Oecologia (2009) 161:279–290

DOI 10.1007/s00442-009-1371-4

PLANT-ANIMAL INTERACTIONS - ORIGINAL PAPER

High-quality seed dispersal by fruit-eating Wshes in Amazonian Xoodplain habitats

Jill T. Anderson · Joe Saldaña Rojas · Alexander S. Flecker

Received: 17 April 2008 / Accepted: 4 May 2009 / Published online: 24 May 2009© Springer-Verlag 2009

Abstract Seed dispersal is a critical stage in the life his-tory of plants. It determines the initial pattern of juveniledistribution, and can inXuence community dynamics andthe evolutionary trajectories of individual species. Verte-brate frugivores are the primary vector of seed dispersal intropical forests; however, most studies of seed dispersalfocus on birds, bats and monkeys. Nevertheless, SouthAmerica harbors at least 200 species of frugivorous Wshes,which move into temporarily Xooded habitats duringlengthy Xood seasons and consume fruits that fall into thewater; and yet, we know remarkably little about the qualityof seed dispersal they eVect. We investigated the seed dis-persal activities of two species of large-bodied, commer-cially important Wshes (Colossoma macropomum and

Piaractus brachypomus, Characidae) over 3 years inPacaya-Samiria National Reserve (Peru). We assessed thediet of these Wshes during the Xood season, conducted ger-mination trials with seeds collected from digestive tracts,and quantiWed fruit availability. In the laboratory, we fedfruits to captive Colossoma, quantiWed the proportion ofseeds defecated by adult and juvenile Wsh, and used theseseeds in additional germination experiments. Our resultsindicate that Colossoma and Piaractus disperse large quan-tities of seeds from up to 35% of the trees and lianas thatfruit during the Xood season. Additionally, these seeds cangerminate after Xoodwaters recede. Overexploitation hasreduced the abundance of our focal Wsh species, as well aschanged the age structure of populations. Moreover, olderWsh are more eVective seed dispersers than smaller, juvenileWsh. OverWshing, therefore, likely selects for the poorestseed dispersers, thus disrupting an ancient interactionbetween seeds and their dispersal agents.

Keywords Colossoma macropomum · Germination · OverWshing · Piaractus brachypomus · Regeneration

Introduction

Seed dispersal profoundly inXuences the ecological andevolutionary dynamics of plant species. Dispersal estab-lishes the initial spatial distribution of plants, dictates thepool of interacting species, and thereby contributes to com-munity structure and the maintenance of species diversity(Howe and Smallwood 1982; Russo and Augspurger 2004;Seidler and Plotkin 2006). Gene Xow through seed dis-persal can determine the extent of population diVerentiation(e.g., Gibson and Wheelwright 1995; Garnier et al. 2002),thus inXuencing the evolutionary trajectories of lineages.

Communicated by Jacqui ShykoV.

Electronic supplementary material The online version of this article (doi:10.1007/s00442-009-1371-4) contains supplementary material, which is available to authorized users.

J. T. Anderson · A. S. FleckerDepartment of Ecology and Evolutionary Biology, Cornell University, Corson Hall, Ithaca, NY 14853, USA

A. S. Fleckere-mail: asf3@cornell.edu

J. Saldaña RojasCooperación para el Desarrollo de la Amazonía, CODEA, Pasaje Buena Vista 190, Iquitos, Perue-mail: forest_boy23@yahoo.com

Present Address:J. T. Anderson (&)Department of Biology, Duke University, P.O. Box 90338, Durham, NC 27708, USAe-mail: jill.anderson@duke.edu

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Long-distance seed dispersal also facilitates colonization ofunoccupied patches, permits range expansions, and canconnect plant populations in fragmented landscapes (Howeand Smallwood 1982; Nathan and Muller-Landau 2000;Levey et al. 2005). Furthermore, dispersal can enhanceseed germination and seedling establishment by decreasingthe likelihood of attack from host-speciWc natural enemiesnear maternal plants (Janzen 1970; Connell 1971).

The dispersal process is mediated by both abiotic andbiotic vectors, which can vary greatly in eVectiveness (e.g.,Murray 1988; Wenny and Levey 1998; Jordano et al.2007). In tropical systems, vertebrate frugivores disperseseeds of the vast majority of plant species (Howe andSmallwood 1982; Haugaasen and Peres 2007). Studies ofseed dispersal by animals have focused primarily on birdsand mammals (e.g., Jordano 1995). Frugivorous Wshes maybe the dominant biotic seed dispersers in the more than300,000 km2 of Xoodplain forest and savannahs along theAmazon, Orinoco, and their tributaries (Goulding 1980;Kubitzki and Ziburski 1994; Saint-Paul et al. 2000; Evaet al. 2004); however, they have been overlooked in theseed dispersal literature until recently (Correa et al. 2007;Galetti et al. 2008; Lucas 2008). High-quality seed dispers-ers move large quantities of seeds to sites suitable for sub-sequent germination and establishment (Schupp 1993).Fruit-eating Wshes potentially satisfy these criteria due totheir voracious appetites and extensive mobility (Goulding1980; Makrakis et al. 2007; Santos et al. 2007). Previousstudies suggest that seed dispersal by Wsh may be crucialfor the maintenance of plant diversity in Xoodplain habitats;however, there have been few eVorts to integrate botanicaland ichthyological data to elucidate the importance of Wshin the dispersal ecology of Neotropical plants (Kubitzki andZiburski 1994; Banack et al. 2002; Correa et al. 2007;Galetti et al. 2008).

At least 200 species of frugivorous Wshes are knownfrom tropical South America; during lengthy annual Xoods,these Wshes move into wetlands to consume fruits, whichare primarily produced during the Xood season (Goulding1980; Lowe-McConnell 1987; Goulding 1993; Junk et al.1997; Haugaasen and Peres 2007). Some species of Wsh,such as Colossoma macropomum (Characidae), accumulatefat reserves during the Xood season to sustain them afterXoodwaters recede (Junk 1985). Fish clearly rely on Xood-plain forests for food; the question remains to what extentthese forests rely on the seed dispersal services of frugivo-rous Wsh.

