What drives seed dispersal effectiveness?

Seed dispersal is a critical phase in plant reproduction and forest regeneration. In many systems, the vast majority of woody species rely on seed dispersal by fruit-eating animals. Animals differ in their size, movement patterns, seed handling, gut physiology, and many other factors that affect the number of seeds they disperse, the quality of treatment each individual seed receives, and consequently their relative contribution to plant fitness. The seed dispersal effectiveness framework (SDE) was developed to allow systematic and standardized quantification of these processes, offering a potential for understanding the large-scale dynamics of animal-plant interactions and the ecological and evolutionary consequences of animal behavior for plant reproductive success. Yet, despite its wide acceptance, the SDE framework has primarily been employed descriptively, almost always in the context of local systems. As such, the drivers of variation in SDE across systems and the relationship between its components remain unknown. We systematically searched studies that quantified endozoochorous SDE for multiple animal species dispersing one or more plant species in a given system and offered an integrative examination of the factors driving variation in SDE. Specifically, we addressed three main questions: (a) Is there a tradeoff between high dispersal quality and quantity? (b) Does animal body mass affect SDE or its main components? and (c) What drives more variation in SDE, seed dispersal quality, or quantity? We found that: (a) the relationship between quality and quantity is mediated by body size; (b) this is the result of differential relationships between body mass and the two components, while total SDE is unaffected by body mass; (c)neither quality nor quantity explain more variance in SDE globally. Our results also highlight the need for more standardized data to assess large-scale patterns in SDE.

The ecological and evolutionary significance of effectiveness landscapes in mutualistic interactions.

Mutualism effectiveness, the contribution of an interacting organism to its partner's fitness, is defined as the number of immediate outcomes of the interactions (quantity component) multiplied by the probability that an immediate outcome results in a new individual (quality component). These components form a two-dimensional effectiveness landscape with each species' location determined by its values of quantity (x-axis) and quality (y-axis). We propose that the evolutionary history of mutualistic interactions leaves a footprint that can be identified by three properties of the spatial structure of effectiveness values: dispersion of effectiveness values, relative contribution of each component to the effectiveness values and correlation between effectiveness components. We illustrate this approach using a large dataset on synzoochory, seed dispersal by seed-caching animals. The synzoochory landscape was clumped, with effectiveness determined primarily by the quality component, and with quantity and quality positively correlated. We suggest this type of landscape structure is common in generalised coevolved mutualisms, where multiple functionally equivalent, high-quality partners exert similarly strong selection. Presumably, only those organisms located in high-quality regions will impact the evolution of their partner. Exploring properties of effectiveness landscapes in other mutualisms will provide new insight into the evolutionary and ecological consequences of mutualisms.

Advancing an interdisciplinary framework to study seed dispersal ecology.

Although dispersal is generally viewed as a crucial determinant for the fitness of any organism, our understanding of its role in the persistence and spread of plant populations remains incomplete. Generalizing and predicting dispersal processes are challenging due to context dependence of seed dispersal, environmental heterogeneity and interdependent processes occurring over multiple spatial and temporal scales. Current population models often use simple phenomenological descriptions of dispersal processes, limiting their ability to examine the role of population persistence and spread, especially under global change. To move seed dispersal ecology forward, we need to evaluate the impact of any single seed dispersal event within the full spatial and temporal context of a plant's life history and environmental variability that ultimately influences a population's ability to persist and spread. In this perspective, we provide guidance on integrating empirical and theoretical approaches that account for the context dependency of seed dispersal to improve our ability to generalize and predict the consequences of dispersal, and its anthropogenic alteration, across systems. We synthesize suitable theoretical frameworks for this work and discuss concepts, approaches and available data from diverse subdisciplines to help operationalize concepts, highlight recent breakthroughs across research areas and discuss ongoing challenges and open questions. We address knowledge gaps in the movement ecology of seeds and the integration of dispersal and demography that could benefit from such a synthesis. With an interdisciplinary perspective, we will be able to better understand how global change will impact seed dispersal processes, and potential cascading effects on plant population persistence, spread and biodiversity.

