COMMUNITY AND ECOSYSTEM ECOLOGY Consequences of Habitat Fragmentation for the Prairie-Endemic aeneus

EMILY C. KLUGER,1 STEWART H. BERLOCHER,1 JOHN F. TOOKER,2 1,3 AND LAWRENCE M. HANKS

Environ. Entomol. 40(6): 1388Ð1396 (2011); DOI: http://dx.doi.org/10.1603/EN11054 ABSTRACT Widespread destruction of tallgrass prairies in the midwestern United States has fragmented communities with the result that populations of endemic species have become geographically isolated from one another. The goal of the research summarized here was to evaluate the potential for conserving endemic prairie species of herbivorous by managing their host . Our study species was the weevil (Boehman), adults of which feed on pollen of plants in the genus (: Heliantheae). The female clip the peduncles of ßower heads and oviposit into the heads, where the larvae feed on the ovules. The research was conducted in 12 prairie sites in eastern Illinois. An allozyme analysis revealed that most populations of H. aeneus at the various prairie sites were genetically differentiated from one another, but the degree of differentiation was not associated with geographic distance between sites. Adult H. aeneus fed and oviposited on the plant species Silphium laciniatum L., S. integrifolium Michx., and S. terebinthinaceum Jacq, which differ in bloom phenology. There was no evidence of genetic differ- entiation of weevil populations with respect to host plant species, and adult weevils strongly preferred S. terebinthinaceum. We conclude that the oligophagous nature of the weevil assures its survival in small prairie remnants even where some of the host plant species are absent. Although H. aeneus can have a signiÞcant impact on reproduction of host plants by clipping ßower heads, the perennial nature of Silphium species prevents their local extinction.

KEY WORDS plant- interaction, phytophagy, insect conservation, Curculionidae

Fragmentation of habits because of anthropogenic emies are in low abundance, and outbreak of herbi- disturbance has altered the structure of plant com- vores can result in local extinction of host plants munities, disrupted food webs, and resulted in local (Groom 2001, Schops 2002, Ryall and Fahrig 2005, extinction of endemic species (Terborgh 1992, Stef- Borrvall and Ebenman 2006, Whiles and Charlton fan-Dewenter and Tscharntke 2002, Johst and Schops 2006, Wilmers et al. 2006). There is a growing con- 2003, Ryall and Fahrig 2005). Researchers have sought sensus that effective management of endemic ecosys- to counter the negative impact of habitat fragmenta- tems requires an understanding of multitrophic inter- tion by identifying the attributes of prairie ecosystems actions and how they ultimately shape the structure of that serve to sustain species diversity (Tscharntke communities (Kremen et al. 1993, Didham et al. 1996, 1992, Schops 2002, Ryall and Fahrig 2005, Aguilar et al. Steffan-Dewenter and Tscharntke 2002). 2006, Borrvall and Ebenman 2006). Much of this re- The goal of the research summarized here was to search has centered on the composition of plant com- gain insight into the conservation of insect species by munities (Kremen et al. 1993, Panzer and Schwartz characterizing ecological interactions between an en- 1998), perhaps with the expectation that increased demic species of weevil and its host plants in a threat- diversity at lower trophic levels will translate upwards into enhanced diversity of consumers. This expecta- ened ecosystem, the North American tallgrass prairie. tion assumes that insect communities are regulated Tallgrass prairies have been subject to extensive re- primarily by bottom-up processes. duction and fragmentation throughout North America Nevertheless, top-down forces also can strongly in- over the last 200 yr, with the result that prairies of Ͻ ßuence the stability of endemic communities. For Illinois now represent 0.01% of the original 2 million example, populations of herbivorous insects may be ha (Samson and Knopf 1994). The once extensive and poorly regulated where their specialized natural en- contiguous prairie ecosystem has been reduced to patches that are embedded in agricultural ecosystems 1 Department of Entomology, University of Illinois at Urbana- and urbanized landscapes. Very little is known about Champaign, Urbana, Illinois 61801. insect communities of these surviving prairie ecosys- 2 Department of Entomology, The Pennsylvania State University, University Park, Pennsylvania 16902. tems (Kosztarab and Schaefer 1990, Arenz and Joern 3 Corresponding author, e-mail: [email protected]. 1996).

