Consistent individual differences in seed disperser quality in a seed-eating fish.

Animal-mediated seed dispersal (zoochory) is considered to be an important mechanism regulating biological processes at larger spatial scales. To date, intra-specific variation in seed disperser quality within seed-dispersing animals has not been studied. Here, I employed seed feeding trials to quantify individual differences in disperser quality within the common carp (Cyprinus carpio) using seeds of two aquatic plants: unbranched bur-reed (Sparganium emersum, Sparganiaceae) and arrowhead (Sagittaria sagittifolia, Alismataceae). I found substantial variation among carp individuals in their propensity to ingest seeds and their ability to digest them, resulting in up to 31-fold differences in the probability of seed dispersal. In addition, there were significant differences in the time that seeds are retained in their digestive systems, generating a twofold difference in the maximum distance over which they can potentially disperse seeds. I propose that seed-eating animal species consist of individuals that display continuous variation in disperser quality, with at one end of the continuum individuals that are likely to eat seeds, pass them unharmed through their digestive tract and transport them over large distances to new locations (i.e. high-quality seed dispersers) and at the other end individuals that rarely eat seeds, destroy most of the ones they ingest and transport the few surviving seeds over relatively short distances (low-quality seed dispersers). Although individual differences in seed dispersal quality could be the result of a variety of factors, these results underline the ecological and evolutionary potential of such variation for both plants and animals.

A non-destructive sampling protocol for field studies of seed dispersal by fishes.

This paper presents a standardized protocol for the non-lethal capture of fishes, sampling of stomach contents and quantification of seed dispersal efficiency by frugivorous fishes. Neotropical pacu Piaractus mesopotamicus individuals were collected with fruit-baited hooks. The diets of 110 fish were sampled using a lavage method, which retrieved >90% of stomach contents of both juveniles and adults and allowed individuals to recover within 5 min of treatment. The proportional volume of six food categories was similar for stomachs and whole digestive tracts retrieved by dissection. Fruit pulp was proportionally lower in the stomach. The abundance and species richness of intact seeds increased with fish size independent of whether only stomachs or whole digestive tracts were analysed. The analysis of stomach contents accounted for 62·5% of the total species richness of seeds dispersed by P. mesopotamicus and 96% of common seeds (seed species retrieved from more than one fish). Germination trials revealed that seed viability was similar for seeds collected from the stomach via lavage and seeds that passed through the entire digestive tract. Therefore, stomach contents provide an unbiased representation of the dietary patterns and seed dispersal of frugivorous fishes.

Phenotypic convergence is more frequent and stronger in herbivorous freshwater fishes.

Constraints on phenotypic evolution can lead to patterns of convergent evolution, by limiting the 'pool' of potential phenotypes in the face of endogenous (functional, developmental) or exogenous (competition, predation) selective pressures. Evaluation of convergence depends on integrating ecological and morphological data within a robust, comparative phylogenetic context. The staggering diversity of teleost fishes offers a multitude of lineages adapted for similar ecological roles, and therefore, offers numerous replicated evolutionary experiments for exploring phenotypic convergence. However, our understanding of fish feeding systems has been primarily shaped by marine species, with the monolithic exception of freshwater cichlids. Here we use piranhas and pacus (Serrasalmidae) to explore the evolution of different feeding ecologies and their morphological proxies in Neotropical freshwater environments. Specifically, we explore whether convergence is more widespread among plant-eating fishes, arising from strong constraints on phenotypic evolution in herbivores. Using osteological micro-computed tomographic imaging (µCT), we describe the major axes of morphological variation in pacus and piranhas, regarding their diet and feeding behaviors. Next, we evaluated whether herbivorous niches are less labile than other dietary guilds and whether herbivorous species' phenotypes evolve at a slower evolutionary rate than other taxa. We then assess how convergent herbivorous taxa are, using three different suites of morphological characters (dental, jaw, and abdominal morphometrics). Ecologically, herbivory is not a dead end, exhibiting similar observed transition rates as those between carnivores and omnivores. However, we documented widespread convergence in herbivores and that herbivores have slower rates of phenotypic evolution than carnivores. Most instances of convergence are found in herbivorous taxa, specifically in frugivores and folivores. Moreover, instances of 'complete' convergence, indicated by positive convergence metrics observed in more than one morphometric dataset, were only found in herbivores. Herbivores do appear to evolve under constrained circumstances, but this has not limited their ecological lability.

Neotropical fish-fruit interactions: eco-evolutionary dynamics and conservation.

