Oecologi (27) 153:461 47 DOI 1.17/s442-7-743-x COMMUNITY ECOLOGY Invding rinow trout usurp terrestril prey susidy from ntive chrr nd reduce their growth nd undnce Colden V. Bxter Kurt D. Fusch Msshi Murkmi Phillip L. Chpmn Received: 6 Mrch 27 / Accepted: 26 Mrch 27 / Pulished online: 26 My 27 Springer-Verlg 27 Astrct Movements of prey orgnisms cross ecosystem oundries often susidize consumer popultions in djcent hitts. Humn disturnces such s hitt degrdtion or non-ntive species invsions my lter the chrcteristics or fte of these prey susidies, ut few studies hve mesured the direct evects of this disruption on the growth nd locl undnce of predtors in recipient hitts. Here we present evidence, otined from comined experimentl nd comprtive study in northern Jpn, tht n invding strem Wsh usurped the Xux of llochthonous prey to ntive Wsh, consequently ltering the diet nd reducing the growth nd undnce of the ntive species. A lrge-scle Weld experiment showed tht excluding terrestril Communicted y Pete Peterson. Electronic supplementry mteril The online version of this rticle (doi:1.17/s442-7-743-x) contins supplementry mteril, which is ville to uthorized users. C. V. Bxter K. D. Fusch Grdute Degree Progrm in Ecology, nd Deprtment of Fish, Wildlife, nd Conservtion Biology, Colordo Stte University, Fort Collins, CO 8523, USA M. Murkmi Field Science Center for the Northern Biosphere, Tomkomi Reserch Sttion, Hokkido University, Tomkomi, 53-35, Jpn P. L. Chpmn Deprtment of Sttistics, Colordo Stte University, Fort Collins, CO 8523, USA C. V. Bxter (&) Deprtment of Biologicl Sciences, Idho Stte University, Poctello, ID 8329, USA e-mil: xtcold@isu.edu invertertes tht fell into the strem with mesh greenhouse reduced terrestril prey in diets of ntive Dolly Vrden chrr (Slvelinus mlm) y 46 7%, nd reduced their growth y 25% over six weeks. However, when nonntive rinow trout (Oncorhynchus mykiss) were introduced, they monopolized these prey nd cused n even greter reduction of terrestril prey in chrr diets of 82 93%, nd reduced chrr growth y 31% over the sme period. Adding oth greenhouse nd rinow trout tretments together produced similr results to dding either lone. Results from comprtive Weld study of six other strem sites in the region corroorted the experimentl Wndings, showing tht t invded sites rinow trout usurped the terrestril prey susidy, cusing more thn 75% decrese in the iomss of terrestril invertertes in Dolly Vrden diets nd forcing them to shift their forging to insects on the strem ottom. Moreover, t sites with even low densities of rinow trout, iomss of Dolly Vrden ws more thn 75% lower thn t sites without rinow trout. Disruption of resource Xuxes etween hitts my e common, ut unidentiwed, consequence of invsions, nd n dditionl mechnism contriuting to the loss of ntive species Keywords Hokkido Jpn Invsion ecology Oncorhynchus mykiss Resource susidies Slvelinus mlm Introduction Ecologists hve recently focused reserch on the movement of prey, mterils, nd energy cross hitt oundries in order to understnd the importnce of lndscpe physiognomy nd connectivity to popultion nd ecosystem
462 Oecologi (27) 153:461 47 processes (Polis et l. 1997, 24; Power nd Riney 2; Nkno nd Murkmi 21). In prticulr, susidies of prey from donor to recipient hitts my support n incresed undnce of predtors, which in turn depresses locl prey popultions nd results in cscding indirect evects on the recipient communities. Indeed, these indirect evects hve received gret del of ttention from reserchers (Nkno et l. 1999c; Murkmi nd Nkno 22; So nd Power 22). In contrst, considerly less ttention hs een given to studying the direct evects of prey susidies on the ehvior, growth, nd undnce of recipient predtors themselves (ut see Duggins et l. 1989; So nd Power 22; Kwguchi et l. 23), despite the importnce of understnding these linkges for predicting popultion responses to humn-cused disturnces of lndscpes. Hitt degrdtion nd introductions of non-ntive species re two importnt humn disturnces tht my lter these prey susidies. Evidence otined from experiments on linked strem-forest ecosystems indictes tht either type of disturnce cn trigger complicted indirect evects in the recipient food wes (Nkno et l. 1999c; So nd Power 22; see Bxter et l. 25 for review). For exmple, we recently reported results from Weld experiment which showed tht n invding strem Wsh dominted terrestril inverterte prey susidy nd cused trophic cscde within the strem community, ut it lso hd indirect evects tht reduced reciprocl susidy of emerging insects ck to the forest nd cused riprin spiders to decline s result (Bxter et l. 24). In contrst, to dte there hve een no focused studies of the direct evects of non-ntive species invsions on ntive consumers y ltering the fte or chrcteristics of prey susidies. Moreover, knowledge of the individul nd popultion-level responses of consumers tht precipitte the indirect evects is often key to understnding higher-order