Moving from frugivory to seed dispersal: Incorporating the functional outcomes of interactions in plant-frugivore networks.
ABSTRACT: There is growing interest in understanding the functional outcomes of species interactions in ecological networks. For many mutualistic networks, including pollination and seed dispersal networks, interactions are generally sampled by recording animal foraging visits to plants. However, these visits may not reflect actual pollination or seed dispersal events, despite these typically being the ecological processes of interest. Frugivorous animals can act as seed dispersers, by swallowing entire fruits and dispersing their seeds, or as pulp peckers or seed predators, by pecking fruits to consume pieces of pulp or seeds. These processes have opposing consequences for plant reproductive success. Therefore, equating visitation with seed dispersal could lead to biased inferences about the ecology, evolution and conservation of seed dispersal mutualisms. Here, we use natural history information on the functional outcomes of pairwise bird-plant interactions to examine changes in the structure of seven European plant-frugivore visitation networks after non-mutualistic interactions (pulp pecking and seed predation) have been removed. Following existing knowledge of the contrasting structures of mutualistic and antagonistic networks, we hypothesized a number of changes following interaction removal, such as increased nestedness and lower specialization. Non-mutualistic interactions with pulp peckers and seed predators occurred in all seven networks, accounting for 21%-48% of all interactions and 6%-24% of total interaction frequency. When non-mutualistic interactions were removed, there were significant increases in network-level metrics such as connectance and nestedness, while robustness decreased. These changes were generally small, homogenous and driven by decreases in network size. Conversely, changes in species-level metrics were more variable and sometimes large, with significant decreases in plant degree, interaction frequency, specialization and resilience to animal extinctions and significant increases in frugivore species strength. Visitation data can overestimate the actual frequency of seed dispersal services in plant-frugivore networks. We show here that incorporating natural history information on the functions of species interactions can bring us closer to understanding the processes and functions operating in ecological communities. Our categorical approach lays the foundation for future work quantifying functional interaction outcomes along a mutualism-antagonism continuum, as documented in other frugivore faunas.
Project description:Frugivory, that is feeding on fruits, pulp or seeds by animals, is usually considered a mutualism when interactions involve seed dispersal, and an antagonism when it results in the predation and destruction of seeds. Nevertheless, most frugivory interactions involve both benefits and disadvantages for plants, and the net interaction outcomes thus tend to vary along a continuum from mutualism to antagonism. Quantifying outcome variation is challenging and the ecological contribution of frugivorous animals to plant demography thus remains little explored. This is particularly true for interactions in which animals do not ingest entire fruits, that is in seed-eating and pulp-eating. Here, we provide a comprehensive review of Neotropical palm-frugivore interactions, with a focus on how frugivore consumption behaviour (i.e. digestive processing, fruit-handling ability and caching behaviour) and feeding types (fruit-eating, pulp-eating and seed-eating) influence interaction outcomes at different demographic stages of palms. We compiled a total of 1043 species-level palm-frugivore interaction records that explicitly captured information on which parts of palm fruits are eaten by animals. These records showed consumption of fruits of 106 Neotropical palm species by 273 vertebrate species, especially birds (50%) and mammals (45%), but also fish (3%) and reptiles (2%). Fruit-eating involved all four taxonomic vertebrate classes whereas seed-eating and pulp-eating were only recorded among birds and mammals. Most fruit-eating interactions (77%) resulted in positive interaction outcomes for plants (e.g. gut-passed seeds are viable or seeds are successfully dispersed), regardless of the digestive processing type of vertebrate consumers (seed defecation versus regurgitation). The majority of pulp-eating interactions (91%) also resulted in positive interaction outcomes, for instance via pulp removal that promoted seed germination or via dispersal of intact palm seeds by external transport, especially if animals have a good fruit-handling ability (e.g. primates, and some parrots). By contrast, seed-eating interactions mostly resulted in dual outcomes (60%), where interactions had both negative effects on seed survival and positive outcomes through seed caching and external (non-digestive) seed dispersal. A detailed synthesis of available field studies with qualitative and quantitative information provided evidence that 12 families and 27 species of mammals and birds are predominantly on the mutualistic side of the continuum whereas five mammalian families, six mammal and one reptile species are on the antagonistic side. The synthesis also revealed that most species can act as partial mutualists, even if they are typically considered antagonists. Our review demonstrates how different consumption behaviours and feeding types of vertebrate fruit consumers can influence seed dispersal and regeneration of palms, and thus ultimately affect the structure and functioning of tropical ecosystems. Variation in feeding types of animal consumers will influence ecosystem dynamics via effects on plant population dynamics and differences in long-distance seed dispersal, and may subsequently affect ecosystem functions such as carbon storage. The quantification of intra- and inter-specific variation in outcomes of plant-frugivore interactions - and their positive and negative effects on the seed-to-seedling transition of animal-dispersed plants - should be a key research focus to understand better the mutualism-antagonism continuum and its importance for ecosystem dynamics.
