Oecologi (26) 8:85 92 DOI.7/s442-5-3524-y COMMUNITY ECOLOGY ORIGINAL RESEARCH Fitness enefits of the fruit fly Rhgoletis lternt on non ntive rose host Kim Meijer,2 Christin Smit Menno Schilthuizen,3 Leo W. Beukeoom Received: 4 Jnury 25 / Accepted: 2 Decemer 25 / Pulished online: 8 Jnury 26 The Author(s) 26. This rticle is pulished with open ccess t Springerlink.com Astrct Mny species hve een introduced worldwide into res outside their nturl rnge. Often these nonntive species re introduced without their nturl enemies, which sometimes leds to uncontrolled popultion growth. It is rrely reported tht n introduced species provides new resource for ntive species. The rose hips of the Jpnese rose, Ros rugos, which hs een introduced in lrge prts of Europe, re infested y the ntive monophgous tephritid fruit fly Rhgoletis lternt. We studied differences in fitness enefits etween R. lternt lrve using R. rugos s well s ntive Ros species in the Netherlnds. R. lternt pupe were lrger nd hevier when the lrve fed on rose hips of R. rugos. Lrve feeding on R. rugos were prsitized less frequently y prsitic wsps thn were lrve feeding on ntive roses. The differences in prsitiztion re proly due to morphologicl differences etween the ntive nd non-ntive rose hips: the hypnthium of R. rugos hip is thicker nd provides the lrve with the possiility to feed deeper into the hip, mening tht the prsitoids cnnot rech them with their ovipositor nd the lrve escpe prsitiztion. Our study shows tht ntive species switching to novel non-ntive Communicted y Rolnd A. Brndl. * Christin Smit c.smit@rug.nl 2 3 Groningen Institute of Evolutionry Life Sciences (GELIFES), University of Groningen, P.O. Box 3, 97 CC Groningen, The Netherlnds Altenurg & Wymeng, Ecologicl Consultnts, P.O. Box 32, 9269 ZR Veenwouden, The Netherlnds Nturlis Biodiversity Center, Drwinweg 2, 2333 CR Leiden, The Netherlnds host cn experience fitness enefits compred to the originl ntive host. Keywords Herivory Non-ntive species Prsitiztion Enemy escpe Fitness Introduction Over the pst centuries, mny species of plnts nd nimls hve een introduced into new res worldwide, oth intentionlly nd unintentionlly (Willimson 996). Some of these species mnge to estlish, integrting into the novel ecosystems nd intercting with the ntive species present. Such non-ntive species cn hve lrge negtive effects on economics (Pimentel et l. 25), humn helth (Zisk nd Culfield 2) nd ntive ecosystems (Willimson 996). In mny cses, non-ntive species hve ecome very successful (i.e., invsive) nd negtively ffect ntive species y competition or predtion (e.g. Pelicice nd Agostinho 28; Perdereu et l. 2). However, conversely, nonntive species my lso provide new niches for ntive species to utilize, which ultimtely my led to popultion differentition nd the evolution of new host rces or (su) species. The est descried exmple of such host shift comes from the North Americn pple mggot fly Rhgoletis pomonell (Dipter: Tephritide). This species shifted from the ntive hwthorn (Crtegus spp.) to introduced pple (Mlus domesticus) (Bush 969; McPheron et l. 988). Within 4 yers, the popultions on oth hosts ecme geneticlly differentited host rces (Feder et l. 988; McPheron et l. 988), differing in ehvior, host preference nd timing of reproduction (Feder nd Filchk 999; Filchk et l. 2; Prokopy et l. 988). Similr exmples 3
