Determinants of parasitoid abundance and diversity in woodland habitats
SALLY E. M. FRASER, CALVIN DYTHAM and PETER J. MAYHEW
Department of Biology, University of York, York YO10 5YW, UK
Summary
1.
Insect parasitoids comprise a large fraction of terrestrial biodiversity. Because of thisdiversity, species-level conservation of most parasitoid species is impractical and habitatconservation must substitute. However, habitat indicators of parasitoid abundance anddiversity are poorly known.
2.
To identify such habitat indicators, parasitoid wasps in four ichneumonid subfamilieswere sampled in the field herb layer of 15 woodlands in the Vale of York, UK, usingMalaise traps. The catch was related to vegetation characteristics.
3.
A total of 1543 individuals in 60 species was recorded, representing 36% of UKspecies in the taxa sampled. Parasitoids tended to be more abundant and species rich inwoodlands with a high broadleaf content and tree species richness. This pattern wasobserved in the ichneumonid subfamilies Pimplinae, Poemeniinae and Diacritinae.
4.
However, the ichneumonid subfamily Diplazontinae was found to vary in abundanceand richness within rather than between woodlands and showed no association withmeasured habitat variables.
5.
Reserve selection analyses indicated that coniferous woodlands, and woodlands witha low abundance and richness of parasitoids, none the less can contribute to maximizingparasitoid diversity at the landscape scale.
6.
Synthesis and applications
. At the individual woodland scale, broadleaved woodlandswith high tree species richness appear best for conserving parasitoid abundance anddiversity. At a landscape scale however, a variety of woodland habitat types can maxi-mize diversity of all parasitoid taxa. We hypothesize that the degree of associationbetween parasitoid abundance and diversity, and characteristics of the vegetation withinhabitats will decrease with an increase in the number of trophic links that separate them.
Little studied but ecologically important taxa make upmuch of the planet’s biodiversity (May 1988). In mostcases neither the time nor resources will exist to planconservation strategies for each individual speciesbelonging to such taxa (Hughes, Daily & Ehrlich 2000).An alternative to species-level conservation is a habitat-based approach, where priority habitats for target taxaare identified and conserved, therefore protecting wholecommunities.
Parasitoids are insects, mainly wasps (Hymenoptera),that develop to maturity by feeding on the body ofanother host arthropod, eventually killing it. The par-asitoid wasps are extremely species rich and essential tothe maintenance of species diversity in other organisms(LaSalle & Gauld 1991). Yet, despite their ecologicalinfluence, relatively little is known about their biology,distribution and diversity. For large-scale conservationof parasitoids, habitat conservation may be the onlypractical approach (Hochberg 2000). However, thereare few studies of parasitoid diversity at the habitatscale on which to base conservation recommendations.
Greater plant architectural complexity would beexpected to increase the species richness of herbivores,which form the hosts of many parasitoids (Strong,
Correspondence: Peter J. Mayhew, Department of Biology,University of York, York YO10 5YW, UK ([email protected]).
Lawton & Southwood 1984). One could therefore pre-dict that habitats rich in plant species and with complexplant architecture would be richer in parasitoids.However, host specificity amongst parasitoids is knownto vary across different habitats (Price 1991) and, as aresult, findings from studies at the host level do noteasily translate into predictions within whole habitats(Menalled
et al
. 1999). Parasitoid diversity at thehabitat level will be an emerging property derived fromnumerous biological processes (Price 1991), not all ofwhich will operate in the same way across taxa.
Much of what is known concerning the diversity ofparasitoid communities comes from literature-basedstudies of parasitoids reared from their individual insecthosts (Hawkins 1994). Of the little work concerning theeffect of habitat characteristics, most has concentratedon agro-ecosystems as a result of interest in the potentialuse of parasitoids for biological control (Altieri, Cure& Garcia 1993). These agricultural studies may notsimply translate to other systems and thus there is aneed for studies at the habitat level to identify generalpatterns and, ultimately, the mechanisms behind them.
