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Tachinid (Diptera: ) Parasitoid Diversity and Temporal Abundance at a Single Site in the Northeastern United States Author(s): Diego J. Inclan and John O. Stireman, III Source: Annals of the Entomological Society of America, 104(2):287-296. Published By: Entomological Society of America https://doi.org/10.1603/AN10047 URL: http://www.bioone.org/doi/full/10.1603/AN10047

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. CONSERVATION BIOLOGY AND BIODIVERSITY Tachinid (Diptera: Tachinidae) Parasitoid Diversity and Temporal Abundance at a Single Site in the Northeastern United States

1 DIEGO J. INCLAN AND JOHN O. STIREMAN, III

Department of Biological Sciences, 3640 Colonel Glenn Highway, 235A, BH, Wright State University, Dayton, OH 45435

Ann. Entomol. Soc. Am. 104(2): 287Ð296 (2011); DOI: 10.1603/AN10047 ABSTRACT Although tachinids are one of the most diverse families of Diptera and represent the largest group of nonhymenopteran parasitoids, their local diversity and distribution patterns of most in the family are poorly known. In this study, 2 yr of samples from a Malaise trap were used to analyze the local richness and temporal distribution of a tachinid community in southwestern Ohio. In total, 883 tachinid specimens were collected, consisting of 117 species belonging to 69 genera. The majority of the specimens were collected in fall, followed by summer and spring, with 67, 22, and 11%, respectively. Estimated rarefaction curves indicate a predicted species richness of 217 species and suggest that we have sampled only a fraction of the diversity of Tachinidae occurring at this particular site. The species recorded in this study represent 16 and 19% of the species that are likely to occur in the northeastern United States and Ohio, respectively. In North America, there have been few, if any, previous attempts to quantify the diversity of tachinids on a local scale. Our results provide a baseline for understanding the temporal and spatial diversity of these ecologically and agronomically important parasitoids.

KEY WORDS Tachinidae, species richness, parasitoid diversity, temporal distribution, voltinism

Diptera or true ßies are one of the most anatomically There have been several recent studies focused on varied and ecologically diverse groups of . This species diversity and temporal distributions of tachin- group represents 10Ð15% of the worldÕs biodiversity ids in the Palaearctic region, such as Belshaw (1992, (Brown 2005, Yeates et al. 2007) and contains 1993, 1994), Ford and Shaw (1991), Ford et al. (2000), Ϸ157,000 described species (Thompson 2008). Esti- Avci and Kara (2002), Cerretti et al. (2004), and Rich- mates of the total diversity of Diptera suggest that this ter (2005), but there are few such studies for speciÞc order contains a minimum of 1,000,000 (Brown 2001b) areas of the Nearctic region (OÕHara 2002, Strazanac to 1,700,000 species (Stork 1997), suggesting that et al. 2001, Strazanac and Butler 2005, Tooker et al. Ͼ90% of Diptera species remain undescribed. In the 2006, Stireman 2008). Nearctic region, which probably has the best known In the Nearctic region, the family Tachinidae in- fauna after the Palearctic region, an estimated 65% of cludes 1,345 described species, classiÞed in 304 genera Diptera have been described, Ͻ25% have been revised of which 20% are endemic to the region (OÕHara taxonomically, and less than one percent have been 2008). In this region, there have been several studies studied in detail (Thompson 2009). Thus, document- of the tachinid parasitoid communities associated with ing and describing the diversity of Diptera represents particular host groups. For example, tachinids attack- a special need to Þll the large void in our knowledge ing Lepidoptera in Canada (McGugan 1958), northern of diversity. United States (Schaffner and Griswold 1934), eastern The parasitic ßy family Tachinidae includes United States (Strazanac et al. 2001), and southeastern Ϸ10,000 described species worldwide, classiÞed into Arizona (Stireman and Singer 2003). Similarly, coarse Ͼ1,500 genera (Brown 2001a,b; Irwin et al. 2003; information on the spatial distribution of tachinids can OÕHara 2008). Although tachinids are one of the most be gleaned from regional catalogs (e.g., OÕHara and species-rich families of Diptera (Irwin et al. 2003) and Wood 2004), but these provide little indication of the represent the largest group of nonhymenopteran para- richness of particular tachinid communities. To our sitoids (Belshaw 1994), the ecology of most species in knowledge, there is only a single published study the family is poorly known. Currently, our knowledge (Stireman 2008) documenting in detail the richness is limited in terms of the diversity and distribution of and composition of a tachinid community at a partic- populations across time and space, especially in the ular geographic locale in North America (although see Nearctic and Neotropical regions (Stireman 2008). Strazanac and Butler (2005) for an multiyear analysis of the abundance of macrolepidoptera attacking Ta- 1 Corresponding author, e-mail: [email protected]. chinidae). This is unfortunate given the diversity of