evects in communities nd ecosystems (Werner 1992; Pecor nd Werner 1997; Trussell et l. 23). A second issue is tht lthough experiments on these food we susidies hve ll een conducted in the Weld, nd t reltively lrge scles, most hve een reltively short term, rising concern out whether they cn e generlized to rel popultions in complex lndscpes (Peckrsky et l. 1997; Englund nd Cooper 23). A useful strtegy for ddressing these concerns is to conduct oth controlled Weld experiments nd comprtive Weld studies (Dimond 1986; Polis et l. 1998; Power et l. 1998), which llows more sophisticted understnding of the extent to which the experimentl results cn e scled up to the lndscpe level nd generlized to longer time periods. Such complementry pproches re reltively rre in ecology, ut they re essentil ecuse they provide oth experimentl evidence for mechnisms of ecologicl processes nd empiricl evidence for their generlity in rel systems (Resetrits nd Bernrdo 1998). Here we report new results from our lrgescle Weld experiment tht show the direct evects of n invding strem Wsh on the diet nd growth of the ntive Wsh species. We couple this with Wndings from complementry, comprtive Weld study, imed t (1) testing whether the evects on diet tht we found in our experiment in one strem could e demonstrted in set of other similr strems (i.e., expnding the sptil scle), nd (2) evluting the long-term consequences of this invsion for the undnce of the ntive species (extending the temporl scle). Mterils nd methods We chose study system in which terrestril inverterte prey re n importnt susidy for ntive strem Wsh, ut which is simultneously eing invded y non-ntive Wsh tht my disrupt this susidy. Ntive Dolly Vrden chrr (Slvelinus mlm; S1 of Supplementry Mteril) inhit strems of Hokkido Islnd, northern Jpn, nd derive out 5% of their nnul energy from terrestril invertertes (Nkno et l. 1999c; Kwguchi nd Nkno 21; Nkno nd Murkmi 21; Kwguchi et l. 23), ut the evect of ltering this susidy on chrr growth is unknown. Non-ntive rinow trout (Oncorhynchus mykiss) re rpidly invding Hokkido strems (Tkmi nd Aoym 1999; Fusch et l. 21) nd this species lso forges preferentilly on terrestril invertertes (Nkno et l. 1999). Therefore, if the non-ntive Wsh usurps the susidy of terrestril prey, we predicted tht this would hve direct negtive evects on the diet, growth, nd undnce of the chrr. Field experiment We conducted lrge-scle Weld experiment imed t mesuring the evects of the non-ntive trout invder on the susidy of terrestril prey nd, consequently, on the diet nd growth of the chrr. These evects were compred to those from n experimentl mnipultion tht reduced the susidy directly. The experiment ws conducted in Horoni Strem, smll spring strem drining n undistured wtershed in the Hokkido University Tomkomi Experimentl Forest (descried in detil in Nkno et l. 1999c). Terrestril prey input nd rinow trout were mnipulted in 2 2 fctoril design, which hs een descried previously in Bxter et l. (24). The four tretments were: (1) control (Dolly Vrden t nturl density); (2) wild rinow trout dded t nturl densities; (3) mesh greenhouse tht reduced the input of terrestril prey (Nkno et l. 1999c); (4) oth rinow trout nd the mesh greenhouse dded. We used rndomized complete lock design in which 16
Oecologi (27) 153:461 47 463 fenced reches [length 27.5.7 m (men 1 SE), 1- m 2 surfce re] were divided into four locks, from upstrem to downstrem, nd four replictes of ech tretment were rndomly ssigned within ech lock. After removing ll slmonids, ntive wild Dolly Vrden [134.1.9 mm (men SE) fork length (FL)] were dded to ech rech to chieve densities similr to those previously mesured in undistured Hokkido strems (.4/ m 2 ; Fusch et l. 1994; Nkno et l. 1999). Likewise, wild rinow trout of similr sizes (144.9 2.3 mm) were dded to hlf the reches t the density previously estimted for Horoni Strem (.2/m 2 ; Nkno et l. 1999). This dditive design hs een recommended for mesuring evects of non-ntive Wshes ecuse it mimics the initil stges of invsion (Fusch 1998; Peterson nd Fusch 23). Greenhouses constructed of trnsprent 1-mm nylon mesh supported y luminum frmes (see Bxter et l. 24; Fig. 2) were used to cover hlf of the reches to exclude the input of terrestril prey, nd extended 25 m upstrem to reduce the mount of prey drifting into reches. The mesh ws pinned long the strem nks to exclude flling input from ll ut very nrrow strip of vegettion (<.5 m wide), nd oth ends were locked to prevent Xying insects from entering. Roof windows were cut t ech end to llow emerging qutic insects to escpe (Nkno et l. 1999c). The greenhouses hd miniml evects on light nd wter temperture eneth the closed deciduous forest cnopy (Bxter et l. 24). The experiment ws conducted for 6 weeks, from 11 June to 22 July 22, which is time period when terrestril prey input to the strem is normlly reltively high (Nkno nd Murkmi 21). In ech rech we mesured the iomss of flling nd drifting