetorganisms "Spellerberg 0880#[ For example\ lichensare well!known indicators of air pollution "Richard!son 0881#\ and monitoring of water quality is oftenbased on aquatic invertebrates "Barndt\ Bohn +Ko�hler 0881#[ However\ bioindication may be used ina much broader\ ecological sense\ indicating changesin population vulnerability\ community structure\ spe!cies| interactions or ecosystem functioning[ Withrespect to the scienti_c basis of ecosystem manage!ment\ the success and e.cacy of management actionshave to be tested with bioindication groups "Chris!tensen et al[ 0885#[

The literature on bioindication in relation to natureconservation programmes is largely biased towardsthe use of plants[ For example\ the occurrence ofBromus erectus indicates dry or nutrient!poor grass!land sites\ whereas Arrhenatherum elatius pro_ts fromnutrient!rich patches "Ellenberg 0885#[ Presence:absence data\ not only for single plant species but alsofor whole plant communities\ are widely used for theclassi_cation and evaluation of habitats[

Bioindication in natural habitat monitoring reliespredominantly on vegetation or vertebrates\ butshould also include insects\ which account for morethan half of all species "Strong\ Lawton + Southwood0873^ Landres\ Verner + Thomas 0877#[ The enor!mous species richness of insects allows a more subtledi}erentiation of habitat features than mapping of~ora "Rosenberg\ Danks + Lehmkuhl 0875^ Kremen0881#[ Many animals rely on habitat propertiesdi}erent from those indicated by the ~ora[ This canbe exempli_ed by bees and wasps[ "i# Since the abun!dance of soil!inhabiting bees and wasps is often lim!ited by a lack of suitable nesting places caused by adense cover of vegetation\ experimental removal ofgrassland vegetation can increase nest abundance bya factor of 3Ð09 times or even more\ i[e[ plant lossescan be associated with insect population increases"Ste}an!Dewenter + Tscharntke 0884^ Wesserling +Tscharntke 0884a#[ "ii# Above!ground nesting beesand wasps are more abundant when nesting oppor!tunities increase\ e[g[ when old trees with high per!centages of dead wood are part of the grassland\despite otherwise identical vegetation "see the Results\Study 1#[

Most biodiversity monitoring or evaluation rely onindirect methods because of the di.culty of coveringall species in a habitat or region[ Six approaches havebeen suggested for representative habitat evaluations[0[ Species richness of indicator taxa\ at best a suite ofindicators from unrelated taxa "plant\ invertebrate\vertebrate# or representatives from di}erent trophiclevels "Pearson 0883#[ Prendergast et al[ "0882# ques!

tion the reliability of biodiversity indicator taxa\because species!rich areas frequently do not coincidefor di}erent taxa[1[ Abiotic habitat characteristics\ such as richness ofsoil\ or microclimate as predictor variables of bio!diversity "Hill + Keddy 0881^ Huston 0882#[2[ Predictions of species richness based on the richnessof higher taxa "Gaston + Williams 0882^ Williams +Gaston 0883^ but see Prance 0883#[3[ Extrapolations from one focal group to largergroups "or from taxon to taxon\ site to site\ sampleto inventory# with calibration of ratios "Hammond0883#[ Similar approaches include the concept ofumbrella species\ whose requirements are believed tocover the needs of other species\ and the selection offocal species\ which are used to de_ne the attributesof viable landscapes "Lambeck 0886#[4[ Calculation of species richness using the numberof easily separated {morphospecies| "Oliver + Beattie0885#[5[ Small and easy!to!handle communities with infor!mation on both species richness "of di}erent taxa# andecological interactions "or food web structure#\ e[g[trap!nesting bees and wasps "this paper#\ cow!dungcommunities\ or plantÐinsect communities "Vo�lklet al[ 0882^ Kruess + Tscharntke 0883^ Tscharntke0884#[

Trap!nesting bees and wasps can be expected tore~ect ecological change through their "i# species rich!ness and related parameters\ and "ii# ecological func!tions or interactions] pollination\ predation\ and themortality due to their natural enemies[ Trap!nestingbees and wasps "Hymenoptera] Apidae\ Sphecidae\Eumenidae\ Pompilidae# nest in above!ground holes"in dead wood or grass stems# and include about 4)of all bee and wasp species "Krombein 0856#[ They areknown to be bioindicators sensitive to environmentalchange "Westrich 0878\ 0885^ Schmid!Egger\ Schmidt+ Doczkal 0885# and play a vital role in ecosystems[Pollination by bees signi_cantly increases the yield ofmany crops such as alfalfa and fruit trees as well asmany wild plant species "Corbet 0876^ Corbet\ Wil!liams + Osborne 0880^ Drescher 0881^ Matheson0883#[ Accordingly\ loss of bee species\ e[g[ due tohabitat fragmentation e}ects\ is known to be associ!ated with losses of ecological functions\ in that someallogamous plants su}er from reduced seed set "Jen!nersten 0877^ Didham et al[ 0885^ Ste}an!Dewenter +Tscharntke 0886a^ see also the Results\ Study 3#[Wasps can also be considered to be indicators of ben!e_cial interactions because they may be e}ective pred!ators of other insects[ Harris "0883# found eumenidwasps to control pest caterpillars[

