Sandra Bibiana Correa

Evolutionary Perspectives on Seed Consumption and Dispersal by Fishes

ABSTRACT Fishes probably were the first vertebrate seed dispersers, yet little research has examined this phenomenon. We review evidence of fruit and seed consumption by fishes, and analyze the evolution of frugivory and granivory using South American serrasalmids as a model. Frugivory and granivory are observed among diverse fish taxa worldwide, although most reports are from the Neotropics. Frugivory and granivory among serrasalmids apparently are derived from omnivory, with powerful jaws and specialized dentition appearing as major adaptations. No particular fruit traits seem to be associated with seed dispersal by fishes (ichthyochory). Recent experimental evidence of ichthyochory suggests that fishes can influence riparian vegetation dynamics. Because of deleterious human impacts on aquatic ecosystems worldwide, many critical interactions between plants and fishes have been disrupted before they could be studied. Exotic frugivorous fishes have recently become established on foreign continents, with unknown ecological consequences.

Niche partitioning among frugivorous fishes in response to fluctuating resources in the Amazonian floodplain forest

In response to temporal changes in the quality and availability of food resources, consumers should adjust their foraging behavior in a manner that maximizes energy and nutrient intake and, when resources are limiting, minimizes dietary overlap with other consumers. Floodplains of the Amazon and its lowland tributaries are characterized by strong, yet predictable, hydrological seasonality, seasonal availability of fruits, seeds, and other food resources of terrestrial origin, and diverse assemblages of frugivorous fishes, including morphologically similar species of several characiform families. Here, we investigated how diets of frugivorous fishes in the Amazon change in response to fluctuations in food availability, and how this influences patterns of interspecific dietary overlap. We tested predictions from classical theories of foraging and resource competition by estimating changes in diet breadth and overlap across seasons. We monitored fruiting phenology to assess food availability, and surveyed local fish populations during three hydrological seasons in an oligotrophic river and an adjacent oxbow lake in the Colombian Amazon. We analyzed stomach contents and stable isotope data to evaluate temporal and interspecific relationships for dietary composition, breadth, and overlap. Diets of six species of characiform fishes representing three genera changed according to seasonal fluctuations in food availability, and patterns of diet breadth and interspecific overlap during the peak flood pulse were consistent with predictions of optimal foraging theory. During times of high fruit abundance, fishes consumed items to which their functional morphological traits seemed best adapted, potentially enhancing net energy and nutritional gains. As the annual flood pulse subsided and availability of forest food resources in aquatic habitats changed, there was not a consistent pattern of diet breadth expansion or compression. Nonetheless, shifts in both diet composition and stable isotope ratios of consumer tissues during this period resulted in trophic niche segregation in a pattern consistent with competition theory.

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.

Fish assemblage structure is consistent through an annual hydrological cycle in habitats of a floodplain-lake in the Colombian Amazon

I investigated changes in abundance and spatial distribution of medium- and large-sized fishes (>100 mm) in an oxbow lake of the lower Apaporis River, Colombian Amazon, across three seasons (falling, low, and rising water). Fifty-three species in 13 families were collected from six habitats: lagoon channels, stream, flooded forests, isolated shrub patches, muddy beaches, and rocks. Abundance, biomass, and species richness were higher during the rising-water season and lower during falling-water season. Correspondence analysis (CA) showed that fish assemblages were associated to two basic habitat types. One assemblage of fishes was associated with densely vegetated and structurally complex habitats (flooded forest, lagoon channels, stream, and isolated shrub patches), and a second assemblage of fishes was associated with muddy beaches. These assemblages persisted despite seasonal fluctuations in water level. Species in the structurally complex habitats assemblage were mostly omnivores, whereas the beach habitat assemblage included mainly piscivores and detritivores. Results from this study suggest that overall abundance of fishes in habitats within and surrounding Taraira Lake is highly variable among seasons, but species habitat affinity is maintained through seasons.

Stability and generalization in seed dispersal networks: a case study of frugivorous fish in Neotropical wetlands

When species within guilds perform similar ecological roles, functional redundancy can buffer ecosystems against species loss. Using data on the frequency of interactions between fish and fruit, we assessed whether co-occurring frugivores provide redundant seed dispersal services in three species-rich Neotropical wetlands. Our study revealed that frugivorous fishes have generalized diets; however, large-bodied fishes had greater seed dispersal breadth than small species, in some cases, providing seed dispersal services not achieved by smaller fish species. As overfishing disproportionately affects big fishes, the extirpation of these species could cause larger secondary extinctions of plant species than the loss of small specialist frugivores. To evaluate the consequences of frugivore specialization for network stability, we extracted data from 39 published seed dispersal networks of frugivorous birds, mammals and fish (our networks) across ecosystems. Our analysis of interaction frequencies revealed low frugivore specialization and lower nestedness than analyses based on binary data (presence–absence of interactions). In that case, ecosystems may be resilient to loss of any given frugivore. However, robustness to frugivore extinction declines with specialization, such that networks composed primarily of specialist frugivores are highly susceptible to the loss of generalists. In contrast with analyses of binary data, recently developed algorithms capable of modelling interaction strengths provide opportunities to enhance our understanding of complex ecological networks by accounting for heterogeneity of frugivore–fruit interactions.