86 Oecologi (26) 8:85 92 of shift to non-ntive host plnt hve een documented in, e.g., the goldenrod gll midge Dsineur folliculi (Dipter: Cecidomyiide) (Dorchin et l. 29), the Europen corn orer Ostrini nuillis (Lepidopter: Crmide) (Bethenod et l. 25; Thoms et l. 23) nd the soperry ug Jder hemtolom (Hemipter: Rhoplide) (Crroll nd Boyd 992). These host shifts re often ccompnied y morphologicl, physiologicl nd ehviorl chnges in the herivores. Even though non-ntive plnt species my e colonized y ntive herivores, they re in generl ttcked less thn ntive species (Colutti et l. 24; Meijer et l., unpulished). This escpe from enemies is most likely one of the fctors influencing the success of non-ntive plnts (nd other orgnisms), s predicted y the Enemy Relese Hypothesis (Willimson 996). Interestingly, ntive herivore species tht (prtly) shift to non-ntive host species my in turn enefit from escpe of their ntive enemies, if predtors nd prsites re less likely to visit the non-ntive plnt. For exmple, Feder (995) showed tht R. pomonell lrve re prsitized much less on the non-ntive Mlus domesticus (3 %) thn on the ntive host plnt Crtegus species (46 %). Very few ntive/non-ntive systems hve een studied in detil in terms of such tri-trophic interctions. Such studies re, however, needed to understnd nd predict the success of non-ntive species. In this study, we focus on the three-wy interction etween plnts, their herivorous (phytophgous) insects nd the prsitoids of the herivores. In the Netherlnds, lrve of the tephritid fruit fly R. lternt (Dipter: Tephritide) feed on the fruits of ntive rose species (Ros spp.) nd the non-ntive Jpnese rose (Ros rugos). The lrve re prsitized y severl prsitic wsp species (Hymenopter: Brconide). We test whether there re differences in lrvl size, prsitiztion frequency nd ccessiility y prsitic wsps etween lrve feeding on the fruits of ntive nd nonntive roses. Methods Study species The lrve of the Europen rose-hip fruit fly, R. lternt (Dipter, Tephritide), re monophgous fruit herivores of rose hips. Nowdys, the most common hosts in Europe re ntive species of the Ros cnin complex s well s the introduced Jpnese rose R. rugos (Leclire nd Brndl 994). R. lternt is univoltine (one genertion per yer) with dults emerging in erly June. Eggs re lid under the skin of rose hips from June until August. The lrve feed in the hypnthium of the fruit until Octoer, fter which the mture third-instr lrve leve the fruit to pupte in the soil (Buer 986). R. rugos is ntive in Jpn, Kmchtk nd northestern Chin (Weidem 26). It ws first recorded in Europe in 796, ut hs now een reported from 5 different countries in Western, Centrl nd Estern Europe. It is cultivted in prks, grdens nd long rods, nd it hs lso ecome estlished in mny nture res (Leclire nd Brndl 994). It flowers somewht erlier thn the ntive R. cnin; hips ripen t the turn of August to Septemer, wheres fruits of the ntive roses ripen in Octoer. Hip densities re equl etween ntive roses nd R. rugos, ut the hips of R. rugos re lrger thn those of ntive roses. Therefore, hip iomss per unit ush re is higher in R. rugos (Leclire nd Brndl 994). Prsitic wsps re the min enemies of Rhgoletis lrve (Buer 986). Scmus nnultus (Hymenopter: Ichneumonide), Utetes mgnus (synonym Opius mgnus) nd Psyttli crint (synonyms: P. rhgoleticol, Opius rhgoleticol nd O. crint) (Hymenopter: Brconide) hve een reported s prsitoids of R. lternt (Buer 986; Hoffmeister 992). Collection In Septemer nd Octoer 2, rose hips were collected on three different loctions in the Netherlnds: Hren, province of Groningen (53.7 N 6.6 E), Amelnd, province of Frieslnd (53.45 N 5.77 E) nd Schiermonnikoog, province of Frieslnd (53.49 N 6.22 E). On ech loction, oth ntive roses (Ros spp.) nd non-ntive roses (R. rugos) were smpled in n re of 5 km 2. Approximtely 2 5 rose hips per plnt were collected from totl of 5 plnts in these three res together (24 ntive nd 26 non-ntive roses). The rose hips were stored in continers (l w h: 6.5 2 6 cm) nd covered with fine netting (mesh size < mm). The continers were kept outdoors, protected from rin nd direct sunlight to mimic nturl wether conditions. Within few dys fter collection, R. lternt lrve emerged from the rose hips, pupting soon fter. Pupe were collected nd stored individully in tues (h ø: 6.5 cm) under these sme outdoor conditions. The next spring the continers were checked for emerging dults severl times per week. In the summer ll remining pupe were checked once more nd scored into three ctegories: either n dult fly or dult prsitoid wsp hd emerged, or the pup hd died during the winter. Pupl size, weight nd prsitiztion rte Aout three weeks fter collection, the size (length, mesured under inoculr microscope) nd weight of the pupe were mesured (ccurcy.5 mm nd μg, resp.). As size nd weight of the pupe were highly correlted (R 2 =.759), only size ws mesured for ll pupe nd weight (which ws much more lor intensive) for only 3
