Importance of Body Size in Determining Dominance Hierarchies among Diverse Tropical Frugivores1

Most studies examining dominance hierarchies have focused at the intraspecific level. While some examples of interspecific hierarchies have been noted, these have usually been limited to a few species in the same taxonomic group that utilize resources in similar ways. Here, we examine evidence for dominance interference competition among vertebrates comprising a diverse frugivore community, including 19 species of birds, squirrels, and primates in a mature Central African rainforest. A total of 38 fruiting trees from 18 species were observed for 2058 h to record dominance interactions between foraging vertebrates. We show that interference competition occurs within and between taxonomically diverse species of vertebrates at fruiting trees. The resulting cross‐taxonomic dominance hierarchy includes larger vertebrates, such as primates and hornbills, as well as smaller ones, such as squirrels and parrots. Within this hierarchy, the dominance rank of each species is highly correlated with body mass, and is shown to significantly affect the number of fruits removed from a given tree. Because a majority of tropical tree species depend on vertebrates to disperse their seeds, and particular vertebrates may preferentially disperse the seeds of specific tree species, results may have important conservation implications for the maintenance of tree diversity in regions where populations of larger frugivores have been depressed or extirpated.     

Vertically stratified frugivore community composition and interaction frequency in a liana fruiting across forest strata

Vertical stratification is a key feature of tropical forests and structures plant–frugivore interactions. However, it is unclear whether vertical differences in plant-frugivore interactions are due to differences among strata in plant community composition or inherent preferences of frugivores for specific strata. To test this, we observed fruit removal of a diverse frugivore community on the liana Marcgravia longifolia in a Peruvian rain forest. Unlike most other plants, Marcgravia longifolia produces fruits across forest strata. This enabled us to study effects of vertical stratification on fruit removal without confounding effects of plant species and stratum. We found a high number of visits of a few frugivore species in the understorey and a low number of visits of many different frugivores in the canopy and midstorey. Whereas partial and opportunistic frugivores foraged across strata with differing frequencies, obligate frugivores were only found eating fruits in the higher strata. Avian frugivores foraging in the canopy were mainly large species with pointed wings, whereas under- and midstorey avian foragers were smaller with rounded wings. Our findings suggest a continuous shift in the frugivore community composition along the vertical gradient, from a few generalized frugivores in the understorey to a diverse set of specialized frugivores in the canopy. This shift in the frugivore community leads to correlated, reciprocal changes from specialized to generalized plant-frugivore interactions. Thus, we conclude that vertical niche differentiation between species in tropical forests persists even when food resources are available across strata. This highlights its role for promoting biodiversity and ecosystem functioning.     

Global patterns in fruiting seasons

Aim   To identify geographical and climatic correlates of the timing of fruit production in fleshy fruited plant communities.
Location   Global.
Methods   We searched the literature for studies documenting monthly variation in the number of fleshy fruited species bearing ripe fruits in plant communities (i.e. fruit phenologies). From these data, we used circular vector algebra to characterize seasonal peaks in fruit production (mean date, as an angle) and the length of fruiting seasons (as a circular standard deviation). Generalized linear models and circular correlations were used to assess whether latitudinal patterns in fruit phenologies could be explained by variation in temperature, precipitation and actual evapotranspiration (AET).
Results   Dates of peak fruit production and the length of fruiting seasons showed consistent differences with latitude. Annual peaks in fruit production occurred 1 to 3 months after the summer solstice at high-latitude sites in both hemispheres. Fruiting seasonality increased with latitude, indicating that fruiting seasons were longer in the tropics and shorter toward the poles. AET was the best climatic predictor of fruit phenologies. Annual peaks in fruit production were positively associated with annual peaks in AET and temperature, while fruiting seasons were shorter in areas with pronounced annual variation in AET.
Main conclusions   Global patterns in fruiting seasons are associated with global variation in climate. Across the globe, fleshy fruits are produced after annual periods of elevated water–energy availability. Fruiting seasonality is also more pronounced in areas with strongly seasonal water–energy inputs. Therefore, the timing of reproduction in fleshy fruited plant communities appears to be determined, at least in part, by spatial and temporal variation in energy supplies needed to subsidise plant reproduction.     