Project description:Frugivory is a widespread mutualistic interaction in which frugivores obtain nutritional resources while favoring plant recruitment through their seed dispersal services. Nonetheless, how these complex interactions are organized in diverse communities, such as tropical forests, is not fully understood. In this study we evaluated the existence of plant-frugivore sub-assemblages and their phylogenetic organization in an undisturbed western Amazonian forest in Colombia. We also explored for potential keystone plants, based on network analyses and an estimate of the amount of fruit going from plants to frugivores. We carried out diurnal observations on 73 canopy plant species during a period of two years. During focal tree sampling, we recorded frugivore identity, the duration of each individual visit, and feeding rates. We did not find support for the existence of sub assemblages, such as specialized vs. generalized dispersal systems. Visitation rates on the vast majority of canopy species were associated with the relative abundance of frugivores, in which ateline monkeys (i.e. Lagothrix and Ateles) played the most important roles. All fruiting plants were visited by a variety of frugivores and the phylogenetic assemblage was random in more than 67% of the cases. In cases of aggregation, the plant species were consumed by only primates or only birds, and filters were associated with fruit protection and likely chemical content. Plants suggested as keystone species based on the amount of pulp going from plants to frugivores differ from those suggested based on network approaches. Our results suggest that in tropical forests most tree-frugivore interactions are generalized, and abundance should be taken into account when assessing the most important plants for frugivores.
Project description: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.
Project description:Forest disturbance causes specialization of plant-frugivore networks and jeopardizes mutualistic interactions through reduction of ecological redundancy. To evaluate how simplification of a forest into an agroecosystem affects plant-disperser mutualistic interactions, we compared bat-fruit interaction indexes of specialization in tropical montane cloud forest fragments (TMCF) and shaded-coffee plantations (SCP). Bat-fruit interactions were surveyed by collection of bat fecal samples. Bat-fruit interactions were more specialized in SCP (mean H2 ' = 0.55) compared to TMCF fragments (mean H2 ' = 0.27), and were negatively correlated to bat abundance in SCP (R = -0.35). The number of shared plant species was higher in the TMCF fragments (mean = 1) compared to the SCP (mean = 0.51) and this was positively correlated to the abundance of frugivorous bats (R= 0.79). The higher specialization in SCP could be explained by lower bat abundance and lower diet overlap among bats. Coffee farmers and conservation policy makers must increase the proportion of land assigned to TMCF within agroecosystem landscapes in order to conserve frugivorous bats and their invaluable seed dispersal service.
Project description:Endozoochory, a mutualistic interaction between plants and frugivores, is one of the key processes responsible for maintenance of tropical biodiversity. Islands, which have a smaller subset of plants and frugivores when compared with mainland communities, offer an interesting setting to understand the organization of plant-frugivore communities vis-a-vis the mainland sites. We examined the relative influence of functional traits and phylogenetic relationships on the plant-seed disperser interactions on an island and a mainland site. The island site allowed us to investigate the organization of the plant-seed disperser community in the natural absence of key frugivore groups (bulbuls and barbets) of Asian tropics. The endemic Narcondam Hornbill was the most abundant frugivore on the island and played a central role in the community. Species strength of frugivores (a measure of relevance of frugivores for plants) was positively associated with their abundance. Among plants, figs had the highest species strength and played a central role in the community. Island-mainland comparison revealed that the island plant-seed disperser community was more asymmetric, connected, and nested as compared to the mainland community. Neither phylogenetic relationships nor functional traits (after controlling for phylogenetic relationships) were able to explain the patterns of interactions between plants and frugivores on the island or the mainland pointing toward the diffused nature of plant-frugivore interactions. The diffused nature is a likely consequence of plasticity in foraging behavior and trait convergence that contribute to governing the interactions between plants and frugivores. This is one of the few studies to compare the plant-seed disperser communities between a tropical island and mainland and demonstrates key role played by a point-endemic frugivore in seed dispersal on island.