Compounding the limited information on Wsh as seeddispersers is the high susceptibility of fruit-eating Wsh tooverexploitation (e.g., Isaac and RuYno 1996). Fish consti-tute the most important source of animal protein for humanconsumption in Amazonia and frugivores are a majorcomponent of South American Wsheries (e.g., Bayley and

Petrere 1989; Goulding et al. 1996). For example, C.macropomum comprised over 40% of the Wsh sold in mar-kets in Manaus, Brazil in the late 1970s (Bayley and Petrere1989), which is astonishing because Neotropical freshwaterWsh diversity is estimated to be over 5,000 species (Lund-berg et al. 2000). Due to overexploitation, the catch of C.macropomum declined by almost 90% from the mid-1970sto the mid-1990s (Isaac and RuYno 1996; Santos et al.2007). OverWshing also changes age and size structures,skewing wild populations of fruit-eating Wsh to smaller,younger individuals (Isaac and RuYno 1996; Reinert andWinter 2002; Santos et al. 2007). Kubitzki and Ziburski(1994) found the proportion of intact (potentially viable)seeds of two species in the digestive tract increased withsize for C. macropomum. Additionally, Galetti et al. (2008)reported a positive relationship between the size of Piarac-tus mesopotamicus (Characidae) and the number of intactseeds of the palm, Bactris glaucescens. If seed-dispersaleVectiveness increases through ontogeny, overWshing couldalter the relationship between fruit-eating Wsh populationsand Xoodplain plant species (Correa et al. 2007; Galettiet al. 2008).

We conducted a comprehensive study of seed dispersalby fruit-eating Wshes, arguably among the most importantvectors of dispersal for Xeshy fruited plant species in SouthAmerican Xoodplain habitats. Our speciWc objectives were:(1) to investigate the abundance and diversity of seeds dis-persed by C. macropomum Cuvier, and Piaractus brachyp-omus Cuvier, (2) to assess the viability of consumed seeds,and (3) to determine whether seed dispersal eVectivenessincreases with Wsh size and age. This study highlights thecritical role of fruit-eating Wshes in the dispersal ecology ofXoodplain forests and savannahs.

Materials and methods

Study site and focal species

Floodplain forests and other wetlands comprise 90% ofPacaya-Samiria, a 21,924-km2 blackwater NationalReserve in northeastern Peru (Kvist and Nebel 2001;Tobler et al. 2007). We conducted this study in the east-central portion of the reserve (5°21�S; 74°30�W) duringthree Xood seasons (2004–2006). From January to June,forests in this region Xood predictably to a depth of up to 6–8 m, and mean annual precipitation exceeds 2,500 mm(Kvist and Nebel 2001). C. macropomum and P. brachypo-mus (hereafter: Colossoma and Piaractus) are common atthis site. These species are among the largest Wshes in trop-ical South America and are extremely important commer-cially (Goulding 1980; Bayley and Petrere 1989; Isaac andRuYno 1996; Junk et al. 1997). Colossoma can live for at

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least 65 years (Reinert and Winter 2002). Colossoma andPiaractus can both masticate seeds and defecate intactseeds (Goulding 1980).

Dietary analyses

During the height of the Xood seasons of 2004, 2005, and2006 (March–June), we analyzed the stomach and intestinalcontents of adult Colossoma (n = 230) and Piaractus(n = 56 in 2005 and 2006 only). We also studied Colos-soma (n = 29) during receding waters (mid-June 2005 and2006) to assess seasonal dietary shifts. Adults of the focalspecies were collected in gill nets (50 m length, 4 m height;85 mm mesh) established in Xoodplain forests and Xoodedsavannahs within a 2-km radius of our Weld station. Thefocal species were routinely encountered in both habitattypes. We recorded the species composition and abundanceof seeds present in digestive tracts. In 2005 and 2006 wealso noted the standard length (measured from the tip of thesnout to the posterior extremity of the hypural bones) andweight of each Wsh, collected seeds for germination studies,and assessed the volume (§1 ml) of major food categories:fruit pulp, intact seeds, masticated seeds, vegetation, detri-tus, and animal prey (invertebrates and Wsh). Intact (poten-tially viable) seeds were easily distinguished frommasticated (non-viable) seeds.

We conducted a mixed model repeated measuresANOVA with year as a random eVect to determinewhether: (1) Piaractus and Colossoma consume propor-tionally more fruit and seed matter than other foods duringthe Xood season, and (2) Colossoma undergoes a dietaryshift from the Xood to the dry season (Proc Mixed, SASversion 9.2; SAS Institute, N.C.). The analyses for Piarac-tus and Colossoma were conducted separately. Individualidentity was included as a repeated factor because all dietcategories were measured for each Wsh; these data weremodeled using an unstructured covariance matrix (Littellet al. 1998).

If seed dispersal eVectiveness increases with body size,then the digestive tracts of larger Wsh should contain agreater volume of intact seeds than those of smaller Wsh. Toevaluate this hypothesis, we regressed intact seed volumeagainst standard length of Wsh, Wsh species, and year (a ran-dom eVect). We included masticated seed volume as acovariate to control statistically for an overall increase inseed consumption with Wsh size. We excluded Wsh that hadno seed matter in their digestive tracts, as they were actingneither as seed dispersers nor predators. Zero values wereover-represented for intact seed volume, the response vari-able. We handled this zero inXation by conducting two sep-arate analyses. First, we used logistic regression (ProcGlimmix) to model the presence of intact seeds; this analy-sis addressed whether larger Wsh had a greater probability

of containing intact seeds. Second, we removed all individ-uals with no intact seeds in their digestive tracts, and usedmultiple regression (Proc Mixed) to determine whether thevolume of intact seeds could be predicted from the samemain eVects and covariate. Interaction terms were evalu-ated, but proved non-signiWcant. When necessary, we usedstandard data transformations, as speciWed in the results, toimprove normality and homoscedasticity.

Botanical inventory

To determine fruit availability, and the percentage of plantspecies whose seeds are dispersed by Wsh, we established50 £ 10-m2 transects in Xoodplain forests (n = 19 transects)and Xooded savannahs (n = 11) from March to June 2006.We located all fruiting trees and lianas and counted thenumber of fruits on each individual using binoculars. Whennecessary, members of the Weld crew climbed trees toachieve a better vantage point from which to count. We col-lected voucher specimens of all morphospecies and identi-Wed these species with the aid of botanists in the herbariumof the Universidad de la Amazonia Peruana, where speci-mens were deposited (Iquitos, Peru). Twenty transects weremonitored multiple times from May to June to ensureextensive sampling. We present the maximum number offruits/individual for those transects over the sampled inter-vals. We did not record data on non-fruiting individuals.