Diet and Dietary Preferences of the Southern Cassowary (Casuarius casuarius) in North Queensland, Australia

We investigated the diet of the southern cassowary (Casuarius casuarius) by identifying the seeds and fruits in fecal droppings encountered on a set of transects over 2 yr in upland rain forest in the wet tropics of North Queensland. A total of 198 droppings containing 56 plant species were found. We surveyed fleshy fruit availability over the subsequent 68 mo on transects in the same area to ascertain fruiting patterns in the study area. The number of droppings found each month did not correspond to the pattern of available fruit biomass. There was no relationship between the fruit traits of moisture content, flesh to seed mass ratio, color, or crop size to contribution of a species to the diet. During the lean fruiting season (May–July) cassowaries relied more on species that fruited continuously throughout the year as they were significantly over‐represented in droppings, while annual fruiting species were under‐represented. During months of high fruit availability (October–December), continuously fruiting species were still over‐represented in the diet but became less important while annual and biennial species became more important. Significantly more species with large fruit and large seeds appeared in the diet than expected and we confirm that the cassowary contributes to the continued dispersal of these species over long distances and in large quantities.     

An analysis of diet specialization in frugivorous Pteropus poliocephalus (Megachiroptera) in Australian subtropical rainforest

Abstract The Grey-headed flying fox Pteropus poliocephalus Temminck 1825 is the only mammalian frugivore to occupy substantial areas of the subtropical rainforests of eastern Australia. The composition of the P. poliocephalus diet and diet specialization in the species are therefore pertinent to studies of trophic structure, seed dispersal and evolutionary processes in these forests. During a three-year diet study, P. poliocephalus used fruits from 44 species of canopy and edge plants. Their taxonomically diverse diet was dominated by the Myrtaceae and Moraceae. Dietary specialization by P. poliocephalus was examined using two criteria: the influence of fruit morphology on diet choice and dietary overlap with sympatric avian frugivores. There was no evidence from either approach that they were specialist feeders. Initial analyses comparing the morphological characters of diet fruits with fruits available to P. poliocephalus during the study period showed a preference for white fruits, berries, syconia and fruits with multiple seeds, and avoidance of black fruits and drupes. However, these significant results were not sustained when the confounding effects of correlations between fruit morphology and other traits were considered. All, except the response to berries, could be attributed to either avoidance by P. poliocephalus of secondary compounds in the Lauraceae or selection for the beneficial phenology of Ficus. Dietary overlap with frugivorous birds was notably high and the fruit diet of P. poliocephalus formed a subset of the avian diet. Associations between fruit colour, size and protective mechanisms have been documented in other rainforest areas and have been proposed as indicators of coadaptive relationships between vertebrate frugivores and their diet plants. However, these associations were not apparent in the morphological characters of fleshy fruits from Australian subtropical rainforest trees. An explanatory hypothesis of primarily avian influence on fruit traits is presented.     

Did fleshy fruit pulp evolve as a defence against seed loss rather than as a dispersal mechanism?

Relatively few studies have examined the evolution of the mutualism between endozoochorous plants and seed dispersers. Most seed dispersal studies are ecological and examine the role of fruit pulp in promoting seed dispersal. This interaction is often assumed to have originated due to selection stemming from seed dispersers. Here I suggest a "defence scenario" wherein fleshy fruits originated as mechanisms to defend seeds and secondarily became structures to promote seed dispersal. I suggest that frugivory followed from herbivores that specialized on consuming seed defensive tissues and that enhanced seed dispersal was initially a consequence of seed defence. The proposed defence scenario is not posited as an explanation for the sequence that led to all modern frugivores. However, it is suggested that seed predation was the initial source of selection that led to fleshy fruits; the necessary precursor to frugivory. Support is described from the fossil record and from modern structures and interactions. Testable predictions are made in hope that greater interest will be focused on the defensive role of fleshy fruit pulp both in modern interactions and historically.     