Project description:The study of plant-frugivore interactions is essential to understand the ecology and evolution of many plant communities. However, very little is known about how interactions among frugivores indirectly affect plant reproductive success. In this study, we examined direct interactions among vertebrate frugivores sharing the same fruit resources. Then, we inferred how the revealed direct interspecific interactions could lead to indirect (positive or negative) effects on reproductive success of fleshy fruited plants. To do so, we developed a new analytical approach that combines camera trap data (spatial location, visitor species, date and time, activity) and tailored null models that allowed us to infer spatial-temporal interactions (attraction, avoidance or indifference) between pairs of frugivore species. To illustrate our approach, we chose to study the system composed by the Mediterranean dwarf palm, Chamaerops humilis, the Iberian pear tree, Pyrus bourgaeana, and their shared functionally diverse assemblages of vertebrate frugivores in a Mediterranean area of SW Spain. We first assessed the extent to which different pairs of frugivore species tend to visit the same or different fruiting individual plants. Then, for pairs of species that used the same individual plants, we evaluated their spatial-temporal relationship. Our first step showed, for instance, that some prey frugivore species (e.g. lagomorphs) tend to avoid those C. humilis individuals that were most visited by their predators (e.g. red foxes). Also, the second step revealed temporal attraction between large wild and domestic frugivore ungulates (e.g. red deer, cows) and medium-sized frugivores (e.g. red foxes) suggesting that large mammals could facilitate the C. humilis and P. bourgaeana exploitation to other smaller frugivores by making fruits more easily accessible. Finally, our results allowed us to identify direct interaction pathways, that revealed how the mutualistic and antagonistic relations between animal associates derived into indirect effects on both plants seed dispersal success. For instance, we found that large-sized seed predators (e.g. ungulates) had a direct positive effect on the likelihood of visits by legitimate seed dispersers (e.g. red foxes) to both fleshy fruited plants. Then, seed predators showed an indirect positive effect on the plants' reproductive success. Our new analytical approach provides a widely applicable framework for further studies on multispecies interactions in different systems beyond plant-frugivore interactions, including plant-pollinator interactions, the exploitation of plants by herbivores, and the use of carcasses by vertebrate scavengers.
Project description:Species interactions, both mutualistic and antagonistic, are widely recognized as providing important ecosystem services. Fruit-eating animals influence plant recruitment by increasing germination during gut passage and moving seeds away from conspecifics. However, relative to studies focused on the importance of frugivores for plant population maintenance, few studies target frugivores as ecosystem service providers, and frugivores are underappreciated as ecosystem service providers relative to other mutualists such as pollinators. Here, we use an accidental experiment to elucidate the role of seed dispersal by frugivores for maintaining a culturally and economically important plant, the donne' sali chili (Capsicum frutescens) in the Mariana Islands. One of the islands (Guam) has lost nearly all of its native forest birds due to an invasive snake (Boiga irregularis), whereas nearby islands have relatively intact bird populations. We hypothesized that frugivore loss would influence chili recruitment and abundance, which could have economic and cultural impacts. By using video cameras, we confirmed that birds were the primary seed dispersers. We used captive bird feeding trials to obtain gut-passed seeds to use in a seedling emergence experiment. The experiment showed that gut-passed seeds emerged sooner and at a higher proportion than seeds from whole fruits. Consistent with our findings that birds benefit chilies, we observed lower chili abundance on Guam than on islands with birds. In a survey questionnaire of island residents, the majority of residents reported an association between the wild chili and local cultural values and traditions. In addition, we identified a thriving market for chili products, suggesting benefits of wild chilies to people in the Marianas both as consumers and producers. Our study therefore documents seed dispersal as both a cultural and a supporting ecosystem service. We provide a comprehensive case study on how seed-dispersed plants decline in the absence of their disperser, and how to apply mixed-methods in ecosystem service assessments. Furthermore, we suggest that scientists and resource managers may utilize fruit-frugivore mutualisms concerning socially valuable plants to gather support for frugivore and forest conservation efforts.
