Anna Traveset

The Ecology of Seed Dispersal

Seed dispersal has long been a topic of interest to naturalists, but it has not been until the last three decades that the ecology of dispersal has received much rigorous scientific attention. Many theoretical and empirical advances have recently been made, although important lacunae in our understanding still need to be filled before dispersal ecology becomes a coherent body of knowledge. A major goal of this chapter is to review the existing literature on seed dispersal, highlighting these essential but missing kinds of information. This review is divided into two sections, the first dealing with the evolution of dispersal mechanisms and the second with the consequences of dispersal at population and community levels. Dispersal can occur in both space and time, but only the former will be treated here, except where some relationship between the two axes is known (Venable and Brown, 1988; Leck et al., 1989; Eriksson and Ehrlen, 1998a; see also Murdoch and Ellis, Chapter 8, this volume).

Annual Variability in Seed Production by Woody Plants and the Masting Concept: Reassessment of Principles and Relationship to Pollination and Seed Dispersal

By analyzing 296 published and unpublished data sets describing annual variation in seed output by 144 species of woody plants, this article addresses the following questions. Do plant species naturally fall into distinct groups corresponding to masting and nonmasting habits? Do plant populations generally exhibit significant bimodality in annual seed output? Are there significant relationships between annual variability in seed production and pollination and seed dispersal modes, as predicted from economy of scale considerations? We failed to identify distinct groups of species with contrasting levels of annual variability in seed output but did find evidence that most polycarpic woody plants seem to adhere to alternating supra‐annual schedules consisting of either high or low reproduction years. Seed production was weakly more variable among wind‐pollinated taxa than animal‐pollinated ones. Plants dispersed by mutualistic frugivores were less variable than those dispersed by either inanimate means or animals that predominantly behave as seed predators. We conclude that there are no objective reasons to perpetuate the concept of mast fruiting in the ecological literature as a shorthand to designate a distinct biological phenomenon. Associations between supra‐annual variabiity in seed output and pollination and seed dispersal methods suggest the existence of important reproductive correlates that demand further investigation.

EARLY EMERGENCE ENHANCES PLANT FITNESS: A PHYLOGENETICALLY CONTROLLED META‐ANALYSIS

The time at which a seedling emerges can determine its future success as a plant. Despite the large number of studies that have examined the effect of emergence time on different components of plant fitness (survival, growth, and/or fecundity), the potential evolutionary response to selection on seedling emergence date is still poorly known. In this study, we review 55 of those studies by a random-effects meta-analysis, considering the phylogenetic relatedness among taxa. We test the following hypotheses: (1) early emergence increases seedling survival, growth, and fecundity, (2) early emergence is more advantageous to large-seeded species than to small-seeded ones, as the former can compensate for the lower number of seeds by increasing seedling survival, (3) perennial plants benefit more than annuals from early emergence, as the iteroparity of the former allows them to risk seedling emergence to the best conditions each year, whereas the semelparity of the latter forces them to spread the risk of emergence over time, and (4) the effect of emergence time may depend upon the experimental conditions (field vs. controlled experiments in a greenhouse or laboratory). Our results show that early emergence differentially affects components of plant fitness, with no effect on seedling survival but large benefits to seedling growth and fecundity. Such effects vary depending upon intrinsic factors like seed size or life-form, and also upon methodology (census time and experimental conditions). Large-seeded species gain from emerging early by growing more during their first growing seasons, although they survive and reproduce similarly to small-seeded species. The survival benefit of early emergence is greater in perennial than in annual species, thus supporting hypothesis 3. The relationship between emergence time and seedling growth appears to be stronger under controlled conditions than in the field, probably as a result of the unlimited nutrient and water resources of the former. In field conditions, in contrast, limited resources probably decelerate the growth of early seedlings, precluding the detection of differences between these and late seedlings.

A meta-analysis of impacts of alien vs. native plants on pollinator visitation and reproductive success of co-flowering native plants

Alien plant species can alter pollinator visitation and, in turn, the sexual reproduction of natives. Using a conventional and a phylogenetically controlled meta-analytical approach on a data set of 40 studies, we evaluated the effect of alien neighbour plant species (aliens) on visitation to and reproduction of native co-flowering focal species (focals), and compared such effect to that of native neighbours (natives). An overall significantly negative effect of aliens on visitation to and reproduction of focals was confirmed. Interestingly, aliens differed from natives in their effect on visitation, but not on reproductive success. The negative effect of aliens on visitation and reproductive success increased at high relative alien plant abundance, but this increase was proportionally lower than the increase in relative plant abundance. Likewise, effect of aliens on visitation and reproductive success was most detrimental when alien and focal species had similar flower symmetry or colour. The phylogenetic relatedness between alien neighbours and focals influenced the reproductive success effect size. Results of the phylogenetic meta-analysis were only partly consistent with those of the conventional meta-analysis, depending on the response variable and on whether we controlled for the phylogeny of neighbour or focal species, which calls for special attention to control for species relatedness in this type of review. This study demonstrates the predominant detrimental impact of alien plants on pollination and reproduction of natives, and highlights the importance of phenotypic similarity to the outcome of the interaction.