Recruitment trade-offs and the evolution of dispersal mechanisms in plants

In this study we place seed size vs. seed number trade-offs in the context of plant dispersal ability. The objective was to suggest explanations for the evolution of different seed dispersal mechanisms, in particular fleshy fruits, wind dispersal and the maintenance of unassisted dispersal. We suggest that selection for improved dispersal may act either by increasing the intercept of a dispersal curve (log seed number vs. distance) or by flattening the slope of the curve. 'Improved dispersal' is defined as a marginal increase in the number of recruits sited at some (arbitrary) distance away from the parent plant. Increasing the intercept of the dispersal curve, i.e. producing more seeds, is associated with a reduction in seed size, which in turn affects the recruitment ability, provided that this ability is related to seed size. If recruitment is related to seed size there will be a recruitment cost of evolving increased seed production. On the other hand, a flattening of the slope by evolving dispersal attributes is likely to be associated with a fecundity cost. An exception is wind dispersal where smaller (and hence more numerous) seeds may lead to more efficient dispersal. We derive two main predictions: If recruitment is strongly related to seed size, selection for improved dispersal acts on the slope of the dispersal curve, i.e. by favouring evolution of dispersal attributes on seeds or fruits. If, on the other hand, recruitment is only weakly related to seed size (or not related, or negatively related), selection for improved dispersal favours increased seed production. Despite its simplicity, the model suggests explanations for (i) why so many plant species lack special seed dispersal attributes, (ii) differences in dispersal spectra among plant communities, and (iii) adaptive radiation in seed size and dispersal attributes during angiosperm evolution. This revised version was published online in July 2006 with corrections to the Cover Date.     

How intraspecific variation in seed‐dispersing animals matters for plants

Seed dispersal by animals is a complex phenomenon, characterized by multiple mechanisms and variable outcomes. Most researchers approach this complexity by analysing context‐dependency in seed dispersal and investigating extrinsic factors that might influence interactions between plants and seed dispersers. Intrinsic traits of seed dispersers provide an alternative way of making sense of the enormous variation in seed fates. I review causes of intraspecific variability in frugivorous and granivorous animals, discuss their effects on seed dispersal, and outline likely consequences for plant populations and communities. Sources of individual variation in seed‐dispersing animals include sexual dimorphism, changes associated with growth and ageing, individual specialization, and animal personalities. Sexual dimorphism of seed‐dispersing animals influences seed fate through diverse mechanisms that range from effects caused by sex‐specific differences in body size, to influences of male versus female cognitive functions. These differences affect the type of seed treatment (e.g. dispersal versus predation), the number of dispersed seeds, distance of seed dispersal, and likelihood that seeds are left in favourable sites for seeds or seedlings. The best‐documented consequences of individual differences associated with growth and ageing involve quantity of dispersed seeds and the quality of seed treatment in the mouth and gut. Individual specialization on different resources affects the number of dispersed plant species, and therefore the connectivity and architecture of seed‐dispersal networks. Animal personalities might play an important role in shaping interactions between plants and dispersers of their seeds, yet their potential in this regard remains overlooked. In general, intraspecific variation in seed‐dispersing animals often influences plants through effects of these individual differences on the movement ecology of the dispersers. Two conditions are necessary for individual variation to exert a strong influence on seed dispersal. First, the individual differences in traits should translate into differences in crucial characteristics of seed dispersal. Second, individual variation is more likely to be important when the proportions of particular types of individuals fluctuate strongly in a population or vary across space; when proportions are static, it is less likely that intraspecific differences will be responsible for changes in the dynamics and outcomes of plant–animal interactions. In conclusion, focusing on variation among foraging animals rather than on species averages might bring new, mechanistic insights to the phenomenon of seed dispersal. While this shift in perspective is unlikely to replace the traditional approach (based on the assumption that all important variation occurs among species), it provides a complementary alternative to decipher the enormous variation observed in animal‐mediated seed dispersal.     

Mutualism or opportunism? Tree fuchsia (Fuchsia excorticata) and tree weta (Hemideina) interactions