Oecologi (26) 8:85 92 su-smple. The mesurements on the pupe from which flies emerged were used to test for differences etween individuls feeding on the ntive nd non-ntive rose, using liner mixed model. The model included sttus (ntive vs. non-ntive rose) s fixed fctor nd plnt individul nd collection loction s rndom fctors. The difference in prsitiztion rte (numer of wsps/totl numer of pupe tht yielded flies or wsps) etween ntive nd non-ntive roses ws tested using generlized liner mixed model (GLMM) with inomil error terms, gin with sttus s fixed fctor nd plnt individul nd collection loction s rndom fctors. Accessiility of lrve y prsitic wsps To determine the ccessiility of the fly lrve y the prsitic wsps, the length of the ovipositor of the emerged prsitic wsps ws compred to the thickness of the hypnthium, nd to the depth of the mines mde y the R. lternt lrve for oth the ntive nd non-ntive roses. The length of the ovipositor ws mesured under inoculr microscope (ccurcy.5 mm). To determine the thickness of the hypnthium nd the depth of the mines, digitl photos were mde of cross sections of hips (collected in utumn 2), ccompnied y ruler. Inkscpe.48 (inkscpe.org) ws used to mesure the thickness of the hypnthium nd the mine depth (Fig. ). The thickness of the hypnthium ws mesured t five positions, rnging from the top to the ottom of the rose hip (Fig. 2). The depth of the lrvl mines ws mesured in four sections, rnging from the top to the ottom (indicted y d 87 in Fig. 2). The distnce ws mesured etween the exocrp nd the lrvl mine (), nd etween the endocrp nd the lrvl mine (). Susequently, the reltive depth of the lrvl mines ws determined s: /( + ), rnging from [touching the exocrp (outer lyer)] to (touching the endocrp/seeds) (Fig. ). Both the differences in thickness of the hypnthium nd depth of the lrvl mine etween ntive nd nonntive roses were tested using liner mixed model, with sttus (ntive vs. non-ntive) s fixed fctor, nd rose hip individul nd mesuring position/section s rndom fctors. The difference in thickness of the hypnthium ws tested seprtely for ll five positions, using liner mixed model with sttus s fixed fctor nd rose hip individul s rndom fctor. The depth of the lrvl mines ws tested for ll four seprte sections, using liner mixed model with sttus s fixed fctor nd rose hip individul s rndom fctor. If lrve hve no preference for feeding either deep or shllow, the verge reltive depth will e.5. If, on the other hnd, lrve do prefer to feed either deep or shllow, the verge reltive depth will e, respectively, higher or lower thn.5. We tested whether the reltive depth of lrvl mines ws different etween ntive nd non-ntive rose hips. Furthermore, we tested if the reltive depth of the lrvl mines ws equl, higher or lower thn.5. All nlyses were done in R (R Development Core Tem 2), using the lme4 lirry (Btes et l. 2). In ll nlyses, the effect of the fixed fctors ws tested y compring the model with nd without this fctor, using ANOVA. Reltive depth if: < = > + = -.5.5.5- exocrp depth hypnthium thickness chenes (seeds) Endocrp (seeds) endocrp Fig. Thickness mesurement of the outer lyer of rose hips (hypnthium). Only this lyer is edile for Rhgoletis lternt lrve. The thickness of this lyer ws mesured from top (exocrp) to ottom (endocrp). The depth of the lrvl mines in the hypnthium ws mesured from the exocrp to the top of the mine. The reltive depth of the lrvl mines ws clculted y: / +, resulting in rtio from to ( the distnce etween the exocrp to the top of the mine; the distnce etween the endocrp to the ottom of the mine) 3