Feeding trials

We fed fruits to Colossoma: (1) to collect gut-processedseeds for germination experiments, (2) to compare the seeddispersal eVectiveness of juveniles and adults, and (3) toassess gut retention time to generate dispersal kernels(detailed in J. T. Anderson et al., unpublished manuscript).Wild Colossoma behaved erratically in enclosures in theWeld; therefore, we conducted feeding trials in tanks(0.3 m3) with captive-raised individuals acquired eitherfrom the Instituto para la Investicación de la AmazoniaPeruana (Iquitos, Peru) or from the local aquarium trade.One Wsh was placed in each tank and hand-fed a knownquantity of seeds encased in their fruit pulp (gathered at theWeld site in Pacaya-Samiria) for one to three feeding trialsper species of seed (2004, n = 5 adults; 2005, n = 5 adults;2006, n = 3-5 adults and 4–5 juveniles, depending on thespecies of seed; see Electronic Supplementary Material S1).The number of seeds fed to Wsh varied between three and200 per trial based on the size of the seed, and only one spe-cies of seed was included in each trial (Electronic Supple-mentary Material S1). We collected defecated seeds everyhour for 2–12 days until the majority of the seeds passedthrough the digestive system. We supplemented Wsh withan extruded diet consisting of 25% crude protein (e.g., de

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Carvalho Gomes et al. 2006). We used seeds that wereimportant components in the diets of Wsh: Cecropia latiloba(Urticaceae) and Duroia duckei (Rubiaceae) in 2004, 2005and 2006, Cayaponia cruegeri (Cucurbitaceae) in 2005,and Annona muricata (Annonaceae), Cayaponia tubulosa(Cucurbitaceae), Bactris bidentula (Arecaceae), and Crat-eva tapia (Capparaceae) in 2006.

The addition of juvenile Wsh in 2006 allowed us to testthe hypothesis that the quality of seed dispersal increasesthrough ontogeny (Galetti et al. 2008). We used logisticregression (Proc Glimmix) to analyze the proportion ofintact seeds defecated relative to the number fed to Wsh asa function of life history stage (adult or juvenile), speciesof seed, and the interaction. We included an R-sided ran-dom statement for the identity of the Wsh and a G-sidedrandom statement for the number of trials of each speciesof seed; the R-sided random statement in Proc Glimmix isequivalent to a repeated statement and accounts for non-independence of seeds processed by the same Wsh (ProcGlimmix documentation: http://support.sas.com/rnd/app/papers/glimmix.pdf).

Germination experiments

Since frugivores can improve the germination success ofseeds by removing fruit pulp and/or by scarifying seeds(Traveset et al. 2008), we compared seeds consumed byWsh with uningested seeds encased within entire fruits anduningested seeds manually extracted from their fruit pulp(Samuels and Levey 2005). In the Wrst set of experiments,

we used seeds dissected out of the digestive systems ofwild-caught Colossoma and Piaractus. These seeds pro-vided data on viability of the diverse assemblage of seedspecies consumed by these Wsh. In the second set of experi-ments, we compared uningested seeds with seeds defecatedby Colossoma in the feeding trials. Unlike seeds dissectedfrom wild-caught individuals, these defecated seeds passedthrough the whole digestive system and could, therefore,have either enhanced or reduced germination success. Allseeds from these experiments were planted in individualpots in local soil and watered routinely. We monitoredseeds every 1–2 days for up to 9 months.

Germination I: seeds collected from wild individuals

We compared seeds from the digestive tracts of wild Colos-soma (2005 and 2006) and Piaractus (2006) with unin-gested control seeds with and without their fruit pulp. In2005, we only tested seeds of Cecropia spp. from the diges-tive tracts of Piaractus. Germination trials were conductedprimarily in Pacaya-Samiria reserve during the Weld season.However, in 2006, at the end of the Weld season, we trans-ported ungerminated seeds to Iquitos to continue the exper-iments. Sample sizes, which are indicated in Table 1, variedby species depending on the availability of fruits and thenumber of seeds in the digestive tracts of Wsh. We assessedgermination success using logistic regression (ProcGlimmix) with year as a random eVect. Tukey’s adjust-ments for multiple comparisons were used to comparetreatments. In an initial analysis, species of seed, treatment,

Table 1 Germination of seeds collected in Wsh digestive tracts relative to uningested seeds. DiVerent letters indicate diVerences in germinationsuccess for each species after Tukey’s adjustment for multiple comparisons (P < 0.05). Control seeds were not always available

a Seeds consumed by Wsh included Cecropia latiloba and Cecropia membranacea; control seeds were C. latiloba. Initial seed number was esti-mated based on fruit weight for control seeds with pulp

Seed species Time (days)

Percentage of seeds that germinated (sample size)

Colossoma Piaractus Seeds without pulp Seeds with pulp

Cecropia spp.a 110 76% (n = 335) a 78% (n = 300) a 92.8% (n = 650) b 7.25% (n = 46,479) c

Duroia duckei 120 40% (n = 65) 56% (n = 75) 47.5% (n = 480)

Bactris maraja 280 0% (n = 16) 0% (n = 16) 0% (n = 16)

Bactris bidentula 280 36.6% (n = 41) 26.7% (n = 15) 30.8% (n = 65) 34.8% (n = 66)

Crateva tapia 70 0% (n = 37) a 28% (n = 50) b 51.1% (n = 280) c

Cayaponia cruegeri 17 76.7% (n = 30)

Annona muricata 160 65% (n = 26) a 23% (n = 26) b 13.3% (n = 90) b

Cayaponia tubulosa 120 11.5% (n = 27) 29.4% (n = 17) 25% (n = 40) 21.05% (n = 38)

Genipa spruceana 107 78.6% (n = 42)Ternstroemia penduliXora 58 24% (n = 41)

Leonia glycycarpa 25 33.3% (n = 3)

Dulacia candida 9 100% (n = 1)

Carica microcarpa 15 16% (n = 44)

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and their interaction were highly signiWcant predictors ofgermination success; therefore, we analyzed each seedspecies separately.

