Personality-dependent dispersal: characterization, ontogeny and consequences for spatially structured populations

Dispersal is one of the most fundamental components of ecology, and affects processes as diverse as population growth, metapopulation dynamics, gene flow and adaptation. Although the act of moving from one habitat to another entails major costs to the disperser, empirical and theoretical studies suggest that these costs can be reduced by having morphological, physiological or behavioural specializations for dispersal. A few recent studies on different systems showed that individuals exhibit personality-dependent dispersal, meaning that dispersal tendency is associated with boldness, sociability or aggressiveness. Indeed, in several species, dispersers not only develop behavioural differences at the onset of dispersal, but display these behavioural characteristics through their life cycle. While personality-dependent dispersal has been demonstrated in only a few species, we believe that it is a widespread phenomenon with important ecological consequences. Here, we review the evidence for behavioural differences between dispersers and residents, to what extent they constitute personalities. We also examine how a link between personality traits and dispersal behaviours can be produced and how personality-dependent dispersal affects the dynamics of metapopulations and biological invasions. Finally, we suggest future research directions for population biologists, behavioural ecologists and conservation biologists such as how the direction and the strength of the relationship between personality traits and dispersal vary with ecological contexts.     

The interactive effects of competition and predation risk on dispersal in an insect

Dispersal dynamics have significant consequences for ecological and evolutionary processes. Previous work has demonstrated that dispersal can be context-dependent. However, factors affecting dispersal are typically considered in isolation, despite the probability that individuals make dispersal decisions in response to multiple, possibly interacting factors. We examined whether two ecological factors, predation risk and intraspecific competition, have interactive effects on dispersal dynamics. We performed a factorial experiment in mesocosms using backswimmers (Notonecta undulata), flight-capable, semi-aquatic insects. Emigration rates increased with density, and increased with predation risk at intermediate densities; however, predation had minimal effects on emigration at high and low densities. Our results indicate that factorial experiments may be required to understand dispersal dynamics under realistic ecological conditions.     

Personality-dependent dispersal in the invasive mosquitofish: group composition matters

Understanding/predicting ecological invasions is an important challenge in modern ecology because of their immense economical and ecological costs. Recent studies have revealed that within-species variation in behaviour (i.e. animal personality) can shed light on the invasion process. The general hypothesis is that individuals' personality type may affect their colonization success, suggesting that some individuals might be better invaders than others. We have recently shown that, in the invasive mosquitofish (Gambusia affinis), social personality trait was an important indicator of dispersal distance, with more asocial individuals dispersing further. Here, we tested how mean personality within a population, in addition to individual personality type, affect dispersal and settlement decisions in the mosquitofish. We found that individual dispersal tendencies were influenced by the population's mean boldness and sociability score. For example, individuals from populations with more asocial individuals or with more bold individuals are more likely to disperse regardless of their own personality type. We suggest that identifying behavioural traits facilitating invasions, even at the group level, can thus have direct applications in pest management.     

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.     

Differences in Attack Avoidance and Mating Success between Strains Artificially Selected for Dispersal Distance in Tribolium castaneum

Individuals of both dispersal and non-dispersal types (disperser and non-disperser) are found in a population, suggesting that each type has both costs and benefits for fitness. However, few studies have examined the trade-off between the costs and benefits for the types. Here, we artificially selected for walking distance, i.e., an indicator of dispersal ability, in the red flour beetle Tribolium castaneum and established strains with longer (L-strains) or shorter (S-strains) walking distances. We then compared the frequency of predation by the assassin bug Amphibolus venator and the mating frequency of the selected strains. L-strain beetles suffered higher predation risk, than did S-strain beetles. L-strain males had significantly increased mating success compared to S-strain males, but females did not show a significant difference between the strains. The current results showed the existence of a trade-off between predation avoidance and mating success associated with dispersal types at a genetic level only in males. This finding can help to explain the maintenance of variation in dispersal ability within a population.     