Beyond species loss: the extinction of ecological interactions in a changing world

Summary 1. The effects of the present biodiversity crisis have been largely focused on the loss of species. However, a missed component of biodiversity loss that often accompanies or even precedes species disappearance is the extinction of ecological interactions. 2. Here, we propose a novel model that (i) relates the diversity of both species and interactions along a gradient of environmental deterioration and (ii) explores how the rate of loss of ecological functions, and consequently of ecosystem services, can be accelerated or restrained depending on how the rate of species loss covaries with the rate of interactions loss. 3. We find that the loss of species and interactions are decoupled, such that ecological interactions are often lost at a higher rate. This implies that the loss of ecological interactions may occur well before species disappearance, affecting species functionality and ecosystems services at a faster rate than species extinctions. We provide a number of empirical case studies illustrating these points. 4. Our approach emphasizes the importance of focusing on species interactions as the major biodiversity component from which the ‘health’ of ecosystems depends.

A meta-analysis of the effect of gut treatment on seed germination.

The dispersal of seeds by vertebrate frugivores is a process that usually implies the consumption of fruit pulp and the regurgitation or defecation of viable seeds (Ridley, 1930). An important advantage of seed ingestion by frugivores is a presumed increase in germination percentage (germinability) and rate (speed) (Krefting and Roe, 1949; van der Pijl, 1982). Recent analyses show, however, that such enhancement is far from universal and that several variables intrinsic to the plant or to the frugivore can influence the response of seeds to gut treatment (Traveset, 1998). Three mechanisms determine how frugivores can directly affect seed germination: (i) possible mechanical and/or chemical scarification of the seed-coat, which may depend upon gut retention time and on the type of food ingested with seeds (e.g. Agami and Waisel, 1988; Barnea et al., 1990, 1991; Izhaki and Safriel, 1990; Yagihashi et al., 1998); (ii) separation of seeds from pulp because germination is reduced or precluded if seeds remain associated with pulp (e.g. Rick and Bowman, 1961; Temple, 1977; Izhaki and Safriel, 1990; Barnea et al., 1991; Engel, 2000; Traveset et al., 2001); and (iii) the effect that results from faecal material surrounding the seeds, which may influence germination and/or future seedling growth. For example, seedlings emerging from ingested seeds tend to be more vigorous than those emerging from uningested ones because remaining faecal material fertilizes the seedlings, especially in the case of large-mammalian faeces, which often take a long time to decompose (e.g. Dinerstein and Wemmer, 1988; Quinn et al., 1994; Ocumpaugh et al., 1996; Paulsen, 1998; Traveset et al., 2001; T.R. Paulsen, unpublished). The importance of the first mechanism – the modification of seed-coat traits (e.g. permeability of the coat to water and gases) after gut treatment, which changes the capacity of germination and/or the speed at which seeds germinate – is the focus of this study. A review of this effect has recently been published (Traveset, 1998). In this review, Traveset analysed the results of studies on nearly 200 plant species in 68 families, using a slight variation of the ‘vote-counting’ method (Light and Pillemer, 1971; Hedges and Olkin, 1980). This method is conservative and has the advantage of being simple, but it has the disadvantage of

Meta-Analysis of the Effects of Human Disturbance on Seed Dispersal by Animals

Animal-mediated seed dispersal is important for sustaining biological diversity in forest ecosystems, particularly in the tropics. Forest fragmentation, hunting, and selective logging modify forests in myriad ways and their effects on animal-mediated seed dispersal have been examined in many case studies. However, the overall effects of different types of human disturbance on animal-mediated seed dispersal are still unknown. We identified 35 articles that provided 83 comparisons of animal-mediated seed dispersal between disturbed and undisturbed forests; all comparisons except one were conducted in tropical or subtropical ecosystems. We assessed the effects of forest fragmentation, hunting, and selective logging on seed dispersal of fleshy-fruited tree species. We carried out a meta-analysis to test whether forest fragmentation, hunting, and selective logging affected 3 components of animal-mediated seed dispersal: frugivore visitation rate, number of seeds removed, and distance of seed dispersal. Forest fragmentation, hunting, and selective logging did not affect visitation rate and were marginally associated with a reduction in seed-dispersal distance. Hunting and selective logging, but not fragmentation, were associated with a large reduction in the number of seeds removed. Fewer seeds of large-seeded than of small-seeded tree species were removed in hunted or selectively logged forests. A plausible explanation for the consistently negative effects of hunting and selective logging on large-seeded plant species is that large frugivores, as the predominant seed dispersers for large-seeded plant species, are the first animals to be extirpated from hunted or logged forests. The reduction in forest area after fragmentation appeared to have weaker effects on frugivore communities and animal-mediated seed dispersal than hunting and selective logging. The differential effects of hunting and selective logging on large- and small-seeded tree species underpinned case studies that showed disrupted plant-frugivore interactions could trigger a homogenization of seed traits in tree communities in hunted or logged tropical forests.