Germination II: seeds defecated by Colossoma in feeding trials

We conducted the second series of germination experi-ments with uningested and gut-processed seeds of: Cecro-pia latiloba (Weld seasons: 2004, 2006), D. duckei (2004,2006), Cayaponia cruegeri (2005), and A. muricata (2006).Treatments included: (1) seeds defecated by adult Wsh(2004–2006); (2) uningested seeds extracted from fruit pulp(2004–2006); (3) uningested seeds encased in fruit pulp(2004–2006); (4) uningested seeds without pulp that weresoaked in water for 30 days (2004–2006); (5) uningestedseeds encased in fruit pulp that were soaked in water for30 days (2005–2006); and (6) seeds defecated by juvenileWsh (2006). We selected these species based on the abun-dance of their seeds in the digestive tracts of Wsh and theavailability of fruits in Xooded habitats at our Weld sites. Weincluded treatments 4 and 5 because seeds remain sub-merged for several months after dispersal in AmazonianXoodplain habitats, and submersion may be necessary tobreak dormancy (Kubitzki and Ziburski 1994). In 2006, wewere able to test whether germination rates of seeds pro-cessed by adults exceeded those of seeds processed byjuveniles. We did not have suYcient seeds to include treat-ments 4 and 5 in our germination study of A. muricata.

In the dry season in Amazonian Xoodplain habitats, thereis only a limited time for germination and seedling estab-lishment prior to the onset of Xooding; it is, therefore,important to assess whether Wsh promote rapid germination.We used Cox proportional hazards models (i.e., survivor-ship analysis, Proc PHREG) to determine whether treat-ments diVered in germination rate. When theproportionality assumption was violated, we included atime-dependent treatment predictor in the model (Cox1972). Since main eVects and interaction terms were highlysigniWcant when species were analyzed together, we con-ducted separate analyses for each seed species in each yeardue to slightly diVerent treatment combinations.

Results

Diet: number and diversity of intact seeds

From 2004 to 2006, we found 699,963 intact seeds from 21plant species in the digestive tracts of 144 Colossoma indi-viduals. In 2005 and 2006, Wfty-one Piaractus individualshad 407,558 intact seeds from 23 plant species in theirstomachs and intestines (the species and quantity of seeds

are enumerated in Electronic Supplementary Material S2).The remaining 115 Colossoma and four Piaractus individu-als had empty digestive systems, or contained no intactseeds. We found intact seeds of 36 species of trees andlianas in digestive tracts of both species combined (Elec-tronic Supplementary Material S2). Cecropia spp. (Urtica-ceae) accounted for over 99% of the seeds in the diets ofColossoma and Piaractus, but only 78.7% (Colossoma) and68.7% (Piaractus) of the volume of intact seed matterbecause these seeds are extremely small (wet seed mass:mean § S.D.; 0.0054 § 0.001 g, n = 15 groups of seeds,ranging from 150 to 2,500 seeds). Species accumulationcurves did not level oV over the course of the study (Elec-tronic Supplementary Material S3) and Colossoma and Pia-ractus likely disperse additional species of seeds.

Botanical inventory

During the 2006 Xooding season, we encountered 79 spe-cies of fruiting trees and lianas in the botanical transects(Electronic Supplementary Material S4), which is withinthe range of species richness reported in other South Amer-ican Xoodplain forests (Ter Steege et al. 2000). Since fruit-ing generally coincides with Xooding in these systems (e.g.,Parolin et al. 2004; Haugaasen and Peres 2007), we likelysampled the majority of Xoodplain species at our site. How-ever, 24 plant species were present in the digestive contentsof Wsh, but absent from the botanical survey (ElectronicSupplementary Material S2). Either these species did notfruit in 2006, or they were rare. We estimate that during ourstudy Colossoma and Piaractus dispersed seeds of up to35% (36 of 79 + 24) of the species that fruit during theXood season. Continued sampling would likely reveal addi-tional plant species both at the site and in the diets of thesespecies of Wsh.

Diet: Wsh size and volumetric gut content analyses

Colossoma individuals ranged from 31.5 to 74.5 cm in stan-dard length (mean § SE: 43.8 § 0.52 cm, n = 182), andPiaractus ranged from 34.0 to 50.0 cm (41.0 § 0.49 cm,n = 55). These individuals were substantially smaller thanmaximum recorded sizes (Colossoma, 90 cm; Piaractus,85 cm; Goulding 1980). The diets of Colossoma and Pia-ractus consisted primarily of fruits and seeds during theXood season (Fig. 1). Piaractus individuals had a signiW-cantly greater volume of intact seeds in their stomach andintestines than any other food category (F5,54 = 34.05,P < 0.0001). The volume of food in the digestive tracts ofColossoma was signiWcantly inXuenced by food category(F5,180 = 30.26, P < 0.0001) and the interaction betweenfood category and season (F5,180 = 18.09, P < 0.0001), butnot the main eVect of season (F1,180 = 0.02, P = 0.9). These

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data demonstrate a dietary shift from frugivory during theXood season to detritivory during falling water levels whenColossoma returns to rivers and lakes. Both species hadlarge volumes of intact and masticated seeds, and acted asdispersers and predators of seeds.

Diet: seed dispersal eVectiveness as a function of Wsh size

Among Colossoma and Piaractus individuals with intactand/or masticated seeds in their digestive systems, therewas a signiWcantly positive relationship between Wsh size(standard length) and the presence and volume of intactseeds. The logistic regression results indicated that forevery 1-cm increase in standard length, the odds of intactseed presence increased by 11.4% (odds ratio: 1.114; 95%CI; 1.024–1.211; F1,191 = 6.42, P = 0.012). However, thepresence of intact seeds was negatively correlatedwith masticated seed volume (odds ratio: 0.98; 95% CI;0.966–0.99; F1,191 = 11.3, P = 0.0009). Colossoma had a

signiWcantly lower probability of having intact seeds thanPiaractus (odds ratio: 0.29; 95% CI; 0.1–0.85;F1,191 = 5.12, P = 0.025). We obtained similar results fromthe multiple regression that excluded individuals with nointact seeds. Intact seed volume (natural log transformed)increased with standard length (natural log transformed;F1,128 = 9.27, P = 0.0028), and decreased with masticatedseed volume (square root transformed; F1,128 = 5.77,P = 0.018). Colossoma had a lower volume of intact seedsthan Piaractus (F1,128 = 44.6, P < 0.0001). We present thepartial residual plot (Fig. 2) because it shows the relation-ship between Wsh size and intact seed volume after control-ling statistically for masticated seed volume.