terrestril invertertes nd the diets nd growth of Wsh. Methods for mesuring these components hve een descried in detil in Bxter et l. (24) nd generlly followed those used in previous reserch (Nkno et l. 1999c; Kwguchi nd Nkno 21; Nkno nd Murkmi 21). The iomss of terrestril invertertes flling into ech rech ws mesured four times during the experimentl period for 3-dy intervls using pn trps, nd the iomss drifting into ech rech ws mesured twice for 2-min intervls using drift nets set t dusk. To estimte the terrestril nd qutic prey in the Wsh diets, we recptured Wsh from ech rech t the middle nd end of the experiment y two-pss electrowshing. Ten to Wfteen of the recptured Wsh per species from ech rech were then nesthetized nd the diet contents collected using pipette to Xush prey items from the stomchs (Giles 198). Diet dt for the second hlf of the experiment hve een reported in Bxter et l. (24), ut these re included here for completeness to llow comprisons. To mesure growth, we mrked ll Wsh efore the experiment with Xuorescent elstomer dye (red, yellow, pink, nd ornge; Northwest Mrine Technology, Shw Islnd, Wsh.). Ech Wsh received unique comintion of two mrks, rryed mong Wn rys, dipose tissue ehind the eyes, nd the ventrl surfce of the lower jw. All mrked Wsh tht were recptured in ech smple were mesured (nerest 1 mm FL), nd the ody mss ws determined using n electronic lnce (nerest.1 g). After recovery, the Wsh were returned to their rech. Dt from the experiment were nlyzed using two-wy ANOVA for rndomized complete-lock designs with repeted mesures (SAS 1999). The greenhouse nd rinow trout tretments were oth Wxed fctors. In one rech with the rinow trout tretment, the Wsh suvered hevy predtion y mink (Mustel vison), which resulted in n inevective tretment. This tretment ws susequently excluded from the dt nlysis. Fish growth dt were trnsformed using logrithms to stilize vrince. We used plots of residuls versus predicted vlues to evlute the heterogeneity of vrinces nd skewness, ut none were detected. When two- or three-wy interctions etween min evects were detected, tretment mens were compred individully for ech time period using lest signiwcnt diverence (LSD) comprisons. When interctions mong min evects were not detected, the evect of fctor ws exmined y verging over one or more of the other fctors. Comprtive Weld study To determine how well the results from our experiment in one strem scle up, we conducted comprtive study from mid-june to mid-july 23 to mesure Wsh diets nd Wsh density nd size structure in six similr Hokkido strems. We selected pproximtely 1-m reches [length 1.6 5.6 m (men 1 SE)] of smll spring strems similr to Horoni Strem (Supplementry Mteril, S1 nd S2) tht emerge from the Xnks of Yoteizn, lrge volcno in southwestern Hokkido (42 49 N, 14 48 E). The reches were chosen sed on rod survey of Wshes using single-pss electrowshing t 2 sites throughout this region of the Shirietsu River sin. Two of the six reches chosen hd only ntive Dolly Vrden in lloptry, nd four hd oth rinow trout nd Dolly Vrden in symptry. Becuse we nticipted the evects of rinow trout on chrr might vry with invder undnce, we selected two symptric sites with low reltive undnce of rinow trout nd two with higher undnce. To estimte the mount of terrestril nd qutic prey in the Wsh diets, Wsh were cptured y electrowshing during the fternoon on one dte in mid-june t ech site, nd the stomch contents were collected from 1 2 Wsh (minimum FL = 85 mm) per species using stomch lvge (Giles 198). Species undnce nd size structure ws estimted on one dte during mid-july t ech site y three-pss
464 Oecologi (27) 153:461 47 removl electrowshing fter locking the ends of ech site with 4-mm-mesh seines (Riley nd Fusch 1995). Cre ws tken to secure the ottom of the seines with rocks to prevent Wsh from escping. Fish cptured in ech pss were nesthetized, mesured (FL, nerest 1 mm), nd retined in live skets until the electrowshing ws completed. For undnce estimtion, Wsh of ech species were divided into two ge clsses (ge vs. ge 1 nd older) identiwed from length-frequency histogrms. Mximum likelihood popultion estimtes nd prowle likelihood 95% conwdence intervls (Otis et l. 1978) were clculted for ech ge clss of ech species using the progrm CAPTURE (White et l. 1982). The iomss of ech species nd ge clss in ech site ws estimted y multiplying the popultion estimte y the men mss of individul Wsh. The ltter ws estimted using length-weight regressions developed for Dolly Vrden from nother strem in the sin nd for rinow trout from Horoni Strem (C.V. Bxter nd K.D. Fusch, unpulished dt). Chrcteristics of the strem hitt nd riprin vegettion were lso mesured t ech site. Chnnel units were clssiwed s pools, runs, or rizes, nd the length of ech ws mesured. Depth ws mesured t three equidistnt points on trnsect perpendiculr to the Xow t the midpoint of ech chnnel unit, long with wetted width. In the pools, depths nd width were mesured