Bene_cial functions of trap!nesting bees and waspscan easily be increased when large numbers of trapsare o}ered[ This e}ect is used for the augmentationof wild bees "especially Megachile rotundata# in the_eld or glasshouse "Richards 0873^ Torchio 0876^Dorn + Weber 0877^ Richards 0882#[ In a _eld experi!

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Trap!nesting beesand wasps


ment with a large number of trap nests on grasslandsand _eld margins\ the abundance of trap!nesting beesand wasps could be doubled within 2 years"Gathmann + Tscharntke 0886#[

In this paper\ four _eld studies are presented toshow applications of trap!nesting bees and wasps forbioindication or habitat evaluation[

Materials and methods

Traps consisted of 049Ð079\ 04Ð19!cm long\ inter!nodes of common reed Phragmites australis "Cav[#Trin[\ put into tins or plastic tubes of 09Ð02 cm diam!eter[ A range of reed diameter from 1 to 09 mm wasused "Gathmann\ Greiler + Tscharntke 0883#[Wooden posts about 0=4 m long were equipped with1Ð09 of such reed!_lled tins or tubes and exposed inthe middle of the target habitat[ The traps were set upin the _eld during April and sampled in October\so the _rst generation of bivoltine species was notconsidered[ In the laboratory\ reed nests were openedand examined for species identi_cation and mortalitydue to parasitism and predation[ The internal diam!eter of the internode "mm# and cell length "cm# weremeasured using vernier callipers[ After hibernation\adults emerged and could be identi_ed to species"scienti_c authorities of species are given in theAppendix#[ Identi_cation keys for the species involvedare given elsewhere "Gathmann + Tscharntke 0888#[Regression and ANOVA statistics were done with Stat!graphics "0884#[ Best!_t regression lines were gen!erated using log!transformed and untransformed vari!ables[

STUDY 0

Crop and set!aside _elds were compared in the upperRhine valley in south!west Germany near Karlsruhe"Figs 0 and 1^ data from Gathmann\ Greiler + Tsch!arntke 0883#[ The 39 _elds "crop _elds\ set!aside\ mea!dows# belonged to 09 _eld types\ had a _eld size rang!ing from 9=1 to 9=6 ha\ and were studied in 0889^ set!aside _elds had been used to grow cereals earlier[Traps exposed within each of the 39 _elds consistedof six 749!ml tins _lled with reed internodes[ Numbersof plant species per _eld were based on a threefoldmapping of 38!m1 plots "May\ July\ October#[ Set!aside _elds and meadows were cut once between lateJune and early July[

STUDY 1

The signi_cance of trap numbers per habitat wastested in three habitat types] "i# solitary fruit trees thatwere surrounded by narrow grassland strips "meanarea 09 m1# and isolated in the agricultural landscape"×49 m from the nearest tree#\ "ii# old "i[e[ ×29 yearsold# and extensively managed meadows without trees\and "iii# old "×29 years old# orchard meadows with

Fig[ 0[ Number of species of trap!nesting bees and wasps andnatural enemies[ Arithmetic means and standard errors ofspecies numbers in 09 _eld types based on n � 39 _elds "i[e[four replicates# are given "F � 3=20\ n � 39\ P ³ 9=990#[Homogeneous groups "Tukey!test# are indicated by the sameletter[ Sown and naturally developed _elds are separated[Field type abbreviations] Pea^ Bar � Barley^ Whe � Wheat^Pha � Phacelia tanacetifolia^ Clo � CloverÐgrass mixtures^0mf � 0!year old\ once!mown fallow "set!aside#^ 0uf � 0!year old\ unmown fallow "set!aside#^ 1mf � 1!year!old\ once!mown fallow "set!aside#^ 1uf � 1!year!old\ unmown fallow"set!aside#^ Orc � old orchard meadows[

Fig[ 1[ Number of trap!nesting species per _eld in relation tothe number of traps used to construct nests "y � 0 ¦ 9=1x\r1 � 55)\ n � 39\ P ³ 9=990#[ Species include bees\ waspsand natural enemies[ Data are from the study of Fig[ 0[

several old fruit trees "apples\ pears\ or cherries# scat!tered over the meadow "mean area of the meadows0=0 ha#[ Traps were established on eight habitats perhabitat type "i[e[ 13 habitats altogether#\ ranging from2 or 5 to 01 or 07 traps "reed!_lled tins# on eachhabitat[ The experiments were done near Karlsuhe in0881 "data from Jagsch 0882#[

STUDY 2

From 0883 to 0885\ _ve habitat types were comparedin the Go�ttingen area\ northern Germany] three _eldmargin strips sown with a species!rich ~ower mixturein 0882^ three set!aside _elds sown in 0882 with grass!clover mixture^ three extensively used\ nutrient!richgrasslands^ three nutrient!poor and dry chalk grass!

