Acta Oecologica 37 (2011) 561e577 Contents lists available at ScienceDirect Acta Oecologica journal homepage: www.elsevier.com/locate/actoec Original article Seed dispersal by fishes in tropical and temperate fresh waters: The growing evidence Michael H. Horn a,*, Sandra Bibiana Correa b, Pia Parolin c, B.J.A. Pollux d, Jill T. Anderson e, Christine Lucas f, Peter Widmann g, Albertus Tjiu h, Mauro Galetti i, Michael Goulding j a Department of Biological Science, California State University, Fullerton, 800 North State College Boulevard, Fullerton, CA 92834-6850, USA b Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX, USA c Biocentre Klein Flottbeck and Botanical Garden, University of Hamburg, Hamburg, Germany d Department of Animal Sciences, Wageningen University, Wageningen, The Netherlands e Department of Biology, Duke University, Durham, NC, USA f Department of Wildlife Ecology & Conservation, University of Florida, Gainesville, FL, USA g Fakultas Kehutanan, Universitas Tanjungpura, Pontianak 78124, West Kalimantan, Indonesia h World Wildlife Fund Indonesia, Jalan DR. Rubini No. 9A, Pontianak 78121, West Kalimantan, Indonesia i Departamento de Ecologia, Universidade Estadual Paulista, Rio Claro, São Paulo, Brazil j Wildlife Conservation Society, Bronx, NY, USA article info abstract Article history: Fruit-eating by fishes represents an ancient (perhaps Paleozoic) interaction increasingly regarded as Received 1 January 2011 important for seed dispersal (ichthyochory) in tropical and temperate ecosystems. Most of the more than Accepted 8 June 2011 275 known frugivorous species belong to the mainly Neotropical Characiformes (pacus, piranhas) and Available online 28 July 2011 Siluriformes (catfishes), but cypriniforms (carps, minnows) are more important in the Holarctic and Indomalayan regions. Frugivores are among the most abundant fishes in Neotropical floodplains where Keywords: they eat the fruits of a wide variety of trees and shrubs. By consuming fruits, fishes gain access to rich Frugivory sources of carbohydrates, lipids and proteins and act as either seed predators or seed dispersers. With Ichthyochory fi Fish diversity their often high mobility, large size, and great longevity, fruit-eating shes can play important roles as fl Biogeographic regions seed dispersers and exert strong in uences on local plant-recruitment dynamics and regional biodi- Floodplains versity. Recent feeding experiments focused on seed traits after gut passage support the idea that fishes Human impacts are major seed dispersers in floodplain and riparian forests. Overfishing, damming, deforestation and logging potentially diminish ichthyochory and require immediate attention to ameliorate their effects. Much exciting work remains in terms of fish and plant adaptations to ichthyochory, dispersal regimes involving fishes in different ecosystems, and increased use of nondestructive methods such as stomach lavage, stable isotopes, genetic analyses and radio transmitters to determine fish diets and movements. Ó 2011 Elsevier Masson SAS. All rights reserved. 1. Introduction species involved and the intact functioning of ecosystems (Howe and Smallwood, 1982; Nathan and Muller-Landau, 2000; Herrera, 1.1. Importance of seed dispersal by animals 2002; Tiffney, 2004; Bolmgren and Eriksson, 2010). In the tropics, where contemporary biotic dispersal is most diversified, birds and Animals are major dispersers of fruits and seeds with 30% of mammals, especially bats and monkeys, are principal dispersers of angiosperm families biotically dispersed and another 22% with tree seeds in rain forests (Fleming et al., 1987; Howe and Westly, both biotic and abiotic dispersal (Tiffney and Mazer, 1995; Tiffney, 1988). Half to over 90% of tropical trees and shrubs depend on 2004). Moreover, nearly two-thirds (64%) of gymnosperm fami- fruit-eating vertebrates to disperse their seeds (Howe and lies are biotically dispersed (Herrera, 1989). This planteanimal Smallwood, 1982), and frugivorous species can compose 80% of interaction is an integral part of the biology of the individual the bird and mammal biomass in tropical moist forests (Terborgh, 1986). Only in recent decades have fishes been considered to be important seed dispersers, even though early fishes might have fi * Corresponding author. Tel.: þ1 657 278 3707; fax: þ1 657 278 3426. been the rst vertebrate seed dispersers, perhaps 300 million years E-mail address: [email protected] (M.H. Horn). ago (Tiffney, 2004). 