the sme wy on three trnsects t the midpoints of the lower, middle nd upper thirds of the unit, respectively. Mesurements were then used to estimte hitt volume for ech site. The numer of pieces of lrge wood ( 3 cm dimeter, 1 m length) in ech rech nd the dominnt sustrte type [modiwed Wentworth scle (Orth 1983), estimted visully t ech depth mesurement] were lso recorded. Wter temperture ws monitored t 24-min intervls ner the mid-point of ech site from mid-june to mid-july using dt logger (Onset Corp., Pocsset, Mss.). At ech site, the dominnt species of understory nd overstory riprin vegettion were visully ssessed nd lef re index (LAI, lef re per unit ground re) ws mesured t 1-m intervls long the rech (LAI- 2 Plnt Cnopy Anlyzer; Li-COR Biosciences, Lincoln, Ne.). Dt from the comprtive study were nlyzed using one-wy ANOVA in which sites were nested within tretment. Plnned comprisons mong sites of the three types, s well s etween the two Wsh species, were conducted y the LSD method (SAS 1999). Results Field experiment During the experiment, the flling input of terrestril invertertes into Horoni Strem ws reduced nerly 7% y the greenhouse cover [12.9 2.5 vs. 41.7 6. mg m 2 dy 1 (men 1 SE) in the eight reches with greenhouses vs. eight without; P <.1 y t-test], wheres the drifting input of terrestril invertertes ws similr etween these tretments (.4.1 vs..4.7 mg m 3 ). However, flling input to control reches during the Wrst 3 weeks [herefter period 1; 59. 7.7mgm 2 dy 1 (men 1 SE)] ws more thn twice tht during the lst 3 weeks (period 2; 24.4 3.3mgm 2 dy 1 ; P =.1 y ANOVA for time evect). There were no diverences in terrestril inverterte inputs mong locks during the experiment (P =.85), nor were there signiwcnt lock or lock tretment evects for ny of the response vriles mesured (P >.1). Dolly Vrden in control reches trcked the chnges in terrestril inverterte input through time, ecuse their diets contined twice s much terrestril prey iomss during period 1 s in period 2 (Fig. 1; P =.1 y LSD fter ANOVA). Likewise, the growth in mss of chrr cptured t the end of period 2 ws, on verge, less thn doule tht of those cptured t the end of period 1 in control reches (Fig. 2), indicting tht they grew more during period 1 when the prey susidy ws higher. For ech period, growth ws mesured from the strt of the experiment to enle ll of the dt to e used ecuse diverent suset of Wsh ws recptured in ech smple. Fish in ll tretments grew during the experiment, indicting tht the size of enclosures nd the densities of Wsh were pproprite. Experimentlly reducing terrestril inverterte input to the strem using mesh greenhouses resulted in lower iomss of terrestril prey in the diets of Dolly Vrden chrr (Fig. 1) nd more iomss of enthic strem insects. The min evect of the greenhouse cover on terrestril prey iomss ws not signiwcnt (P =.46), ut there ws signiwcnt two-wy interction (rinow trout greenhouse; P =.9), nd greenhouse time interction ws detected though not signiwcnt (P =.8). When dt from ech smpling period were exmined seprtely, two-wy interctions etween the min evects were signiwcnt for oth time periods (period 1: P =.1; period 2: P =.3). Therefore, LSD comprisons were mde, which showed tht Dolly Vrden diets consisted of 46 7% less terrestril prey in greenhouse versus the control reches during periods 1 nd 2 (period 1: P =.4, period 2: P =.4 y LSD fter ANOVA). Due to the loss of terrestril prey, the diets of Dolly Vrden in reches with greenhouses consisted of 3.1- to 7.5-fold higher iomss of enthic strem insects thn those in control reches [period 1: 1.9.8 vs..62.13 mg (men 1SE), period 2: 1.2.38 vs..16.6 mg]. The min evect of the greenhouse cover on the iomss of enthic prey in Dolly Vrden diets ws signiwcnt (P =.4), s ws the evect of time (P =.5). For period 2, the two-wy interction ws
Oecologi (27) 153:461 47 465 Terrestril invertertes in diet (mg) 3 2 1 15 1 5 3 weeks 6 weeks CTL GH RBT BOTH Tretments Fig. 1 Men iomss of terrestril invertertes in diets of individul Dolly Vrden (Slvelinus mlm, Wlled squre) nd rinow trout (Oncorhynchus mykiss, Wlled circle) fter 3 () nd 6 weeks () in four tretments control (ntive Dolly Vrden only, CTL), greenhouse cover (reduced susidy of terrestril invertertes to strem, GH), rinow trout (non-ntive rinow trout dded, RBT), nd oth greenhouse nd trout dded (BOTH) in reches of Horoni Strem during the summer of 22. Vlues re mens 1SE (n = 4 except n =3 for RBT tretment; see text). DiVerent lowercse letters indicte signiwcnt diverences (P <.5) mong tretments within periods sed on LSD comprisons fter ANOVA of log-trnsformed dt. Dt for pnel re from Bxter et l. (24) lso signiwcnt (rinow trout greenhouse; P =.4), nd the susequent LSD comprison showed tht the diets of Dolly Vrden in the greenhouse reches hd signiwcntly more iomss of enthic insects thn those in the control reches during this period (P =.2). When terrestril prey inputs were reduced with the greenhouse cover, the