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lands\ and three orchard meadows "Fig[ 2^ data fromGathmann + Tscharntke 0886#[ Each of the 04 habi!tats had _ve wooden posts with 09 traps each[ Map!ping of vegetation was done twice "May and August0883# on 38!m1 plots\ so plant species richness\ plantcover ")#\ and habitat age "years# could be used aspredictor variables of insect diversity[ Further\ speciesrichness of trap!nesting bees and wasps was comparedwith the species richness of sweep!net samples "0883Ð85^ all habitats were visited four times per year\ May\June\ July and August\ so each habitat sample wasbased on 2 × 3 � 01 visits#[ On each visit\ bees andwasps were sampled with sweep!netting in the veg!etation "099 times# and with a speci_c sample of the~ower!visiting species "for 29 min#[

STUDY 3

In 0884\ 31 islands made of one wooden post withfour traps\ surrounded by four 7=4!L pots planted withthe annual\ self!incompatible plants Sinapis arvense

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Fig[ 2[ Number of species of trap!nesting bees\ wasps andnatural enemies from "i# solitary fruit trees "n � 7 habitats#\"ii# meadows without trees "n � 7 habitats# and "iii# orchardmeadows "n � 7 habitats# "each _eld type with either 2Ð5or 01Ð07 traps#[ "a# Both the number of trap nests "F � 6\P � 9=906# and the habitat type "F � 7=2\ P � 9=992# sig!ni_cantly in~uenced the number of species "two!wayANOVA^ interactions] P � 9=00#[ Arithmetic means and stan!dard errors are given[ "b# Number of species of the trap nestcommunity in relation to the number of exposed trap nestsper habitat[ Meadows without trees "triangles and dashedline^ y � 1=7 ¦ 9=32x\ r1 � 41)\ n � 7\ P � 9=990# andorchard meadows "circles and solid line^ y � 5=8 ¦ 9=31x\r1 � 24)\ n � 7\ P � 9=990# are separated[ Intercepts of thetwo regression lines di}ered signi_cantly "F � 7=3\P � 9=994#[

and Raphanus sativus\ were installed in the clearedagricultural landscape near Go�ttingen[ The distanceof these habitat islands to one of eight large and spec!ies!rich chalk grasslands was maximally 0999 m "datafrom Ste}an!Dewenter 0886^ Ste}an!Dewenter +Tscharntke 0886a\b#[ Seed set per plant was estimatedat 24 patches of Raphanus sativus using 0099 pods[

Results

In Germany\ 016 species have been reared from trapnests\ including 22 bees "excluding parasitic bees#\ 22digger wasps\ 06 eumenid wasps\ _ve pompilid waspsand 28 natural enemies "Appendix 0#[ Natural enemiesinclude many parasitoids\ e[g[ ichneumonid and chal!cid wasps\ but also predators such as ptinid beetlesand drosophilid ~ies[ Results from four studies mayexemplify the potential value of bioindication usingtrap!nesting bees and wasps[

STUDY 0

Forty _elds\ belonging to 09 di}erent _eld types in theagricultural landscape and with six trap!nests per _eld\were compared using trap!nesting bees and wasps[Field type was a factor signi_cantly explaining di}er!ences in species richness "Fig[ 0#[ Sown _elds\ in par!ticular crop _elds sown with peas or cereals and set!aside _elds sown with Phacelia tanacetifolia\ sup!ported a much less diverse hymenopteran communitythan the set!aside land with naturally developed veg!etation[ Altogether\ the 19 sown _elds were colonizedby nine trap!nesting species from 63 nests\ while the19 naturally developed _elds had 07 species from 107nests[

These di}erences resulted mainly from the di}er!ential colonization success of the bees "Apidae#\ butnot the wasps "Sphecidae and Eumenidae#[ The lattershowed a rather uniform distribution over the _eldtypes[ Sown _elds were colonized by only four out ofthe 02 nesting bee species\ but by all of the _ve nestingwasp species[ Accordingly\ bee species had a greatercoe.cient of variation "CV � 9=7\ n � 09 _eld types#than wasp species "CV � 9=3\ n � 09#[ This patterncould be substantiated by the fact that bees spentabout twice as long for cell provision on 0!year set!aside compared to old meadows "Osmia caerulescens]on average 27 vs[ 04 min^ Megachile versicolor] 23 vs[04 min#\ but not wasps "Ancistrocerus gazella] 19 vs[11 min^ Gathmann\ Greiler + Tscharntke 0883#[