0046-225X/11/1388Ð1396$04.00/0 ᭧ 2011 Entomological Society of America December 2011 KLUGER ET AL.: IMPACT OF HABITAT ISOLATION ON PRAIRIE-ENDEMIC WEEVIL 1389

Table 1. Characteristics of managed prairies that were study sites in 2006 (see Fig. 1 for locations; N. P. indicates nature preserves, Illinois Department of Natural Resources)

Est. no. of Silphium Site Area a No. Study site County GPS coordinates plants descriptionb (ha) S. l. S. i. S. t. 1 Somme Woods Forest Preserve Cook 42Њ 8Ј17.85 Љ N; 87Њ 49Ј22.21Љ W Restoration 28 120 17,000 140 2 Wayside Woods Cook 42Њ 2Ј30.81Љ N; 87Њ 47Ј24.98Љ W Restoration 1.6 290 3,000 14,000 3 Wolf Road Prairie N. P. Cook 41Њ 50Ј14.03Љ N; 87Њ 54Ј11.26Љ W Restoration 32 80 1,210,000 28,000 4 Sundrop Prairie N. P. Cook 41Њ 37Ј13.18Љ N; 87Њ 42Ј11.09Љ W Restoration 22 100 3,200 0 5 Gensburg-Markham Prairie N. P. Cook 41Њ 36Ј21.10Љ N; 87Њ 41Ј13.28Љ W Restoration 24 15 380 1,200 6 Goose Lake Prairie N. P. Grundy 41Њ 22Ј 23.61Љ N; 88Њ 17Ј 31.41Љ W Remnant 1,028 215 25,000 80 7 Loda Cemetery Prairie N. P. Iroquois 40Њ 31Ј34.67Љ N; 88Њ 4Ј34.82Љ W Remnant 1.4 6,500 5,600 41,000 8 Prospect Cemetery Prairie N. P. Ford 40Њ 26Ј43.14ЉЉ N; 88Њ 5Ј50.16Љ W Remnant 2 100 13,000 120 9 Windfall Prairie N. P. Vermillion 40Њ 12Ј59.13Љ N; 87Њ 44Ј 45.09Љ W Remnant 13 0 16,000 55 10 Meadowbrook Prairie Champaign 40Њ 4Ј47.90Љ N; 88Њ 12Ј15.20Љ W Restoration 24 1,300 2,400 190 11 Lincoln Prairie Grass Trail Coles 39Њ 29Ј51.19Љ N; 88Њ 14Ј39.99Љ W Restoration 2.4 120 34,000 140 12 Prairie Ridge State Natural Area Jasper 38Њ 55Ј11.84Љ N; 88Њ 11Ј24.55Љ W Remnant 1,133 30 11,000 5,400

a Abbreviations of plant species names: S. l. (Silphium laciniatum), S. i. (Silphium integrifolium), S. t. (Silphium terebinthinaceum). b Prairie remnantsÕ are areas that have never been cropped, whereas restorationsÕ have been replanted with prairie vegetation after crop production.