Should dispersers be fast learners? Modeling the role of cognition in dispersal syndromes

Both cognitive abilities and dispersal tendencies can vary strongly between individuals. Since cognitive abilities may help dealing with unknown circumstances, it is conceivable that dispersers may rely more heavily on learning abilities than residents. However, cognitive abilities are costly and leaving a familiar place might result in losing the advantage of having learned to deal with local conditions. Thus, individuals which invested in learning to cope with local conditions may be better off staying at their natal place. In order to disentangle the complex relationship between dispersal and learning abilities, we implemented individual‐based simulations. By allowing for developmental plasticity, individuals could either become a ''resident'' or ''dispersal'' cognitive phenotype. The model showed that in general residents have higher learning abilities than dispersers. Dispersers evolve higher learning ability than residents when dispersers have long life spans and when dispersal occurs either early or late in life, thereby maximizing the time in one habitat patch. Time is crucial here, because the longer an individual resides in a location where it can use its learned knowledge or behavior, the more often it profits from it and thus eventually obtains a net benefit from its investment into learning. Both, longevity and the timing of dispersal within lifecycles determine the time individuals have to recoup that investment and thus crucially influence this correlation. We therefore suggest that species'' life history will strongly impact the expected cognitive abilities of dispersers, relative to their resident conspecifics, and that cognitive abilities might be an integral part of dispersal syndromes.     

Sizing up your enemy: individual predation vulnerability predicts migratory probability

Partial migration, in which a fraction of a population migrate and the rest remain resident, occurs in an extensive range of species and can have powerful ecological consequences. The question of what drives differences in individual migratory tendency is a contentious one. It has been shown that the timing of partial migration is based upon a trade-off between seasonal fluctuations in predation risk and growth potential. Phenotypic variation in either individual predation risk or growth potential should thus mediate the strength of the trade-off and ultimately predict patterns of partial migration at the individual level (i.e. which individuals migrate and which remain resident). We provide cross-population empirical support for the importance of one component of this model--individual predation risk--in predicting partial migration in wild populations of bream Abramis brama, a freshwater fish. Smaller, high-risk individuals migrate with a higher probability than larger, low-risk individuals, and we suggest that predation risk maintains size-dependent partial migration in this system.     

Impact of habitat structure and fruit abundance on avian seed dispersal and fruit predation

So far, it is poorly understood how differential responses of avian seed dispersers and fruit predators to changes in habitat structure and fruit abundance along land-use gradients may translate into consequences for the seed dispersal of associated plants. We selected a gradient of habitat modification (forest, semi-natural, and rural habitat) characterized by decreasing tree cover and a high variation in local fruit availability. Along this gradient we quantified fruit removal by avian seed dispersers and fruit predators from 18 Sorbus aucuparia trees. We analyzed the relative importance of tree cover and fruit abundance in explaining species richness, abundance and fruit removal rates of both guilds from S. aucuparia trees. Species richness and abundance of seed dispersers decreased with decreasing tree cover, whereas fruit removal by seed dispersers decreased with decreasing fruit abundance independent of tree cover. Both variables had no effect on species richness, abundance and fruit removal by fruit predators. Consequently, seed dispersers dominated relative fruit removal in fruit-rich sites but the dispersal/predation ratio shifted in favor of predation in fruit-poor habitat patches. Our study demonstrates that variation in local habitat structure and fruit abundance can cause guild-specific responses. Such responses may result in a shift in fruit removal regimes and might affect the dispersal ability of dependent fruiting plants. Future studies should aim at possible consequences for plant recruitment and guild-specific responses of frugivores to disturbance gradients on the level of entire plant–frugivore associations.     