These early and mid!successional _elds di}ered inplant species richness "29 vs[ 49 species# and cor!responding availability of a rich and diverse nectarÐpollen resource[ Mean plant species richness provedto be a good predictor of total species richness of trap!nesting Hymenoptera per _eld type\ explaining 65)of the variance in this relationship[ Phacelia _eldsattracted many honey bees\ and bee!keepers claimthat they are important for enhancement of all bee

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species\ but none of the trap!nesting bees was foundhere[ Numbers of species and numbers of occupiednests were closely correlated "Fig[ 1#\ explaining 55)of the variance in this relationship[ Accordingly\counting the number of occupied nests in the _eldgives a good idea of the species richness[

STUDY 1

The signi_cance of the number of exposed traps forthe number of successfully colonizing trap!nestingspecies was studied in three habitat types of the agri!cultural landscape] "i# isolated solitary trees\ "ii# mea!dows without trees\ and "iii# orchard meadows"Fig[ 2a#[ Increases in trap numbers only enhanced beeand wasp abundance in the two types of meadows\but less than could be expected from the number ofexposed traps] a tripling of trap numbers resulted onlyin a doubling of nest numbers[ The slope of increasewas similar in meadows without trees and orchardmeadows\ but the intercept was signi_cantly lower inmeadows without trees "Fig[ 2b# because\ due to thenesting facilities of fruit trees\ orchard meadowsappeared to support signi_cant bee and wasp popu!lations already[

STUDY 2

In a comparison of _eld margin strips\ set!aside _elds\nutrient!rich grasslands\ poor chalk grasslands andorchard meadows\ species richness of trap!nestingbees and wasps could be best explained by plant spec!ies richness "Fig[ 3a#\ but not plant cover or habitatage[ Species richness of bees and wasps increasedthreefold "from 4 to 04# when plant species richnessincreased _vefold "from 09 to 49#[ Percentage mor!tality due to parasitism and predation of trap!nestinhabitants was on average 17) and increased withhabitat age\ but not with plant diversity "Fig[ 3b#[There appeared to be a threshold\ with mortality"parasitism and predation# rising from about 19) to29) when habitats became older than 4 years[ Inaddition\ species numbers of bees and wasps sampledby trap nests were closely correlated with those sam!pled with sweep nets "Fig[ 4#[

STUDY 3

With increasing distance from the nearest chalk grass!land\ characterized by species!rich plant and insectcommunities\ species numbers of natural enemiesattacking trap!nesting bees and wasps decreased"Fig[ 5a#[ In addition to this loss in biodiversity\ per!centage mortality due to parasitism and predation\on average 10=1)\ declined with distance from chalkgrassland "Fig[ 5b#[ Isolation at a distance of 429 mhalved the percentage of mortality due to parasitismand predation\ and 594 m halved the species numberof natural enemies^ isolation at a distance of 095 m

Fig[ 3[ Species richness of trap!nesting bees and wasps andthe impact of natural enemies in a comparison of _eld marginstrips "E#\ set!aside _elds sown with a grass!clover mixture"Ž#\ nutrient!rich grasslands "ž#\ nutrient!poor chalk grass!lands "�# and orchard meadows "�#[ "a# Dependence ofspecies richness of bees and wasps on species richness of thevegetation "y � −03=7 ¦ 09=3 lnx^ r1 � 37)\ n � 04\P � 9=993#[ "b# Dependence of percentage mortality\ due toparasitism and predation\ on _eld age "years# "y � 19 ¦ 2=0lnx^ r1 � 25)\ n � 04\ P � 9=907#[

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Fig[ 4[ Number of species of bees and wasps from sweep!netsamples in relation to the number of species found in trapnests[ For data and symbols see Fig[ 3[ "y � 8=4 ¦ 0=0x\r1 � 70=5)\ n � 04\ P ³ 9=990#[

reduced mortality by 09) and at 010 m species num!ber of natural enemies by 09)[ Accordingly\ losses inthe species richness of natural enemies were associatedwith losses in percentage mortality "Fig[ 5c#\ i[e[ thedecrease in biodiversity paralleled the disruption ofecological functions[ In addition\ the number of seedsper plant "of Raphanus sativus# was negatively cor!related with the number of trap!nesting bee species

