Frugivory and seed dispersal in a hyperdiverse plant clade and its role as a keystone resource for the Neotropical fauna

Background and AimsMuch 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.MethodsWe 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.Key Results 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.ConclusionsThe 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.     

高榕隐头果内小蜂群落的动态变化

高榕隐头果内的小蜂群落是我国目前所知榕小蜂群落中最为丰富多样的群落。通过600个果内78063号小蜂标本的分类、统计,在高榕果内共有25种榕小蜂,隶属于7科、14属,其中两种为传粉小蜂,23种为非传传粉小蜂。在榕小蜂群落中,传粉小蜂优势度较为明显,除1月份为18.42%外,其余月份均达51.62%以上,有时甚至达100%。在单个榕果内,小蜂的种类和数量呈现较大变幅,有1~8种,普遍寄生2~4种;榕小蜂数量从1~561只/果不等,寄生100~200只/果较多。1年中不同小蜂出现的相对频度差异也较大,E up ristina sp.和Sy coscap ter sp.2每月都出现,有的非传粉小蜂仅于特定月份出现,并且数量极少。榕小蜂的丰富度随着月份而变化,变幅3~19种,并于1月、4月和8月出现3个高峰。自然群落中,传粉小蜂与非传粉小蜂的数量变化呈显著负相关;多样性指数与传粉小蜂比例呈显著负相关,与非传粉小蜂比例呈显著正相关,而且都具较高的拟合优度。通过3个不同生境样地的多样性指数、丰富度和均匀度比较,结果表明:在人为干扰较严重的样地内,3项指标都较低,除均匀度指标未达显著外,多样性指数和丰富度均达显著水平。但生境对传粉小蜂和非传粉小蜂的影响却不相同,非传粉小蜂会随生境的恶化而迅速消亡,而传粉小蜂的种群则急速膨大,占领全部生境。反之,随着生境的改善,传粉小蜂的种群数量将有所下降,而非传粉小蜂的种类和数量将增加。     

Competition between relatives and the evolution of dispersal in a parasitoid wasp

Evolutionary theory predicts that levels of dispersal vary in response to the extent of local competition for resources and the relatedness between potential competitors. Here, we test these predictions by making use of a female dispersal dimorphism in the parasitoid wasp Melittobia australica. We show that there are two distinct female morphs, which differ in morphology, pattern of egg production, and dispersal behaviour. As predicted by theory, we found that greater competition for resources resulted in increased production of dispersing females. In contrast, we did not find support for the prediction that high relatedness between competitors increases the production of dispersing females in Melittobia. Finally, we exploit the close links between the evolutionary processes leading to selection for dispersal and for biased sex ratios to examine whether the pattern of dispersal can help distinguish between competing hypotheses for the lack of sex ratio adjustment in Melittobia.     

Differential dispersal and female-biased sex allocation in a parasitic wasp

1. Differential dispersal of males and females from a population is predicted to result in biased sex-allocation decisions, even in the absence of sibmating.
2. Mated Bracon hebetor Say (Hymenoptera: Braconidae) females produce distinctly female-biased sex ratios (≈ 30% male), yet sibmating is not a feature of the mating biology of this species. Therefore the dispersal behaviour of male and female B. hebetor from caged subpopulations was examined.
3. A higher proportion of females than males dispersed from the caged subpopulations. Furthermore, females dispersed earlier than males. This suggests that the level of competition for mates experienced by males is higher than the level of competition for hosts experienced by sisters.
4. Roughly half of the dispersing females left after they had mated. Females generally mate once in their lifetimes, suggesting that competition between brothers for mates may be high.     

Kin competition promotes dispersal in a male pollinating fig wasp

Despite theoretical predictions, there is little empirical evidence that kin competition avoidance promotes dispersal. We show that dispersal by male Platyscapa awekei pollinating fig wasps is promoted by both low returns in the natal fig and kin competition avoidance, with strategies depending on the interaction between phenotype (body size) and local conditions. We discuss the paucity of similar work, how males might assess conditions, and then contrast male dispersal and fighting behaviour. This indicates that differences in the scale at which behaviours affect competition can mean that they are the product of dissimilar selective forces even when they have the same recipients. More generally, this could explain why other social interactions are often mixtures of cooperation and conflict.     