Feeding trials: proportion of seeds defecated

Captive Colossoma defecated, intact, the majority of seedsthey consumed (Table 2). The odds of defecating intactseeds were 1.89 times greater for adults than juveniles(95% CI of odds ratio: 1.01–3.53; F1,77 = 4.07, P = 0.047).There was also a signiWcant eVect of seed species(F5,77 = 3.49, P = 0.0068). Fish defecated a greater propor-tion of intact Cecropia latiloba and Duroia duckei thanCrateva tapia seeds (Cecropia vs. Crateva, t77 = 3.02,P = 0.04; Duroia vs. Crateva seeds, t77 = 3.61, P = 0.007).No other contrasts were signiWcant. The interaction

Fig. 1 Volumetric gut contents of a Colossoma macropomum(n = 182) and b Piaractus brachypomus (n = 55) in 2005 and 2006.b DiVerent letters indicate signiWcant diVerences between treatments.a For clarity of presentation, signiWcant contrasts are not indicated

Vol

umet

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60

70

0

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20

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70 Flooded seasonTransition to dry season

Fruit pulp

Viable seeds

Masticated seeds

VegetationDetritus Animal prey

b Piaractus brachypomus

Food category: p<0.0001

B

B

C

A

a Colossoma macropomum

Food category: p<0.0001 Season: p=0.9 Food category X Season: p<0.0001

CC

Fig. 2 Intact seed volume as a function of Wsh size (standard length;SL). Plot of partial residuals from multiple regression, after statisticalcorrection for the volume of masticated seeds. The residuals of the pre-dictor variable SL were generated by a regression of the square root ofthe volume of masticated seeds (predictor) on the natural logarithm ofSL (response). The residuals of the response variable (intact seed vol-ume) are from a regression of the square root of masticated seed vol-ume (predictor) on the natural logarithm of intact seed volume(response). Transformations were made to improve normality andhomoscedasticity. The units of partial residual plots do not correspondwith the units of the raw data

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idua

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act s

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Residuals of standard length

Fish species: p<0.0001Standard length: p=0.0028

Colossoma macropomum

Piaractus brachypomus

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between seed species and Wsh life history was nonsigniW-cant and was removed from the model.

Germination I: seeds collected from wild Wsh

Intact seeds found in the digestive tracts of Wsh had rela-tively high germination success rates (Table 1). In the over-all analysis, germination success varied with the species ofseed, treatment, year, and the interaction between speciesand treatment. The species-speciWc analyses indicated thattreatment was a signiWcant predictor of germination successfor A. muricata (F2,138 = 11.2, P < 0.0001), Cecropia spp.(F3,47759 = 486.6, P < 0.0001), and Crateva tapia. None ofthe C. tapia seeds from the digestive tracts of Colossomagerminated, which prevented the logistic regression fromconverging due to quasi-separation of data points; there-fore, we implemented Firth’s procedure (Heinze andSchemper 2002) in LogXact (version 8.0, Cytel). Unin-gested C. tapia seeds had signiWcantly greater germinationrates than Wsh-processed seeds (�2 = 40.3, df = 2,P < 0.0001). For A. muricata, seeds consumed by Piaractushad signiWcantly greater germination success than unin-gested seeds with (t138 = 4.71, P < 0.0001) and without fruitpulp (t138 = 2.85, P = 0.0051). Cecropia spp. seeds col-lected from the digestive tracts of Colossoma and Piaractushad signiWcantly greater germination success than unin-gested seeds with fruit pulp (Colossoma vs. seeds withpulp, t47759 = 21.5, P < 0.0001; Piaractus vs. seeds withpulp, t47759 = 28.2, P < 0.0001), but signiWcantly lower suc-cess than uningested seeds without fruit pulp (Colossoma

vs. seeds without pulp, t47759 = –6.67, P < 0.0001; Piarac-tus versus seeds without pulp, t47759 = ¡7.83, P < 0.0001).Germination success did not diVer as a function of treat-ment for C. tubulosa (F3,116 = 0.92, P = 0.43), D. duckei(F2,616 = 2.07, P = 0.13) and B. bidentula (F3,181 = 1.31,P = 0.27).

Germination II: seeds defecated by captive Wsh

In all cases except one (D. duckei in 2004), seeds defecatedby captive Colossoma outperformed seeds in at least oneuningested control treatment. We report the results of spe-cies-speciWc analyses (Fig. 3):

C. cruegeri

Germination rate varied by treatment for this species(�2 = 91.3, df = 4, P < 0.0001, n = 60 for all treatments;Fig. 3a). Seeds processed by Colossoma had signiWcantlygreater germination rates than uningested seeds withoutfruit pulp (�2 = 9.3, df = 1, P = 0.002), did not diVer fromuningested seeds with pulp (�2 = 2.1, df = 1, P = 0.15), andhad lower germination rates than uningested seeds soakedfor 1 month, both with (�2 = 9.3, df = 1, P = 0.002) andwithout fruit pulp (�2 = 42.1, df = 1, P < 0.0001).

A. muricata

There was no eVect of treatment on the time until germina-tion (�2 = 6.08, df = 3, P = 0.108, n = 15 for adult and

Table 2 Percentage of seeds that were defecated intact by captive Wshin the feeding trials (averaged across individuals). The overall statisti-cal analysis from 2006 trials including all species of seeds indicate thatgut processing by juveniles destroys a signiWcantly greater proportion

of seeds than processing by adults (see text). Results from 2005feeding trials of adults are included in this table to illustrate similaritiesbetween years

Species Family Year Fish life history stage

Trial length (days)

% of seeds defecated (mean § SE)