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Fig[ 5[ Species richness and percentage mortality due to para!sitoids and predators attacking trap!nesting bees and wasps[Altogether 31 habitat islands were established in the clearedagricultural landscape and eight on chalk grasslands "as con!trols#[ These islands di}ered in distance from one of theeight nearest species!rich chalk grasslands[ "a# Dependenceof species richness of natural enemies on the distance fromthe nearest chalk grassland[ "y � 9=991x − 1=31\ r1 � 19)\n � 31\ P � 9=992#[ "b# Dependence of percentage mortality"parasitism and predation# on the distance from the nearestchalk grassland[ "y � 10=1Ð9=91x\ r1 � 06)\ n � 31\P � 9=997#[ "c# Dependence of percentage mortality on thespecies richness of natural enemies[ "y � 3=5 ¦ 6=0x\r1 � 54)\ n � 31\ P ³ 9=990#[

"r1 � 27)\ n � 24 islands out of Raphanus pots\P ³ 9=990#^ both seed set and bee diversity declinedwith distance to the nearest grassland[

Discussion

The results of four studies on trap!nesting bees andwasps showed some potential ecological applications[There are several characteristics that make such small

communities particularly easy and successful forbioindication[

Aculeate Hymenoptera can be used as sensitiveindicators of habitat quality or environmental change[Results in this paper show that species richness andabundance of bees "and\ to a lesser extent\ wasps# arehighly variable and usually closely related to plantspecies richness "Fig[ 3a#[ Diverse vegetation obvi!ously supplies a greater diversity of nectarÐpollenresources and greater amounts of nutritious pollen\thereby supporting more bee species "Gathmann\ Gre!iler + Tscharntke 0883# and also more butter~y spec!ies "Feber\ Smith + Macdonald 0885^ Ste}an!Dew!enter + Tscharntke 0886c#[ Bees need much less timeto provision their nests in the diverse vegetation ofnaturally developed _elds than in the uniformenvironment of sown _elds[ In addition\ many smallspecies\ which are missing in uniform environments\inhabit diverse habitats[ Accordingly\ mean bodylength of trap!nesting bees and wasps per habitatdecreases with increasing plant species richness\ andbody length of solitary bees and wasps is positivelycorrelated with home range "Gathmann\ Greiler +Tscharntke 0883^ Wesserling + Tscharntke 0884b#[Trap!nesting bees and wasps also indicate habitatcharacteristics that di}er from those indicated by veg!etation[ Besides suitable food resources "pollen:nectarand insect prey#\ bees and wasps depend on nestingplaces that often appear to play a key role in popu!lation dynamics "Ste}an!Dewenter + Tscharntke0884^ Wesserling + Tscharntke 0884a#[ Meadows withor without old fruit trees but otherwise identical veg!etation di}ered greatly in species richness "Fig[ 2a#[Nesting facilities in dead wood supported populationsof bees and wasps that appeared to colonize quicklythe exposed traps[ However\ a threefold increase intraps resulted only in a twofold increase in speciesnumbers[ Possibly\ local populations were not largeenough to use more traps\ or competitive interferenceof females prevented more complete use of nestingsites[ Trap!nesting bees and wasps can also indicatethe island status of habitats] "i# traps near isolatedtrees were colonized less than traps on meadows withmany trees "Fig[ 2a#\ and "ii# with increasing isolationof the habitat\ species richness declined "Fig[ 5a^Ste}an!Dewenter + Tscharntke 0886a\b#[

The sensitivity of this bioindication system pro_tsfrom the fact that evaluations rely not only on pres!ence:absence data\ descriptive population attributesor diversity indices\ but also on interactions or eco!logical functions "ecological functions can be de_nedas interactions of organisms with their biotic or abioticenvironment#[ Ecological responses or processesdependent on more or less complex food webs arepoorly known\ but results on such multitrophic inter!actions or trophic cascades are much needed "Spel!lerberg 0880^ Christensen et al[ 0885^ Tscharntke0886#[ Bees are important pollinators\ and losses inbee species could dramatically a}ect reproduction or

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_tness of many crops and wild plant species "Corbet\Williams + Osborne 0880#[ Habitat fragmentationcauses extinction of bees and thereby reduces pol!lination success in many allogamous wild plants"Aizen + Feinsinger 0883^ Didham et al[ 0885^ Ste}an!Dewenter + Tscharntke 0886a\b#[ Wasps may beimportant in biological control "Harris 0883#[

Above all\ population or community monitoring issupplemented with species interactions inside nests]mortality due to parasitism and predation of trap!nesting bees and wasps was negatively correlated withisolation of the habitat "Fig[ 5#[ Accordingly\ loss ofspecies was associated with a loss in ecological func!tions in that mortality due to natural enemiesdecreased[ Parasitism and predation increased withproximity and age of habitats "Figs 3b\ 5b#\ and otherhabitat features "like plant species richness# did notexplain additional variation in the data[ The thresholddistance to the nearest habitat was 095Ð429 m for a09Ð49) decrease in mean mortality due to parasitismand predation "or 010Ð594 m for a 09Ð49) decreasein species richness of natural enemies#[ The impact ofnatural enemies "parasitism and predation# increasedgreatly in habitats that were older than 4 years[ Ingeneral\ both a continuum of habitats and old habitatsappear to be of particular importance in managementplans for the augmentation of natural enemies "Kar!eiva 0889^ Thies et al[ 0886^ Tscharntke + Kruess0888#[