88 Oecologi (26) 8:85 92 Ntive Non-ntive n= n= Section 27 22 Section 2 Section 3 Section 4 27 29 3 c d chenes (seeds) hypnthium d c 2 2 9 Section 5 3 9 2 3 2 3 Thickness of hypnthium (mm ± SE) Thickness of hypnthium (mm ± SE) Fig. 2 Thickness of rose hip hypnthium in reltion to prsitic wsp ovipositor length. Fruit fly lrve cn escpe prsitiztion if they live deep enough in the hypnthium. Shown re cross sections of ntive (left, Ros sp.) nd non-ntive (right, R. rugos) rose hip. Thickness of the hypnthium ws mesured t five different positions, rnging from the top to the ottom prt of the rose hip. Brs show the verge thickness of the rose hips, including stndrd errors nd smple sizes. The depth of the lrvl mines ws mesured t four different sections of the hypnthium ( d) (dt not shown in this figure). The verticl lines represent the verge length of the ovipositor of the prsitic wsps; dotted line: Utetes ferrugtor, dshed line: Psyttli crint Results A totl of 366 R. lternt pupe were collected, 78 from ntive nd 288 from non-ntive rose hips. Three-hundred-nd-twenty pupe (23.43 %) died during winter. From the remining 46 pupe, 953 (69.77 %) dult R. lternt flies nd 93 (6.8 %) prsitic wsps emerged. Size nd weight Pupe collected from non-ntive rose hips were significntly lrger (7.4 %) nd hevier (22.79 %) thn those from ntive rose hips (Fig. 3; Tle ). Size nd weight of the pupe were highly correlted (R 2 =.759, Tle ). Pupl size (mm ± SE) 5.2 5 4.8 4.6 4.4 *** 2 *** 775 78 Ntive Non-ntive Pupl weight (mg ± SE) 66 Ntive Non-ntive Fig. 3 Size () nd weight () of pupe of Rhgoletis lternt tht emerged from ntive roses (Ros spp.) nd non-ntive roses (R. rugos). Shown re the verge ±SE, including smple size nd significnce level (***p <.). Note Y-xis is truncted 9 8 7 Prsitiztion rte Ninety-three of 46 (8.89 %) R. lternt pupe were prsitized y the rconid wsps U. ferrugtor (Goureu, 862) nd Psyttli crint (Thomson, 895). U. ferrugtor ws y fr the most common (87 individuls, 8.32 % of the fly pupe), wheres P. crint ws found only occsionlly (six individuls,.57 % of the fly pupe). In oth species, the sex rtio ws femle ised (3 nd 33 % mles, respectively). The prsitiztion rte of pupe collected on the ntive rose ws significntly higher (lmost four times) thn on the non-ntive rose (Fig. 4; Tle ). Accessiility of lrve y prsitic wsps The hypnthium of the non-ntive rose hips ws thicker thn those of the ntive rose hips t ll five positions mesured (Tle ; Fig. 2). Overll, the hypnthium of the nonntive rose hips ws lmost 7 % thicker thn tht of the ntive rose hips (Tle ; Fig. 5). The ovipositors of oth prsitic wsp species re short,.73 ±.2 mm (n = 58) in U. ferrugtor nd 2.5 ±.2 mm (n = 3) in P. crint. The thickness of the hypnthium of the ntive rose hips ws only slightly greter thn the verge length of the ovipositor of U. ferrugtor, while in the non-ntive rose hips, the hypnthium ws more thn twice s thick s the length of the ovipositor (Fig. 5, dotted line). However, the thickness of the hypnthium of the ntive rose hips ws less thn the verge length of the ovipositor of P. crint, nd in non-ntive rose hips, it ws only 4.6 % lrger thn the length of the ovipositor (Fig. 5, dshed line). 3