0013-8746/11/0287Ð0296$04.00/0 ᭧ 2011 Entomological Society of America 288 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 104, no. 2 this group and their importance as parasitoids of other [Lonicera maackii (Rupr.) Maxim.]. The trap was insects (Stireman et al. 2006). Because tachinids be- monitored from 25 June until 17 November in 2008 and long to a higher trophic level, they may serve as sen- on 4 March until 12 November in 2009. It was peri- sitive indicators of the diversity and dynamics of pop- odically checked, once or twice per week, for the 2008 ulations of their host taxa. An understanding of how and 2009 seasons. Potassium cyanide was used as the tachinid communities vary over space and time can be killing agent in a dry trap head. Material collected in used as a proxy for understanding diversity patterns of the trap was taken to a laboratory at Wright State other insects, particularly Lepidoptera (Stireman et al. University, Dayton, OH, where specimens were 2006). Such information could provide an indication sorted, pinned, and identiÞed. of the health of ecological communities and poten- Identification. Tachinid specimens were initially tially inform local conservation efforts. Similarly, doc- sorted by morpho-species and then identiÞed to umenting occurrence/abundance patterns over time using the key to Nearctic genera of Tachinidae by can provide insight into tachinid life history, voltinism Wood (1987). Once the genus was identiÞed, species and developmental time, and potential host associa- identiÞcations were attempted using keys and descrip- tions, which could be used to assess their potential for tions from primary literature. Species designations biological control in forest and agricultural systems. were further reÞned or conÞrmed by comparison with Unfortunately, tachinids are a difÞcult group to iden- type or paratype specimens housed in the National tify, due in part to their great richness and diversity Museum of Natural History (NMNH) in Washington, and the incomplete taxonomic literature available for DC; the Canadian National Collection (CNC) in Ot- the identiÞcation of species. This remains an imped- tawa, ON, Canada; or both. For some particularly iment to their study and use as ecological indicators. difÞcult taxa (e.g., Townsend, Myopharus Here, we document and analyze the tachinid spe- Brauer & Bergenstamm, and Robineau- cies richness obtained from a single trap over two Desvoidy), Þnal identiÞcations were made with the seasons and assess the temporal distribution of aid of Dr. D. M. Wood (Agriculture and Agri-Food abundance and voltinism of the tachinid commu- Canada). nity. This information provides a point estimate for Analysis. Estimated species accumulation curves understanding the geographic distribution of ta- (rarefaction curves) were calculated for sample and chinid diversity and potentially the diversity of their specimen accumulation. The 2008Ð2009 rarefaction host taxa. We also examine how tachinid abundance curve of samples and its 95% CL was calculated and and diversity varies seasonally and examine the phe- plotted using 1,000 permutations with the function nological patterns of a broad array of tachinid spe- “specaccum” from the vegan package (Oksanen et al. cies. Several new geographic records of Tachinidae 2007). Rarefaction curves using samples for individual also are documented. years were calculated using 1,000 randomizations with the function “spp.est” from the fossil package in R (Vavrek 2009). Similarly, rarefaction curves of spec- Materials and Methods imens for 2008Ð2009, and individual years were cal- Collection. Tachinid specimens were collected in culated and plotted using 1,000 randomizations. Sim- a single 2.5- by 1.8-m white mesh Townes style ilarity indices between years were estimated with Malaise trap located in Greene County, southwest- Sorensen binary coefÞcients, which compute the sim- ern Ohio, in the Huffman Metropark (39Њ48Ј27.91Љ N, ilarity of two samples based on presentÐabsence of 84Њ05Ј35.58ЉW, Ϸ250 m in elevation). This Ϸ114-ha species (Southwood and Henderson 2000). Finally, largely undeveloped park is surrounded by suburban we used fossil package to estimate ACE, ICE, Chao-1, development, Wright-Patterson Air Force Base, and Chao-2, and Jack-1 species richness estimators for some intensive cornÐsoybean [Zea mays L.ÐGycine sample-based and specimen-based species accumula- max (L.) Merr.[rqb] agriculture. However, it is con- tion, and their 95% CL based on 1,000 randomizations nected to other seminatural wooded and prairie areas (Vavrek 2009). through riparian forest along the Mad River, which We used a multivariate analysis with nonmetric ßows through the park. The trap was placed adjacent dimensional scaling (NMDS) of sampling dates and and perpendicular to the forest edge on the northwest species to explore patterns in species composition side of an Ϸ10-m-wide NWÐSE-oriented narrow grass- over time. An advantage of NMDS is that the proce- and forb-dominated Þeld in a powerline right-of-way. dure is less dependent on data distribution than con- This Þeld is periodically mowed every one to two strained methods, such as principal component anal- years. Sampling this “edge” habitat is likely to maxi- yses (Hochkirch and Adorf 2007). Increasing distance mize total richness and diversity because it draws between sites in NMDS ordination space is indicative tachinids from both open and forest-associated com- of greater compositional dissimilarity. We calculated munities. The plant community in the immediate vi- the NMDS using the function “metaMDS” in the sta- cinity of the trap was dominated primarily by Aster- tistical package vegan in R (Oksanen et al. 2007). In aceae (e.g., Solidago spp., Symphyotrichum spp.) and vegan, metaMDS Þrst transforms the data by Wiscon- Poaceae (e.g., Sorghastrum nutans Nash). The narrow sin double standardization, a method which Þrst stan- Þeld was bordered by second growth deciduous forest dardizes species and subsequently the samples by to- consisting largely of maples (Acer spp.), ashes (Fraxi- tals (Faith et al. 1987, Minchin 1987). We used BrayÐ nus spp.), hickory (Carya spp.), and honeysuckle Curtis dissimilarities as a measure of ecological March 2011 INCLAN AND