Intrinsic and extrinsic drivers of intraspecific variation in seed dispersal are diverse and pervasive.

There is growing realization that intraspecific variation in seed dispersal can have important ecological and evolutionary consequences. However, we do not have a good understanding of the drivers or causes of intraspecific variation in dispersal, how strong an effect these drivers have, and how widespread they are across dispersal modes. As a first step to developing a better understanding, we present a broad, but not exhaustive, review of what is known about the drivers of intraspecific variation in seed dispersal, and what remains uncertain. We start by decomposing 'drivers of intraspecific variation in seed dispersal' into intrinsic drivers (i.e. variation in traits of individual plants) and extrinsic drivers (i.e. variation in ecological context). For intrinsic traits, we further decompose intraspecific variation into variation among individuals and variation of trait values within individuals. We then review our understanding of the major intrinsic and extrinsic drivers of intraspecific variation in seed dispersal, with an emphasis on variation among individuals. Crop size is the best-supported and best-understood intrinsic driver of variation across dispersal modes; overall, more seeds are dispersed as more seeds are produced, even in cases where per seed dispersal rates decline. Fruit/seed size is the second most widely studied intrinsic driver, and is also relevant to a broad range of seed dispersal modes. Remaining intrinsic drivers are poorly understood, and range from effects that are probably widespread, such as plant height, to drivers that are most likely sporadic, such as fruit or seed colour polymorphism. Primary extrinsic drivers of variation in seed dispersal include local environmental conditions and habitat structure. Finally, we present a selection of outstanding questions as a starting point to advance our understanding of individual variation in seed dispersal.

The total dispersal kernel: a review and future directions.

The distribution and abundance of plants across the world depends in part on their ability to move, which is commonly characterized by a dispersal kernel. For seeds, the total dispersal kernel (TDK) describes the combined influence of all primary, secondary and higher-order dispersal vectors on the overall dispersal kernel for a plant individual, population, species or community. Understanding the role of each vector within the TDK, and their combined influence on the TDK, is critically important for being able to predict plant responses to a changing biotic or abiotic environment. In addition, fully characterizing the TDK by including all vectors may affect predictions of population spread. Here, we review existing research on the TDK and discuss advances in empirical, conceptual modelling and statistical approaches that will facilitate broader application. The concept is simple, but few examples of well-characterized TDKs exist. We find that significant empirical challenges exist, as many studies do not account for all dispersal vectors (e.g. gravity, higher-order dispersal vectors), inadequately measure or estimate long-distance dispersal resulting from multiple vectors and/or neglect spatial heterogeneity and context dependence. Existing mathematical and conceptual modelling approaches and statistical methods allow fitting individual dispersal kernels and combining them to form a TDK; these will perform best if robust prior information is available. We recommend a modelling cycle to parameterize TDKs, where empirical data inform models, which in turn inform additional data collection. Finally, we recommend that the TDK concept be extended to account for not only where seeds land, but also how that location affects the likelihood of establishing and producing a reproductive adult, i.e. the total effective dispersal kernel.

Consequences of intraspecific variation in seed dispersal for plant demography, communities, evolution and global change.

As the single opportunity for plants to move, seed dispersal has an important impact on plant fitness, species distributions and patterns of biodiversity. However, models that predict dynamics such as risk of extinction, range shifts and biodiversity loss tend to rely on the mean value of parameters and rarely incorporate realistic dispersal mechanisms. By focusing on the mean population value, variation among individuals or variability caused by complex spatial and temporal dynamics is ignored. This calls for increased efforts to understand individual variation in dispersal and integrate it more explicitly into population and community models involving dispersal. However, the sources, magnitude and outcomes of intraspecific variation in dispersal are poorly characterized, limiting our understanding of the role of dispersal in mediating the dynamics of communities and their response to global change. In this manuscript, we synthesize recent research that examines the sources of individual variation in dispersal and emphasize its implications for plant fitness, populations and communities. We argue that this intraspecific variation in seed dispersal does not simply add noise to systems, but, in fact, alters dispersal processes and patterns with consequences for demography, communities, evolution and response to anthropogenic changes. We conclude with recommendations for moving this field of research forward.