The focus of our study was the prairie-endemic Decker 2002), but that crop was not grown in the weevil Haplorhynchites aeneus (Boehman), which de- vicinity of our studies. pends for its survival on prairie plants in the astera- Differences in bloom period between Silphium spe- ceous tribe Heliantheae (for biology of the weevil, see cies apparently have driven genetic differentiation of Hamilton 1973, 1981, 1994). The adults aggregate on gall wasps in the genus Antistrophus (Hymenoptera: the stems and consume the pollen, and females par- Cynipidae) whose larvae develop in their stems (see tially clip the peduncles, invariably ovipositing into Tooker et al. 2004). Antistrophus rufus Gillette origi- the dangling heads (E.C.K. unpublished data). The nally was considered oligophagous across multiple Sil- larvae feed on the ovules. Fourth instars drop from phium species, but is now known to comprise at least ßower heads in late summer and autumn and burrow three cryptic species, each of which apparently is into the soil, where they pupate and overwinter. monophagous on different Silphium species in prairie In the area of our study, eastern Illinois, host plants habitats of eastern Illinois (Tooker et al. 2004). The of H. aeneus include the prairie-endemic species Sil- season-long ßight period of the gall wasps therefore is phium laciniatum L., S. integrifolium Michx., and S. because of synchronization of multiple Antistrophus terebinthinaceum Jacq (Gleason and Cronquist 1991, species with their different host plant species (Tooker Pleasants and Jurik 1992, Clevinger and Panero 2000). et al. 2004). These species have been listed as threatened or en- We examine the H. aeneus and Silphium system from dangered in some states (Cooperrider 1982, Walter a conservation biology perspective by conducting ex- and Gillett 1998). They often are conspicuous mem- periments in 12 prairies in eastern Illinois that varied bers of plant communities in remnants of tallgrass in the species composition and density of their plant prairie, and in restored prairie habitats (Tooker and communities. We Þrst used allozyme analysis to test Hanks 2004b), because they produce multiple stems the hypothesis that populations of the weevil are ge- that may reach 3 m tall, and as many as 200 ßower netically differentiated across patches of prairie hab- heads (J.F.T. unpublished data). The species differ itat because of geographic isolation. That hypothesis somewhat in stem height (S. integrifolium is usually was supported (see Results). We also used allozymes half the height of the other two species), and breadth to conÞrm that H. aeneus comprises a single species, of ßower heads (S. laciniatum has the broadest heads). and not multiple genetically-distinct races, or even They also differ in bloom phenology (S. terebinthina- cryptic species that are specialized to feed on different ceum blooming later than the other two species), with Silphium species. That hypothesis also was supported the result that ßower heads of Silphium species are (see Results): H. aeneus is oligophagous across all available continuously from early June through Sep- three Silphium species. Finally, we conducted an ex- tember (Tooker et al. 2002, Tooker and Hanks 2004b). periment to determine whether the weevil prefers Adult H. aeneus are active throughout the period certain host species over others, which could have that Silphium species are in bloom (J.F.T. and E.C.K., important implications for conserving weevil popula- personal observations). They can have a dramatic im- tions in prairie habitats. pact on plant communities (Pilson and Decker 2002), and in some years clipping 100% of the ßower heads Materials and Methods of Silphium species at certain prairie sites in our area (J.F.T. and E.C.K., personal observations). The weevil Study Sites. Study sites were 12 areas of prairie also can be an economically important pest of culti- habitat in eastern Illinois (Table 1; Fig. 1), Þve of vated sunßower (Helianthus annuus L.) (Pilson and which were remnants of virgin tallgrass-mesic prairies, 1390 ENVIRONMENTAL ENTOMOLOGY Vol. 40, no. 6

of the patches (m2) based on approximate patch shape (usually roughly circular or oval). Densities of the