Isotopic variation among Amazonian floodplain woody plants and implications for food-web research

Isotopic variation within food sources adds uncertainty to models intended to reconstruct trophic pathways. Understanding this variation is pivotal for planning sampling protocols for food-web research. This study investigates natural variation in C and N stable isotopes among plant species in two western Amazon flooded forests with contrasting watershed biogeochemistry (white-water varzea-forest and black-water igapo-forest). Our objectives were to compare δ13C and δ15N of leaves and fruits between sites; assess the magnitude of within-site variation in δ13C and δ15N of leaves (varzea: 28 spp., igapo: 10 spp.) and fruits (varzea: 22 spp., igapo: 22 spp.); determine within-plant variation in δ13C and δ15N of leaf, wood and fruit tissues; and test whether inter-specific variation in δ13C and δ15N influence the results of a mixing model predicting the contribution of terrestrial C sources to an aquatic consumer. Mean δ13C values of leaves and fruits were not statistically different between the two sites despite regional differences in biogeochemistry and floristic composition. In contrast, mean δ15N of leaves and fruits were significantly lower at the varzea than at the igapo site. The high floristic diversity of both forests was reflected in large within-site interspecific variation in both δ13C and δ15N. Paired comparisons revealed that δ13C of wood and fruits and δ15N of fruits were generally greater than values obtained for leaves from the same plant. The predicted contribution of different carbon sources to the consumer biomass changed between models as a function of source variability. We discuss implications of source variation for designing sampling protocols, interpreting isotopic signatures, and establishing trophic links between plants and consumers. Our findings highlight the importance of in situ sampling to establish reliable primary production baselines for local food webs.

Diet shift of Red Belly Pacu Piaractus brachypomus (Cuvier, 1818) (Characiformes: Serrasalmidae), a Neotropical fish, in the Sepik-Ramu River Basin, Papua New Guinea

Introduction of fish species is a globally widespread practice that causes losses of native species and homogenization of diversity within and across continents. Diet assessments are important tools to depict the ecological function of species introduced into novel ecosystem and possible direct and indirect ecological effects. In this study, we compare the diet of Piaractus brachypomus, a mainly frugivorous Neotropical fish, introduced into the Sepik-Ramu River Basin (Papua New Guinea) nearly two decades ago, to that of similar size individuals from Neotropical populations in the Amazon and Orinoco River basins (South America). In contrast to native populations that feed mainly on terrestrial plants and invertebrates, the diet of introduced P. brachypomus is mainly composed of fish remains and aquatic plants, while terrestrial plants are frequently consumed but in relatively smaller amounts. These findings show that P. brachypomus has an inherently plastic diet that can be adjusted when displaced to a novel geographic area. While trophic plasticity increases the likelihood of a species to establish breeding populations after its introduction, it also reduces our ability to predict negative effects on native species. La introduccion de peces es una practica que se extiende globalmente y que causa perdida de especies nativas y homogenizacion de la diversidad dentro y entre continentes. Los estudios de dieta son herramientas utiles para definir la funcion ecologica de una especie introducida en un ecosistema nuevo y los posibles efectos directos e indirectos. En este estudio describimos la dieta de Piaractus brachypomus, una especie de pez Neotropical principalmente frugivora, que fue introducida en el rio Sepik (Papua Nueva Guinea) hace casi dos decadas; y la comparamos con aquella de individuos de tamano corporal similar de poblaciones nativas en las cuencas de los rios Amazonas y Orinoco (America del Sur). En contraste con las poblaciones nativas que se alimentan principalmente de frutas y semillas, plantas e invertebrados terrestres, la dieta de individuos de P. brachypomus introducidos se compone principalmente de restos de peces y plantas acuaticas, mientras que plantas terrestres son consumidas frecuentemente pero en pequenas cantidades. Estos resultados indican que P. brachypomus tiene una dieta plastica que puede adaptarse cuando la especie se desplaza a un area geografica nueva. A pesar de que la plasticidad trofica aumenta la probabilidad de que una especie establezca poblaciones reproductivas despues de la introduccion, tambien reduce nuestra habilidad de predecir los efectos negativos sobre especies nativas.