1146-609X/$ e see front matter Ó 2011 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.actao.2011.06.004 562 M.H. Horn et al. / Acta Oecologica 37 (2011) 561e577 1.2. Context of fishes among other vertebrate seed dispersers consume large quantities of fruits. Among Neotropical serrasalmid (Characiformes) fishes, for instance, fruit consumption is important Seed dispersal by fishes, or ichthyochory, is an ancient (possibly for species of two clades with conspicuous morphological traits in Paleozoic) ecological interaction that is beginning to receive more dentition and gut morphology that can be correlated to a more attention as new evidence demonstrates that the consumption of efficient use of fruit resources (Correa et al., 2007). By contrast, fruits by fishes is not a rare process concerning just a few fish and species in a third, carnivorous, clade display different traits. This plant species in a particular area (Correa et al., 2007; Galetti et al., difference suggests that seasonal, highly abundant fruit types in 2008; Lucas, 2008; Anderson et al., 2009). Rather, fruit consump- Amazonian floodplain forests constitute an additional niche tion by fishes is a widespread phenomenon that has been docu- dimension that could have driven adaptive radiation of serrasalmid mented in all biogeographic regions and involves more than 275 frugivorous fishes, similar to that for the radiation of frugivorous fish (Table 1; Appendix A) and numerous plant species. Fishes are mammals during the Eocene (Eriksson, 2008). likely to be the earliest vertebrate seed dispersers, a hypothesis Whether fruit-eating fishes are opportunistic or selective derived from the distribution patterns of diverse cordaitalean trees consumers remains an open question. In a meta-analysis of fruits (extinct coniferophytes) in wetlands, lowland rivers, and estuarine types consumed by Neotropical fishes, Correa et al. (2007) found channels during the late Carboniferous (Tiffney, 1984, 1986). that drupes, palm fruits, capsules and berries were the most Increasing fossil evidence demonstrates that diverse assemblages common types, accounting for 76% of 431 cases of fruit consump- of angiosperms were already established in the early Cretaceous tion. Several studies report fishes consuming fruits of many plant (Eriksson et al., 2000; Friis et al., 2010). These assemblages were species, but, in the majority of cases, the fruits of only one or two composed of shrubs and herbaceous species, including aquatic species account for most of the total volume of consumed items in forms associated with wetlands and characterized by fleshy fruits the main, 2e3 month feeding period during high water (e.g., with small seeds (Friis et al., 2010). Thus, fishes could have had an Goulding, 1980; Lucas, 2008; Anderson et al., 2009). The relative important role in seed dispersal of early angiosperms before the dominance of one or few fruits in the diet can be a result of foraging radiation of small terrestrial vertebrates (i.e. multituberculates, specialization or an opportunistic strategy where fishes consume primates and rodents), which occurred nearly 80 million years (late the most abundant fruit species. Anderson et al. (2009) conducted Cretaceous and early Tertiary, Eriksson, 2008) after the first a three-year study on feeding patterns of two large species of fruit- angiosperms evolved. Reluctance to consider fishes among poten- eating fishes in the Peruvian Amazon (Colossoma macropomum and tial seed dispersers in recent paleontological studies of the evolu- Piaractus brachypomus, Serrasalmidae, Characiformes) and found tion of angiosperms and seed dispersal systems (e.g., Tiffney, 2004; no evidence of selective feeding at the site investigated. This study Eriksson, 2008; Friis et al., 2010) largely results from the failure of was the first to try to determine how fruit availability influenced ichthyologists to recognize and describe fishes as seed dispersers consumption. Interestingly, however, these two fish taxa consumed even though nineteenth-century naturalists such as Richard Spruce only 35% of the fruit species available to fishes at the study site. (1908) had mentioned such fishes. As mostly generalized feeders, frugivorous fishes overlap the Ichthyochory can be considered a generalized dispersal system, in diets of other vertebrate seed dispersers and in some cases consume which fruit-eating fishes consume fruits of plants that are visited by fruits only on a seasonal basis. A question arises about how ich- other frugivores and supplement their diet with alternative food thyochory compares to hydrochory (i.e. seed dispersal by water) or resources when fruits are scarce (Correa et al., 2007)orwhenthe seed dispersal by other vertebrates. Fruit-eating fishes can be highly fishes feed opportunistically on fruits or seeds. Even though diverse in some systems (e.g., Amazonian floodplains), and locally a generalized dispersal system yields large overlap among frugivores, abundant, even in systems where only one or few fish species the collective effect on