three plant species (log10; from Table 1) differed across study sites, averaging (ϮSE) 2.04 Ϯ 0.27, 4.03 Ϯ 2.4, and 2.69 Ϯ 0.39 plants/m2 for S. laciniatum, S. integrifolium, and S. terebinthinaceum, respectively ϭ (overall analysis of variance [ANOVA)] F13,35 3.26, ϭ ϭ ϭ P 0.007, plant species term F2,35 12.7, P 0.0002). Silphium integrifolium was signiÞcantly more abun- dant than the other two species (REGWQ means separation test; SAS Institute 2001). Study sites did not differ signiÞcantly in numbers of plants across Sil- phium species because of this great amount of varia- ϭ ϭ tion (same ANOVA, study site term F11,35 1.55, P 0.19). Genetic Structure of Populations: Geographic and Host Plant Effects. Horizontal starch gel electropho- resis (Murphy et al. 1996) was used on larvae of H. aeneus to provide allozyme markers for the genetic analysis. We dissected as many as 15 weevil larvae of unknown age from ßower heads of Silphium species in September and October 2006 at ten of the 12 study sites (N ϭ 37Ð131 larvae per site, total ϭ 823 larvae; Table 1; excluding Sundrop and Meadowbrook prai- ries, where weevils were scarce). Larvae were stored at Ϫ80ЊC until being electrophoresed. Loci were ini- tially selected that were known to be polymorphic in other species (Crouau-Roy 1989, Briese et al. 1996, Gonzalez-Rodriguez et al. 2002). Eight loci that yielded consistent stains were surveyed, of which seven were polymorphic in at least one population: aconitate hydratase (Acon, EC 4.2.1.3), alcohol dehy- drogenase (Adh, EC 1.1.1.1), aspartate aminotransfer- ase (Aat, EC 2.6.1.1), esterase (Est, EC 3.1.1.1), beta- hydroxyacid dehydrogenase (Had, EC 1.1.1.30), isocitrate dehydrogenase (Idh, EC 1.1.1.42), and phos- phoglucomutase (Pgm, EC 5.4.2.2). One enzyme, Fig. 1. Location of prairie remnants and restorations in malate dehydrogenase NADPϩ (Me, EC 1.1.1.40) was eastern Illinois that were study sites (see Table 1 for names; monomorphic in all populations. The following four ordered by decreasing latitude). gel buffer systems were used (Murphy et al. 1996): 1) tris/citrate pH 8.6 for Est and Me; 2) tris/citrate pH 8.6 ϩ and seven were “restored” prairies: farmland or fallow with 0.5 ml NAD added to the gel buffer before Þelds to which endemic plant species have been re- degassing for Adh, Had, Idh, and Pgm; 3) lithium hy- introduced. All sites were geographically isolated from droxide/citrate pH 8.1/8.5 for Aat and Acon; and 4) one another by at least 2 km (Fig. 1) and were sur- morpholine/citrate pH 6.1 for Had. rounded by agricultural Þelds (primarily rotated corn The genetic structure of populations was analyzed [Zea mays L.] and soybean [Glycine max (L.) Merr.]) with Arlequin 3.1 (ExcofÞer et al. 2005), or Microsoft urban landscape, or both. All three Silphium species Excel and a Monte Carlo simulator of anRxCexact were present at the study sites, except for Sundrop and test (MONTE CARLO RxC 2.2, Macintosh OS nine Windfall prairies, each of which were missing one program provided by W. Engels, Department of Ge- plant species (Table 1). Few weevils were seen on netics, University of Wisconsin, Madison, WI). HardyÐ plants other than Silphium species throughout the Weinberg equilibrium was assessed using exact tests. season. Because only small numbers of weevils had complete The Silphium species grew in discrete patches at genotypes (see Results), linkage disequilibium was most of our study sites, probably because of limited