Dissection of nests makes it possible to reconstructevents during the past vegetation period\ e[g[ the lay!out of the cells and signi_cance of mortality factors[The position of hosts and parasites within the lineartrap!nests reveals the sequence of\ for example\ para!sitism or other mortality factors\ but of course nestsof any one species will be started at a variety of dates[With respect to such reconstruction of past events\trap nests are very much like plant galls\ which alsoallow comparatively easy analyses of tritrophic inter!actions and a survey of past events "Redfern + Askew0881^ Tscharntke 0883#[

All species used for bioindication with trap!nests atleast reproduce in the target habitat\ so they are notjust short!term visitors or tourists[ In addition\ theyoften also collect their o}spring provisions withintheir nesting habitat\ but this should di}er with respectto the species involved "large body size implies largehome range\ see above# and the habitat type "smallhabitats with nearby _elds o}ering large amounts ofnutritious food may only be used for nesting#[ Thispoint contrasts with many descriptive studies in habi!tat evaluation that cannot separate the indigenousfauna from the external non!indigenous fauna[

Exposure of the identical number and kind of nest!ing sites in di}erent target habitats is an experimentthat excludes many possibly in~uencing or disturbingfactors that are usually associated with insect mappingin the _eld[ Spatial and temporal habitat comparisonscan be standardized with the exposure of equal num!

bers and types of traps[ Trap nests provide a way ofmonitoring throughout the year\ while insect mappingis often dependent on frequent site inspections by atrained entomologist[ Further\ trap nests can be char!acterized easily by many simple variables] height andorientation of traps^ numbers of reed internodes^diameter and length of internodes or nests^ and sizeand content of nest cells[ Traps are easily constructedand cheap[ Exposure in the target area is simple[ Inaddition\ trap exposure can be manipulated\ for exam!ple with respect to height or orientation\ which isknown to change species composition[ Traps can alsoeasily be used for observations and experiments\ e[g[learning\ orientation or foraging behaviour of bees"Steinmann 0865\ 0870^ Thiede 0870^ Theunert 0885#[

Communities of trap!nesting bees and wasps arelarge enough to examine community structure andinteractions\ but small enough to be dealt with easily[Maximally 04Ð19 species colonize the traps exposedon a meadow\ so undergraduate students or natureconservationists with little knowledge in entomologycan adequately check the traps and identify the inhabi!tants within a short time[ Numbers of occupied reedinternodes\ which can be simply measured in the _eldeven by non!entomologists\ give a good prediction ofspecies richness "Fig[ 1#[ In addition\ the total numberof bees and wasps "mainly soil!inhabiting species#sampled by sweep nets followed a similar distributionpattern among habitats "Fig[ 4#] species richness fromtrap nests could be used to predict the total number ofbee and wasp species\ explaining 71) of the variance[

These advantages make the application of trap nestsfor bees and wasps useful in bioindication and moni!toring[ The trap!nest communities meet the criterionof indicator taxa in that they are taxonomically wellknown\ their life!history is understood\ readily sur!veyed and manipulated\ and they are distributed overa broad range of habitats\ sensitive to habitat or stresschanges\ responsive to biodiversity patterns in othertaxa "e[g[ vegetation\ butter~ies#\ and of potentialeconomic importance "Noss 0889^ Kremen 0881^Pearson 0883#[ Moreover\ these easy!to!handle andsmall communities meet the need for a bioindicationor monitoring scheme that greatly relies on ecosystemfunctions or ecological interactions "Noss 0889^ Chris!tensen et al[ 0885^ Gange + Brown 0886#[ Such anapproach also avoids the occasionally negative imageof the mapping of ~ora and fauna\ in favour of anexperimentally orientated hypothesis testing[

Acknowledgements

We are grateful to Sarah A[ Corbet\ Jason M[ Weeksand an anonymous referee for useful comments on themanuscript[ Financial support came from the GermanScience Foundation "DFG#[

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Received 8 September 0886^ revision received 16 August 0887

606



Appendix 0

Trap!nesting bees and wasps known from Germany\ including natural enemies "parasitoids and insect predators#[Abundance "number of papers with records# and food type are indicated[ Data are based on a review byGathmann + Tscharntke "0888#[