Woodland habitats are among the most stable ele-ments of human-dominated landscapes, which nowcover a substantial proportion of the Earth’s surface.As such, they play an important role in the maintenanceof biodiversity (Petit & Usher 1998). We compared theparasitoid faunas of 15 woodlands in the Vale of York,UK. We tested the null hypothesis that parasitoidabundance and diversity are the same across woodlandtypes. If woodlands do differ in parasitoid abundanceand diversity, then it may be possible to identify habitatindicators that explain a significant component of thevariation. We tested the null hypothesis that parasitoidabundance and diversity show no association withwoodland vegetation variables. If vegetation indicatorsof parasitoids can be used to identify woodlands thatare particularly valuable for parasitoid abundance anddiversity, it does not necessarily follow that, at a land-scape scale, it is best to conserve only those woodlandswith the highest abundance and diversity of parasitoids.
To address this scale issue, we tested the null hypothesisthat conserving only one or a variety of woodland typesin the landscape has no effect on the inclusion ofparasitoid species.
Materials and methods
The study was conducted in the Vale of York, UK. Toreduce variation in factors such as topography, weatherand soil type, the area within which woodlands werechosen was limited. Woodlands were all larger than2 ha as smaller patches of habitat may not be capable ofsupporting insect communities distinct from surround-ing habitats (Levenson 1981). Although no maximumsize was determined for the selection of woodlands,selection was limited to farm woodlands that wererelatively small, with none of those used exceeding 20 ha.
Fifteen farm woodlands were chosen to include arange of tree species types giving different woodlandhabitats (broadleaved, mixed and coniferous habitats;Table 1). Broad classification of woodland habitats inBritain is based on canopy type (JNCC 1993) and thisinformation is also displayed on UK Ordnance Surveymaps, so these habitat definitions are directly relevantto conservation.
Four closely related subfamilies of the Ichneumonidaewere chosen for study: Diplazontinae, Pimplinae,Diacritinae and Poemeniinae. These subfamilies haveuseable species-level keys (Beirne 1941; Fitton, Shaw &Gauld 1988), are known to be abundant in many hab-itats and have a wide range of hosts. All species in thesefour subfamilies are winged parasitoids.
The Diplazontinae is a relatively small subfamily,with 55 British species in 12 genera (Broad 2005). Allspecies are thought to be endoparasitoids of aphido-phagous Syrphidae (Diptera), with host records available
Table 1. Location, area and habitat type of the study woodlands. Habitat is as given on 1:25 000 Ordnance Survey maps
Woodland name Woodland code Grid reference Size (ha) Habitat
Copmanthorpe Wood COWO SE 562 450 6 MixedFox Covert FOCO SE 629 417 3·7 MixedGrimstone GRIM SE 660 501 4·9 ConiferousGreenland Wood GRWO SE 563 449 2 BroadleavedHarrop’s Plantation HAPL SE 629 413 5 MixedHacking Wood HAWO SE 644 408 6·6 MixedMelbourne Hall MEHA SE 749 433 3·5 BroadleavedMany Gates Plantation MGPL SE 693 537 2 ConiferousNaburn Wood NAWO SE 609 438 18 ConiferousNew Drive Plantation NDPL SE 753 427 11·2 ConiferousNew Covert NECO SE 732 442 3·3 BroadleavedPark Wood PAWO SE 733 445 2·8 BroadleavedRush RUSH SE 603 443 2·4 BroadleavedWilson’s Plantation WIPL SE 696 539 3 MixedWigman Wood WIWO SE 644 453 4·5 Coniferous
for approximately 50% of species. Oviposition is intothe host egg or larva and emergence of the adult is fromthe host puparium (Fitton & Rotheray 1982). Thecharacteristic of allowing the host to develop afterparasitization defines them as koinobionts, as opposedto idiobionts (see below). Adult females commonly occurnear aphid colonies, searching for hosts and feeding onsyrphid eggs and larvae, or on aphid honeydew (Rotheray1981a). Males of some species have been found to formswarms beneath large tree canopies and others are foundat aphid colonies and flowers (Rotheray 1981b).
The subfamily Pimplinae exhibits a wider range ofbiologies and hosts than any other subfamily of theIchneumonidae (Fitton
et al.
1988). It is also probablythe most extensively studied subfamily, largely becausemany species are parasitoids of economically importantpests. In the British Isles there are 103 species in 30genera (Broad 2005). The subfamily is currently dividedinto three monophyletic tribes, the Delomeristini,Ephialtini and Pimplini, which demonstrate distinctecologies (Gauld, Wahl & Broad 2002; Broad 2005). Inthe British Isles the Delomeristini consists of ninespecies in two genera. Host information for this tribe ispoor but some species in the genus
Delomerista
appearto parasitize cocoons of sawflies and other ichneumonids,while those in the genus
Perithous
appear to be associatedmost frequently with aculeate Hymenoptera (Fitton
et al.