tested using exactRxCtests on genotypes for pairs of dispersion of seeds from parent plants (Pleasants and loci. Hypothesis 1 (weevil populations are genetically Jurik 1992). Population densities of each host plant differentiated across patches of prairie) was tested by species, per study site, were estimated by sampling Þrst carrying out exact tests for signiÞcant allele fre- with 2- by 2-m squares of PVC pipe (four samples per quency differences between populations. Geograph- patch, positioned arbitrarily), counting the number of ical variation was further characterized using analysis plants within the square, and estimating the total area of molecular variance (AMOVA), a Mantel test for December 2011 KLUGER ET AL.: IMPACT OF HABITAT ISOLATION ON PRAIRIE-ENDEMIC WEEVIL 1391 isolation by distance, and regression of allele frequen- mine whether the number of weevils on a particular cies on latitude (using Excel). plant species was correlated with the relative abun- Hypothesis 2 (H. aeneus comprises a single species dance of its ßower heads on certain dates. that feeds on all three Silphium species) was tested ANOVA (blocked by study site) also was used to with exactRxCcontingency tests on allele counts test differences between plant species in the percent- from samples of weevil larvae taken from different age of ßower heads that had clipped by the end Silphium species at the same study site. At least six of the season; assuming a binomial distribution, PROC weevil larvae were dissected from ßower heads of GENMOD, SAS 2001). each Silphium species that were collected in each of Þve study sites where all three plant species were Results blooming in 2006 (Wolf Road, Goose Lake, Loda Cem- etery, Prospect Cemetery, Lincoln Prairie Grass Trail; Genetic Structure of Populations: Geographic and Table 1). Host Plant Effects. Although we electrophoresed 823 Bloom Phenology of Silphium Species. Bloom phe- larvae of H. aeneus (37Ð131 per study site), sample nology of the three Silphium species was character- sizes for individual loci are in many cases smaller ized by determining, for each species and study site, because of difÞculties in scoring loci for all individuals the ordinal date on which the greatest number of new on some gels (a spreadsheet with genotypes for each ßowers were open (i.e., peak bloom), then used individual weevil is available from the corresponding ANOVA to compare mean date of peak bloom for each author). Nevertheless, there was sufÞcient allozyme species, blocked by study site and including a latitude variation for population genetic analysis, with an av- covariate (to determine whether bloom phenology erage of 3.5 alleles across the eight loci, and an overall was correlated with latitude). average heterozygosity of 0.213. With the exception of Utilization of Floral Resources by H. aeneus. Utili- one test for which the P value was Ͻ0.05 (Pgm at Wolf zation of host plants by adult H. aeneus was examined Road, P ϭ 0.047, well within the range of Bonferroni by monitoring the bloom phenology of individual correction), weevil populations conformed to HardyÐ plants (as a measure of resource availability) and also Weinberg expectations at the seven variable loci, in- the abundance of weevils on those plants (as a mea- dicating that mating was random within each popu- sure of the response of the beetle population). At the lation. There was no evidence of signiÞcant linkage beginning of the 2006 growing season, two 