STIREMAN:TACHINID DIVERSITY IN NORTHEASTERN UNITED STATES 289 distance. Weekly or semiweekly samples were pooled perhaps more specialized, species. However, the high into larger samples representing specimens collected number of rare species is probably due in part to the Þrst and second half of each month. To evaluate insufÞcient seasonal and spatial replication of sam- variation in the community, we analyzed variation pling and that many tachinid species may not be ef- between years, seasons, and the interactions between Þciently sampled with the method used. seasons and years by using canonical correspondence At least two species appear to be undescribed; one analysis (CCA) in the R vegan package (Ter Braak species of Rondani, which has been col- 1986, Oksanen et al. 2007). To assess whether tachinid lected previously but never described, and a unique communities differed signiÞcantly between seasons species of Rondani, close to P. aristalis. and years, we performed a signiÞcance test of con- In addition, deÞnitive identiÞcations of seven addi- straints on the CCA ordination (essentially a multi- tional species could not be made despite external variate analysis of variance [ANOVA]) with 500 per- comparison to reliably identiÞed museum specimens. mutations using the function “anova.cca” (Oksanen et These species include three Riboneau-Des- al. 2007). voidy species, one close to C. flavirostris, one close to To evaluate the species observed in this study in a C. falenaria, and one close to C. lagoae; two regional context, we used distributional information Townsend species; a Lixophaga Townsend species; from the “Tachinidae of America north of Mexico” and a species of Brauer & Bergenstamm. regional catalog (OÕHara and Wood 2004). We used This reßects in part lack of suitable material and a need this information to assess the proportion of species for revision of these groups, but some of these, par- present in the entire Nearctic region and the north- ticularly the latter four blondeliine taxa, may repre- eastern United States that we sampled. In addition, we sent additional undescribed species. We found new compared our observed species with the species that locality records for Þve species ( badiceps, are likely to occur speciÞcally in Ohio. To estimate the Billea trivittata, Catharosia minuta, species that are likely to be present in Ohio, we esti- nana, and trudis; see Table 1 for authority mated a rough distributional polygon from the loca- names), which have not previously been recorded tions reported for each species listed in OÕHara and from the northeastern region of America north of WoodÕs (2004) tachinid regional catalog; if the poly- Mexico. In addition, we found new locality records for gon of the species included Ohio, we recorded that two species (Chaetostigmoptera manca and Cylindro- species as present in Ohio. Cases where species were myia interrupta) that have not been recorded from found only in neighboring states or provinces were Ohio (OÕHara and Wood 2004). considered equivocal. This list of potential Ohio spe- The species recorded in this study represent 9 and cies is included as Supp Table S1 [online only]. 23% of all species and genera of Tachinidae described for the Nearctic region, respectively (OÕHara 2008). The Catalog of the Tachinidae (Diptera) of America Results and Discussion North of Mexico by OÕHara and Wood (2004), reports Richness and Composition of Tachinid Taxa. From 649 species in total occurring in the northeastern re- June 2008 to November 2009, in 399 d of sampling, 883 gion, of which 16% were recorded in this study. Spe- tachinid specimens in total were collected, consisting ciÞcally for Ohio, the recorded species in this study of 117 species belonging to 69 genera (see Table 1 for represent 19% of the 547 species that are likely to a complete list of species and genera). We collected occur in Ohio (Supp Table S1 [online only]). 390 specimens classiÞed into 79 species in 2008 and 493 Species Richness Analyses. Estimated rarefaction specimens classiÞed into 82 species in 2009. The sub- curves using both samples (Fig. 2) and specimens families and were the best rep- (Fig. 3) all end with a fairly steep slope, suggesting that resented in samples, comprising 54% (63 species, 34 we have sampled only a fraction of the species of genera, and six tribes) and 21% (25 species, 16 genera, Tachinidae occurring at this particular site. The spec- and 10 tribes) of the total species, respectively. The imen-based Chao-1 estimator of total species richness subfamilies and comprised less predicts that the community of Tachinidae in the than one third of the species with 13% (15 species, sampled area consists of Ϸ205 species (95% CI, 192Ð eight genera, and six tribes) and 12% (14 species, 11 217; Table 2). Similarly, the sample-based Chao-1 es- genera, and Þve tribes) of the total species, respec- timator predicts that the community of Tachinidae in tively (Table 1). Fewer than 50% of the species were the sampled area consists of Ϸ190 species, (95% CI, shared between years. Thirty-Þve species were only 179Ð201; Table 2). Jack-1 species richness estimator found in 2008, and 38 were only found in 2009. Of the resulted in similar estimates (Table 1). These estima- 117 species identiÞed, 36% were represented by only tors indicate that with sufÞcient effort we could po- a single specimen, 20% were represented by two spec- tentially sample over one third of tachinid species imens, and only 20% were well represented by Ն10 likely to occur in Ohio with this single trap. specimens (Fig. 1). The species abundance distribu- It is difÞcult to determine whether the community tion indicates that rare species represent approxi- we have sampled is more or less diverse than other mately two thirds of the species recorded in this stud- areas in North America, because there have been few ied (Fig. 1). This large proportion of rare species may if any previous attempts to quantify the local species reßect transient tachinids that mostly use other hab- richness of tachinids. The only published analysis of a itats (e.g., forest), or they could represent truly rare, community of tachinid ßies in the Nearctic region that 290 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 104, no. 2