1988). The Ephialtini consists of 75 species in 24genera. Host groups for this tribe are varied and arefound across the orders Coleoptera, Hymenoptera,Diptera and Arachnida. The majority of species areectoparasitoids of holometabolous insect larvae, pre-pupae and pupae (Fitton
et al.
1988). The Pimpliniconsists of 20 species in three genera. All are chieflyidiobiont endoparasitoids of the pupae of Lepidoptera(Fitton
et al.
1988). Idiobiont parasitoids permanentlyparalyse or kill the host before the parasitoid egghatches. The host is consumed in the location and statein which it was attacked (Askew & Shaw 1986).
The subfamilies Poemeniinae and Diacritinae werepreviously grouped within the Pimplinae (Fitton
et al.
1988) and were included in this study for that reason,although they are now recognized as distinct subfamilies(Wahl & Gauld 1998; Gauld
et al.
2002). The Poeme-niinae contains six species in Britain (Broad 2005).Members of the Poemeniinae develop as idiobiontectoparasitoids and at least some of these species aremost often collected in association with dead andstanding timber (Fitton
et al.
1988). Diacritinae is oneof the few subfamilies for which the larvae are com-pletely unknown (Wahl & Gauld 1998). In Europe onlyone species is known,
Diacritus aciculatus
(Fitton
et al.
1988).Malaise traps are a form of flight interception trap
that are generally considered to be the best means ofobtaining large, general samples of Ichneumonidae frommost habitats (Fitton
et al.
1988) and have been usedextensively for this purpose (Owen & Owen 1974;Noyes 1989a, 1989b; Owen 1991; Bartlett
et al
. 1999;
Sääksjärvi
et al
. 2004, 2006; Sperber
et al
. 2004). Thetraps used in this study were supplied by Marris HouseNets (Marris House Nets, Bournemouth, UK) andfollowed the design of Townes (1972). These trapssample in the field–herb layer and therefore do not pro-vide data on those species using only the canopy.
Two Malaise traps were set up in each woodlandduring July and August 2003, the main Hymenopteraflight season. The two-trap design was used to investi-gate the influence of trap siting on catch and to providea measure of within-woodland variability. The follow-ing rules were used to locate trapping areas: to controlfor aspect we sampled two areas 10 m either side of themid-point of the southern edge of the woodland. Toaccount for edge effects, these areas were located 10 min from the edge of the woodland habitat. In each ofthese areas we marked out a 20
×
10-m quadrat withinwhich we set a Malaise trap. Traps were open for 2consecutive weeks in every 4, 1–15 July and 29 July
−
12August The trap bottle was changed after 1 week to givetwo samples of 1-week duration in each month.
In order to identify possible habitat indicators ofparasitoid abundance and diversity, a suite of habitatvariables was measured (see Table S1 in the supple-mentary material).
Vegetation was sampled in late July/early August atthe site of the Malaise trap and then more widely acrosseach woodland, using quadrats at two scales: 20
×
20 mfor the canopy trees and shrub layer and 2
×
2 m for thefield and herb layer. Each Malaise trap was at the centreof a 20-m quadrat to give a detailed record of thevegetation present around the trap. At random coordin-ates within this quadrat, five 2-m quadrats weresurveyed. Within the woodland as a whole, two more20-m quadrats were surveyed, their location beingdetermined by generating random coordinates withinthe north-east and north-west quarters of the woodlandand using these as the south-west corner of a quadrat.Again, at random coordinates within the larger quadrats,five 2-m quadrats were surveyed.
In the 20-m quadrats all tree and woody shrub speciestaller than 1 m were counted and identified to species.All woody shrubs less than 1 m in height and herbswithin the 2-m quadrats were identified to species.Ferns, fungi, [grasses + sedges] and [mosses + lichens +liverworts] were not identified to species but were groupedthus. A visual estimate of the percentage total vegeta-tion cover for the herb layer was made. An estimate ofcanopy cover was taken visually from the south-westcorner of each 2-m quadrat using a gridded acetate.The acetate was held at arm’s length towards the can-opy and the number of grid squares in which canopycover was seen were counted. This number was thendivided by the total number of squares on the grid.