Cecropia latiloba Urticaceae 2005 Adult 5–6 91.2 § 5.0%

Cecropia latiloba Urticaceae 2006 Adult 6 92.6 § 3.7%

Cecropia latiloba Urticaceae 2006 Juvenile 6 83.8 § 4.1%

Duroia duckei Rubiaceae 2005 Adult 2–3 100%

Duroia duckei Rubiaceae 2006 Adult 6 94.2 § 2.9%

Duroia duckei Rubiaceae 2006 Juvenile 6 89.5 § 4.4%

Cayaponia cruegeri Cucurbitaceae 2005 Adult 3 100%

Cayaponia tubulosa Cucurbitaceae 2006 Adult 12 73.3 § 6.7%

Cayaponia tubulosa Cucurbitaceae 2006 Juvenile 11 83.3 § 9.6%

Crateva tapia Capparaceae 2006 Adult 6 50.8 § 3.05%

Crateva tapia Capparaceae 2006 Juvenile 6 42.5 § 13.2%

Bactris bidentula Arecaceae 2006 Adult 6 33.3 § 33.3%

Bactris bidentula Arecaceae 2006 Juvenile 6 65 § 12.7%

Annona muricata Annonaceae 2006 Adult 8 95.2 § 4.8%

Annona muricata Annonaceae 2006 Juvenile 8 95 § 5%

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286 Oecologia (2009) 161:279–290

juvenile treatments, and 24 for controls; Fig. 3b). How-ever, Wsh-processed seeds had signiWcantly greater germi-nation success than uningested control seeds with fruit pulp(adults vs. seeds with pulp, �2 = 4.16, df = 1, P = 0.041;juveniles vs. seeds with pulp, �2 = 8.2, df = 1, P = 0.0042).There was no diVerence between seeds processed by juve-niles and adults (P = 0.4).

D. duckei

In 2004, Wsh inhibited the germination of D. duckei seeds(�2 = 52.4, df = 3, P < 0.0001, n = 50 for all treatments;Figs. 3c, d). Seeds processed by Wsh had signiWcantly lowergermination rates than uningested seeds with (�2 = 7.6,df = 1, P = 0.0058) and without pulp (�2 = 12.7, df = 1,P = 0.0004), and soaked seeds (�2 = 14.4, df = 1,

P = 0.0001). In contrast, in 2006, Wsh enhanced germinationof D. duckei seeds (�2 = 59.3, df = 5, P < 0.0001, n = 60 foradult and juvenile treatments, and 100 for uningested treat-ments). Seeds consumed by adults and juveniles did notdiVer in germination rate (�2 = 0.26, df = 1, P = 0.61).Seeds defecated by both adults and juveniles had faster ger-mination rates than seeds in uningested treatments. (Con-trast statements for adults and juveniles vs. all uningestedcontrols: �2 ranged from 18.4 to 34.05, df = 1, P < 0.0001.)

C. latiloba

In 2004, Wsh promoted seed germination by removing fruitpulp (�2 = 10.52, df = 3, P = 0.015, n = 50 for all treat-ments; Figs. 3e, f). SpeciWcally, the germination rate ofseeds defecated by Wsh was almost indistinguishable from

Fig. 3 Germination rates of seeds fed to captive Colossoma relative to uningested seeds for the following species: a Cayapo-nia cruegeri (2005), b Annona muricata (2006), c Duroia duck-ei (2004), d D. duckei (2006), e Cecropia latiloba (2004), f Cecropia latiloba (2006). Not all treatments were applied to every seed species or in every year. SEs from survivorship analyses are included

0

0.1

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b Annona muricata (2006)

0 10 20 30 40 50 600 10 20 30 40 50 60

a Cayaponia cruegeri (2005)

c Duroia duckei (2004)

Time since planting (days)

Cum

ulat

ive

germ

inat

ion

(pro

port

ion)

e Cecropia latiloba (2004)

0 10 20 30 0 10 20 30 40 50

f Cecropia latiloba (2006)

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Oecologia (2009) 161:279–290 287

uningested seeds without fruit pulp (�2 = 0.009, df = 1,P = 0.92), but was signiWcantly more rapid than seeds withpulp (�2 = 7.08, df = 1, P = 0.0078), and seeds soaked with-out pulp (�2 = 3.75, df = 1, P = 0.05). Germination curvesalso diVered as a function of treatment in 2006 (�2 = 33.92,df = 5, P < 0.0001, n = 60 for Wsh treatments, and n = 100for control treatments). Seeds defecated by adults had sig-niWcantly greater germination rates than seeds defecated byjuveniles (�2 = 10.2, df = 1, P = 0.0014) and uningestedsoaked seeds with (�2 = 9.09, df = 1, P = 0.0026) and with-out fruit pulp (�2 = 9.7, df = 1, P = 0.0019), but did notdiVer from unsoaked control seeds with (�2 = 0.49, df = 1,P = 0.48) and without fruit pulp (�2 = 2.7, df = 1, P = 0.1).Cecropia seeds encased in fruit pulp had substantiallygreater germination success in experiments from the feed-ing trials (germination II) than in experiments with seedsfrom the digestive tracts of wild Wsh (germination I). Theentire panicle (fruit) was included as a control in germina-tion I, whereas in germination II, smaller sections of thepanicle were used, exposing a greater proportion of seeds inthe panicle.

Discussion

We conducted a comprehensive set of studies on an under-studied, but highly important, vector of seed dispersal:fruit-eating Wsh. Our results indicate that C. macropomumand P. brachypomus are highly eVective seed dispersers.These species disperse large quantities seeds of at least 36species of trees and lianas, which represent up to 35% ofthe plant species that fruit during the Xood season at ourWeld site. Colossoma and Piaractus from other regions ofSouth America consume diVerent species of fruits than theindividuals in our study (e.g., Goulding 1980; Lucas 2008).In a pilot study in Venezuela, we found 3039 intact seeds of16 species in the digestive contents of 15 Piaractus individ-uals and 786 intact seeds from 33 species in the digestivetracts of 104 individuals of Brycon bicolor Pellegrin (Char-acidae; Electronic Supplementary Materials S5 and S6).There was almost no species overlap between the digestivecontents of Wsh captured in Venezuela and Peru; Piaractusindividuals contained intact Cecropia and Astrocaryumseeds in both countries, but shared no other genera. Addi-tionally, a recent study of the diet of Colossoma and Pia-ractus over one Xood season in Brazil found an almostentirely diVerent species composition of seeds than ourstudy (Lucas 2008). In our system, Colossoma and Piarac-tus show no evidence for selective feeding; that is, theseWshes appear to consume seed species in proportion to theavailability of fruits. Clearly, these species have Xexiblefeeding habits and disperse seeds of a large number of plantspecies.