Rapid changes in seed dispersal traits may modify plant responses to global change.

When climatic or environmental conditions change, plant populations must either adapt to these new conditions, or track their niche via seed dispersal. Adaptation of plants to different abiotic environments has mostly been discussed with respect to physiological and demographic parameters that allow local persistence. However, rapid modifications in response to changing environmental conditions can also affect seed dispersal, both via plant traits and via their dispersal agents. Studying such changes empirically is challenging, due to the high variability in dispersal success, resulting from environmental heterogeneity, and substantial phenotypic variability of dispersal-related traits of seeds and their dispersers. The exact mechanisms that drive rapid changes are often not well understood, but the ecological implications of these processes are essential determinants of dispersal success, and deserve more attention from ecologists, especially in the context of adaptation to global change. We outline the evidence for rapid changes in seed dispersal traits by discussing variability due to plasticity or genetics broadly, and describe the specific traits and biological systems in which variability in dispersal is being studied, before discussing some of the potential underlying mechanisms. We then address future research needs and propose a simulation model that incorporates phenotypic plasticity in seed dispersal. We close with a call to action and encourage ecologists and biologist to embrace the challenge of better understanding rapid changes in seed dispersal and their consequences for the reaction of plant populations to global change.

Synzoochory: the ecological and evolutionary relevance of a dual interaction.

Synzoochory is the dispersal of seeds by seed-caching animals. The animal partner in this interaction plays a dual role, acting both as seed disperser and seed predator. We propose that this duality gives to synzoochory two distinctive features that have crucial ecological and evolutionary consequences. First, because plants attract animals that have not only positive (seed dispersal) but also negative (seed predation) impacts on their fitness, the evolution of adaptations to synzoochory is strongly constrained. Consequently, it is not easy to identify traits that define a synzoochorous dispersal syndrome. The absence of clear adaptations entails the extra difficulty of identifying synzoochorous plants by relying on dispersal traits, limiting our ability to explore the full geographic, taxonomic and phylogenetic extent of synzoochory. Second, the positive and negative outcomes of interactions with synzoochorous animals are expressed simultaneously. Consequently, synzoochorous interactions are not exclusively mutualistic or antagonistic, but are located at some point along a mutualism-antagonism continuum. What makes synzoochory interesting and unique is that the position of each partner along the continuum can be evaluated for every plant-animal interaction, and thus the continuum can be precisely described by assessing the relative frequency of positive and negative interaction events in each pairwise interaction. Herein we explore these two main features of synzoochory with a comprehensive quantitative survey of published studies on synzoochory. Synzoochory has been recorded for at least 1339 plant species differing in life forms, from annual and short-lived herbs to long-lived trees, belonging to 641 genera and 157 families widely distributed across the globe and across the seed plant phylogeny. Over 30 animal families belonging to five disparate taxonomic groups (rodents, marsupials, birds, insects, and land crabs) potentially act as synzoochorous dispersers. Although synzoochory appears to be fundamentally a secondary dispersal mode, many abundant and dominant trees are primarily synzoochorous. In addition, we found evidence of the existence of diplosynzoochory (caching animals acting both as primary and secondary dispersers of the same individual seed), mostly in nut-bearing trees. Finally, we found that synzoochorous interactions are widely spread across the mutualism-antagonism continuum. Nevertheless, there were some differences among disperser species and functional groups. Corvids and some rodents (cricetids, nesomyids, sciurids) were located in the positive-effects region of the continuum and presumably behave mostly as dispersers, whereas land crabs and insects were located in the negative-effects extreme and behave mostly as seed predators. Our review demonstrates that synzoochory is not an anecdotal ecological interaction. Rather, it is pivotal to the functioning of many ecosystems where the natural regeneration of keystone plant species depends on the activity of granivorous animals that play a dual role. This distinctive interaction should not be ignored if we wish to have an accurate understanding of the functioning of natural systems.