growth of Dolly Vrden chrr lso decresed, ut this evect ws not mnifested until the end of the experiment. The min evect of the greenhouse cover on growth ws not signiwcnt (P =.28), ut the evect of time ws (P =.1), nd three-wy interction (rinow trout greenhouse time) ws detected, lthough it ws not signiwcnt (P =.9). When dt from ech time period were exmined seprtely, two-wy interctions etween the c c c c min evects were not signiwcnt fter 3 weeks (P =.84), ut they were nerly signiwcnt fter 6 weeks (P =.6). The greenhouse hd no detectle evect on chrr growth fter the Wrst 3 weeks (Fig. 2; P =.7 for greenhouse min evect), ut chrr growth ws 25% lower in the greenhouse versus the control reches y the end of the experiment, which ws signiwcnt diverence (P =.3, y LSD). In the tretment where rinow trout were dded, they consumed most of the terrestril invertertes, pprently forcing Dolly Vrden to shift to forging on enthic insects from the stremed. Rinow trout cused n 82 93% reduction in the iomss of terrestril prey in Dolly Vrden diets during the two smple periods compred to control reches (Fig. 1; period 1: P <.1, period 2: P =.4, y LSD; see ove for interction evects). In turn, this resulted in 1.6- to 4.5-fold increse in the iomss of enthic insects in Dolly Vrden diets compred to controls [period 1:.97.34 vs..62.13 mg (men 1SE), P =.49 for rinow trout min evect; period 2:.72.12 vs..16.6 mg, P =.8, y LSD; see ove for interction. However, the switch to enthic forging did not occur s soon or s strongly s tht induced y the greenhouse tretment. The ddition of rinow trout lso cused 38 nd 31% reduction in the growth of Dolly Vrden y the end of periods 1 nd 2, respectively (Fig. 2), with the decresed growth ppering sooner thn in the greenhouse cover tretment in which prey inputs were directly reduced. Chrr growth ws lower in reches with rinow trout thn in control reches during period 1 (P =.9 for rinow trout min evect; see ove for non-signiwcnt rinow trout greenhouse interction) nd ws lso signiwcntly lower y the end of the experiment (P =.2 y LSD; see ove for interction). Furthermore, rinow trout gined signiwcntly more weight thn symptric Dolly Vrden when verged over the entire experiment (Fig. 2; P =.2 y LSD; the evect of time ws not signiwcnt, P =.13) ut grew similr mount s Dolly Vrden in control reches. Tken together, the results from the two single tretments showed tht the evect of dding rinow trout on diet nd growth of ntive Dolly Vrden ws s strong, or stronger, in every cse thn experimentlly excluding terrestril prey input using mesh greenhouse. Adding oth the greenhouse nd rinow trout tretments together produced similr results to dding either lone (Figs. 1, 2). In these reches, there ws similr reduction of terrestril prey in chrr diets compred to controls (period 1: P <.1, period 2: P =.2, y LSD), nd corresponding increse in enthic insects consumed [period 1: 1.4.24 vs..62.13 mg (men 1SE), see signiwcnt greenhouse min evect ove; period 2:.95.22 vs..16.6 mg, P =.2, y LSD]. Chrr growth ws reduced reltive to control reches y 41% during the Wrst 3 weeks nd 24% over 6 weeks (period 1:
466 Oecologi (27) 153:461 47 Chnge in fish mss (g) 8 6 4 2 8 6 4 2 Fig. 2 Growth of Dolly Vrden (Wlled squre) nd rinow trout (Wlled circle) fter 3 () nd 6 weeks () in four tretments control (CTL), greenhouse cover (GH), rinow trout (RBT), nd oth greenhouse cover nd trout (BOTH) in reches of Horoni Strem during the summer of 22. Vlues re mens 1SE (n = 4 replictes except n =3 for RBT tretment, see text). See text for signiwcnce of tretment evects for the 3-week period. DiVerent lowercse letters indicte signiwcnt diverences (P <.5) mong tretments for the 6-week-period sed on LSD comprisons fter ANOVA of log-trnsformed dt P =.15; period 2: P =.4, y LSD). We hd expected tht the evects of rinow trout on chrr might e excerted y excluding terrestril prey, ut insted we oserved tht either tretment lone reduced chrr growth to threshold eyond which the dded tretment elicited no further response. Rinow trout growth ws diminished even more thn chrr growth when terrestril prey inputs were reduced, ut the greenhouse evect for rinow trout ws mrginlly signiwcnt due to the high vrition reltive to smple size (P =.6; neither the evect of time or the time greenhouse interction were signiwcnt, P >.1). Comprtive study 3 weeks 6 weeks CTL GH RBT BOTH Tretments The six sites selected for the comprtive study hd similr strem hitt nd riprin vegettion (S2), nd strem width, depth, hitt volume, lrge wood, nd lef re index did not diver etween sites with nd without rinow trout (P.25 y one-wy ANOVA). However, sites without rinow trout hd lower (though not signiwcntly diverent) men tempertures in June July 23 thn those with rinow trout [S2; 7..1 vs. 1.5.6 C (men 1SE); P =.9 y ANOVA]. We sw no evidence of ngling t ny site. In ccordnce with our experimentl results, Dolly Vrden t sites with rinow trout hd 78% lower iomss of terrestril