Species Records� Food type$ Natural enemies

ApidaeAnthidium lituratum "Panzer 0790# 0 Asteraceae Melittobia acasta\ Stelis punctulatissimaChelostoma campanularum "Kirby 0 Campanula0791#Chelostoma distinctum Stoeckert 1 Campanula0818Chelostoma ~orisomne "Linnaeus 6 Ranunculus0647#Chelostoma fuliginosum "Panzer 09 Campanula Anthrax anthrax\ Ephialtes brevis\ Melittobia0687# acasta\ Sapyga clavicornis\ Stelis minutaHeriades crenulatus Nylander 0745 2 Asteraceae Coelopencyrtus arenarius\ Melittobia acastaHeriades truncorum "Linnaeus 0647# 00 Asteraceae Chrysis cyanea\ Gasteruption asectator\

Melittobia acasta\ Omalus auratus\ Poemeniacollaris\ Sapyga decemguttata\ Stelis breviuscula\Stelis ornatula

Hylaeus angustatus "Schenck 0750# 0 PolylecticHylaeus annularis "Kirby 0791# 0 PolylecticHylaeus communis Nylander 0741 01 Polylectic Coelopencyrtus arenarius\ Gasteruption asectatorHylaeus confusus Nylander 0741 3 Polylectic Gasteruption assectatorHylaeus difformis "Eversmann 0741# 2 PolylecticHylaeus gibbus Saunders 0749 0 PolylecticHylaeus punctulatissimus Smith 0731 0 AlliumHylaeus signatus "Panzer 0687# 0 ResedaMegachile alpicola Alfken 0813 5 Polylectic Amthrax anthrax\ Coelioxys inermis\ Coelioxys

mandibularis\ Melittobia acastaMegachile ericetorum Lepeletier 0 Fabaceae0730Megachile lapponica Thomson 0761 3 Epilobium Melittobia acastaMegachile rotundata "Fabricius 2 Polylectic0673#Megachile versicolor Smith 0733 6 Polylectic Anthrax anthrax\ Coelioxys mandibularis\

Melittobia acastaMegachile willughbiella "Kirby 0791# 0 PolylecticOsmia adunca "Panzer 0687# 2 EchiumOsmia brevicornis "Fabricius 0687# 5 BrassicaceaeOsmia caerulescens "Linnaeus 0647# 6 Polylectic Melittobia acasta\ Ptinus sexpunctatus\ Sapyga

clavicornis\ Sapyga quinquepunctata\ Stelisbreviuscula

Osmia claviventris "Thomson 0761# 1 PolylecticOsmia cornuta "Latreille 0794# 1 PolylecticOsmia fulviventris "Panzer 0687# 1 Asteraceae Sapyga clavicornisOsmia gallarum Spinola 0797 1 Fabaceae Sapyga quinquepunctataOsmia leaiana "Kirby 0791# 7 Asteraceae Cacoxenus indagator\ Melittobia acasta\ Sapyga

quinquepunctata\ Stelis phaeopteraOsmia leucomelana "Kirby 0791# 1 Polylectic Stelis ornatulaOsmia parietina Curtis 0717 1 PolylecticOsmia rufa Linnaeus 0647 02 Polylectic Anthrax anthrax\ Cacoxenus indagator\

Megatoma undata\ Melittobia acasta\Monodontomerus obscurus\ Ptinus sexpunctatus\Sapyga clavicornis\ Trichodes sp[

Osmia uncinata Gersta�cker 0758 2 Polylectic Cacoxenus indagator\ Chrysis hirsuta\ Sapygaclavicornis\ Sapyga similis\ Stelis ornatula

EumeninaeAllodynerus rossii "Lepeletier 0730# 3 Microlepidoptera

"Gelechiidae#Ancistrocerus antilope "Panzer 0687# 6 Microlepidoptera Chrysis ignita\ Melittobia acasta

"Tortricidae\Crambidae#\Noctuidae\Chrysomelidae

607




Ancistrocerus gazella "Panzer 0687# 8 Microlepidoptera Chrysis ignita\ Melittobia acastaAncistrocerus nigricornis "Curtis 01 Microlepidoptera Anthrax anthrax\ Chrysis ignita\ Ephialtes mani!0715# "Tortricidae# festor\ Melittobia acastaAncistrocerus parietinus "Linnaeus 2 Microlepidoptera\ Melittobia acasta0650# ChrysomelidaeAncistrocerus trifasciatus "Mu�ller 5 Microlepidoptera\ Melittobia acasta0665# ChrysomelidaeDiscoelius zonalis "Panzer 0790# 1 Microlepidoptera Melittobia acastaEuodynerus notatus "Jurine 0796# 0 Microlepidoptera\

NoctuidaeEuodynerus quadrifasciatus "Fab! 1 Microlepidopteraricius 0682# "Tortricidae#\