Plant height diversity and plant architectural diver-sity were measured within the field–herb layer using the
method of Southwood, Brown & Reader (1979). A 2-mhigh sampling pin was marked at height intervals of5 cm, 10 cm and successive 20 cm until 1 m and 25-cmintervals thereafter. The total number of touches ineach height category was recorded and used to providea measure of plant height diversity. Plant architecturaldiversity was measured by recording the number andtypes of plant structures that were touching the pin (seeTable S2 in the supplementary material). Five sampleswere taken using the pin at random coordinates withineach 2-m quadrat. The diversity of both plant heightand plant architectural diversity was estimated usingthe log series diversity index
α
, following Southwood
et al.
(1979).
Species accumulation curves were calculated to indicatethe extent to which the regional fauna was sampled,and how many species each extra woodland would add.Curves were generated by running 15 sequences ofaccumulations, one with each of the 15 woodlands atthe start and then adding one woodland at randomuntil all 15 were used.
Comparison of woodlands
To test the null hypothesis that parasitoid abundanceand diversity are the same across different woodlands,a mixed-model nested analysis of variance (
) wascarried out on the data for individual traps in each ofthe 4 sampling weeks. Factors in the analysis were trap,woodland, habitat and week (time). Habitat was a fixedeffect classifying woods as either predominantly broad-leaved (> 50%) or predominantly coniferous (> 50%).Traps (a random effect) were nested within woods (arandom effect) and woods within habitat. This was arepeated-measures design so week was included in theanalysis to account for the problem of pseudoreplicationby repeat visits to the same trap sites. Non-significantfactors and interaction terms were sequentiallyremoved from the model to leave only those explainingsignificant proportions of variation in the data. Abun-dance data were log
10
(
x
+ 1) transformed to reduceright skew.
Habitat indicators
In addition to exploring patterns in abundance andrichness, the Simpson’s index (
D
) was used to explorepatterns in the evenness of parasitoid assemblages inrelation to habitat variables. Simpson’s index is recom-mended as a good estimate of diversity for relativelysmall sample sizes (Magurran 2004). The index is heavilyweighted towards the most abundant species in thesample while being less sensitive to species richness.The index is expressed here as the reciprocal (1/
D
) andthe value of the measure will rise as the assemblagebecomes more even.
To test the null hypothesis that woodland vegetationvariables are not associated with parasitoid abundanceand diversity, parasitoid abundance, richness and 1/
D
were used as response variables in a backwards step-wise regression analysis. Explanatory variables werethe habitat variables measured from each woodland.The stepwise procedure was allowed to select the pre-dictors using the criteria probability of
F
to enter
≤
0·05and probability of
F
to remove > 0·05.
The landscape scale
To test whether a variety of woodland types in the land-scape maximizes the conservation of parasitoid species,we conducted two tests. In the first test we asked whichwas the best selection of woods for maximizing parasitoiddiversity. Two simple reserve selection algorithms wereused. In the first algorithm, based on species richness, thewoodland with the highest species richness was identified.Then all the species that were found in that woodlandwere removed from the data set and the woodland withthe highest remaining richness was identified. This pro-cess was run five times to select the five most importantwoodlands for conservation. To determine whether thewoodlands selected by this analysis performed betterthan a random collection of woodlands, we ran 1000repetitions of the data for each higher taxon to calculatethe mean number of species conserved by randomlyselecting five woodlands. In the second algorithm, whereselecting woodlands in order of their contribution ofrare species to the data set, the system was the same asfor species richness except species were weighted bythe number of woodlands in which they occurred.Species found in all woodlands were worth 1/15, thosefound in two woodlands 2/15, and so on until thosefound in just one were worth 15/15. For both algorithmswe then simply examined
post-hoc
what woodland typeswere represented in the optimal reserve selections.
As the results of this test suggested that a mixture ofwoodland types, both coniferous and broadleaved,would be best at preserving landscape-level diversity,we conducted a further reserve selection experiment totest the generality of this finding. In this further test, weselected five woodlands at random from the data andcounted the number of species included. However, aswell as choosing woodlands from the data set as awhole, which allowed a mixture of woodland types, wealso restricted choice to either only coniferous woodsor only deciduous woods. We ran 10
5
repetitions foreach set of woodland types.