Risky movements? Natal dispersal does not decrease survival of a large herbivore

Natal dispersal is assumed to be a particularly risky movement behavior as individuals transfer, often long distances, from birth site to site of potential first reproduction. Though, because this behavior persists in populations, it is assumed that dispersal increases the fitness of individuals despite the potential for increased risk of mortality. The extent of dispersal risk, however, has rarely been tested, especially for large mammals. Therefore, we aimed to test the relationship between dispersal and survival for both males and females in a large herbivore. Using a radio‐transmittered sample of 398 juvenile male and 276 juvenile female white‐tailed deer (Odocoileus virginianus), we compared survival rates of dispersers and nondispersers. We predicted that dispersing deer would experience greater overall mortality than philopatric deer due to direct transfer‐related risks (e.g., vehicular collision), indirect immigration‐related mortality attributable to colonization of unfamiliar habitat, and increased overwinter mortality associated with energetic costs of movement and unfamiliarity with recently colonized habitat. For both male and female yearlings, survival rates of dispersers (male = 49.9%, female = 64.0%) did not differ from nondispersers (male = 51.6%, female = 70.7%). Only two individuals (both female) were killed by vehicular collision during transfer, and overwinter survival patterns were similar between the two groups. Although dispersal movement likely incurs energetic costs on dispersers, these costs do not necessarily translate to decreased survival. In many species, including white‐tailed deer, dispersal is likely condition‐dependent, such that larger and healthier individuals are more likely to disperse; therefore, costs associated with dispersal are more likely to be borne successfully by those individuals that do disperse. Whether low‐risk dispersal of large mammals is the rule or the exception will require additional research. Further, future research is needed to evaluate nonsurvival fitness‐related costs and benefits of dispersal (e.g., increased reproductive opportunities for dispersers).     

Local predation risk and matrix permeability interact to shape movement strategy

In fragmented landscapes, the reduced connectivity among patches drives the evolution of movement strategies through an increase of transience costs. Reduced movements may further alter heterogeneity in biotic and abiotic conditions experienced by individuals. The joint action of local conditions and matrix permeability may shape emigration decisions. Here, we tested the interactive effects of predation risk and matrix permeability on movement propensity, movement costs and movers’ phenotype in the common toad Bufo bufo. In a full‐crossed experimental design, we assessed the movement propensity of juveniles in three connectivity treatments (from poorly to highly permeable matrix), with or without predation risk in their living patch. We also assessed the relationships between movement propensity and morphological traits (i.e. body and leg length) and how it affected the movement cost (i.e. mass loss). Movement propensity increased in presence of predation risk, while matrix permeability had no effect. However, matrix permeability interacted with predation risk to influence movers’ phenotype and the physiological cost they endured while moving. In particular, a well‐known movement syndrome in toads (i.e. movement propensity positively related to longer legs) depended on the interaction between matrix permeability and predation risk and resulted in differences in mass loss among matrix types. Movers lost more mass on average than residents except when they also displayed longer legs or when they crossed the most permeable matrix in the presence of predation risk. Our results show that matrix permeability shapes the physiological cost of dispersal by changing the identity of individuals moving away from local conditions. As the movers’ phenotype can importantly alter (meta)population dynamics, context‐dependency of dispersal syndromes should be considered in studies predicting the functioning of human‐altered natural systems.     

The Role of Mammals in Creating and Modifying Seedshadows in Tropical Forests and Some Possible Consequences of Their Elimination

Mammal populations are increasingly hunted, yet the consequences of their disappearance from tropical forests have only recently been explored. Here, we summarize current research on the role of mammals in seed dispersal and postdispersal processes, such as seed predation and secondary dispersal, in different tropical regions. We evaluate how mammal features influence seedshadows and ultimately forest regeneration. Finally, we discuss the potential effect of changes in seedshadows caused by the elimination of many medium- and large-sized mammals. The complex role that mammals play in creating and modifying seedshadows in tropical forests cannot be easily quantified, and in this review we emphasize the variation that exists both within and among mammal taxa and across continents. To bridge this gap in information, we suggest that more studies should evaluate the relative importance of the disappearance of both seed dispersers and seed predators for particular plant species so that we may begin to understand the balance between these two influences. We also suggest that future studies identify ecological redundancy in nonhunted vertebrates within any particular community to evaluate compensatory behavior that may help ameliorate some of the negative effects of hunting of large and medium mammals.     