inverterte prey in their diets, on verge, thn chrr t sites without the invding species (Fig. 3; P =.5 y one-wy ANOVA). This ws true whether rinow trout were present t low or pproximtely equl reltive undnce (P =.4 nd.3, respectively, y LSD fter ANOVA) nd could not e explined y diverences in the sizes of chrr smpled for diets, which were similr mong the three groups of sites [FL = 126 2.8 mm (men 1SE); P =.5 y ANOVA]. With respect to proportions, terrestril prey constituted 78% of the iomss of diets of Dolly Vrden in lloptry ut mde up signiwcntly lower proportion (48%, on verge, with corresponding increse in the proportion of enthic strem insects) when rinow trout were present (P =.4 y ANOVA fter rcsine squre root trnsformtion). This reduction ws greter when the reltive undnce of rinow trout ws equl to tht of Dolly Vrden thn when it ws lower [35 6 vs. 6 6% terrestril prey (men 1SE); P =.2 y LSD]. At invded sites, rinow trout consumed similr iomss nd proportion of terrestril invertertes s Dolly Vrden did t lloptric sites (Fig. 3; P =.8 nd.3, respectively, y ANOVA), suggesting tht diverences in Dolly Vrden diets were driven y the presence of rinow trout rther thn y diverences in terrestril prey vilility mong sites. The undnce (Tle 1) nd iomss (Fig. 3) of Dolly Vrden ws lower t sites where rinow trout were present thn t sites where they were sent. The iomss of ll ge clsses of Dolly Vrden comined ws 77% lower, on verge, t sites with rinow trout thn t those where Dolly Vrden were lloptric (P =.8 y ANOVA). Moreover, the iomss of Dolly Vrden ws similrly reduced whether rinow trout were present t low or out equl reltive undnce (P =.4 nd.6, respectively, y LSD). Age- Dolly Vrden were lso lest undnt t sites with rinow trout nd most undnt t one of the sites without rinow trout (Tle 1). Likewise, high undnce of juvenile (ge-1) Dolly Vrden t sites without rinow trout ws ssocited with lower men lengths of ge-1+ chrr thn t sites with rinow trout (Tle 1; P <.3 y LSD fter ANOVA). In contrst, ge- rinow trout were cptured t sites with higher undnce of rinow trout ut not t those with low undnce of
Oecologi (27) 153:461 47 467 Terr est ril inve rte rte s i n di et (mg ) ) -1 Fi sh ioms s (kg h 6 45 3 15 8 6 4 2 Fig. 3 Biomss of terrestril invertertes in Wsh diets () nd of two slmonids (ll ge clsses) () in strem reches in southwestern Hokkido with ntive Dolly Vrden lone (DV), Dolly Vrden nd low densities of non-ntive rinow trout (DV + low RBT), or Dolly Vrden nd rinow trout in out equl reltive undnce (DV = RBT) during the summer of 23. Diets nd iomss of Dolly Vrden (Wlled squre) nd rinow trout (Wlled circle) re shown. Vlues re mens 1SE (n =2). DiVerent lowercse letters indicte signiwcnt diverences (P <.5) mong tretments sed on LSD comprisons fter one-wy ANOVA rinow trout (Tle 1), suggesting tht little recruitment ws occurring for either species t the ltter sites. When estimtes for Dolly Vrden nd rinow trout were comined, we found tht totl slmonid iomss ws similr t sites with higher reltive undnce of rinow trout compred to those with only Dolly Vrden (P =.23 y LSD), ut tht it ws nerly 7% lower t sites where rinow trout were present t low densities (P =.3 y LSD). Discussion DV The comined results of our experimentl nd comprtive studies, coupled with our previous work (Bxter et l. 24), indicte tht invding rinow trout disrupt the DV + low RBT Fish species present DV = RBT susidy of terrestril prey to smll spring strems in Hokkido, with strong consequences for the ehvior, growth, nd undnce of ntive chrr tht depend on this resource. Our experiment showed tht terrestril invertertes were not only n importnt component of the diets of ntive Dolly Vrden chrr (see lso Nkno et l. 1999c; Kwguchi nd Nkno 21; Nkno nd Murkmi 21) ut tht they lso strongly Vected their growth. Dolly Vrden in control reches grew the most during the Wrst hlf of the experiment, when mient terrestril prey Xux to the strem ws the highest. Experimentlly reducing this susidy to Dolly Vrden using mesh greenhouse cused the Wsh to shift to forging on enthic strem insects (Nkno et l. 1999, c) nd reduced their growth y 25% over 6 weeks. Moreover, this evect ws likely conservtive ecuse terrestril inverterte input into Horoni Strem in the summer of 22 ws 34 63% lower thn tht mesured during the summer in two erlier studies (Nkno et l. 1999c; Nkno nd Murkmi 21). Kwguchi et l. (23) conducted similr short-term experiment in the sme strem nd showed tht when terrestril inverterte input ws reduced using greenhouse covers, Wsh iomss in un-fenced 5-m reches (those in our study were fenced) quickly decresed y nerly 5% ecuse Wsh emigrted, pprently redistriuting themselves in proportion to prey vilility. Together, these Wndings indicte tht ny fctor tht lters the chrcteristics or fte of this prey susidy is likely to reduce the growth or the undnce of ntive chrr popultions. Our comined studies lso demonstrted tht invding rinow trout directly