Frugivorous fish play a prominent role in seed dispersal and reproductive dynamics of plant communities in riparian and floodplain habitats of tropical regions worldwide. In Neotropical wetlands, many plant species have fleshy fruits and synchronize their fruiting with the flood season, when fruit-eating fish forage in forest and savannahs for periods of up to 7 months. We conducted a comprehensive analysis to examine the evolutionary origin of fish-fruit interactions, describe fruit traits associated with seed dispersal and seed predation, and assess the influence of fish size on the effectiveness of seed dispersal by fish (ichthyochory). To date, 62 studies have documented 566 species of fruits and seeds from 82 plant families in the diets of 69 Neotropical fish species. Fish interactions with flowering plants are likely to be as old as 70 million years in the Neotropics, pre-dating most modern bird-fruit and mammal-fruit interactions, and contributing to long-distance seed dispersal and possibly the radiation of early angiosperms. Ichthyochory occurs across the angiosperm phylogeny, and is more frequent among advanced eudicots. Numerous fish species are capable of dispersing small seeds, but only a limited number of species can disperse large seeds. The size of dispersed seeds and the probability of seed dispersal both increase with fish size. Large-bodied species are the most effective seed dispersal agents and remain the primary target of fishing activities in the Neotropics. Thus, conservation efforts should focus on these species to ensure continuity of plant recruitment dynamics and maintenance of plant diversity in riparian and floodplain ecosystems.

Juveniles of the overexploited Amazonian fish Colossoma macropomum (Characiformes: Serrasalmidae) as potential seed dispersers of Cecropia spp

Colossoma macropomum is a frugivorous fish from the Amazon and Orinoco river basins. This species has an important economic and social role in both river watersheds; it also has been overfished for more than 40 years, leading to changes in the populations structure. Currently adults are less common in fisheries, while juveniles are more frequently fished and sold in several market places along the Amazon River. Reportedly adult individuals consume a vast quantity of fruits and seeds and has been recognized as effective seed dispersers that plays a significant ecological role. Although frugivorous fishes are important dispersers in tropical rainforests, assessments of their effectiveness in dispersing seeds and in the effect on the germination of these ingested seeds are still insufficient. Cecropia latiloba and Cecropia membranacea are two pioneer tree species that initiate the succession process in the tropical forest and are both widely consumed by C. macropomum. In this study we aimed to verify if the Cecropia seeds that pass through the digestive tract of juveniles of C. macropomum would show improved germination. The results obtained through controlled experiments confirm that seeds that pass through the digestive tract of C. macropomum retained their germination capacity. Although the responses in the improvement of the germination variables (germination capacity, minimum imbibition time, time necessary for reaching 50 % germination capacity, emergence velocity index and germination mean time) did not show statistical differences between treatments, the seedlings that grew from the seeds consumed by the fish were taller than those without the digestive treatment. We conclude that juveniles of C. macropomum have the possibility to disperse the seeds of these Cecropia species.

Colossoma macropomum es un pez frugívoro de las cuencas del Amazonas y el Orinoco. Esta especie tiene un importante papel económico y social en ambas cuencas; sin embargo, ha sido sobreexplotada por más de 40 años, lo que ha llevado a cambios en la estructura de sus poblaciones. Actualmente los adultos son menos comunes en las pesquerías, mientras que los juveniles son atrapados y vendidos en varios mercados a lo largo del río Amazonas con mayor frecuencia. Se ha reportado que los individuos adultos consumen grandes cantidades de frutas y semillas, y han sido reconocidos como dispersores efectivos con un papel ecológico vital. A pesar de que los peces frugívoros son dispersores importantes en los bosques tropicales, los estudios sobre su efectividad en la dispersión de semillas y sobre la capacidad de germinación y la viabilidad de las semillas ingeridas son aún insuficientes. Cecropia latiloba y Cecropia membranacea son dos especies de árboles pioneros que inician el proceso de sucesión en los bosques tropicales; ambas son ampliamente consumidas por C. macropomum. El objetivo de este estudio fue verificar si las semillas de Cecropia que pasaron por el tracto digestivo de los juveniles de C. macropomum mejorarían su germinación. Los resultados obtenidos a través de experimentos controlados confirmaron que las semillas que pasan a través del tracto digestivo de C. macropomum mantienen su capacidad de germinar. Aunque las variables de germinación (capacidad de germinación, tiempo de imbibición mínimo, tiempo necesario para alcanzar el 50 % de la capacidad de germinación, índice de velocidad de emergencia y tiempo medio de germinación) no mostraron diferencias estadísticas entre tratamientos, las plántulas que crecieron de las semillas consumidas por los peces crecieron más que aquellas provenientes de semillas no ingeridas. Concluimos que los juveniles de C. macropomum tienen la posibilidad de dispersar las semillas de estas especies de Cecropia.