Results
The 30 Malaise traps captured a total of 1543 individualsand 60 species over the 4 weeks (see Table S3 in the sup-plementary material; the full data set is available fromP. J. Mayhew).
The species accumulation curve for all species (Fig. 1)and sites did not reach an asymptote. The accumula-tion curves for Diplazontinae and Poemeniinae (Fig. 1)reached an asymptote relatively rapidly, suggestingthat the results of analyses for these taxa were robust.For the Pimplinae the curve did not plateau after sam-pling at 15 woodlands (Fig. 1). Notably, the rank order
of species richness of pimplines and diplazontineschanged as more woods were sampled: if only a fewwoods were sampled, more diplazontine species werefound than pimplines. However, if many woods weresampled, more pimpline species were found than dipla-zontines (Fig. 1).
Woodlands differed in parasitoid abundance and rich-ness but different taxa were found to differ in the scaleof their response (Table 2). Preliminary analysis of datafor the pimpline tribes, Pimplini and Ephialtini, high-lighted differences between them, therefore separateanalyses were conducted for these taxa (only two indi-viduals of the third tribe, Delomeristini, were caught,therefore they were not considered separately). Wood-lands differed significantly in the abundance of allspecies combined and
Diacritus aciculatus
, and in theabundance and richness of the Pimplinae, Pimplini andPoemeniinae. For all species combined,
Diacritus acicu-latus
, the Pimplinae and Pimplini, woodland habitats(broadleaved or coniferous habitat) differed significantlyin parasitoid abundance and/or richness (Table 2). Nosignificant differences between woodlands or habitatwere found for the Diplazontinae and Ephialtini,although there were significant differences for parasitoid
Fig. 1. Species accumulation curves for all species (blackcircles), Diplazontinae species (white circles), Pimplinae species(inverted triangles) and Poemeniinae species (triangles)(means ± 95% confidence intervals).
Table 2.
Results of the mixed-model nested
s. Non-significant factors were sequentially removed from the initial model to leave only those factorsexplaining significant variation in the data. Habitat was a fixed effect, wood and trap were random effects. Wood(habitat) indicates that the factor woodis nested within the factor habitat. A non-significant result is signified as NS; *
abundance and richness between traps, within woodlands,for these taxa (Table 2). For all taxa, abundance andrichness varied significantly between weeks (Table 2).
Overall, the best indicators of a high parasitoid abun-dance, richness and diversity were tree/shrub speciesrichness and broadleaf content (Table 3 and Fig. 2).These habitat variables showed a consistently positiverelationship with parasitoid abundance, richness and1/
D
. Canopy cover was found to show a consistent neg-ative relationship with a number of parasitoid variables.The Diplazontinae were found to show little associa-tion with the vegetation.
Where selecting woodlands in order of priority basedon either their contribution to species richness or rarity,some coniferous woodlands and woodlands with lowspecies richness (e.g. NDPL and HAPL; see Table S3 inthe supplementary material) were included in the bestselection of five (Table 4). Only four runs of the reserveselection analysis were needed to ensure a set of wood-lands was attained that contained all the species ofDiplazontinae present in the data set (Table 4). Com-paring the performance of the reserve selection algo-rithm for species richness against the selection of fiverandom woodlands, the algorithm performed signifi-cantly better for each taxon (Table 5).
Table 3. Results of backwards stepwise regression. Parasitoid data used were those combined over the 4 trapping weeks and twotraps for each woodland. The values of the standardized coefficients (Beta) are given with the significance of the variables in thefinal model. Independent variables are listed in order of decreasing importance (measured by number of asterisks; ***P < 0·001,**P < 0·01, *P < 0·05)
Table 4. Results from reserve selection algorithms based on richness and rarity. Richness scores are the number of speciesconserved by the addition of that woodland. Rarity scores represent the sum of the values for all species present in the woodlandand not already represented in a previously selected woodland. Habitat categories for each woodland are given in parentheses;B, broadleaf; C, coniferous
Richness Rarity
All Score Pimplinae Score Diplazontinae Score All Score Pimplinae Score Diplazontinae Score
The mean (2·5 and 97·5 percentiles) number of spe-cies included in five randomly selected woods was 39·42(38, 41) if only coniferous woods were selected, 42·73(40, 46) if only deciduous woods were selected, and42·48 (38, 47) if there was no restriction on choice ofwoods. Both the best (50 parasitoid species) and worst(36 parasitoid species) selection of five woods weremixtures of broadleaved and coniferous woods.