usurped the susidy of terrestril inverterte prey from Dolly Vrden. Fish diet dt from our experiment showed tht rinow trout were evective t monopolizing the prey susidy, nd forced the ntive chrr to shift their forging to picking enthic insects from the stremed (see Fusch et l. 1997; Nkno et l. 1999). The comprtive study showed tht the iomss of terrestril prey in Dolly Vrden diets in other smll spring strems in Hokkido ws reduced y more thn 75% when rinow trout were present t either lesser or equl densities, indicting tht this shift in forging ehvior is generl phenomenon. Moreover, in the experiment, rinow trout reduced the iomss of terrestril prey in diets of Dolly Vrden during oth periods y 82 93%, which ws more reduction thn ws cused y the direct exclusion of terrestril prey using the greenhouse. Likewise, the 31% reduction in chrr growth cused y rinow trout during the experiment ws greter thn tht cused y excluding terrestril prey inputs ltogether. Underwter oservtions suggested tht the min mechnism for these evects ws tht rinow trout not only usurped the prey susidy, ut lso dominted the chrr ehviorlly, forcing them to leve loctions prowtle for drift forging (Bxter et l. 24) nd reducing their totl dytime forging rte (drift
468 Oecologi (27) 153:461 47 Tle 1 Estimtes of Wsh undnce for ge- nd ge-1 nd older (ge-1+) Wsh from the six sites surveyed in the comprtive study of strems in southwestern Hokkido during the summer of 23. Dt re sed on mximum likelihood popultion estimtes from removl electrowshing. Numers in prentheses show the prowle likelihood 95% conwdence intervls.the totl numer of Wsh cptured is shown for three cses where either smll smple size or the lck of depletion precluded clculting undnce estimtes. Also shown re fork lengths (mm, men 1 SE) for ge-1+ Wsh Slmonid Site Dolly Vrden Rinow trout composition Aundnce Age-1 + Aundnce Age-1 + men length men length Age- Age-1+ Age- Age-1+ DV NN 345 (287 475) 364 (349 386) 92.5 (1.) DV SN 27 c 199 (179 24) 88.5 (1.6) DV + low RBT UM 24 (22 35) 1 (1 13) 126.2 (7.5) 9 (9 9) 133.3 (14.5) DV + low RBT UK 4 (4 5) 22 (22 24).8 (4.9) 7 (7 7) 176.3 (16.) DV = RBT LM 51 (45 74) 11 (11 13) 142 (6.8) 15 (15 21) 19 (19 19) 144.7 (8.2) DV = RBT LK 2 11 (11 13) 134.2 (8.7) 6 27 (27 42) 132.1 (9.) Sites hd either ntive Dolly Vrden chrr in lloptry (DV), Dolly Vrden nd low reltive undnce of non-ntive rinow trout (DV + low RBT), or Dolly Vrden nd rinow trout in pproximtely equl reltive undnce (DV = RBT) NN, North Fork Nnetsu Strem; SN, South Fork Nnetsu Strem; UM, Upper Mohnrin Strem; UK, Upper Kshunetsu Strem; LM, Lower Mohnrin Strem; LK, Lower Kshunetsu Strem c Shllow, complex, side-chnnel hitt prevented dequte depletion of ge- Dolly Vrden t this site nd enthic comined) y 66% (D.J. Jordn nd C.V. Bxter, unpulished dt). Thus, despite eing similr in size, the invder ws pprently superior due to comintion of oth exploittive nd interference competition. An lterntive hypothesis to explin the reduced chrr growth cused y rinow trout in the Weld experiment is tht the incresed totl Wsh density speciwed y the dditive design simply reduced verge prey vilility to ll Wsh. However, in ddition to the ehviorl oservtions reported just ove, the oservtionl study showed tht the iomss of terrestril invertertes in Dolly Vrden diets ws gretly reduced in the presence of either low or high undnce of rinow trout, even when totl Wsh iomss ws lower thn when chrr were lone. Tken together, this evidence indictes tht the forging shift y Dolly Vrden nd the resulting evects on chrr growth were due primrily to the presence of rinow trout, nd not solely to diverences in Wsh density. We suspect tht ntive slmonids in other regions might e similrly Vected ecuse mny of these consume terrestril prey (Bxter et l. 25), nd rinow trout re the most widely introduced Wsh species in the world (Fusch et l. 21). Our experimentl nd comprtive study results indicte tht domintion of the terrestril inverterte susidy y rinow trout, coupled with interference competition, my e the primry reson tht ntive Dolly Vrden popultions were lower when rinow trout were present. Rinow trout invsion pprently resulted in 77% decrese in Dolly Vrden iomss, on verge, t the invded sites in the comprtive study, even though the hitt ws similr. To our knowledge, there re no resons other thn the presence of rinow trout tht cn explin this low Dolly Vrden undnce. Dolly Vrden were historiclly common in smll strems of this region (Ishigki 1984; Fusch et l. 1994), the hitt ws suitle t ll sites nd throughout the length of invded strems to sustin undnt Dolly Vrden, nd there ws no evidence of ngling. Likewise, the temperture ws within the optimum rnge for chrr t ll sites smpled (Kitno et l. 1995; Nkno et l. 1996; Tkmi et l. 1997). Although the mechnisms responsile for ntive chrr declines re uncertin, loss of the terrestril susidy diminishes Dolly Vrden growth, which proly reduces fecundity nd recruitment. Indeed, t