ChrysomelidaeGymnomerus laevipes Shuckard 0 Curculionidae"0726#Microdynerus nugdunensis "Saussure 1 Curculionidae0745#Symmorphus angustatus "Zetterstedt# 0 ChrysomelidaeSymmorphus bifasciatus "Linnaeus 09 Chrysomelidae Ephialtes spatulata0650#Symmorphus connexus "Curtis 0715# 1 Chrysomelidae\ Chrysis mediata

MicrolepidopteraSymmorphus crassicornis "Panzer 3 Chrysomelidae Chrysis mediata0687#Symmorphus gracilis "Brulle 0721# 6 Chrysomelidae\

CurculionidaeSymmorphus murarius "Linnaeus 1 Melasoma Chrysis fulgida\ Chrysis mediata\ Omalus aeneus0647# "Chrysomelidae#

PompilidaeAgenioideus cinctellus "Spinola 0797# 0 Arachnida Melittobia acastaAuplopus carbonarius "Scopoli 0652# 5 Arachnida Chrysis cyanea\ Melittobia acastaDipogon bifasciatus "Geo}roy 0674# 0 Arachnida Melittobia acastaDipogon subintermedius "Magretti 6 Arachnida Melittobia acasta0775#Dipogon variegatus "Linnaeus 0647# 0 Arachnida Melittobia acasta

SphecidaeCrossocerus capitosus "Shuckard 0 Diptera0726#Crossocerus cetratus "Shuckard 0726# 1 DipteraCrossocerus cinxius "Dahlbom 0727# 0 DipteraCrossocerus nigritus "Lepeletier + 0 DipteraBrulle 0723#Crossocerus podagricus "van der Lin! 0 Dipteraden 0718#Ectemnius continuus "Fabricius 0793# 0 DipteraNitela borealis Valkeila 0863 1 PsocopteraNitela fallax Kohl 0772 0 UnknownNitela spinolae Latreille 0798 1 UnknownPassaloecus brevilabris Wolf 0847 2 AphidinaPassaloecus corniger Shuckard 0726 8 Aphidina Melittobia acasta\ Omalus aeneus\ Omalus aura!

tus\ Poemenia brachyura\ Poemia collaris\ Poe!menia hectica\ Poemenia notata\ Sapygadecemguttata

Passaloecus eremita Kohl 0782 4 Aphidina Melittobia acasta\ Omalus aeneus\ Omalus aura!tus\ Omalus biaccinctus\ Omalus pusillus\ Omalusviolaceus\ Poemenia brachyura\ Poemia collaris\Poemia hectica\ Poemenia notata

Passaloecus gracilis "Curtis 0723# 5 Aphidina Omalus auratusPassaloecus insignis "van der Linden 8 Aphidina Melittobia acasta\ Omalus biaccinctus\ Omalus0718# pusillus\ Poemenia bachyura\ Poemenia collarisPassaloecus monilicornis Dahlbom 0 Aphidina Poemenia collaris0731Passaloecus singularis Dahlbom 0734 1 Aphidina

608




Passaloecus turionum Dahlbom 0734 3 Aphidina Omalus aeneus\ Poemenia notataPemphredon lethifer "Shuckard 0726# 1 Aphidina Omalus aeneus\ Omalus auratusPemphredon lugens Dahlbom 0731 4 Aphidina Omalus auratusPemphredon lugubris "Fabricius 0682# 1 AphidinaPsenulus brevitarsis Merisuo 0826 1 AphidinaPsenulus concolor "Dahlbom 0732# 0 Psyllina Omalus auratusPsenulus fuscipennis "Dahlbom 0732# 4 AphidinaPsenulus pallipes "Panzer 0686# 6 AphidinaRhopalum clavipes "Linnaeus 0647# 2 DipteraRhopalum coarctatum "Scopoli 0652# 0 DipteraSpilomena beata Blu�thgen 0842 0 ThysanopteraSpilomena troglodytes "van der Lin! 3 Thysanopteraden 0718#Trypoxylon attenuatum Smith 0740 2 ArachnidaTrypoxylon clavicerum Lepeletier + 09 Arachnida Chrysis cyanea\ Ephialtes spatulata\ MelittobiaServille 0714 acasta\ Nematopodius formosusTrypoxylon _gulus "Linnaeus 0647# 02 Arachnida Chrysis cyanea\ Chrysis ignita\ Ephialtes mani!

festor\ Ephialtes spatulata\ Melittobia acastaTrypoxylon medium de Beaument 4 Arachnida Chrysis cyanea\ Melittobia acasta0834Trypoxylon minus de Beaument 0834 5 Arachnida Chrysis cyanea\ Melittobia acasta

� Number of papers with records "Gathmann + Tscharntke 0888#[$ Prey insects are larvae in Eumeninae and adults in Pompilidae and Sphecidae[

Documents

Bioindication using trap-nesting bees and wasps and their natural enemies: community structure and interactions