Fish-processed seeds had relatively high germinationrates. In a limited number of cases (Crateva tapia), Wshinhibited germination success of seeds. However, for otherspecies, Wsh enhance seed germination by removing fruitpulp (e.g., Annona muricata from feeding trials and Cecro-pia spp.). In other cases, seeds ingested by Wsh had greatergermination rates than control seeds without fruit pulp(e.g., Annona muricata from Piaractus digestive tracts andCayaponia cruegeri from feeding trials), suggesting thatthe importance of Wsh could extend beyond simply extract-ing seeds from the fruit. Gut passage by Wsh can promoterapid seed germination, which is likely vital in Amazonianwetlands for seedlings to survive subsequent Xooding.

Colossoma and Piaractus also act as seed predators.Seed predators can play an important role in plant popula-tion dynamics and community structure by diminishingrecruitment close to maternal trees and suppressing theregeneration of dominant species (Janzen 1970; Connell1971). When mammalian seed predators were excludedfrom experimental plots in Peru, seedling community com-position changed and the species richness of seedlingsdecreased (Paine and Beck 2007). Seed predation by fruit-eating Wsh could have similar consequences due to the largevolume of masticated seeds in their diets. Nevertheless, weknow nothing about the community-level implications ofseed predation by Wsh.

Habitat aYnity of fruit-eating Wshes

For seed dispersal by Wsh to be important ecologically,seeds need to settle in Xoodplain forests or savannahs andnot in rivers or lakes. The habitat aYnity of Wsh during theXood season dictates the fate of consumed seeds. If Wshenter seasonally Xooded habitats for short feeding boutsbefore returning to permanent water bodies, seeds wouldsink in unsuitable habitat when defecated. However, Saint-Paul et al. (2000) caught signiWcantly more Colossoma andPiaractus in Xoodplain forests than in open water lakes,despite the longer nets used in the lakes. Furthermore, in arelated study, we found that radiotagged Colossoma inPacaya-Samiria Reserve spent signiWcantly more time inseasonally Xooded forests (41% of the observations) andXooded savannahs (46%) than in lakes or river channels(13%; J. T. Anderson et al., unpublished manuscript). Fishare highly active in temporarily Xooded habitats thatbecome suitable for germination after Xoodwaters recede.Additionally, fruit pulp of Xeshy fruited species tends to beless dense than seeds, so that fruits Xoat and seeds sink inAmazonian Xoodplain habitats (Goulding 1980). As part ofour germination studies, we placed seeds and fruits in waterto determine whether soaking was necessary to break dor-mancy; we found that seeds sank almost immediately,whereas fruits remained buoyant longer before becoming

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waterlogged. Fish defecate de-pulped seeds, which rapidlysink (Kubitzki and Ziburski 1994). The water current mayredistribute seeds, but the current inside the forest tends tobe weak (Goulding 1980). It is likely, therefore, that seedsdispersed by Wsh to Xooded habitats remain in thosehabitats.

Finally, Xooding coincides with fruiting in AmazonianXoodplain habitats (e.g., Parolin et al. 2004). Colossomaexhibited an almost complete dietary shift from frugivoryin the Xood season to detritivory as the Xood watersreceded. Oliveira et al. (2006) detected similar seasonalchanges in Colossoma using stable isotope data; they notedthat fruits and seeds were completely absent from the dietof Colossoma during the dry season. Thus, Colossoma, andpresumably other Wsh, consume fruits only when they haveaccess to seasonally Xooded habitats.

Functional redundancy among seed dispersal vectors

Fruit-eating Wshes in South America are primarily charac-ins (Characidae and Anostomidae) and catWshes (Pimelodi-dae, Doradidae, and Auchenipteridae) (Araujo-Lima andGoulding 1997; Mannheimer et al. 2003). These Wsh rangein size from under 20 cm to 1.3 m (Araujo-Lima and Goul-ding 1997) and can vary in their eVectiveness as seed dis-persers because of diVerences in fruit consumption,abundance and dentition. Piaractus and Colossoma havemulticuspid, molariform teeth, which they use to crush hardseeds (Araujo-Lima and Goulding 1997; Correa et al.2007). CatWsh, in contrast, swallow fruits and seeds whole,and have a lower probability of destroying the seeds(Mannheimer et al. 2003; Correa et al. 2007). Multiple spe-cies of Wsh consume similar suites of fruits (Goulding1980), and could have very diVerent impacts on the repro-ductive ecology of those species.

In Amazonian Xoodplain forests, seed dispersal is alsomediated by water, and frugivores such as birds, monkeys,bats and secondary dispersers like rodents (Kubitzki andZiburski 1994; Haugaasen and Peres 2007). Whereas waterdisperses seeds laterally in the Xoodplain and unidirection-ally downstream, frugivorous Wshes are highly mobile (e.g.,Makrakis et al. 2007) and can move seeds upstream andbetween tributaries (Horn 1997). Indeed, our focal species,and other frugivorous Wshes, migrate during the Xood sea-son (Goulding 1980; Junk et al. 1997). This migratorybehavior could lead to long-distance seed dispersal(J. T. Anderson et al. unpublished manuscript). Indeed, theextensive mobility of these fruit-eating Wsh species couldexplain why 24 plant species present in the digestive con-tents of Colossoma and Piaractus individuals were absentfrom the botanical surveys. These Wsh species are alsoactive in other regions of Pacaya-Samiria reserve, wherethe plant species composition diVers (J. T. Anderson et al.,

unpublished data). Captured individuals likely dispersedseeds into our Weld site from other areas, thus creating adiscrepancy between the diet of these Wshes and local plantspecies composition.