Evolutionary stability of plant communities and the maintenance of multiple dispersal types

S.A. Levin, D. Cohen, and A. Hastings (1984, Theor. Popul. Biol. 19, 169–200) and D. Cohen and S.A. Levin (1991, Theor. Popul. Biol. 39, 63–99) by analytic solution of the problem of invasion of a single dispersal type by any other, have provided a theory for evolutionarily stable strategies for seed dispersal in a random environment. Here the results of Cohen and Levin are extended to describe evolutionarily stable combinations of dispersal types. Such combinations of two types are coalitions that cannot be invaded by any other, although in isolation either of the types in the combination is invasible by others. These combinations appear when there is a negative correlation between the seed production of sites in successive years, or when environments are spatially heterogeneous, or presumably under other circumstances. In this work, we examine only the case of negative correlations. For this situation the configuration of evolutionarily stable strategies (ESS) and evolutionarily stable combinations (ESC) depends upon the ratio of (precompetitive) survival rates of dispersersing and nondispersing seeds, which is denoted by α. For low values of α, the purely nondispersing type is an ESS. At a somewhat higher value of α, the purely dispersing type can invade the nondispersing type, and the two types form an ESC, i.e., a combination that cannot be invaded by any other type. For still larger values of α, the purely nondispersing type is excluded by the ESC. Finally, for the largest values of α, pure dispersal is the ESS. In cases where a single dispersal type cannot exclude all others, the stationary distribution of types has a large spread. It can be adequately approximated by equations for conditional means of the proportions of various types at a site of a given quality, but these means must be conditioned upon the prior history at each site. For some purposes we have found that the history of as many as 8–10 generations is required for a good approximation. This phenomenon appears to preclude simple analytic approximations for the ESC.     

Mistletoe as a keystone resource: an experimental test

Various entities have been designated keystone resources, but few tests have been attempted and we are unaware of any experimental manipulations of purported keystone resources. Mistletoes (Loranthaceae) provide structural and nutritional resources within canopies, and their pervasive influence on diversity led to their designation as keystone resources. We quantified the effect of mistletoe on diversity with a woodland-scale experiment, comparing bird diversities before and after all mistletoe plants were removed from 17 treatment sites, with those of 11 control sites and 12 sites in which mistletoe was naturally absent. Three years after mistletoe removal, treatment woodlands lost, on average, 20.9 per cent of their total species richness, 26.5 per cent of woodland-dependent bird species and 34.8 per cent of their woodland-dependent residents, compared with moderate increases in control sites and no significant changes in mistletoe-free sites. Treatment sites lost greater proportions of birds recorded nesting in mistletoe, but changes in species recorded feeding on mistletoe did not differ from control sites. Having confirmed the status of mistletoe as a keystone resource, we suggest that nutrient enrichment via litter-fall is the main mechanism promoting species richness, driving small-scale heterogeneity in productivity and food availability for woodland animals. This explanation applies to other parasitic plants with high turnover of enriched leaves, and the community-scale influence of these plants is most apparent in low productivity systems.     

Spatial variation in the ongoing and widespread decline of a keystone plant species

Extensive dieback in dominant plant species in response to climate change is increasingly common. Climatic conditions and related variables, such as evapotranspiration, vary in response to topographical complexity. This complexity plays an important role in the provision of climate refugia. In 2008/2009, an island‐wide dieback event of the keystone cushion plant Azorella macquariensis Orchard (Apiaceae) occurred on sub‐Antarctic Macquarie Island. This signalled the start of a potential regime shift, suggested to be driven by increasing vapour pressure deficit. Eight years later, we quantified cover and dieback across the range of putative microclimates to which the species is exposed, with the aim of explaining dieback patterns. We test for the influence of evapotranspiration using a suite of topographic proxies and other variables as proposed drivers of change. We found higher cover and lower dieback towards the south of the island. The high spatial variation in A. macquariensis populations was best explained by latitude, likely a proxy for macroscale climate gradients and geology. Dieback was best explained by A. macquariensis cover and latitude, increasing with cover and towards the north of the island. The effect sizes of terrain variables that influence evapotranspiration rates were small. Island‐wide dieback remains conspicuous. Comparison between a subset of sites and historical data revealed a reduction of cover in the north and central regions of the island, and a shift south in the most active areas of dieback. Dieback remained comparatively low in the south. The presence of seedlings was independent of dieback. This study provides an empirical baseline for spatial variation in the cover and condition of A. macquariensis, both key variables for monitoring condition and ‘cover‐debt’ in this critically endangered endemic plant species. These findings have broader implications for understanding the responses of fellfield ecosystems and other Azorella species across the sub‐Antarctic under future climates.     

Beetles provide directed dispersal of viable spores of a keystone wood decay fungus

Wood decay fungi are considered to be dispersed by wind, but dispersal by animals may also be important, and more so in managed forests where dead wood is scarce. We investigated whether beetles could disperse spores of the keystone species Fomitopsis pinicola. Beetles were collected on sporocarps and newly felled spruce logs, a favourable habitat for spore deposition. Viable spores (and successful germination) of F. pinicola were detected by dikaryotization of monokaryotic bait mycelium from beetle samples. Viable spores were on the exoskeleton and in the faeces of all beetles collected from sporulating sporocarps. On fresh spruce logs, nine beetle species transported viable spores, of which several bore into the bark. Our results demonstrate that beetles can provide directed dispersal of wood decay fungi. Potentially, it could contribute to a higher persistence of some species in fragmented forests where spore deposition by wind on dead wood is less likely.     