Oecologi (26) 8:85 92 89 Tle Overview of the sttisticl nlysis of the effect of host (ntive vs. non-ntive) on herivore size, weight, nd prsitiztion rte, the thickness of the rose hip hypnthium nd the solute nd reltive depth of the mines Size nd weight n χ 2 df p Pupl size mixed model, rndom effects: plnt indiv. nd coll. loction Fixed fctor: sttus 953 7.3 <. Pupl weight mixed model, rndom effects: plnt indiv. nd coll. loction Fixed fctor: sttus 77 9.27.23 Correltion pupl size nd weight n t df p R 2 =.759 77 58.34 75 <. Prsitiztion n Z df p Prsitiztion rte GLMM, rndom effects: plnt indiv. nd coll. loction Fixed fctor: sttus 46 2.4.6 Thickness of the mesocrp n χ 2 df p All positions mixed model, rndom effects: rose hip indiv. nd mesuring position Fixed fctor: sttus 244 56.83 <. Positions seprtely mixed model, rndom effects: rose hip indiv. Position, fixed fctor: sttus 49.5.8 Position 2, fixed fctor: sttus 47 45. <. Position 3, fixed fctor: sttus 5 62. <. Position 4, fixed fctor: sttus 49 42.58 <. Position 5, fixed fctor: sttus 47 45. <. Depth of the lrvl mines n χ 2 df p All selections mixed model, rndom effects: rose hip indiv. nd mesuring section Fixed fctor: sttus 66 2.6.4 Positions seprtely mixed model, rndom effects: rose hip indiv. Position, fixed fctor: sttus 46.82.772 Position, fixed fctor: sttus 25 3.67.554 Position c, fixed fctor: sttus 49.8.3692 Position d, fixed fctor: sttus 46.7.7 Reltive depth of the lrvl mines n χ 2 df p All selections mixed model, rndom effects: rose hip indiv. Fixed fctor: sttus thickness hypnthium 57.3.2883 Fixed fctor: sttus 57.63.23 Fixed fctor: thickness hypnthium 57 3.83.54 Overll depth one smple proportion test Devition from.5 55 43.38 <. The thickness of the hypnthium ws mesured t five different positions, rnging from the top (position ) to the ottom (position 5) of the rose hip. The solute depth of the mines in the hypnthium ws mesured t four different sections in etween these five positions (see Fig. 2 for detils) Overll, the lrvl mines were more thn twice s deep in the non-ntive rose hips compred to in the ntive rose hips (Tle ; Fig. 5). The depth differed etween ntive nd non-ntive rose hips in two out of four sections (Tle ; Fig. 2). The verge depth of the mines in the ntive rose hips ws much less thn the verge length of the ovipositor of the wsps (Fig. 5). Respectively, 95.8 nd 99.3 % of the mines were within rech of the ovipositors of U. ferrugtor nd P. crint. In the non-ntive rose hips, mny lrvl mines were positioned deeper thn the length of the ovipositor of the wsps, nd only 65.2 nd 82.6 % of the mines were within rech of the ovipositors of U. ferrugtor nd P. crint, respectively. The reltive depths of the lrvl mines did not differ etween ntive nd non-ntive rose hips (Tle ; Fig. 6). Most lrvl mines (76.4 %) were in the deeper prts of the hypnthium, nd in oth the ntive nd non-ntive rose hips, the verge reltive depth ws lrger thn.5 (Tle ), i.e., on verge the 3
9 Oecologi (26) 8:85 92 Prsitiztion rte (% ± SE) 2 5 5 n=863 Host: Ntive Non ntive * n=83 Fig. 4 Prsitiztion rte of pupe from ntive roses (Ros spp.) nd non-ntive roses (R. rugos). Shown re the verge ±SE, smple size nd significnce level (*p <.5). Averges nd SEs re derived from the model estimtes tht were ck trnsformed using the inverse logit (verge: exp(p)/(exp(p) + ); SE: exp(p ± SE)/ (exp(p ± SE) + )) Reltive mine depth.75.5.25 n.s. 42 23 Ntive Non-ntive.75.5.25..2.3 Proportion of mines Fig. 6 Reltive depth of the lrvl mines in the hypnthium. The verge reltive depth of the lrvl mines in ntive nd non-ntive rose hips (); shown re the verge ±SE, including smple size nd significnce level. The histogrm shows the distriution of the reltive depth of lrvl mines in ntive nd non-ntive rose hips comined (). In oth grphs, the dotted line represents reltive depth of.5 Thickness hypnthium (± mm) 4 3 2 lrvl mines re in the inner prt of the hypnthium, wy from the ccess points of the wsps (Fig. 6). Discussion 43 Ntive Non-ntive Depth lrvl mines (± mm) *** 4 *** 43 23 Ntive Non-ntive Fig. 5 Thickness of the hypnthium () nd depth of the lrvl mines () in ntive roses (Ros spp.) nd non-ntive roses (R. rugos). Shown re the verge ±SE, including smple size nd significnce level. Mesurements of the thickness of the hypnthium t ll five positions (Fig. 2, 5) nd mesurements of the depth of the lrvl mines t ll four sections (Fig. 2 d) re comined. The horizontl lines represent the verge length of the ovipositor of the prsitic wsps; dotted line: Utetes ferrugtor, dshed line: Psyttli crint In this study, we compred the differences in size nd prsitiztion frequency etween lrve of the tephritid fruit fly (R. lternt) feeding on the fruits of ntive rose species (Ros spp.) nd the non-ntive rose R. rugos. These differences were linked to the size of the rose hips nd the ccessiility of the fruit fly lrve y prsitoids. Differences in these fruit fly trits indicte possile fitness enefits for R. lternt. 3 2 The hips of R. rugos re much hevier thn the hips of ntive roses (Leclire nd Brndl 994). Therefore, differences cn e expected etween herivores tht feed on them. Leclire nd Brndl (994) showed tht R. lternt lrve feeding on rose hips of R. rugos re hevier nd tht their developmentl time is shorter compred with lrve feeding on ntive roses. This corresponds with our findings tht R. lternt pupe re oth lrger nd hevier when the lrve fed on rose hips of R. rugos. This size difference will proly give the flies fitness dvntge during their dult life, since lrvl ody size is positively correlted with fecundity in mny insect species (Liedo et l. 992; Leclire nd Brndl 994; Yoshimur 23). On the other hnd, fitness of flies nd prsitoids my e differentilly ffected y the feeding of irds nd other frugivores on the rose hips. If we ssume tht non-ntive hosts re eten more often, this would result in n overestimtion of fly nd prsitoid survivl on non-ntive roses. To our knowledge, no studies hve thus fr reported on differentil rose hip consumption etween ntive nd nonntive roses. The difference in prsitiztion rte etween the ntive nd non-ntive roses ws very lrge. R. lternt lrve were prsitized five times less frequently in R. rugos hips thn in the ntive roses. This mens tht lrve hve incresed survivl chnces when feeding on R. rugos. Comprison of the length of the ovipositor of the wsps, the thickness of the hypnthium nd the (reltive) depth of the lrvl mines suggest tht the lrve escpe prsitiztion. In the hips of the ntive roses, most of the lrvl mines were within rech of the wsp s ovipositor, while in the hips of the non-ntive roses, mny were out of rech. Furthermore, the fct tht most mines were positioned in the inner prt of the hypnthium, wy from the ccess 3
Oecologi (26) 8:85 92 points of the wsps, suggests ctive voidnce of prsitiztion y the lrve. Similr results hve een found in the olive fruit fly Bctrocer olee (Dipter: Tephritide), which is prsitized y different species of rconid wsps, e.g., Psyttli concolor nd Brcon celer (Sime et l. 26, 27; Dne et l. 28). The prsitiztion rte is ffected y the thickness of the mesoderm of the olives (Ole europe), rnging from ±6 % in smll olives to < % in lrge olives (López et l. 999; Wng et l. 29, ). Prsitiztion rte my depend on severl fctors. Higher host densities my led to higher prsitiztion rtes ecuse prsitoids sty longer in rich res (Godfry 994). We did not determine rose hip infesttion rtes, ut Leclire nd Brndl (994) found threefold higher numer of eggs per rose hip in Europen study. We collected fewer non-ntive rose hips nd found fewer lrve in them, ut we do not know the numer of lrve per rose hip. We cn therefore not determine whether non-ntive roses provide richer host environment for the prsitoids. However, we find lower prsitiztion rte t non-ntive roses, which indictes tht lrve in non-ntive rose hips hve lower chnce of prsitiztion. There re few spects of our study tht need further investigtion. Determining ctul prsitiztion rtes requires the counting of eggs nd mesuring deth of non-prsitized (flies) nd prsitized hosts (wsps) t erly developmentl stges. Survivl rtes of fly eggs nd lrve, either prsitized or not, might e influenced y pthogens in the