25-m tran- disequilibrium. sects were established, intersecting and at approxi- The allozyme data supported hypothesis 1 (weevil mate right angles to one another, through patches of populations are genetically differentiated across the plants at each study site. For each species, 12 plants patches of prairie). The exact tests of population dif- were tagged that were separated by at least 2 m within ferentiation revealed signiÞcant (P Ͻ 0.05), to highly the transects. Study sites were visited 13 times (every signiÞcant (P Ͻ 0.0005) differences in allele frequen- 8Ð11 d from mid-June through October 2006) to re- cies between populations for 41 out of 45 comparisons cord, for each tagged plant, the number of ßower buds, (Table 2). Although the allele frequency differences open ßower heads, senesced ßower heads (indicated were certainly signiÞcant, the magnitudes of the dif- by wilted petals), the number of adult weevils on the ferences at all loci were small, as measured by FST Ͻ plant, and the number of ßower heads that had been (Table 3). The overall FST of 0.016 (P 0.001) is in the clipped. range that Wright (1978) characterized as “slight”. Host species preference in adult H. aeneus was ex- Using the well-known equation of Wright (1978), ϭ Ϫ amined by comparing the percentage of weevils that Nm (1/4 FST) 1, the estimated number of migrants were on plants of one species with the relative abun- is 14.6 per generation, a large number for such geo- dance of the ßowers of that species (i.e., the percent- graphically isolated populations. No regressions of al- age of all open ßowers of Silphium species that were lele frequency on latitude were signiÞcant, nor was of that species; logistic regression, PROC GENMOD, there evidence of isolation by distance between sites SAS 2001). This test was conducted for pairs of Sil- (Mantel test P ϭ 0.19). phium species during periods in which they over- These results also supported hypothesis 2 (H. aeneus lapped in blooming period (see Results): S. laciniatum comprises a single species that feeds on all three Sil- and S. integrifolium (samples between ordinal dates phium species). There were no signiÞcant genetic 180 and 200, when only these two Silphium species differences between weevil subsamples from different were in bloom; see Fig. 1); and S. integrifolium and S. host plant species at any of the study sites. Hypothesis terebinthinaceum (sample dates after date 230, when 2 also is supported by the excellent Þt to HardyÐ those two species accounted for most of the ßower Weinberg expectations in all populations where mul- heads). This analysis included data from all sample tiple host plant species were present. dates and study sites for which there was an average Bloom Phenology of Silphium Species. The three of at least Þve weevils on the plant species in question Silphium species differed signiÞcantly in the timing of (including multiple dates for some study sites; N ϭ 30 peak bloom across study sites, with ordinal peak bloom for the comparison between S. laciniatum and S. in- dates averaging (ϮSE) 205.1 Ϯ 1.3, 218.8 Ϯ 1.9, and tegrifolium; N ϭ 18 for the comparison of S. integrifo- 239.0 Ϯ 2.5 for S. laciniatum, S. integrifolium, S. tere- lium and S. terebinthinaceum). Regression analysis binthinaceum, respectively (mean signiÞcantly differ- ϭ Ͻ (PROC REG; SAS Institute 2001) was used to deter- ent; overall ANOVA F3,33 55.3, P 0.0001; plant 1392 ENVIRONMENTAL ENTOMOLOGY Vol. 40, no. 6