Furthermore, the combined eVects of large populationsizes of fruit-eating Wshes (e.g., Santos et al. 2007) and theirvoracious appetites likely mean that Wsh are among thehighest quality seed dispersers in Amazonian Xoodplains(Kubitzki and Ziburski 1994). Banack et al. (2002) foundthat the characid fruit-eating Wsh, Brycon guatemalensis,and three species of bats were the most eVective dispersersof Wg seeds along Costa Rican streams, whereas howlermonkeys (Alouutta palliata) and kinkajous (Potos Xavus)were low-quality dispersers. They based this conclusion onseveral criteria including frugivore abundance, fruit con-sumption, and germination success of gut-processed seeds(Banack et al. 2002). Galetti et al. (2008) also indicate thatP. mesopotamicus likely provides higher quality seed dis-persal for B. glaucescens than other frugivores that con-sume seeds of this palm. Future studies of functionalredundancy are needed to illuminate the relative role of Wshin the dispersal ecology of Amazonian Xoodplain plants.Furthermore, studies of seed movement and seedling regen-eration in the presence and absence of frugivorous Wshesare needed to assess the ecological importance of seed dis-persal by Wsh. Experimental exclosures of these large Wshesare logistically diYcult to construct in deeply Xooded for-ests. However, comparisons of forests with intact andexploited populations of Colossoma, Piaractus, and otherWshes could be conducted to address these issues.

Seed dispersal of Cecropia spp. has been studied exten-sively and frugivorous birds, primates, and other mammalsfrom Neotropical forests vary greatly in Cecropia fruit con-sumption and germination success of gut-processed seeds(Estrada et al. 1984; Fleming and Williams 1990). Forexample, Cecropia spp. seeds represent a large portion ofthe diets of frugivorous bats (Fleming and Williams 1990;Lobova et al. 2003); nevertheless, Lobova et al. (2003)found Cecropia seeds in only 135 of 936 fecal samples withdiaspores from 14 species of bats in French Guiana. Simi-larly, Fleming and Williams (1990) report that Cecropiapeltata seeds occurred in 7-50% of the fecal matter sampledfrom nine species of bats over 10 years. In contrast, Cecro-pia seeds occurred in the digestive tracts of >70% of indi-viduals with diaspores in this study. Whereas birds and batseat only small sections of a Cecropia infructescence duringa feeding bout (Fleming and Williams 1990), we routinelyfound large portions of the infructescence in the digestivetracts of Wsh. Additionally, over the course of this study, weencountered over 1 million Cecropia spp. seeds in thedigestive systems of Colossoma (n = 144) and Piaractus(n = 51) individuals. Furthermore, the germination successof Cecropia seeds defecated by Colossoma and dissected

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Oecologia (2009) 161:279–290 289

from the digestive tracts of both Colossoma and Piaractusvaried between 68 and 88%. Similar proportions (58–86%)of Cecropia spp. seeds germinated after ingestion byhowler and capuchin monkeys and three species of under-story birds (Estrada et al. 1984; Wehncke and Dalling2005). However, Cecropia peltata seeds found in fecalmatter from capuchin (Cebus capuchinus) and spider mon-keys (Ateles geoVroyi) did not germinate under controlledconditions (Chapman 1989). Thus, Colossoma and Piarac-tus are likely among the most eVective dispersers of Cecro-pia seeds in the Neotropics.

Ontogenetic shifts in seed dispersal eVectiveness

Our results indicate that seed dispersal eVectivenessincreases with Wsh size and age. The probability that Colos-soma and Piaractus individuals had intact seeds in theirdigestive tracts and the volume of intact seeds bothincreased with Wsh size. Furthermore, adult Colossoma def-ecated a higher proportion of intact seeds in the feeding tri-als than juvenile Wsh. Finally, Cecropia latiloba seedsdefecated by Colossoma adults had higher germinationrates than those defecated by juveniles. Kubitzki and Zibur-ski (1994) and Galetti et al. (2008) also found evidence thatlarger Colossoma and P. mesopotamicus (respectively) hada greater proportion of intact than masticated seeds of sev-eral species in their digestive tracts. OverWshing reducespopulation and individual sizes and decreases the averageage of fruit-eating Wsh (Isaac and RuYno 1996; Reinert andWinter 2002; Santos et al. 2007). Overexploitation, there-fore, likely selects for the poorest seed dispersers by elimi-nating the largest individuals, which provide high-qualitydispersal of a large quantity of seeds (Galetti et al. 2008).Nevertheless, we do not yet understand the implications ofoverWshing on the dispersal ecology of South AmericanXoodplain habitats (Galetti et al. 2008).

Overharvesting of frugivorous vertebrates disrupts seeddispersal, can alter the species composition of plant com-munities, and even decrease diversity, thereby causing myr-iad indirect changes to the biotic landscape (Stoner et al.2007). No study to-date has explored the implications ofoverexploitation of frugivorous Wshes for plant communitystructure, as has been done with other major vertebrate fru-givores (Stoner et al. 2007). Santos et al. (2007) estimatedthat 7.7–10.4 million Colossoma individuals per yeararrived at the major Wsh market in Manaus Brazil in the1970s, whereas only 1.5 million individuals arrived peryear in the mid-1990s despite an increase in Wshing eVortduring the intervening decades. Fossils of C. macropomumteeth have been found in Miocene formations in Colombia(Lundberg et al. 1986) and Venezuela (Dahdul 2004); thisspecies has likely played a profound role in the structureand evolution of Xooded plant communities. Overharvesting

of these Wshes could disrupt an ancient interaction betweenseeds and their dispersal agents, potentially leading todeclines in plant species abundance and even species diver-sity (Kubitzki and Ziburski 1994; Correa et al. 2007;Galetti et al. 2008).

Acknowledgements Funding for this study was provided by theWildlife Conservation Society, the National Geographic Society (grantno. 7979-06), and the Cornell Center for the Environment. Animal careprotocols were approved by the Cornell University Institutional Ani-mal Care and Use Committee. F. Vermeylen helped with the statisticalanalyses. C. del Busto Rojas, J. Barrera Macedo, J. Vásquez,R. Rosales, S. Vázquez, S. Pérez, L. Ramírez, E. Yumbato, A. Sima,O. Yumbato, and V. Saldaña provided assistance in the Weld. We thankM. Geber and lab, P. Marks, T. Pendergast, M. Vellend, J. Bellemare,J. ShykoV and two anonymous reviewers for constructive criticisms onprevious drafts of the manuscript. We would like to thank the InstitutoNacional de Recursos Naturales (Peru), the Ministerio de la Produc-ción (Peru), and the Ministerio de Agricultura y Cria (Venezuela) forpermits to conduct this research and the Instituto para la Investicaciónde la Amazonia Peruana (Peru) for logistical support. This study com-plies with the laws of Peru and Venezuela.

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