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.     

Potential for ants and vertebrate predators to shape seed-dispersal dynamics of the invasive thistles <Emphasis Type="Italic">Cirsium arvense</Emphasis> and <Emphasis Type="Italic">Carduus nutans</Emphasis> in their introduced range (North America)

The population dynamics of invasive plants are influenced by positive and negative associations formed with members of the fauna present in the introduced range. For example, mutualistic associations formed with pollinators or seed dispersers may facilitate invasion, but reduced fitness from attack by native herbivores can also suppress it. Since population expansion depends on effective seed dispersal, interactions with seed dispersers and predators in a plant species introduced range may be of particular importance. We explored the relative contributions of potential seed dispersers (ants) and vertebrate predators (rodents and birds) to seed removal of two diplochorous (i.e., wind- and ant-dispersed), invasive thistles, Cirsium arvense and Carduus nutans, in Colorado, USA. We also conducted behavior trials to explore the potential of different ant species to disperse seeds, and we quantified which potential ant dispersers were prevalent at our study locations. Both ants and vertebrate predators removed significant amounts of C. arvense and C. nutans seed, with the relative proportion of seed removed by each guild varying by location. The behavior trials revealed clear seed preferences among three ant species as well as differences in the foragers’ abilities to move seeds. In addition, two ant species that acted as potential dispersal agents were dominant at the study locations. Since local conditions in part determined whether dispersers or predators removed more seed, it is possible that some thistle populations benefit from a net dispersal effect, while others suffer proportionally more predation. Additionally, because the effectiveness of potential ant dispersers is taxon-specific, changes in ant community composition could affect the seed-dispersal dynamics of these thistles. Until now, most studies describing dispersal dynamics in C. arvense and C. nutans have focused on primary dispersal by wind or pre-dispersal seed predation by insects. Our findings suggest that animal-mediated dispersal and post-dispersal seed predation deserve further consideration.     

Social personalities influence natal dispersal in a lizard

Animal personalities are common across taxa and have important evolutionary and ecological implications. Such consistent individual differences correlate with important life-history traits such as dispersal. Indeed, some environmental conditions are supposed to determine dispersers with a specific personality. For example, an increased density should promote the departure of individuals with less social tolerance. Therefore, we hypothesized that dispersers from high-density populations should primarily be asocial individuals, whereas dispersers from low-density populations should be social individuals. In the common lizard (Lacerta vivipara), we measured attraction towards the odour of conspecifics on juveniles at birth as a metric of social tolerance. We then released these juveniles into populations of different densities and measured dispersal and settlement behaviours with regard to social tolerance. One year later, we again measured the social tolerance of surviving individuals. The social tolerance is constant across time and strongly reflects the individual's dispersal and settlement patterns with respect to population density. These results strongly suggest that social personalities exist and influence dispersal decisions. Further studies will help to elucidate the proximate and ultimate determinants of social personalities.     

Emigration to new habitats by voles: the cost of dispersal paradox

We tested the hypothesis that dispersal and philopatry are components of a mixed evolutionarily stable strategy (ESS). The hypothesis predicts that fitness of dispersers should be equal to that of philopatric individuals. Alternatively, fitness of dispersers could be lower (the resident fitness hypothesis) or greater (the cost of dispersal hypothesis) than that of philopatric individuals. We compared fitness of individuals that moved to new habitats (emigrants) and those that remained within habitat boundaries (residents) in populations of the prairie vole, Microtus ochrogaster, and the meadow vole, M. pennsylvanicus. We established vole populations in four enclosures (). Within each enclosure, voles were free to move between four types of habitats that varied in the availability of supplemental food and the amount of vegetative cover. We analysed two fitness components: the survival rates of all individuals, and pregnancy rates of females. Our study showed that emigrants generally had greater fitness than residents and that the difference in fitness was habitat dependent (i.e. was greater when individuals were emigrating from low-quality habitats than from high-quality habitats). High-food, high-cover habitats were the only habitat types for which fitness of emigrants was lower than that of residents. Similar patterns occurred in both prairie voles and meadow voles. Our results support the cost of dispersal hypothesis.     