Table 1. Tachinid species and their seasonality distribution over summer 2008 to fall 2009, Huffman Metropark, OH

Season Subfamily/tribe/genus ESP MSP LSP ES MS LS EF MF LF Total Mar. April May June July Aug. Sept. Oct. Nov. 2 1 2 1 2 1 2 1 2 1 2 1 2 1 2 1 Dexiinae Campylochetini Campylochaeta plathypenae 112 (Sabrosky) Dexiini Billea trivittata (Curran) 1 Zelia tricolor (Coquillet) 3 Epigrimyiini Epigrimyia polita Twn.* 5 Thelairini Spathidexia cerussata Reinhard 2 Spathidexia clemonsi Twn.* 1 Spathidexia dunningii (Coquillet) 11 Thelaira americana Brooks 5 Blepharomyia tibialis (Curran) 1 Eulasiona aperta (Reinhard) 21 Eulasiona cinerea (Curran) 6 Kirbya setosa (Twn.*) 7 Periscepsia laevigata (van der Wulp) 2 Voria aurifrons (Twn.*) 1 Exoristinae Admontia badiceps Reinhard 35 Admontia degeerioides (Coquillet) 2 eufitchiae (Twn.*) 4 Blondelia hyphantriae (Tothill) 7 diabroticae (Shimer) 12 Chaetostigmoptera manca (Greene) 10 theutis (Walker) 3 Eucelatoria dimmocki (Aldrich) 8 Eucelatoria sp. 1 1 Eucelatoria sp. 2 1 Euhalidaya genalis (Coquillet) 1 Euthelyconychia xylota (Curran) 10 Lixophaga discalis (Coquillet) 23 Lixophaga fasciata Curran 12 Lixophaga plumbea Aldrich 3 Lixophaga sp. 1 1 Lixophaga variabilis (Coquillet) 7 barbata (Coquillet) 22 Medina quinteri (Twn.*) 28 (Riley) 2 Myiopharus infernalis (Twn.*) 1 Myiopharus macellus (Reinhard) 1 Myiopharus sp. nr. ancilla (Walker) 2 Opsomeigenia pusilla (Coquillet) 1 Oxynops anthracinus (Bigot) 19 Thelairodoria setinervis (Coquillet) 1 leibyi (Twn.*) 9

Continued on following page we know of analyzed the richness and seasonal diver- suggesting a richer tachinid community at our site in sity of tachinids in an upland savanna in southeastern Ohio. However, the number of species collected per Arizona (Stireman 2008). In this study, Stireman year is quite similar across these studies (i.e., Ϸ80). (2008) recorded a community of 79 species with an The similarity of these two communities, as calculated estimated total of 122 species from eight monthly pan with the Sorensen index, is 16%. This low similarity is trap samples. We recorded a community of 117 species not surprising given the vast distance between these with an estimated total of 179Ð217 species (Table 1), two sampling points, the large difference in the veg- March 2011 INCLAN AND STIREMAN:TACHINID DIVERSITY IN NORTHEASTERN UNITED STATES 291

Table 1. Continued

Season Subfamily/tribe/genus ESP MSP LSP ES MS LS EF MF LF Total Mar. April May June July Aug. Sept. Oct. Nov. 2 1 2 1 2 1 2 1 2 1 2 1 2 1 2 1 theclarum (Scudder) 30 Carcelia reclinata (A. & W.**) 1 Carcelia laxifrons Villenueve 1 Carcelia sp. nr. flavirostris (Wulp) 1 Carcelia sp. nr. falenaria (Rondani) 4 Carcelia sp. nr. lagoae (Twn.*) 1 rhoeo (Walker) 1 aletiae (Riley) 6 Lespesia cuculliae (Webber) 1 Lespesia flavifrons Beneway 3 Lespesia schizurae (Twn.*) 1 Lespesia stonei Sabrosky 1 radicis (Twn.*) 1 erecta (Coquillet) 2 Nilea valens (A. & W.**) 2 curriei (Coquillet) 1 crassiseta (A. & W.**) 1 phyciodis (Coquillet) 12 claripennis (Macquart) 1 Exorista dydas (Walker) 2 Exorista trudis (Reinhard) 2 unifasciata (R.-D.***) 28 Blepharipa n. sp. 1 analis (van der Wulp) 1 aldrichi Tothill 23 sternalis (Coquillet) 1 virilis (A. & W.** ) 1 bicolor (Macquart) 2 Leschenaultia reinhardi T. & G.**** 1 Masiphyini confusa Aldrich 23 pyste (Walker) 1 Winthemia quadripustulata (F.) 5

Winthemia manducae S. & DeL.***** 3 Winthemia occidentis Reinhard 1 Winthemia rufopicta (Bigot) 5 Winthemia sinuata Reinhard 10 Phasiinae Catharosiini Catharosia minuta (Twn.*) 21 Catharosia nebulosa (Coquillet) 5 Cylindromyia binotata (Bigot) 5 Cylindromyia euchenor (Walker) 14 Cylindromyia fumipennis (Bigot) 4 (Meigen) 2 Cylindromyia nana (Twn.*) 2 aurata R.-D.*** 1 Gymnosomatini immaculata (Macquart) 4 Gymnoclytia occiuda (Walker) 1 par Walker 8

Continued on following page 292 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 104, no. 2