Mutualisms or interspecific interactions involving net mutual benefits, are an important component of ecological theory, although effectively demonstrating mutualism is notoriously difficult. Among two New Zealand endemics, a slightly elevated germination rate of Fuchsia excorticata (Onagraceae) seeds after passage through tree weta (Orthoptera: Anostostomatidae) compared with seeds manually extracted from fruit, led to the proposal that a mutualistic relationship exists between this plant and animal. An improved germination rate, or any other single trait, however, does not alone constitute evidence for mutualism; the relative costs and benefits of numerous components of the interaction need to be accounted for. We considered the costs and benefits to F. excorticata of the putative seed dispersal mutualism with tree weta. Tree weta provided with F. excorticata fruits destroyed 78% of the seeds they consumed, did not move fruit; and faeces containing seeds were deposited near their roost holes (which are naturally in trees). The seeds remaining after fruit consumption and those that are ingested but survive gut passage are unlikely to be deposited in suitable habitat for seedling survival. Plant food preferences of captive tree weta assessed using pairwise leaf choice tests showed that the leaves of F. excorticata were the least preferred of six commonly encountered plants. In addition, we found that tree weta did not show a preference for F. excorticata fruit over a standard leafy diet, indicating they are unlikely to be actively seeking fruit in preference to other sources of food. These observations indicate that any interaction between tree weta and F. excorticata is likely to be opportunistic rather than mutualistic, and highlight the difficulty of characterizing such interactions.     

Frugivores and seed dispersal: mechanisms and consequences for biodiversity of a key ecological interaction

The 5th Symposium on Frugivores and Seed Dispersal, held in Montpellier (France), 13-18 June 2010, brought together more than 220 researchers exemplifying a wide diversity of approaches to the study of frugivory and dispersal of seeds. Following Ted Fleming and Alejandro Estrada's initiative in 1985, this event was a celebration of the 25th anniversary of the first meeting in Veracruz, Mexico. Frugivory and seed dispersal are active research areas that have diversified in multiple directions since 1985 to include evolution (e.g. phylogenetic diversity and dispersal adaptations), physiology (e.g. sensory cues and digestion), landscape ecology (movement patterns), molecular ecology (e.g. gene flow, genetic diversity and structure), community ecology (e.g. mutualistic interaction networks) and conservation biology (effects of hunting, fragmentation, invasion and extinction), among others. This meeting provided an opportunity to assess conceptual and methodological progress, to present ever more sophisticated insights into frugivory in animals and dispersal patterns in plants, and to report the advances made in examining the mechanisms and consequences of seed dispersal for plants and frugivores.     

Fig-eating by vertebrate frugivores: a global review

The consumption of figs (the fruit of Ficus spp.: Moraceae) by vertebrates is reviewed using data from the literature, unpublished accounts and new field data from Borneo and Hong Kong. Records of frugivory from over 75 countries are presented for 260 Ficus species (approximately 30% of described species). Explanations are presented for geographical and taxonomic gaps in the otherwise extensive literature. In addition to a small number of reptiles and fishes, 1274 bird and mammal species in 523 genera and 92 families are known to eat figs. In terms of the number of species and genera of fig-eaters and the number of fig species eaten we identify the avian families interacting most with Ficus to be Columbidae, Psittacidae, Pycnonotidae, Bucerotidae, Sturnidae and Lybiidae. Among mammals, the major fig-eating families are Pteropodidae, Cercopithecidae, Sciuridae, Phyllostomidae and Cebidae. We assess the role these and other frugivores play in Ficus seed dispersal and identify fig-specialists. In most, but not all, cases fig specialists provide effective seed dispersal services to the Ficus species on which they feed. The diversity of fig-eaters is explained with respect to fig design and nutrient content, phenology of fig ripening and the diversity of fig presentation. Whilst at a gross level there exists considerable overlap between birds, arboreal mammals and fruit bats with regard to the fig species they consume, closer analysis, based on evidence from across the tropics, suggests that discrete guilds of Ficus species differentially attract subsets of sympatric frugivore communities. This dispersal guild structure is determined by interspecific differences in fig design and presentation. Throughout our examination of the fig-frugivore interaction we consider phylogenetic factors and make comparisons between large-scale biogeographical regions. Our dataset supports previous claims that Ficus is the most important plant genus for tropical frugivores. We explore the concept of figs as keystone resources and suggest criteria for future investigations of their dietary importance. Finally, fully referenced lists of frugivores recorded at each Ficus species and of Ficus species in the diet of each frugivore are presented as online appendices. In situations where ecological information is incomplete or its retrieval is impractical, this valuable resource will assist conservationists in evaluating the role of figs or their frugivores in tropical forest sites.     