Table 2. Global tests of allele frequency differences in pair-wise comparisons among ten populations of H. aeneus (site numbers as in Table 1; Fig. 1) by using exact P values

Site 1 235678911 2 **a 3 *** *** 5 * - *** 6 *** *** *** *** 7 *** ** *** * ** 8 * ** *** *** -- 9 * * *** - *** *** *** 11 ** ** *** *** *** *** *** ** 12 ** ** *** * *** *** *** * ***

a SigniÞcant differences from exact tests of population differentiation are indicated as follows: “-” (P Ͼ 0.05); “*” (P Ͻ 0.05); “**” (P Ͻ 0.005); “***” (P Ͻ 0.0005).

ϭ Ͻ species term F2,33 79.2, P 0.0001). The timing of when both S. integrifolium and S. terebinthinaceum peak bloom was not signiÞcantly inßuenced by lati- both were in bloom, nearly all weevils were on the tude (ANOVA covariate P Ͼ 0.05). latter species, irrespective of the relative abundance of Even though the Silphium species differed in timing plant species (Fig. 3, bottom; logistic regression not of peak bloom, they overlapped broadly over the sea- signiÞcant, P ϭ 0.46), with the exception of one date son in the periods that they were in bloom (Fig. 2, solid for one site where ßower heads of S. terebinthinaceum lines), with S. laciniatum and S. integrifolium coming were scarce. into bloom Þrst and nearly synchronously, but S. in- The preference of weevils for S. terebinthinaceum tegrifolium blooming for a longer period and overlap- also was reßected in their cumulative impact on plants. ping more broadly with S. terebinthinaceum. Flowers The plant species differed signiÞcantly in the percent- of Silphium species in general were present continu- ages of ßower heads that were clipped by the end of ously from late June through early September. ϭ ϭ the season (PROC GENMOD F12,29 3.91, P Utilization of Floral Resources by H. aeneus. Adult 0.0042), being higher in S. terebinthinaceum (58.3 Ϯ weevils were present on both S. laciniatum and S. 5.7) than in the other two species (28.3 Ϯ 4.4 and integrifolium throughout the early bloom period (or- 16.5 Ϯ 2.6 for S. integrifolium and S. laciniatum, re- dinal dates Ϸ180Ð210; Fig. 2, top and middle, dashed spectively). Study sites did not differ signiÞcantly in line). In fact, the number of weevils on plants ap- the percentage of ßower heads that were clipped peared to anticipate blooming phenology by Ϸ3wkfor (ANOVA site effect, P ϭ 0.62). both plant species. The weevils began aggregating on plants when only a few ßowers had opened and were available for feeding and oviposition. Weevils were randomly distributed across S. laciniatum and S. integ- Discussion rifolium during the period when those were the only It is not surprising that populations of H. aeneus have two species of host plants in bloom, and regardless of become genetically differentiated, because the rem- their relative density (Fig. 3, top; logistic regression nant and restored prairies that were our study sites ϭ not signiÞcant, P 0.44). were small in size and isolated within unsuitable ag- The numbers of weevils on S. laciniatum and S. ricultural or urbanized landscapes. Moreover, many of integrifolium began to decline rapidly before either the prairie habitats were subjected periodically to plant species had reached peak bloom, clearly as a prescribed burning that is intended to maintain the result of their shifting to S. terebinthinaceum (Fig. 2). endemicity of the plant community (Steinauer and Weevil adults colonized S. terebinthinaceum very Ϸ Collins 1996, Pauly 1997), but may have a devastating early, anticipating the onset of blooming by 7wk impact on communities of herbivorous insects (Swen- (Fig. 2, bottom), suggesting that weevils had a strong gel 2001, Tooker and Hanks 2004a). It is therefore preference for that host species. During the period likely that population densities of the weevil have at intervals been greatly reduced, resulting in population bottlenecks (Nei et al. 1975, Templeton 1980, Crouau- Table 3. FST values for the seven polymorphic allozyme loci of H. aeneus, and the overall FST Roy 1989). Nevertheless, two aspects of the genetic data sug- Locus FST P value gest that weevils can move between patches of prairie, Idh 0.02720 0.00000 and that gene ßow is not prohibited by habitat frag- Pgm 0.03192 0.00000 mentation. First, the low level of F strongly suggests Adh 0.04011 0.00000 ST Acon 0.01910 0.00000 that ongoing gene ßow is relatively high. Although Had 0.00175 0.37537 inferring number of migrants from FST is fraught with Est 0.01073 0.01955 a number of assumptions and complications, the in- Aat 0.00596 0.07918 ferred number of migrants per generation, 14.6, is well Overall 0.01579 0.00000 above what would be considered negligible. Second, December 2011 KLUGER ET AL.: IMPACT OF HABITAT ISOLATION ON PRAIRIE-ENDEMIC WEEVIL 1393

Ϯ Fig. 2. Relationship between ordinal date and mean ( 1 SE) percentage of ßower heads that were in bloom, and log10 density of adult H. aeneus at 12 study sites in east central Illinois for the host plant species (a) Silphium laciniatum, (b) Silphium integrifolium, and (c) Silphium terebinthinaceum. Means for the same sample date are shifted1dtoavoid overlap of error bars. the lack of evidence for isolation by distance suggests that would buffer populations from the effects of ge- that some weevils must indeed travel long distances. netic drift. Such delayed diapause has been reported There are several possible explanations for the high for other weevil species (Menu and Desouhant 2002, rate of gene ßow between populations of H. aeneus. Maeto and Ozaki 2003). The weevil species may be Delayed diapause may result in an accumulation of less strongly inßuenced by prairie burning than sus- weevils in the soil, essentially a “seed bank” of weevils, pected. Silphium and other species of host plants scat- 1394 ENVIRONMENTAL ENTOMOLOGY Vol. 40, no. 6