Discussion
In this study woodlands were found to differ in theirparasitoid abundance and richness, but parasitoid taxawere found to differ in their response to habitat varia-bles. For certain taxa, tree/shrub species richness andbroadleaf content were identified as possible indicators
of high parasitoid abundance and diversity. However,the selection of woodlands that maximizes parasitoiddiversity at a landscape scale includes both deciduousand coniferous woods.
Despite the fact that parasitoids are always at least twotrophic levels above the vegetation, it appears that, forsome taxa at least, vegetation characteristics may pre-dict parasitoid abundance and diversity. This is impor-tant because it would generally be impractical to usethe hosts as indicators. Often we have little or no host–parasitoid information and the potential host range ofa single parasitoid species, let alone whole taxa, makessampling all hosts impractical.
In this study, although broadleaf content was foundto be a useful indicator of abundance and diversity insome taxa, tree/shrub species richness was found to bethe most important indicator of high parasitoid diver-sity. This result is in agreement with Sperber
et al
. (2004),who found an increase in the number of parasitoidfamilies with tree species richness, which was ascribedto an increased heterogeneity and availability of resources(Sperber
et al
. 2004). Sääksjärvi
et al
. (2006) also founda positive association between plant species richnessand ichneumonid species richness in Amazonian forest.There was no relationship in this study, or that of Sperber
et al
. (2004), to the species richness of the ground veg-etation. This is in contrast with results from croppingsystems (Risch 1979; Altieri 1984; Letourneau 1987) and
Fig. 2. Relationships between the abundance or richness of parasitoid taxa and woodland habitat variables. Lines are regressionsthrough the points shown.
Table 5. A comparison of species richness conserved throughthe selection of 5 woodlands by either a reserve selectionalgorithm or random selection
suggests that results from such simplified agriculturalsystems may not translate to more complex ecosystems.
Although this study was not designed to answerquestions regarding the biological mechanisms under-lying the resulting patterns, we can hypothesize as towhat they may be. Notably, those taxa whose abundanceand diversity differed between woodlands and whichwere associated with the vegetation, particularly thepimpline tribe Pimplini, are parasitoids of herbivores.The most abundant species of Pimplini caught inthis study were Pimpla insignatoria (Gravenhorst)(171 individuals captured), Pimpla contemplator (Müller)(142) and Pimpla flavicoxis Thomson (51). Together,these three species accounted for 67% of all thePimplinae sampled and 89% of all the Pimplini. All areparasitoids of macrolepidoptera and are thought to be,at least in part, arboreal (Fitton et al. 1988). Such hostassociations may to some extent be driving the patternswe see in the Pimplinae in relation to broadleaved hab-itats. Habitat characteristics appear less important forthe tribe Ephialtini, for which the host groups are morevaried and are often predators. These hosts are foundacross the orders Coleoptera, Hymenoptera, Dipteraand Arachnida (Fitton et al. 1988). Fraser (2005) con-ducted a second study using the same parasitoid taxa,trapping techniques and two of the same woodlandsused here, in 2004. Patterns of species abundance werefound to be consistent across 2003 and 2004 giving adegree of temporal robustness to our findings.
The abundance and diversity of Diplazontinae werenot significantly different between woodlands orassociated with woodland habitat characteristics, and thespecies accumulation curve (Fig. 1) suggests woodlandsare generally very similar in Diplazontine composition.The aphidophagous Syrphidae hosts (Fitton & Rotheray1982) are themselves already two trophic levels abovethe vegetation. Furthermore, adult syrphids are knownto be highly mobile. When evaluating the potential forSyrphidae as environmental indicators, Sommaggio(1999) suggested they are useful for assessing landscapediversity. It may be therefore that patterns in diplazontinediversity and community composition are also evidentat the landscape scale rather than the woodland scale.