Estimating fitness consequences of dispersal: a road to 'know-where'? Non-random dispersal and the underestimation of dispersers' fitness

1. Many studies investigating fitness correlates of dispersal in vertebrates report dispersers to have lower fitness than philopatric individuals. However, if dispersers are more likely to produce dispersing young or are more likely to disperse again in the next year(s) than philopatric individuals, there is a risk that fitness estimates based on local adult survival and local recruitment will be underestimated for dispersers. 2. We review the available empirical evidence on parent-offspring resemblance and individual lifelong consistency in dispersal behaviour, and relate these studies to recent studies of fitness correlates of dispersal in vertebrates. 3. Of the 12 studies testing directly for parent-offspring resemblance in dispersal propensity, five report a significant resemblance. The average effect size (r) of parent-offspring resemblance in dispersal was 0.15 [95% confidence interval (CI) = 0.07-0.22], with no difference between the sexes (average weighted effect size of 0.12 (0.08-0.16) and 0.16 (0.11-0.20) for females and males, respectively). Only three studies report data on within-individual consistency in dispersal propensity, of which two suggest dispersers to be more likely to disperse again. 4. To assess the magnitude of fitness underestimation expected for dispersing individuals depending on the heritability of dispersal distance and study area size, we used a simulation approach. Even when study area size is 10 times the mean dispersal distance, local recruitment per breeding event may be underestimated by 4-10%, generating a potential difference of 4-60% in average lifetime production of recruits between dispersing and philopatric individuals, with larger differences in long-lived species. 5. Estimates of both fitness correlates of dispersal and parent-offspring resemblance or within-individual consistency in dispersal behaviour have been reported for 11 species. Although some comparisons suggest genuine differences in fitness components between philopatric and dispersing individuals, others, based on adult and juvenile survival, are open to the alternative explanation of biased fitness estimates. 6. We list three potential ways of reducing the risk of making wrong inferences on biased fitness estimates due to such non-random dispersal behaviour between dispersing and philopatric individuals: (a) diagnosing effects of non-random dispersal, (b) reducing the effects of spatially limited study area and (c) performing controlled experiments.     

Notonecta exhibit threat-sensitive,predator-induced dispersal

Dispersal is a central process determining community structure in heterogeneous landscapes, and species interactions within habitats may be a major determinant of dispersal. Although the effects of species interactions on dispersal within habitats have been well studied, how species interactions affect the movement of individuals between habitats in a landscape has received less attention. We conducted two experiments to assess the extent to which predation risk affects dispersal from an aquatic habitat by a flight-capable semi-aquatic insect (Notonecta undulata). Exposure to non-lethal (caged) fish fed conspecifics increased dispersal rates in N. undulata. Moreover, dispersal rate was positively correlated with the level of risk imposed by the fish; the greater the number of notonectids consumed by the caged fish, the greater the dispersal rate from the habitat. These results suggest that risk within a habitat can affect dispersal among habitats in a landscape and thus affect community structure on a much greater scale than the direct effect of predation itself.     

The effect of limited visibility on vigilance behaviour and speed of predator detection: implications for the conservation of granivorous passerines