Project description:In the frugivory networks of many arid and semi-arid Mesoamerican ecosystems, columnar cacti act as keystone species that produce fruits with a high content of water and nutrients attractive to numerous vertebrates. The aim of this investigation was to assess the fruit removal patterns of two guilds of frugivores on the fruits of the woolly torch Pilosocereus leucocephalus. We assessed fruit pulp removal in two ways: by estimating the consumption of seeds given the amount of pulp removed per visit and by estimating the percentage of pulp removal over time. We put exclosures on unripe, intact fruits to keep frugivores from removing material. Once ripe, we removed the exclosures and tracked animal visitation of 69 fruits using camera traps. We obtained a total of 2,162 hr of footage (14:47 hours of them with effective pulp removal). The highest number of visitors is that of diurnal species (n = 12, all birds) versus only four nocturnal (three bats, one rodent). The most effective species in pulp removal are birds. Bats play a modest role in frugivory of this cactus. The significance of this work is twofold: (a) birds and bats consume the fruit pulp of this cactus and likely disperse its seeds, and (b) although bats rank high in pulp removal effectiveness, birds as a guild far outweigh their importance in this system, as they are not only more frequent but also remove more pulp and seeds. Both groups are known to be important in cacti seed dispersal, and our findings are essential in understanding the population dynamics of the woolly torch and in elucidating its seed dispersal ecology.
Project description:<h4>Background and aims</h4>Much of our understanding of the ecology and evolution of seed dispersal in the Neotropics is founded on studies involving the animal-dispersed, hyperdiverse plant clade Miconia (Melastomataceae). Nonetheless, no formal attempt has been made to establish its relevance as a model system or indeed provide evidence of the role of frugivores as Miconia seed dispersers.<h4>Methods</h4>We built three Miconia databases (fruit phenology/diaspore traits, fruit-frugivore interactions and effects on seed germination after gut passage) to determine how Miconia fruiting phenology and fruit traits for >350 species interact with and shape patterns of frugivore selection. In addition, we conducted a meta-analysis evaluating the effects of animal gut passage/seed handling on Miconia germination.<h4>Key results</h4>Miconia produce numerous small berries that enclose numerous tiny seeds within water- and sugar-rich pulps. In addition, coexisting species provide sequential, year long availability of fruits within communities, with many species producing fruits in periods of resource scarcity. From 2396 pairwise interactions, we identified 646 animal frugivore species in five classes, 22 orders and 60 families, including birds, mammals, reptiles, fish and ants that consume Miconia fruits. Endozoochory is the main dispersal mechanism, but gut passage effects on germination were specific to animal clades; birds, monkeys and ants reduced seed germination percentages, while opossums increased it.<h4>Conclusions</h4>The sequential fruiting phenologies and wide taxonomic and functional diversity of animal vectors associated with Miconia fruits underscore the likely keystone role that this plant clade plays in the Neotropics. By producing fruits morphologically and chemically accessible to a variety of animals, Miconia species ensure short- and long-distance seed dispersal and constitute reliable resources that sustain entire frugivore assemblages.
Project description:Although antagonists are hypothesized to impede the evolution of mutualisms, they may simultaneously exert selection favouring the evolution of alternative mutualistic interactions. We found that increases in limber pine (Pinus flexilis) seed defences arising from selection exerted by a pre-dispersal seed predator (red squirrel Tamiasciurus hudsonicus) reduced the efficacy of limber pine's primary seed disperser (Clark's nutcracker Nucifraga columbiana) while enhancing seed dispersal by ground-foraging scatter-hoarding rodents (Peromyscus). Thus, there is a shift from relying on primary seed dispersal by birds in areas without red squirrels, to an increasing reliance on secondary seed dispersal by scatter-hoarding rodents in areas with red squirrels. Seed predators can therefore drive the evolution of seed defences, which in turn favour alternative seed dispersal mutualisms that lead to major changes in the mode of seed dispersal. Given that adaptive evolution in response to antagonists frequently impedes one kind of mutualistic interaction, the evolution of alternative mutualistic interactions may be a common by-product.