most of the sites where rinow trout were present, we found few ge- or juvenile Dolly Vrden. Rinow trout might lso reduce Dolly Vrden y predtion on ge- chrr (see Tniguchi et l. 22) nd y disturing chrr redds (nests) y uilding their own in the sme stremed loctions nd displcing chrr eggs or newly htched fry (Tniguchi et l. 2). In ddition, Kwguchi et l. (23) showed tht excluding terrestril prey, s rinow trout do, cused Dolly Vrden to emigrte. Regrdless of the comintion of mechnisms, the prolem is likely to e widespred ecuse rinow trout re rpidly invding other Hokkido strems (Tkmi nd Aoym 1999) nd hve een reported to displce Dolly Vrden s well s other ntive slmonids such s white-spotted chrr (Slvelinus leucomenis), Skhlin timen (Hucho perryi), nd msu slmon (O. msou; Hsegw et l. 24; Kitno 24; Morit et l. 24). Our use of complementry experimentl nd comprtive studies provided us with more thorough perspective on the importnce of the prey susidy nd the evects of the non-ntive Wsh invsion thn either pproch lone could hve. The controlled experiment llowed us to mesure the
Oecologi (27) 153:461 47 469 evects on ehvior, diet, nd short-term growth responses of the consumer, ut not on movement (ut see Kwguchi et l. 23) or long-term demogrphic responses. In contrst, the comprtive study did not llow for the control of other externl fctors (e.g., Wsh density, diverences in strem nd riprin forest productivity, time since invsion) ut did increse conwdence in the relism of the experiment nd the generlity of our Wndings nd enled n investigtion of popultion responses over longer term nd t lrger sptil scles. Other investigtors reported tht ecologicl processes mesured in smll-scle lortory nd Weld experiments often could not e successfully extrpolted to lrger scles (e.g., Peckrsky et l. 1997; Cooper et l. 1998). In contrst, the processes we discovered using reltively lrge-scle Weld mnipultions in pproximtely 3-m reches rryed over 1.7-km strem segment mtched those mesured in set of similr smll strems elsewhere in Hokkido. This gve us conwdence tht the Weld experiment encompssed criticl ecologicl processes nd sptil heterogeneity, nd tht it ws conducted over suycient time to detect importnt ecologicl evects (Englund nd Cooper 23), such s those on Wsh diet nd Wsh growth. Such integrted, multi-scle pproches hve een proposed s the wy forwrd in ecology (Polis et l. 1998; Power et l. 1998), nd re needed to gin fuller understnding of the role of prey susidies in food wes s well s the possile consequences should they e disrupted or lost (Bxter et l. 25). In the literture on invsion iology, most direct evects reported for invding species re overt, such s driving ntive species extinct y predtion, monopolizing spce, or trnsmitting diseses (SimerloV 1997; Prker et l. 1999). However, our studies hve demonstrted tht invding species cn lso disrupt the Xow of llochthonous resources cross hitt oundries y directly usurping prey orgnisms tht would otherwise susidize ntive consumers. Recent investigtions hve shown tht other similr evects re lso possile, such s invders tht monopolize resources which re importnt to consumers in other hitts. For exmple, non-ntive trout introduced to high-elevtion lkes in Cliforni reduce mphiin lrve through predtion, which my decrese grter snkes (Thmnophis elegns) tht lso prey on these mphiins in oth qutic nd djcent terrestril hitts (Mtthews et l. 22). In ddition, invders my compete directly with the species tht provides the cross-hitt susidy, s occurred when introduced opossum shrimp (Mysis relict) exploited prey of koknee slmon (O. nerk) in Flthed Lke, Montn, which reduced the susidy of migrting dult slmon to egles nd ers (Spencer et l. 1991). Similrly, the invsion of riprin res y non-ntive moo (Bmus spp.) or sltcedr (Tmrix remosissim) ltered the Xux of plnt detritus to strems (O Connor et l. 2; Kennedy nd Hoie 24), susidy tht fuels mny qutic orgnisms. By ny of these mens, disruption of resource Xuxes tht connect hitts my e n unforeseen impct of invsions nd n dditionl mechnism contriuting to the loss of ntive species. Acknowledgments This reserch could not hve een completed without the help of J. Jordn, K. Ttr, Y. Miyke, A. Uesugi, S. Leser, H. Asno, K. Ono, S. Biley, K. Ross, J. Monroe, Y. Ingki, T. Ishii, Y. Tniguchi, M. Inoue, nd L. Wever-Bxter. We lso received ssistnce from D. Fukui, K. Hsegw, T. Iwt, K. Ksugi, N. Kzhri, D. Kishi, B. KondrtieV, M. Mtsud, M. Miur, H. Miyt, K. Motomori, E. Neshim, T. Nkhr, F. Oke, K. Onishi, T. Sugt, K. Tkhshi, G. Tkimoto, T. Tosuji, H. Ure, H. Yorozuy, nd the stv t the Tomkomi Reserch Sttion. We thnk J. Dunhm, J. Olden, J. Monroe, nd four nonymous reviewers for comments tht improved the mnuscript. Protocols for Wsh smpling were pproved y the Animl Cre nd Use Committee of Colordo Stte University (Protocol 1-164A). This study ws supported y Ntionl Science Foundtion grnt (DEB 18222) to K.D. 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