Table 1. Continued

Season Subfamily/tribe/genus ESP MSP LSP ES MS LS EF MF LF Total Mar. April May June July Aug. Sept. Oct. Nov. 2 1 2 1 2 1 2 1 2 1 2 1 2 1 2 1 Leucostonatini Leucostoma gravipes van der Wulp 2 punctigera (Twn.*) 1 Phasia purpurascens (Twn.*) 1 Trichopodini Xanthomelanodes arcuatus (Say) 13 Tachininae Acemyini dentata (Coquillet) 29 comta (Fallen) 2 Graphogastrini Phytomyptera longicornis (Coquillet) 1 Phytomyptera sp. nr. aristalis (Twn.*) 1 Phytomyptera palpigera (Coquillet) 2 turmalis (Reinhard) 2

Genea pavonacea (Reinhard) 122

Minthoini affinis Reinhard 1 Paradidyma conica (Twn.*) 1 Paradidyma petiolata Reinhard 4 Paradidyma singularis (Twn.*) 9 Myiophasiini inaequipes Bigot 1 Gnadochaeta metallica (Twn.*) 1 Gnadochaeta nigrifrons (Twn.*) 2 johnsoni Coquillet 2 americana (Twn.*) 2 autumnalis (Twn.*) 3 Actia interrupta Curran 6 Actia rufescens (Greene) 2 illinoensis Twn.* 2 or cristata (Fabricius) Strongygastrini Strongygaster triangulifera (Loew) 8 apicifer (Walker) 2 Archytas nivalis Curran 1 ruficauda (van der Wulp) 2 Deopalpus hirsutus Twn.* 6

Total 883

3 8143224314921724

Shown are the bars from the log base 2 of the total individuals plus 1; thus 1, 2, 3, 4, 5, and 6 bars represent 1, 2, 5, 11, 22, and 45 specimens, respectively. Seasonality is indicated by ESP, early spring (Mar.); MSP, middle spring (April); LSP, late spring (May); ES, early summer (Jun); MS, middle summer (Jul); LS, late summer (Aug); EF, fall (Sept.); MF, middle fall (Oct.); and LF, late fall (Nov). The number 1 represents the Þrst fortnight and number 2 the second fortnight of each month. *Twn., Townsend; **A. & W., Aldrich & Webber; ***R.-D., Robineau- Desvoidy; ****T. & G., Toma & Guimares; and *****S. & DeL., Sabrosky & DeLoach. etative community, and the different methods of sam- eight malaise traps over 6 mo and found that grass and pling (pan versus Malaise trap). shrub habitats exhibit the richest communities, with There have been a few studies of tachinid commu- Ͼ50 species (over two traps). This is less than half of nities conducted in the Paleartic region, and despite the total species that we recovered with comparable the region and methodological differences, some com- sampling effort in terms of trap-days. However, the parisons can be made with these studies. Belshaw expected difference in species richness of these sam- (1992) sampled four different habitats in England with ples when rareÞed to 51 specimens is much smaller (23 March 2011 INCLAN AND STIREMAN:TACHINID DIVERSITY IN NORTHEASTERN UNITED STATES 293

Fig. 1. Rank-abundance of tachinid species sampled in this study. The x-axis is the log base two of the specimens abundance plus 1.

Belshaw versus 29 current expected species). In Italy, ordination plot was selected after seven tries (Fig. 4). Cerretti et al. (2004) sampled two different habitats, The stress obtained for this dimensionality was 20, ground versus canopy forest, with four malaise traps suggesting that not too much conÞdence should be for a period of 7 mo and found a total of 41 species (30 placed on the details of the plot (McCune and Grace species only in ground traps, Þve exclusively in the 2002). However, clear separation of dates in the canopy, and seven in both habitats). Here, we found NMDS plot (Fig. 4) suggests that the sampled tachinid approximately double this number of species, in each fauna consists of relatively distinct seasonal commu- year, with only one trap. These comparisons suggest a nities as has been found in many other insect groups, signiÞcantly richer fauna at our forest edge site in Ohio including potential tachinid hosts (e.g., Summerville than in these Palearctic sites; however, such compar- and Crist 2003). Spring dates are located at the bottom isons must be treated with caution due to differences left corner, summer dates are at the center top, and fall in habitat and sampling procedures. dates are clustered at the right corner of the plot. The Temporal Distribution. A two-dimensional Þnal so- CCA of the seasonal patterns observed in the NMDS lution was selected for the NMDS. The best species plot was statistically signiÞcant (P ϭ 0.01; Table 3), indicating that the composition of the tachinid com- munity clearly varies over the season. Similarly, year and its interaction with season were statistically sig- niÞcant (P ϭ 0.03; Table 3), indicating substantial

Fig. 2. Accumulation curves of tachinid species against the number of samples. The gray polygon is the species Fig. 3. Accumulation curves of tachinids species against richness for 2008 ϩ 2009 with the species richness accumu- specimen number. (Top) Species richness accumulation for lation in the center Ϯ 95% CI. Circles and diamonds are the 2008 ϩ 2009. (Bottom) Thick and thin curves are the species species richness accumulation curves for 2008 and 2009, re- richness accumulation for 2008 and 2009, respectively. spectively. Curves are based on 1,000 randomizations. Curves are based on 1,000 randomizations. 294 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 104, no. 2

Table 2. Estimates of total species richness of the tachinid community by specimens and samples for 2008–2009, 2008, and 2009, based on 1,000 randomizations