Fig. 3. Relationship between the percentage of adult H. aeneus that were present on ßower heads of a given Silphium species and the percentage of ßower heads that the plant species represented of the total numbers of ßower heads present at the site on a particular date. Pair-wise comparisons of plant species (only those having at least Þve weevils): (a) S. laciniatum and S. integrifolium (samples between ordinal dates 180 and 200; see Fig. 2); (b) S. integrifolium and S. terebinthinaceum (sample dates after ordinal date 230). tered along roadsides and railway right-of-ways may vival of the weevil even in small prairie remnants serve as partial corridors for gene ßow between prairie that do not have the complete set of host plant remnants along which weevils could travel (Hamilton species. In fact, weevils were present at two of our 1973). Finally, weevils may be accidentally trans- study sites that were missing one of the Silphium ported by people, such as by alighting on the vehicles species, including Sundrop Prairie where the fa- of prairie tourists. vored S. terebinthinaceum was entirely absent (Ta- The sequential blooming phenology of the Sil- ble 1). phium species, broadly overlapping throughout the Although the weevil had a signiÞcant impact on season, presents a continuous resource for adults reproduction of host plants by clipping ßower heads, and larvae of the oligophagous H. aeneus, allowing Silphium species are unlikely to be driven to local adults to shift from one species to the next as fresh extinction because they are perennials: some plants ßower heads become available. Other types of her- eventually will succeed in producing enough seed to bivorous insects similarly shift between host plant assure survival of the population, despite the great species that bloom sequentially (Floate et al. 1993, numbers of ßower heads that are sacriÞced in sustain- Hodkinson 1997). Adult H. aeneus used all three ing weevil populations. However, the damage inßicted species of Silphium that were available at our study by H. aeneus may have a signiÞcant impact on other sites, although with a marked preference for S. tere- species that rely on Silphium resources. binthinaceum. Nevertheless, oligophagy assures sur- Pollinators in particular are vital to the survival of December 2011 KLUGER ET AL.: IMPACT OF HABITAT ISOLATION ON PRAIRIE-ENDEMIC WEEVIL 1395 endemic plant communities and are likely to be es- Gonzalez-Rodriguez, A., B. S. Benrey, A. Callejas, and K. pecially sensitive to the sudden decline in ßower Oyama. 2002. Inter- and intraspeciÞc genetic variation heads where weevils are abundant. By clipping ßower and differentiation in the sibling bean weevils Zabrotes heads, the weevil also is likely to inßuence the diverse, subfasciatus and Z. sylvestris (Coleoptera: Bruchidae) but poorly documented community of insects that live from Mexico. Bull. Entomol. Res. 92: 185Ð189. within ßower heads of Silphium plants, including lar- Groom, M. J. 2001. Consequences of subpopulation isola- vae of gall wasps, other species of weevils, caterpillars, tion for pollination, herbivory, and population growth in Clarkia concinna concinna (Onagraceae). Biol. Conserv. and the natural enemies of these species (J.F.T., un- 100: 55Ð63. published data). Selective pressures associated with H. Hamilton, R. W. 1973. Observations on the biology of Hap- aeneus therefore may have played a signiÞcant role in lorhynchites aeneus (Boheman) (Coleoptera: Rhynchiti- shaping the community of insects that rely on Silphium dae). Coleop. Bull. 27: 83Ð85. ßower heads for their survival. Hamilton, R. W. 1981. Description of the larva and pupa of Haplorhynchites aeneus (Coleoptera: Curculionoidea, ). J. Kans. Entomol. Soc. 54: 616Ð624. Acknowledgments Hamilton, R. W. 1994. New life cycle data for two western North American weevils (Coleoptera: Rhynchitidae), We thank M. R. Berenbaum for constructive comments on with a summary of North American rhynchitid biology. an early draft of the manuscript, and M. C. Currier, L. C. Coleopt. Bull. 48: 331Ð343. Sherrick, and M. S. Glasberg for technical assistance in the Hodkinson, I. D. 1997. Progressive restriction of host plant Þeld and lab. We appreciate funding in support of this re- exploitation along a climatic gradient: the willow psyllid search from the Alphawood Foundation (to LMH) and from Cacopsylla groenlandica in Greenland. Ecol. Entomol. 22: Prairie Biotic Research, Inc. (to ECK). 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