These differences across parasitoid taxa suggest thefollowing hypothesis: the degree of association betweenparasitoid abundance and diversity and characteristicsof the vegetation within habitats will decrease with anincrease in the number of trophic links that separate them.Understanding the mechanisms driving associationsbetween habitat variables and patterns in wasp assem-blages may provide a basis for understanding factorsinfluencing the regulation of arthropod assemblages bywasps in the landscape (Lassau & Hochuli 2005).
The results of this study provide important implicationsfor sampling regimes designed to provide informationregarding parasitoid abundance and diversity. The
high variation between weeks for all taxa indicates thatany sampling regime must continue over several con-secutive weeks to account for this temporal variation inparasitoid communities. Also, as illustrated by the vari-ability between traps for the Diplazontinae, samples canvary at small spatial scales and therefore replication oftraps within a single habitat patch is necessary.
The species accumulation curve (Fig. 1) for thePimplinae shows no sign of an asymptote, in commonwith the findings of Sääksjärvi et al. (2004). Most ofthe additional species after nine woodlands are repre-sented by just single individuals, showing the typicallylong abundance ‘tail’ of rare species (Gaston & Blackburn2000). The 16 Pimplinae species that occur as singletonsin our samples were spread over 12 woodlands, sug-gesting that additional sampling would be unlikely toalter the overall patterns we have found. None the less,a more complete species list would require furthersampling of woodlands within the landscape.
This work has suggested that woodlands may play animportant role in the maintenance of biodiversity inagricultural landscapes. For the two larger subfamiliessampled, the Diplazontinae and Pimplinae, 38% and33%, respectively, of the entire UK species lists wererecorded in the 15 woodlands sampled. This is a highproportion in comparison with comparable Britishwoodland samples of other taxa, e.g. macrolepidoptera24% (Usher & Keiller 1998), birds 23% (Mason 2001),Syrphidae 20% and Carabidae 12% (Humphrey et al.1999). Woodland habitats provide parasitoids withresources, such as alternate hosts, food for adults,overwintering habitats and appropriate microclimates(van Emden 1965; Powell 1986; van Emden 1990; Dyer& Landis 1997), and enhance landscape complexity inagricultural landscapes, which has been shown toenhance diversity in other taxa in surrounding fields(Schmidt et al. 2005). A notable species that was foundin four of the farm woodlands in this study was thePimpline Zatypota albicoxa (Walker). Only four indi-viduals of this species have been found previously in theUK, in three localities. This parasitoid has been rearedfrom Achaearanea simulans (Thorell), a spider listedas nationally notable (www.britishspiders.org.uk,accessed 25 December 2004) and used as an ancientwoodland indicator (M. R. Shaw, personal communi-cation). Its presence suggests that farm woodlands canprovide small patches of high-quality habitat allowingwoodland species to persist in agricultural landscapes.
At the whole woodland scale, woodlands with highbroadleaf content and high tree/shrub species richnesswould appear to be most beneficial to taxa such as thePimplinae and Diacritinae. For the Diplazontinae, thetype of woodland would appear relatively unimportantat this scale. However, the optimal reserve selection offive woodlands from our list included both coniferouswoods and woods of low species richness, suggesting
that such woods can contribute to parasitoid diversityat the landscape scale. Selecting only coniferous wood-lands at random resulted in significantly lower averagespecies richness than only selecting deciduous wood-lands or selecting both types. Mixtures of both wood-land types on average were no worse or better than onlydeciduous woods, but could result in fewer species thanconiferous woods only or more species than deciduouswoods only. Clearly, care will also have to be taken withrespect to other habitat variables, such as tree speciesrichness, if parasitoid species richness at the landscapescale is to be maximized.
Acknowledgements
We are grateful to M. Shaw (Pimplinae, Poemeniinaeand Diacritinae), G. Rotheray (Diplazontinae) and E.Diller (Diplazontinae) for help with species identifica-tion, and H. Edwards and R. Shortridge for assistancewith fieldwork. We thank the many landowners forpermission to establish traps in their woodlands. Thiswork was funded by a Natural Environment ResearchCouncil studentship to S. E. M. Fraser.
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Received 12 December 2005; final copy received 15 November2006 Editor: Paul Giller
Supplementary material
The following supplementary material is available aspart of the online article (full text) from http://www.blackwell-synergy.com.
Table S1. Habitat variables measured.
Table S2. Plant architecture structures.
Table S3. Parasitoid abundance and richness per wood.