2008/2009 2008 2009 Estimator by specimens by samples by specimens by samples by specimens by samples No. of observations 883 64 390 31 493 33 Species observed 117 117 80 80 82 82 Chao1 190 205 152 190 126 129 Chao1(lowerÐupper) 179Ð201 192Ð217 139Ð165 172Ð209 115Ð139 117Ð141 Jack1 185 191 134 141 118 121 Jack1(lowerÐupper) 185Ð189 191Ð195 134Ð137 141Ð144 118Ð122 121Ð126 differences in the species composition among years. Cylindromyia fumipennis, Gymnoclytia immaculata, The majority of the specimens were collected in fall, Lespesia flavifrons, Lixophaga discalis, Lixophaga followed by summer and spring, with 67, 22, and 11%, plumbea, Lixophaga variabilis, Periscepsia laevigata, respectively. The relatively low coefÞcient of similar- Phytomyptera palpigera, Vibrissina leibyi, Winthemia ity between 2008 and 2009 (Sorensen index, 55%), sinuata, and Zelia tricolor exhibit a bivoltine distribu- conÞrms the large differences in communities be- tion (Table 1, authority names given only in table). tween years. Conversely, many species were recovered in only a Variation in temporal abundance and seasonality single sampling period or across two neighboring sam- may be explained by ecological characteristics such as pling periods. Many of these have low sample size, species life cycle, voltinism, and seasonal ßuctuations making it difÞcult to assess true voltinism. But univoltine of available hosts. For example, species that were life cycles are strongly suggested for those species for found in multiple, disparate seasons are likely to com- plete several generations per year. SpeciÞcally, Aplo- which appreciable numbers of individuals were obtained mya theclarum, Belvosia unifasciata, Blondelia (e.g., Þve or more) only over a narrow sampling period. eufitchiae, Campylochaeta plathypenae, Celatoria dia- Such taxa include Actia interrupta, Admontia badiceps, broticae, Chaetostigmoptera manca, Cylindromyia Catharosia minuta, Epigrimyia polita, Eulasiona aperta, binotata, Medina barbata, Medina quinteri, Oxynops Eulasiona cinerea, Euthelyconychia xylota, pavona- anthracinus, Siphosturmia phyciodis, Spathidexia dun- cea, Gonia aldrichi, Gymnosoma par, Kirbya setosa, Lespe- ningii, and Thelaira americana are likely to be multi- sia aletiae, Lixophaga fasciata, Masiphya confusa, Para- voltine (Table 1, authority names given only in table). didyma singularis, Strongygaster triangulifera, Winthemia Similarly, the species Blondelia hyphantriae, Cathar- quadripustulata, and Xanthomelanodes arcuatus (Table 1, osia nebulosa, Ceracia dentata, Cylindromyia euchenor, authority names given only in table).

Fig. 4. NMDS ordination plot showing samples dates and points (yellow) for species. The number after month summarizes the collection dates on the (1) Þrst half or the (2) second half of the month. Polygons group spring, summer, and fall seasons. March 2011 INCLAN AND STIREMAN:TACHINID DIVERSITY IN NORTHEASTERN UNITED STATES 295