Strong dispersal in a parasitoid wasp overwhelms habitat fragmentation and host population dynamics

The population dynamics of a parasite depend on species traits, host dynamics and the environment. Those dynamics are reflected in the genetic structure of the population. Habitat fragmentation has a greater impact on parasites than on their hosts because resource distribution is increasingly fragmented for species at higher trophic levels. This could lead to either more or less genetic structure than the host, depending on the relative dispersal rates of species. We examined the spatial genetic structure of the parasitoid wasp Hyposoter horticola, and how it was influenced by dispersal, host population dynamics and habitat fragmentation. The host, the Glanville fritillary butterfly, lives as a metapopulation in a fragmented landscape in the Åland Islands, Finland. We collected wasps throughout the 50 by 70 km archipelago and determined the genetic diversity, spatial population structure and genetic differentiation using 14 neutral DNA microsatellite loci. We compared the genetic structure of the wasp with that of the host butterfly using published genetic data collected over the shared landscape. Using maternity assignment, we also identified full‐siblings among the sampled parasitoids to estimate the dispersal range of individual females. We found that because the parasitoid is dispersive, it has low genetic structure, is not very sensitive to habitat fragmentation and has less spatial genetic structure than its butterfly host. The wasp is sensitive to regional rather than local host dynamics, and there is a geographic mosaic landscape for antagonistic co‐evolution of host resistance and parasite virulence.     

Density-dependent dispersal and relative dispersal affect the stability of predator-prey metacommunities

Although density-dependent dispersal and relative dispersal (the difference in dispersal rates between species) have been documented in natural systems, their effects on the stability of metacommunities are poorly understood. Here we investigate the effects of intra- and interspecific density-dependent dispersal on the regional stability in a predator-prey metacommunity model. We show that, when the dynamics of the populations reach equilibrium, the stability of the metacommunity is not affected by density-dependent dispersal. However, the regional stability, measured as the regional variability or the persistence, can be modified by density-dependent dispersal when local populations fluctuate over time. Moreover these effects depend on the relative dispersal of the predator and the prey. Regional stability is modified through changes in spatial synchrony. Interspecific density-dependent dispersal always desynchronizses local dynamics, whereas intraspecific density-dependent dispersal may either synchronize or desynchronize it depending on dispersal rates. Moreover, intra- and interspecific density-dependent dispersal strengthen the top-down control of the prey by the predator at intermediate dispersal rates. As a consequence the regional stability of the metacommunity is increased at intermediate dispersal rates. Our results show that density-dependent dispersal and relative dispersal of species are keys to understanding the response of ecosystems to fragmentation.     

Rapid environmental degradation in a subarctic ecosystem influences resource use of a keystone avian herbivore

1. Environmental degradation can change resource use strategies of animals and thereby affect survival and fitness. Arctic herbivores may be especially susceptible to the effects of such environmental change because their rapid growth rates demand high-quality forage, which may be limited as environmental conditions deteriorate. We studied the consequences of a trophic cascade, driven by Lesser Snow Goose (Chen caerulescens caerulescens) overgrazing on the south-west coast of Hudson Bay, Canada, which has caused tidal marsh (TM) degradation and the reduction in high-quality forage plants, on gosling growth and resource use. 2. We compared resource use and body size of goslings that inhabited tidal and freshwater marsh (FM) to determine how current foraging strategies influence growth and to test the hypothesis that during early growth goslings require and so consume high-quality TM plants, but that during later growth they may switch to foraging in lower-quality FM. 3. To investigate gosling resource use throughout growth, we measured once a week for 28 days the body size of goslings as well as stable isotope ratios (δ(34) S, δ(15) N and δ(13) C) in multiple tissues of goslings that were collected from both TM and nearby FM. We also measured the stable isotope ratios in forage plants sampled along transects and from gosling foreguts. We used an isotope-mixing model to determine the contribution of FM plants to gosling tissues. 4. Contrary to the proposed hypothesis, goslings inhabiting FM or TM primarily consumed FM plants during early growth. Furthermore, goslings that foraged extensively in FM had similar growth rates and grew to a similar size and body mass, as goslings that foraged in the degraded TM. However, goslings that currently inhabit freshwater or TM were significantly smaller than goslings that inhabited TM in the 1980s prior to habitat degradation. 5. Consequences of smaller overall body size include decreased survival and fecundity for arctic-nesting geese. The ability of phenotypically plastic responses to sustain persistence is limited by reaction norms and the extent of environmental change. Current research is assessing whether those limits have been reached in this system.     