A general framework for effectiveness concepts in mutualisms.

A core interest in studies of mutualistic interactions is the 'effectiveness' of mutualists in providing benefits to their partners. In plant-animal mutualisms it is widely accepted that the total effect of a mutualist on its partner is estimated as (1) a 'quantity' component multiplied by (2) a 'quality' component, although the meanings of 'effectiveness,' 'quantity,' and 'quality' and which terms are applied to these metrics vary greatly across studies. In addition, a similar quantity × quality = total effect approach has not been applied to other types of mutualisms, although it could be informative. Lastly, when a total effect approach has been applied, it has invariably been from a phytocentric perspective, focussing on the effects of animal mutualists on their plant partner. This lack of a common framework of 'effectiveness' of mutualistic interactions limits generalisation and the development of a broader understanding of the ecology and evolution of mutualisms. In this paper, we propose a general framework and demonstrate its utility by applying it to both partners in five different types of mutualisms: pollination, seed dispersal, plant protection, rhizobial, and mycorrhizal mutualisms. We then briefly discuss the flexibility of the framework, potential limitations, and relationship to other approaches.

Effects of community- and neighborhood-scale spatial patterns on semi-arid perennial grassland community dynamics.

Although plant spatial patterns strongly influence community-structuring processes, few empirical studies have addressed pattern effects on perennial community dynamics. We tested the effects of community- and neighborhood-scale patterns in experimental semi-arid grassland communities comprising the stronger competitor crested wheatgrass (Agropyron cristatum) and the weaker competitor Snake River wheatgrass (Elymus wawawaiensis). Treatments consisted of community-scale patterns (Poisson random, regular, and aggregated) and neighborhood-scale patterns (Poisson random, small, and large aggregations) applied to 6.25-m(2) plots, with aggregations generated through simulated realizations of Neyman-Scott cluster processes. Two years of data were collected on aboveground biomass of both species, and variability in light (photosynthetically active radiation; PAR) was also quantified. We found that plant performance was strongly affected by community-scale spatial patterns and time, with additional effects of neighborhood-scale pattern in certain treatments. Mean biomass and relative growth rates of both species were highest in plots with community-scale regularity and random neighborhoods, suggesting a strong effect of pattern on competition that was magnified for the weaker competitor E. wawawaiensis, especially in the second year. There were also significant effects of treatment and time on variability of PAR, supporting past research on the importance of canopy patterns for light distribution near the soil surface. We observed more variable light environments in plots with community-scale aggregation, and variability also increased in the second year. Our research provides new information on the effects of plant patterns on community dynamics, with particular relevance for semi-arid perennial grasslands.

The full path of Janzen-Connell effects: genetic tracking of seeds to adult plant recruitment.

The Janzen-Connell (J-C) model (Janzen 1970; Connell 1971) has been a dominant yet controversial paradigm for forest community dynamics for four decades, especially in the tropics. With increasing distance from the parent plant, the density of dispersed seeds decreases and, because of a reduced impact of distance- and density-responsive seed and seedling enemies, propagule survival increases, resulting in peak recruitment at some distance from the parent and little recruitment near adult conspecifics. This spacing generates gaps near adult trees for the recruitment of heterospecifics, enhancing species coexistence and species richness. Field studies, primarily focused on seeds and young seedlings, have repeatedly demonstrated increasing survival with increasing distance from parents or decreasing density of propagules (e.g. Clark & Clark 1984; Gilbert et al. 1994; Swamy & Terborgh 2010). Yet a meta-analysis of distance-dependent propagule survival failed to support a general pattern of survival increasing with distance from adult conspecifics, suggesting that there is no need for further experimental tests of the J-C hypothesis in terms of diversity enhancement-results are species-specific, not general (Hyatt et al. 2003). However, a lack of consistent experimental results is not surprising. The outcome of tests of the hypothesis can vary as a function of many factors that can affect successive recruitment stages differently (Schupp 1992; Hyatt et al. 2003; Swamy & Terborgh 2010). This highlights a critical gap-a full test of the J-C model requires data demonstrating that effects carry over to recruitment of new reproductive adults, yet few studies have gone beyond early stages. There is strong inferential evidence that adult trees can show the imprint of J-C effects (e.g. Nathan et al. 2000; Howe & Miriti 2004), and focal individual modelling has clearly demonstrated that J-C effects can operate from sapling through adult stages in a significant number of species (Peters 2003). It is likely that such results are not unusual, but there have been few attempts to demonstrate J-C spacing at the adult stage. In this issue of Molecular Ecology, Steinitz et al. (2011) studied the Mediterranean pine Pinus halepensis (Aleppo pine) and combined a unique situation with an innovative approach to provide the most elegant demonstration yet that adult recruits are spaced further from parents than expected from the initial seed distribution, clear evidence of a J-C effect carrying over to reproductive adults. A major advancement of this study is that it incorporates estimates of the initial patterns of seed dispersal and parentage analysis of adult-offspring relationships, illustrating the value of combined field and genetic approaches.