Table 3. Permutation test for canonical correspondence analysis intensive agriculture. The species recorded in this study represent 16 and 19% of the species that are Response df FPlikely to occur in the northeastern United States and Season 2 1.8836 0.01** Ohio, respectively. The sampled species likely repre- Yr 1 1.2693 0.03** sent only a fraction of the total tachinid community in Season ϫ yr 1 1.3526 0.03** Residuals 20 the park and surrounding area. Our primary goal in initiating this study was to provide For each response, 100 permutations were calculated. a point estimate of tachinid species richness in eastern ** Groups are statistically different. North America that can provide some comparative con- text for future studies of Tachinidae. To our knowledge, this study represents the Þrst documented attempt to The signiÞcant effect of season in analyses of the quantify the richness of a tachinid community in the community composition of tachinids in our samples northeastern United States. Despite our limited sam- can be easily understood by noting that many species pling, these results can be used as a baseline for under- were restricted to speciÞc seasons. For example, Cryp- standing the temporal and spatial patterns of diversity of tomeigenia theutis and Gonia aldrichi were found only tachinid communities. We do not know, for example, in spring; Actia interrupta, Eucelatoria dimmocki, Kir- how rapidly tachinid communities turn over with dis- bya setosa, and Masiphya confusa were found only in tance, or how they change with increasing habitat frag- summer; and Actia autumnalis, Admontia badiceps, mentation. Additional data of the sort we have gathered Epigrimyia polita, Eulasiona cincera, Lixophaga fas- here from other habitats and regions can be used to ciata, Paradidyma singularis, Strongygaster triangu- address these and other questions. However, to have a lifera, Winthemia quadripustulata, and Xanthomelan- more complete picture of particular tachinid communi- odes arcuatus were found only in fall (Table 1, ties and understand patterns of spatialÐtemporal distri- authority names given only in table). Several of the bution and their relationship to voltinism, seasonal ßuc- presumed bivoltine species were also seasonally re- tuations of available hosts, and weather conditions, a stricted: Ceracia dentata and Cylindromyia euchenor broader sampling period and additional replicate traps exhibited split distributions over spring and fall, and will be needed. Trapping in other nearby habitats (e.g., Blondelia hyphantriae, Catharosia nebulosa, Lixophaga forest interior and canopy, see Cerretti et al. 2004; Stire- discalis, Winthemia sinuata, and Vibrissina leibyi were man 2008), may provide valuable information on the absent from the spring samples (Table 1, authority habitat speciÞcity of the tachinid community and the names given only in table). Our inferences concerning effect of habitat structure on their seasonal patterns of voltinism and seasonality are preliminary as some of abundance and diversity. these patterns also could reßect changes in host sea- sonality and in habitat use (e.g., attraction to ßoral resources), and must be interpreted with caution. Acknowledgments The signiÞcant difference in community composition We thank all those who, in various ways, made this work among years is probably due to three primary factors. possible. Jim OÕHara, Monty Wood (Invertebrate Biodiver- First, there is probably a great deal of sampling error sity, Agriculture and Agri-Food Canada) and Norm Woodley given that we sampled with a single Malaise trap. Many (Systematic Entomology Laboratory, NMNH) provided ex- taxa were represented by just one or a few individuals as pertise and training in tachinid identiÞcation. Five-Rivers is typical for sampling studies of insects (Coddington et Metroparks of Dayton provided permission to sample Ta- al. 2009), so we would expect differences among years chinidae at Huffman Metropark. Jeremy Heath for assistance solely due to chance. Second, the weather conditions with the Malaise trap, and Hilary Devlin helped to review this manuscript. This study was made possible through support by differed between years. In general, the average temper- Њ National Science Foundation grant DEB 0717092 (to J.O.S.), ature in spring was higher 2009 than 2008 (11.8 and 9.6 C, a Biology Award for Research Excellence from the Depart- respectively), whereas the average temperature for sum- ment of Biological Sciences at Wright State University, and mer was higher in 2008 than 2009 (22.3 and 21.4ЊC, a Dipterology fund award from the North American Dipter- respectively) (NCDC 2010). These changes in temper- ists Society (to D.J.I.). ature might have an effect on temporal distribution of tachinids and their host. Third, each of the species that we collected probably undergoes natural year-to-year References Cited population ßuctuations that are dependent on popula- Avci, M., and K. Kara. 2002. Tachinidae parasitoids of Trau- tion dynamics of their hosts, their enemies, and weather matocampa ispartaensis from Turkey. Phytoparasitica 30: events, leading to a high degree of variation in relative 361Ð364. abundances from year to year. Belshaw, R. 1992. Tachinid (Diptera) assemblages in habi- In conclusion, the current study documents the tats of a secondary succession in southern Britain. Ento- richness and seasonal abundance of a community of mologist 111: 151Ð161. Belshaw, R. 1993. Malaise traps and Tachinidae (Diptera): tachinids in the southwestern Ohio. Both the observed a study of sampling efÞciency. Entomologist 112: 49Ð54. and predicted species richness indicates the presence Belshaw, R. 1994. Life history characteristics of Tachinidae of a highly diverse tachinid fauna at this site, despite (Diptera) and their effect on polyphagy, pp. 145Ð162. In B. the “island-like” nature of the park it was located in, Hawkins and W. Sheehan [eds.], Parasitoid community which is largely surrounded by development and/or ecology. Oxford University Press, Oxford, United Kingdom. 296 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 104, no. 2