A synopsis of the endemic plant genera of Borneo

The large, tropical island of Borneo has some of the world's richest habitats for plant life, but faces increasing pressures from anthropogenic activities that threaten its biodiversity. With a good portion of the Bornean flora not critically studied, a comprehensive documentation of the numerous endemic taxa expected for the island is not yet complete. It is not known what the relative significance of endemic genera is compared to Bornean centres of endemism documented or predicted through modelling, and if they can inform current conservation plans. As a first step, we here present a synopsis of the endemic genera of Borneo, based on a comprehensive study of literature, herbarium specimens and distributional data, and an investigation of whether the genera have been included in molecular phylogenetic studies that confirm their monophyly. Such a review is timely since many generic delimitations have been shaped by molecular evidence used to test morphology-based taxonomy, while botanical collection and revisionary efforts continue. Our findings suggest that 65 vascular plant genera from 25 families may be considered endemic to Borneo. More than two-thirds (48) of these genera have had at least one species included in molecular phylogenetic studies, but of these, only 39 have been sufficiently sampled to be considered monophyletic with high confidence, or they are monotypic. Slightly over half (38) of the endemic genera are herbaceous. A majority of the genera have fruits or seeds specialised for dispersal by abiotic vectors, or unspecialised seeds. Almost two-thirds (42) of the endemic genera are monotypic, and some of these could represent relict lineages. We expect the current list of endemic genera to be relatively stable and aligned with recent taxonomic concepts, and that it serves to illuminate an interesting aspect of Borneo's unique assemblage of endemic species.     

General relationships between consumer dispersal,resource dispersal and metacommunity diversity

One of the central questions of metacommunity theory is how dispersal of organisms affects species diversity. Here, we show that the diversity–dispersal relationship should not be studied in isolation of other abiotic and biotic flows in the metacommunity. We study a mechanistic metacommunity model in which consumer species compete for an abiotic or biotic resource. We consider both consumer species specialised to a habitat patch, and generalist species capable of using the resource throughout the metacommunity. We present analytical results for different limiting values of consumer dispersal and resource dispersal, and complement these results with simulations for intermediate dispersal values. Our analysis reveals generic patterns for the combined effects of consumer and resource dispersal on the metacommunity diversity of consumer species, and shows that hump‐shaped relationships between local diversity and dispersal are not universal. Diversity–dispersal relationships can also be monotonically increasing or multimodal. Our work is a new step towards a general theory of metacommunity diversity integrating dispersal at multiple trophic levels.     

Effects of a short-term climate change experiment on a sub-Antarctic keystone plant species

The cushion plant Azorella selago is widespread across the sub‐Antarctic, and is considered a keystone species in the dominant fellfield vegetation. However, the impact of current changes in climate in the region (increasing temperature and declining rainfall) on this species is unknown. Here, the response of A. selago to reduced rainfall (a direct effect of climate change) and increased shading (a predicted indirect effect of increasing temperatures, via enhanced growth and wider distribution of more responsive competitors and epiphytes) was experimentally determined. Reduced rainfall increased stem mortality and accelerated autumnal senescence. Furthermore, under this treatment senescence was unequally distributed across individual plants, hypothesized to be a consequence of an interactive effect between rainfall and wind patterns. Shaded stems grew more, and carried larger leaves with lower trichome densities, than their exposed equivalents. As a result, shaded plants were less compact and their surface integrity reduced. The species' response to combined drying and shading was generally similar to its response to shading alone, suggesting that, at least over the short term, the indirect effects of climate change could be more severe than the direct effects. Thus, despite the species' slow growth rate and the short duration of the experiment, persistent direct and indirect effects were observed, both with potential longer‐term consequences for A. selago populations. Climate change is, therefore, likely to impact negatively on this long‐lived keystone species, with significant implications for the structure and functioning of fellfield systems.     

Understanding plant dispersal and migration

The Plant Dispersal and Migration workshop was held in Montpellier, France, from 19 to 23 June 2001.     

Distribution and dispersal in populations capable of resource depletion

Summary A simulation model has been used to investigate the influence of animal (insect) distribution and dispersal among exhaustable resource units (food plants). Population size and stability were used as measures of success. The results showed that population size and stability are highest when egg batch size is as large as can be supported by the average food plant or slightly larger if larval dispersal occurs. Clumping of egg batches of food plants increases population stability when egg batches are small by insuring that some food plants will not be overcrowded. Increasing the proportion of larval dispersers or the success of dispersers can increase or decrease population size and stability depending on the original egg batch distribution, but individuals which produce offspring some of which disperse, generally have a selective advantage. Density dependent larval dispersal decreases population stability. Finally, individuals with lower reproductive capacities can have a selective advantage over those with higher reproductive capacities under certain conditions of egg batch size and larval dispersal.