Seed dispersal effectiveness revisited: a conceptual review.

Growth in seed dispersal studies has been fast-paced since the seed disperser effectiveness (SDE) framework was developed 17 yr ago. Thus, the time is ripe to revisit the framework in light of accumulated new insight. Here, we first present an overview of the framework, how it has been applied, and what we know and do not know. We then introduce the SDE landscape as the two-dimensional representation of the possible combinations of the quantity and the quality of dispersal and with elevational contours representing isoclines of SDE. We discuss the structure of disperser assemblages on such landscapes. Following this we discuss recent advances and ideas in seed dispersal in the context of their impacts on SDE. Finally, we highlight a number of emerging issues that provide insight into SDE. Overall, the SDE framework successfully captures the complexities of seed dispersal. We advocate an expanded use of the term dispersal encompassing the multiple recruitment stages from fruit to adult. While this entails difficulties in estimating SDE, it is a necessary expansion if we are to understand the central relevance of seed dispersal in plant ecology and evolution.

Effectiveness of rodents as local seed dispersers of Holm oaks.

In this study we assessed the effectiveness of rodents as dispersers of Quercus ilex in a patchy landscape in southeastern Spain. We experimentally followed the fates of 3,200 marked and weighed acorns from dispersal through the time of seedling emergence over three years. Rodents handled about 99% of acorns, and dispersed 67% and cached 7.4% of the dispersed acorns. Most caches were recovered and consumed, and only 1.3% of the original experimental acorns were found alive in caches the following spring. Dispersal distances were short (mean = 356.2 cm, median = 157 cm) and strongly right-skewed. Heavier acorns were dispersed further and were more likely to be cached and survive than lighter acorns. All caches were in litter or soil, and each contained a single acorn. Rodents moved acorns nonrandomly, mostly to oaks and pines. Most surviving acorns were either in oaks, a poor microhabitat for oak recruitment, or shrubs, a suitable microhabitat for oak recruitment. Our results suggest that rodents, by burying a relatively high proportion of acorns singly in shrubs and pines, act as moderately effective dispersers of Q. ilex. Nonetheless, this dispersal comes at a very heavy cost.

Positive and negative interactions between environmental conditions affecting Cercocarpus ledifolius seedling survival.

We evaluated the balance between positive and negative effects of environmental conditions on first-year seedling survival of the tree Cercocarpus ledifolius during two summers, 1996 and 1997. The experimental design was fully crossed with two levels of water, with and without supplementation, two levels of herbivory, with and without protection, and three major microhabitats, open interspaces, under the canopy of Artemisia tridentata shrubs, and under the canopy of mature C. ledifolius trees. Effects of drought and herbivory on seedling survival depended on the year. Water supplementation and herbivory protection during the dry summer of 1996 (27.7 mm) generally increased seedling survival. Additionally, survival tended to be greatest beneath C. ledifolius canopies. More important ecologically were the significant interactions. In 1996, water supplementation increased survival more with than without herbivory protection. The three-way interaction, treatment-microhabitat combination, was most important; by far the greatest survival was in the water supplementation and herbivory protection in the tree microhabitat. During the wet summer of 1997 (158.5 mm), neither water supplementation, herbivory protection, nor microhabitat were significant as main effects. The water-supplemented and herbivory-protected treatment again combined to yield highest survival, but this time in open interspaces rather than beneath trees. Our study shows how the importance of individual limiting factors and the relative favorableness of particular microhabitats appear to change across years depending on environmental conditions.