Fruit-eating fishes of Banara arguta (Salicaceae) in the Miranda River floodplain, Pantanal wetland / Peixes frugívoros de Banara arguta (Salicaceae) na planície de inundação do Rio Miranda, Pantanal

The role of fish as frugivorous and its ecological consequences are often neglected in ecological studies. However, the importance of the interaction between fish and plants is gaining force in scientific literature, and fish has been considered effective seed dispersers. The fruit-eating fish assemblage of Banara arguta (Salicaceae) was evaluated in Southern Pantanal wetlands. Nine species were reported consuming fruits, with different strategies to capture them. The distribution of B. arguta associated with the Pantanal floodplain and the presence of several species of fruit-eating fish, suggest that ichthyochory can be an important seed dispersal strategy to B. arguta.

O papel de peixes como frugívoros e suas conseqüências ecológicas são frequentemente negligenciados em estudos ecológicos. Entretanto, a importância da interação entre peixes e plantas vem ganhando força na literatura científica, e peixes têm sido considerados como efetivos dispersores de sementes. A comunidade de peixes frugívoros de Banara arguta (Salicaceae) foi avaliada no Pantanal Sul. Nove espécies foram reportadas consumindo os frutos, com diferentes estratégias para capturá-los. A distribuição de B. arguta associada à planície de inundação no Pantanal, além da presença de várias espécies de peixes frugívoros, sugere que a ictiocoria pode ser uma importante estratégia de dispersão de sementes para B. arguta.

Germinação de sementes de Bothriospora corymbosa (Rubiaceae) recuperadas do trato digestório de Triportheus angulatus (sardinha) no Lago Camaleão, Amazônia Central / Seed germination of Bothriospora corymbosa (Rubiaceae) recouped of digestive tract of Triportheus angulatus (sardine) in Camaleão Lake, Central Amazonian

Na Amazônia as áreas inundáveis são cobertas por florestas com alta diversidade de espécies arbóreas que proporcionam a ictiofauna frutos e sementes indispensáveis a sua alimentação. Alguns estudos de alimentação têm mostrado que a estrutura tegumentar de sementes encontradas no trato digestório de peixes, se apresentavam intactas. Assim, este estudo teve como objetivo verificar se Triportheus angulatus (Spix & Agassiz, 1829) pode ser um agente dispersor de Bothriospora corymbosa (Bth) Hook. f. (Rubiaceae). A pesquisa foi desenvolvida no lago Camaleão, Ilha da Marchantaria, Manaus. Após a captura os peixes foram levados ao laboratório de campo, para a remoção do conteúdo do trato digestório, de onde foram retiradas 200 sementes para o experimento. As sementes do controle foram retiradas de frutos maduros. A germinação e emissão da radícula foram controladas diariamente. Neste estudo verificou-se que a principal fonte de alimento de T. angulatus foram frutos e sementes de espécies da várzea. O desempenho germinativo das sementes de B. corymbosa após a passagem pelo trato digestório de T. angulatus foi de 88,5 por cento e do controle 95 por cento. Os Índices de Velocidade de Germinação (IVG) das sementes do trato digestório e do controle apresentaram diferenças significativas, porém, a passagem destas pelo intestino de T. angulatus não alterou a sua viabilidade. Assim, T. angulatus é um dos agentes dispersores de B. corymbosa, contribuindo com a distribuição desta espécie nas florestas de várzea da Amazônia Central.

The Amazon floodplains are covered by forests with a high diversity of tree species that provides ictyofauna indispensable fruits and seeds for its feeding. Some studies of feeding have shown that the tegument structure of seeds found in the digestive tract of fish presented unbroken. Thus, this study had as objective to verify if Triportheus angulatus (Spix & Agassiz, 1829) can be dispersal agent of Bothriospora corymbosa (Bth) Hook. f. (Rubiaceae). The research was developed in the Camaleão Lake, Island of the Marchantaria, Manaus. After the capture the fishes had been taken to the field laboratory, for the removal of the digestive tracts content, where 200 seeds for the experiment had been removed. The seeds of the control had been removed of ripe fruits. The germination and initial radicle emission were controlled daily. In this study it was verified that the main food source of T. angulatus had been fruits and seeds. The germinative performance of the seeds removed from digestive tract was of 88.5 percent and control 95 percent. The Indices of Speed Germination (IVG) of the seeds which had passed through the digestive system and the control, presented significant differences, however, the passage of these through the intestine of T. angulatus did not modify its viability. Thus, T. angulatus is one of the dispersal agents of B. corymbosa, contributing with the distribution of this species in the floodplain forests of the Central Amazonian.