Microsites of seed arrival: spatio–temporal variations in complex seed‐disperser networks

Microsites where seeds arrive during the dispersal process determine plant reproductive success, affecting the quality of dispersal. Despite their crucial role for plant recruitment, very few studies have addressed spatio–temporal variations in microsites of seed arrival in complex seed‐disperser networks. Using an endozoochorous dispersal system, we characterized the microsites of seed arrival of eight fleshy‐fruited plant species dispersed by five mammal species during two consecutive seasons across three sites in a Mediterranean environment (n = 383 feces with seeds; 261 453 seeds). We evaluated spatial and temporal variations in the probability of a seed to arrive at open microsites or at microsites with varying plant cover, considering selection by frugivores and assessing the extent to which seeds of particular species arrived under conspecifics or heterospecifics. We found strong spatio–temporal variations in the amounts of seeds of the eight target species arriving at different microsites. These variations were strongly driven by frugivores’ selection of different landscape elements (i.e. open areas and microsites dominated by different plant species), which differed from expectations based on their local availability. In general, more seeds than expected arrived at vacant (open) microsites. Using bipartite network graphs to connect seeds with their arrival microsites, we found that the proportion of seeds of fleshy‐fruited species arriving near conspecifics or heterospecifics, or at vacant microsites, varied depending on the target plant species, but also on the frugivore species dispersing it, on the study site and on the dispersal season. Our study revealed marked spatio–temporal variations in the microsites of seed arrival, which will potentially have implications for the quality of dispersal effectiveness, ultimately affecting plant population dynamics and community structure. Such a strong context‐dependence in the microsites of seed arrival is likely to confer resilience against unpredictable environmental conditions, like those typical of Mediterranean ecosystems.     

Constraints on plant signals and rewards to multiple mutualists?

Many plants invest substantial resources in signaling to and rewarding two kinds of ‘interguild’ mutualists, pollinators and seed dispersers. The signals and rewards are expressed via traits of flowers and fruits. Pollinators and seed dispersers could act in synergistic or antagonistic ways to influence selection on these traits. Here, we address the issue of whether plant species might be constrained in signaling to and rewarding multiple mutualists that provide different types of benefits to plants. Specifically, does investment in one type of mutualist limit investment in another? We examined the correlation between flower size and fruit size for 472 plant species spanning three regional floras. Our analyses made the assumption that structure size is related to plant investment in signals and/or rewards. We expect that a constraint due to interguild mutualisms would be evidenced by a negative correlation between flower and fruit size. Instead, we found significantly positive relationships between flower size and fruit size in all three regional floras. These relationships remained robust after correcting for plant evolutionary history using phylogenetically independent contrasts. These patterns may reflect synergies in selection by pollinators and seed dispersers, genetically-based or resource-based constraints on investment in reproductive tissues, and/or an underlying trade-off in structure size versus number.     

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.     

The Influence of Temporal Changes in Fruit Availability on Diet Composition and Seed Handling in Blue Monkeys (Cercopithecus mitis doggetti)1

We investigated the relation between temporally varying resources, diet composition, and seed-handling behaviors in a group of blue monkeys (Cercopithecus mitis doggetti) in a tropical montane forest of Rwanda. Changes in diet composition were related to concurrent phenological studies of fruit-producing trees, and density and abundance of tree resources within the monkey's home range. Fruit composed nearly 50 percent of the diet. Over 50 percent of the fruits eaten had juicy fleshy pulp. Observations of seed handling behavior provided insights into the role of these animals as potential seed dispersal agents. The monkeys moved the seeds of 29 species out of parent canopies by defecating seeds intact and by potentially carrying seeds in cheek pouches and dropping them later. Seeds of 18 species were found intact in fecal piles. Our study showed community-level phenology patterns did not indicate a decrease in fruit availability during the study period, but an analysis of the preferred fruits consumed by the monkeys showed distinct periods of low fruit availability. The study period included two dry seasons; only one of these produced a period of fruit scarcity for the animals. The animals employed different strategies during times of preferred fruit scarcity. They increased consumption of leaves and other fleshy fruits, and diet diversity increased, or became mainly seed predators and diet diversity decreased. The variable responses of these monkeys to changes in food availability highlights their dietary plasticity and imposes significant variations in their role as potential seed dispersers.