Ants have been traditionally considered either as predators or dispersers of seeds, but not both. That is, ant dispersal is restricted to myrmecochorous seeds, while almost all seeds removed by seed‐harvesting ants are eaten. However, harvesting ants might be simultaneously antagonistic and mutualistic towards seeds. This study analyzes the predation–dispersal relationship between seed‐harvesting ants and seeds of Lobularia maritima, a non‐myrmechorous perennial herb, in order to disentangle the dual role of ants as dispersers and predators of L. maritima seeds. The results obtained confirm the role of harvesting ants as both predators and dispersers of the non‐myrmechorous seeds of L. maritima. The removal activity of Messor bouvieri on L. maritima seeds is very important, particularly in autumn, which is the flowering and fruiting peak of this plant. It can be estimated that harvesting ants collect more than 85% of seeds, and almost 70% of them are effectively lost to predation. However, these granivorous ants also have drawbacks as seed dispersers. There is a relatively small percent of seeds collected by ants that escape predation, either because they are dropped on the way to the nest (16.4% of seeds harvested), or because they are mistakenly rejected on the refuse pile (0.9%). Abiotic dispersal of L. maritima seeds in the absence of ants occurs over very short distances from the plant stem. As seeds dispersed by ants reach a considerably greater distance than that obtained by gravity, this might represent a real advantage for the species, because it reduces intraspecific adult competition for seedlings, which directly influences seedling survivorship. These results challenge the generalization that seed removal by ants generally leads to successful seed dispersal if done by legitimate seed dispersers, or seed loss if done by seed consumers that eat them, and confirm that harvesting ants might have a dual role as both predators and dispersers of nonmyrmechorous seeds.     

Predicting forest management effects on oak–rodent mutualisms

Wood mice Apodemus sylvaticus are the main dispersers of acorns in highly managed Mediterranean holm‐oak woodlands. Mice mobilize and cache acorns to store them for winter consumption. They carry acorns away from potential competitors, face predation risks during mobilization, and cache acorns in areas where pilfering risks are low. However, mice can act either as net predators or as moderately efficient dispersers, depending on the way landscape management affects intraspecific competition for acorns and shelter availability. To assess the influence of landscape structure and mouse behavior on acorn dispersal, we developed an agent‐based model (ABM) that translates forest management into changes in key environmental factors driving mouse foraging decisions. The model was able to predict accurately acorn dispersal patterns in a wide range of forest management practices based on information on forest habitat availability, stem density and shrub cover. Sensitivity analysis revealed that caching rates emerged from the interplay between intraspecific competition for seeds and predation risk accepted during mobilization. It also showed that intraspecific competition for acorns decreased with increasing habitat loss (due to positive edge effects on acorn production) while landscape resistance to mouse movements increased. As a result, the net benefits of caching declined and acorn predation became the dominant strategy. Finally, we assessed the effects of shrub encroachment as a management practice to enhance dispersal services in savanna‐like landscapes (dehesas). The model predicted non‐linear responses with a 65% threshold of shrub cover needed to achieve relatively high levels of acorn dispersal. This value may not be compatible with the traditional exploitation of dehesas (livestock rearing). Our study shows that integrated approaches that combine environmental change driven by management with behavioral responses of dispersers improve our understanding of the causes of recruitment bottlenecks, and are useful tools for evaluating conservation strategies aimed at enhancing dispersal services.     

Frugivory and Seed Fate in Bursera inversa (Burseraceae) at Tinigua Park,Colombia: Implications for Primate Conservation1

The large ateline primates are efficient seed dispersers in Neotropical forests and hunting is driving their populations to extinction, but we do not know whether other frugivores could substitute primates in their ecological role as seed dispersers. In this study we test this possibility using a potential keystone species (Bursera inversa) at Tinigua Park, Colombia. This plant species allows us to compare seed removal rates between emergent, isolated trees, without primate visitors and trees with connected crowns. We used traps to estimate fruit production and seed removal rates in six different trees, and fruiting trees were observed during 2 yr to quantify the number of seeds manipulated by different animal species. We carried out seed predation experiments to test if seed removal by predators was affected by distance or density effects. We found that the most productive trees attracted more visiting species and seed removal rates differed among trees, the lowest corresponding to trees without primate access. Seed removal rates from the ground by predators were not higher below parental trees than away from them, but the distribution of saplings in the forest suggests that seed dispersal is advantageous. Although it is likely that the effect of primate extinctions will vary depending on tree species traits, conserving the populations of primate seed dispersers is critical to maintain the ecological processes in this forest.