Brown, B. V. 2001a. , gnats, and mosquitoes. 815Ð826p. northeastern part of the United States. U.S. Dep. Agric. In S. A. Levin [ed.], Encyclopedia of biodiversity, vol. 2. Misc. Publ. 188. Academic, London, United Kingdom. Southwood, T. R., and P. A. Henderson. 2000. Ecological Brown, B. V. 2001b. Insects, overview, pp. 479Ð484. In S. A. methods, 3rd ed. Blackwell Publishing, Boston, MA. Levin [ed.], Encyclopedia of biodiversity, vol. 3. Aca- Stireman, J. O. 2008. ␣ and ␤ Diversity of a tachinid para- demic, London, United Kingdom. sitoid community over space and time. Ann. Entomol. Brown, B. V. 2005. Malaise trap catches and the crisis in Soc. Am. 101: 362Ð370. Neotropical dipterology. Am. Entomol. 51: 180Ð183. Stireman, J. O., J. E. O’Hara, and D. M. Wood. 2006. Be- Cerretti, P., D. Whitmore, F. Mason, and A. Taglianti. 2004. havior, ecology and evolution of tachinid parasitoids. Survey on the spatio-temporal distribution of tachinid Annu. Rev. Entomol. 51: 525Ð555. ßiesÐusing Malaise traps (Diptera, Tachinidae), pp. 229Ð Stireman, J. O., and M. S. Singer. 2003. Determinants of 256. In P. Cerretti, S. Hardersen, F. Mason, G. Nardi, M. parasitoid-host associations: insights from a natural ta- Tisato, and M. Zapparoli [eds.], Invertebrati di una chinid-lepidopteran community. Ecology 84: 296Ð310. foresta della Pianura Padana, Bosco della Fontana. Sec- Stork, N. E. 1997. Measuring global biodiversity and its de- ondo contributo. Conservazione Habitat Invertebrati, 3. cline, pp. 41Ð68. In M. L. Reaka-Kudla, D. E. Wilson, and Cierre GraÞca Editore, Verona, Italy. E. O. Wilson [eds.], Biodiversity II: understanding and Coddington, J. A., I. Agnarsson, J. A. Miller, M. Kuntner, and protecting our biological resources. Joseph Henry Press, G. Hormiga. 2009. Undersampling bias: the null hypoth- Washington, DC. esis for singleton species in tropical surveys. J. Strazanac, J. S. and L. Butler [eds.]. 2005. Long term eval- Anim. Ecol. 78: 573Ð584. uation of the effects of Bacillus thuringiensis kurstaki, Faith, P., R. Minchin, and L. Belbin. 1987. Compositional ᭨ gypsy moth nucleopolyhedrosis virus product Gypchek , dissimilarity as a robust measure of ecological distance. and maimaiga on nontarget organisms in Vegetatio 69: 57Ð68. mixed broadleaf-pine forests in the central Appalachians. Ford, T. H., and M. R. Shaw. 1991. Host records of some U.S. Dep. Agric., Forest Health Technology Enterprise West Palearctic Tachinidae (Diptera). Entomol. Rec. J. Team Report. FHTET-2004-14. Var. 103: 23Ð38. Ford, T. H., M. R. Shaw, and D. M. Robertson. 2000. Further Strazanac, J. S., C. D. Plaugher, T. R. Petrice, and L. Butler. host records of some West Palearctic Tachinidae (Dip- 2001. New Tachinidae (Diptera) host records of eastern tera). Entomol. Rec. J. Var. 112: 25Ð36. North American forest canopy Lepidoptera: baseline data Hochkirch, A., and F. Adorf. 2007. Effects of prescribed in a Bacillus thuriengiensis variety kurstaki nontarget burning and wildÞres on Orthoptera in central European study. J. Econ. Entomol. 94: 1128Ð1134. peat bogs. Environ. Conserv. 34: 225Ð235. Summerville, K. S., and T. O. Crist. 2003. Determinants of Irwin, M. E., E. I. Schilinger, and F. C. Thompson. 2003. lepidopteran community composition and species diver- Diptera, true ßies, pp. 692Ð702. In S. M. Goodman and J. P. sity and community composition in eastern deciduous Benstead [eds.], The natural history of Madagascar. Uni- forests: roles of season, ecoregion, and patch size. Oikos versity of Chicago Press, Chicago, IL. 100: 134Ð148. McCune, B., and J. B. Grace. 2002. Analysis of ecological com- Ter Braak, F. 1986. Canonical correspondence analysis: a munities. MjM Software Design, Gleneden Beach, OR. new eigenvector technique for multivariate direct gradi- McGugan, B. M. 1958. The Canadian forest insect survey. In ent analysis. Ecology 67: 1167Ð1179. Proceedings of the Tenth International Congress of En- Thompson, F. C. [ed.]. 2008. Biosystematic database of tomology. 4: 219Ð232. world Diptera. (http://www.sel.barc.usda.gov/Diptera/ Minchin, R. 1987. An evaluation of relative robustness of biosys.htm). techniques for ecological ordinations. Vegetatio 69: 89Ð107. Thompson, F. C. 2009. Neartic Diptera: twenty years later, [NCDC] National Climatic Data Center. 2010. Southwest pp. 3Ð46. In T. Pape, D. Bickel, and R. Meier [eds.], Ohio local temperature. (www.ncdc.noaa.gov/oa/climate/ Diptera diversity: status, challenges and tools. Koninkli- onlineprod/drought/ftppage.html). jke Brill, Leiden, The Netherlands. O’Hara, J. E. 2002. Spring collecting in the Sonoran desert. Tooker, J. F., M. Hauser, and L. M. Hanks. 2006. Floral host Tachinid Times 15: 3Ð4. plants of Syrphidae and Tachinidae (Diptera) of central O’Hara, J. E. 2008. World genera of the Tachinidae (Diptera) Illinois. Ann. Entomol. Soc. Am. 99: 96Ð112. and their regional occurrence. Version 4.0. (http://www. Wood, D. M. 1987. Chapter 110: Tachinidae, pp. 1193Ð1269. nadsdiptera.org/Tach/Genera/Gentach ver4.pdf). In J. F. McAlpine, B. V. Peterson, G. E. Shewell, H. J. O’Hara, J. E., and D. M. Wood. 2004. Catalogue of the Ta- Teske, J. R. Vockeroth, and D. M. Wood [eds.], Manual chinidae (Diptera) of America north of Mexico. Mem. of Nearctic Diptera. Vol. 2. Agriculture Canada Mono- Entomol. Int. 18: 1Ð410. graph 28: 675Ð1332. Oksanen, J., R. Kindt, P. Legendre, B. O’Hara, and M. Ste- Vavrek, M. 2009. fosil: Palaeoecological and palaeogeo- vens. 2007. Vegan: community ecology package. R pack- graphical analysis tools. R package version 0.2-1. (http:// age version 1.15-4. (http://r-forge.r-project.org/proj- cran.r-project.org/web/packages/fossil/fossil.pdf). ects/vegan). Yeates, D., B. Wiegmann, G. Courtney, R. Meier, C. Lamb- Richter, V. A. 2005. new Data on the biology and distribu- kin, and T. Pape. 2007. Phylogeny and systematics of tion of Palaearctic tachinids (Diptera, Tachinidae). En- Diptera: two decades of prospects. Zootaxa 1668: 565Ð590. tomologicheskoe Obozrenie 84: 911Ð915. Schaffner, J. V., and C. L. Griswold. 1934. Macrolepidoptera and their parasites reared from Þeld collections in the Received 25 March 2010; accepted 30 September 2010.