rose hip. Although lortory studies in Drosophil do not show severe effects on lrvl survivl s consequence of ovipositor intrusion, little is known out this under nturl conditions. There my lso e effects of phenology. The ripening of the non-ntive fruits is spred out over lrger time period. Depending on voltinism, erly seson lrve my experience different prsitism rte thn lte seson lrve. It is not exctly known t wht stge of fruit development the flies oviposit nd t wht stge fly lrve re prsitized y the wsps. This my ffect how strongly prsitiztion risk is dependent on ovipositor length nd lrvl mine depth. Solving these issues requires more detiled studies of fly nd wsp oviposition ehvior in reltion to the full rose ripening seson. Host shifting cn led to host-ssocited differentition nd specition. This process hs een documented especilly frequently for herivorous insects. Until now, no genetic differentition hs een found etween R. lternt flies infesting different ntive roses (Kohnen et l. 29; Vupel et l. 27), ut it remins unknown whether there is host-ssocited differentition etween the popultions on the ntive nd those on the non-ntive roses. It is lso of interest tht host-ssocited differentition in herivorous insects cn led to host-ssocited 9 differentition in their prsites nd predtors (Stiremn et l. 26). The gll-inducing fly Eurost solidginis (Dipter: Tephritide), for exmple, formed two different host rces on Solidgo ltissim nd S. gignte. E. solidginis is preyed upon y the tumling flower eetle Mordellisten convict (Coleopter: Mordellide). The predtor M. convict in turn developed host rces tht differ in emergence time, mte ssorttively, prefer flies on the ntl host plnt, nd hve higher survivl on flies from ntive host plnts (Eunks et l. 23). Similrly, the prsitic wsp Dichsm lloeum (Hymenopter: Brconide) diverged into two incipient species following the divergence of its host, pple mggot fly, Rhgoletis pomonell. The ntive hosts re hwthorns (Crtegus spp.) nd the non-ntive hosts re pples (Mlus domesticus) (Fores et l. 29). Our results contriute to the understnding of wht cn hppen to non-ntive species tht re introduced into new res. Mny such introductions my go unnoticed ecuse the introduced species is not dpted to its new environment nd dies out. In some cses, however, species my ecome estlished nd rpidly increse in numer, cquiring the sttus of pest. Such species often hve few or no nturl enemies in their novel environment. The system we studied, however, consists of n introduced plnt eing used s host y ntive herivore. We found cler fitness dvntges of R. lternt lrve feeding on nonntive rose hips compred to ntive rose hips. We do not know whether the estlishment or competitive ility of R. rugos is ffected y this herivory, ut our dt show tht introduction of novel plnt cn crete new niche for ntive insect. Moreover, they revel tht ntive herivore tht switches to novel non-ntive host cn experience fitness enefits through relese from prsitiztion compred to its originl ntive host. Whether this in turn increses the competitive ility of the ntive roses requires further investigtion. Acknowledgments We thnk Kees vn Achtererg (Nturlis Biodiversity Center) for the identifiction of hymenopterns, John Smit (EIS-Nederlnd, Leiden) for informtion on R. lternt, nd Jco Hogendorf for technicl support. We thnk two nonymous reviewers nd Thoms Hoffmeister for vlule comments on this mnuscript. Author contriution sttement KM conceived, designed nd performed the experiments, nlyzed the dt nd wrote the mnuscript; CS, MS nd LWB supervised the project nd ssisted in writing the mnuscript; MS nd LWB otined the funding. Funding This study ws funded y the Uyttenoogrt-Elisen Foundtion. Complince with ethicl stndrds Conflict of interest The uthors declre tht they hve no conflict of interest. 3
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