A review on the role of endozoochory in seed germination.

A large fraction of living plants produce fruits that attract animals (64% and 27% of gymnosperm and angiosperm lineages, respectively; Herrera and Pellmyr, 2002). In consuming them, animals can spread the seeds to more or less distant sites from the parent plant, thus contributing to plant regeneration and colonization of new sites (Willson and Traveset, 2000, and references therein). For millions of years both the pulp and seeds of fruit have been subjected to selective pressures exerted by frugivores and granivores. Fruit consumers, specifically, may show preferences for fruit traits such as size, shape, chemical composition and others, and have specific morphologies and physiologies of the digestive tract that affect the survival probability of the ingested seeds in different ways (Herrera and Pellmyr, 2002, and references therein). Seed traits are under further selective pressures imposed by a number of biotic (antagonistic fungi, insects and microbes; Cipollini and Levey, 1997) and abiotic factors (e.g. light, temperature, rainfall; Holl, 1999; Leishman et al., 2000) that influence the dormancy period, germination time and/or future seedling growth, which can ultimately determine germination and seedling success (Verdú and Traveset, 2005, and references therein). Therefore, the specific seed traits in an endozoochorous plant are a result of the combined selection imposed by frugivores, granivores and other biotic and abiotic factors. In this chapter, we evaluate the role of endozoochory on seed germination. We review the information gathered on germination patterns in experiments aimed at examining the effect of a seed’s passage through a frugivore’s gut, and give further directions on methods for future studies. Fruit treatment in the disperser’s digestive tract (which includes pulp separation from seeds and treatment of the seeds) can determine the capacity of seeds to germinate and, thus, is one of the components of

Effect of birds and bears on seed germination of fleshy-fruited plants in temperate rainforests of southeast Alaska

The effects of avian and mammal seed dispersers on seed germination were investigated for six common plant species (five shrubs and one herb) in the temperate rainforests of southeast Alaska. Patterns of germination behaviour were compared between defecated seeds and control (unpassed) seeds for a period of two years. Seed passage through vertebrate frugivores enhanced germination in two species, Rubus spectabilis and Sambucus racemosa, and a similar trend was observed in Ribes bracteosum. In contrast, it did not affect seed germination in Oplopanax horridus, Streptopus amplexifolius and Vaccinium ovalifolium/alaskaense. No differences in germination behaviour were found between bear- and bird-treated seeds, suggesting that seed retention time (much greater in bears than in birds) in the guts does not relevantly affect germination. Differences among frugivore effects were detected only for Sambucus, with varied thrushes enhancing germination more than American robins and black bears. The two colour morphs of Rubus spectabilis showed similar germination patterns, suggesting that seed dispersers do not exert an important selective pressure contributing to the maintenance of the polymorphism, at least through the mechanism of a differential effect on germination. The results of this study support the idea that the advantages of animal seed dispersal lie more in seed movement away from the parent plant than in seed treatment within the dispersers guts.

Impact of alien plant invaders on pollination networks in two archipelagos.

Mutualistic interactions between plants and animals promote integration of invasive species into native communities. In turn, the integrated invaders may alter existing patterns of mutualistic interactions. Here we simultaneously map in detail effects of invaders on parameters describing the topology of both plant-pollinator (bi-modal) and plant-plant (uni-modal) networks. We focus on the invader Opuntia spp., a cosmopolitan alien cactus. We compare two island systems: Tenerife (Canary Islands) and Menorca (Balearic Islands). Opuntia was found to modify the number of links between plants and pollinators, and was integrated into the new communities via the most generalist pollinators, but did not affect the general network pattern. The plant uni-modal networks showed disassortative linkage, i.e. species with many links tended to connect to species with few links. Thus, by linking to generalist natives, Opuntia remained peripheral to network topology, and this is probably why native network properties were not affected at least in one of the islands. We conclude that the network analytical approach is indeed a valuable tool to evaluate the effect of invaders on native communities.