Effect of treefall gaps on the patchiness and species richness of Neotropical ant assemblages.

Natural formation of treefall gaps plays an integral role in the ecological and evolutionary dynamics of many tropical forests, affecting the spatiotemporal distribution of plants and the animals that interact with them. This study examines the impact of treefall gaps on the spatial and temporal patchiness of ant assemblages in a moist lowland forest in Panama. Using pitfall traps and honey baits, we compared ant assemblages in five 1 to 2-year-old treefall gaps (ca 100 m2) and five adjacent plots (ca 100 m2) in undisturbed forest understory at three different times of year (late wet season, late dry season, and early wet season). We found little evidence that ant assemblages respond dramatically to the formation of treefall gaps and the differences in habitat qualities they produce. Ant abundance, species richness, species composition, and rates of resource discovery did not differ between gaps and forest understory. However, we did find significant differences in numerical abundance related to forest stratum (ground vs vegetation) and resource type in pitfall traps (oil-cockroach vs honey), and significant differences in ant species richness and rates of resource discovery across seasons. While habitat effects by themselves were never statistically significant, habitat and seasonal differences in species richness interacted significantly to produce complex, season-dependent differences among gap and forest habitats. These results suggest that the formation of natural treefall gaps has less of an effect on Neotropical ant assemblages compared to other groups of organisms (e.g., plants, birds) or other causes of patchiness (e.g., ant mosaics, moisture availability, army ant predation). The results of our study also have important implications for the underlying causes of habitat differences in the distribution of ant-defended plants.

Factors affecting post-dispersal seed survival in a tropical forest.

Using the subcanopy tree Faramea occidentalis in Panama, I studied post-dispersal seed survival as a function of five characteristics describing seed locations. By simultaneously considering distance from a conspecific adult, size of the nearest conspecific adult, leaf litter quantity, proximity to logs or tree trunks, and whether or not the seed was in a gap, I was able to analyze the influences of individual factors, as well as the interactions among factors. Seed survival was significantly less in treefall gaps than in the forest understory. Seed survival was also influenced by the size of the nearest adult but in a complex interaction with distance to an adult. For seeds beneath adults, survival decreased with increasing tree size, while for seeds away from adults, survival was independent of the size of the nearest conspecific adult. Distance did not directly affect seed survival, nor did the quantity of leaf litter or the proximity to a tree trunk or a log. In a separate analysis, the relationship between distance and seed survival was consistent over four years, suggesting that single cohort studies may provide accurate insights into the consequences of dispersal. In contrast, the spatial locations of surviving seeds were not consistent over the four-year period. Transects with high survival one year did not tend to have high survival in other years, and the locations of surviving seeds in any particular year could not be predicted from the knowledge of where seeds survived in other years. While survival is patchy within a year, the locations of patches shift from year to year.

Azteca protection of Cecropia: ant occupation benefits juvenile trees.

In this 15 month investigation I experimentally demonstrated that sapling Cecropia aff. obtusifolia in lowland western Ecuador grow more vigorously when occupied by the ant Azteca constructor than when the ants have been removed. Thus the interaction is directly beneficial to Cecropia juveniles. The difference in growth is associated with differences in herbivory and vine cover. Removal of ants significantly increases nocturnal Coleoptera herbivory on unoccupied plants. In contrast to the influence on beetle numbers, Azteca are ineffective against Homoptera and cecidomyiid gall flies. Although ant-occupied saplings had less chewing herbivore damage throughout the study, the ants were more effective protectors in the dry season than in the rainy season, when herbivore pressure increased. In addition to reducing herbivory, Azteca efficiently remove vines from occupied saplings.