Birds as Suppliers of Seed Dispersal in Temperate Ecosystems: Conservation Guidelines from Real‐World Landscapes

Abstract: Seed dispersal by animals is considered a pivotal ecosystem function that drives plant‐community dynamics in natural habitats and vegetation recovery in human‐altered landscapes. Nevertheless, there is a lack of suitable ecological knowledge to develop basic conservation and management guidelines for this ecosystem service. Essential questions, such as how well the abundance of frugivorous animals predicts seeding function in different ecosystems and how anthropogenic landscape heterogeneity conditions the role of dispersers, remain poorly answered. In three temperate ecosystems, we studied seed dispersal by frugivorous birds in landscape mosaics shaped by human disturbance. By applying a standardized design across systems, we related the frequency of occurrence of bird‐dispersed seeds throughout the landscape to the abundance of birds, the habitat features, and the abundance of fleshy fruits. Abundance of frugivorous birds in itself predicted the occurrence of dispersed seeds throughout the landscape in all ecosystems studied. Even those landscape patches impoverished due to anthropogenic disturbance received some dispersed seeds when visited intensively by birds. Nonetheless, human‐caused landscape degradation largely affected seed‐deposition patterns by decreasing cover of woody vegetation or availability of fruit resources that attracted birds and promoted seed dispersal. The relative role of woody cover and fruit availability in seed dispersal by birds differed among ecosystems. Our results suggest that to manage seed dispersal for temperate ecosystem preservation or restoration one should consider abundance of frugivorous birds as a surrogate of landscape‐scale seed dispersal and an indicator of patch quality for the dispersal function; woody cover and fruit resource availability as key landscape features that drive seedfall patterns; and birds as mobile links that connect landscape patches of different degrees of degradation and habitat quality via seed deposition.     

Effect of Edge Structure on the Flux of Species into Forest Interiors

Abstract: A key goal of conservation biology is to prevent the spread of exotic species. Previous work on exotic invasion has two limitations: (1) the lack of a spatially explicit approach and (2) a primary focus on the net effect of invasion by examining invasive species already present in the community. We address these limitations by focusing on the arrival of a potential invader into a community and use a spatially explicit approach to quantify the flow of seeds from the surrounding landscape into the interior of a forest. We hypothesize that the structure of forest-edge vegetation influences how the edge mediates seed flux. To test our hypothesis, we experimentally altered vegetation structure within 20 m of the edge to create two edge treatments: thinned and intact. We quantified the flux of seeds moving into the forest interior across the two treatments. We used seed traps randomly arrayed on transects from 5 to 50 m into the forest. More seeds crossed the thinned treatment than crossed the intact treatment to reach the forest interior. In addition, seeds that crossed the thinned treatment dispersed farther into the forest than those that crossed the intact treatment. These results were consistent throughout the period of maximum autumn dispersal, including periods before and after leaf drop. Our results show that the structure of vegetation on the edge interacts with the flux of wind-dispersed seed across the edge. We demonstrated that an edge with intact vegetation can function as a physical barrier to seed dispersal. Therefore, the structure of vegetation on edges can influence the function of edges as barriers to seed flux into the forest interior.     

Incorporating animal behavior into seed dispersal models: implications for seed shadows

Seed dispersal fundamentally influences plant population and community dynamics but is difficult to quantify directly. Consequently, models are frequently used to describe the seed shadow (the seed deposition pattern of a plant population). For vertebrate-dispersed plants, animal behavior is known to influence seed shadows but is poorly integrated in seed dispersal models. Here, we illustrate a modeling approach that incorporates animal behavior and develop a stochastic, spatially explicit simulation model that predicts the seed shadow for a primate-dispersed tree species (Virola calophylla, Myristicaceae) at the forest stand scale. The model was parameterized from field-collected data on fruit production and seed dispersal, behaviors and movement patterns of the key disperser, the spider monkey (Ateles paniscus), densities of dispersed and non-dispersed seeds, and direct estimates of seed dispersal distances. Our model demonstrated that the spatial scale of dispersal for this V. calophylla population was large, as spider monkeys routinely dispersed seeds >100 m, a commonly used threshold for long-distance dispersal. The simulated seed shadow was heterogeneous, with high spatial variance in seed density resulting largely from behaviors and movement patterns of spider monkeys that aggregated seeds (dispersal at their sleeping sites) and that scattered seeds (dispersal during diurnal foraging and resting). The single-distribution dispersal kernels frequently used to model dispersal substantially underestimated this variance and poorly fit the simulated seed-dispersal curve, primarily because of its multimodality, and a mixture distribution always fit the simulated dispersal curve better. Both seed shadow heterogeneity and dispersal curve multimodality arose directly from these different dispersal processes generated by spider monkeys. Compared to models that did not account for disperser behavior, our modeling approach improved prediction of the seed shadow of this V. calophylla population. An important function of seed dispersal models is to use the seed shadows they predict to estimate components of plant demography, particularly seedling population dynamics and distributions. Our model demonstrated that improved seed shadow prediction for animal-dispersed plants can be accomplished by incorporating spatially explicit information on disperser behavior and movements, using scales large enough to capture routine long-distance dispersal, and using dispersal kernels, such as mixture distributions, that account for spatially aggregated dispersal.     

Spatial and temporal patterns of seed dispersal: an important determinant of grassland invasion.

We measured spatial and temporal patterns of seed dispersal and seedling recruitment for 58 species in a grassland community to test whether seed dispersal could predict patterns of invasion after disturbance. For the 12 most abundant grasses, recruitment of native species was dependent on the propagule supply of both native and exotic species. Variability in seed rain on small spatial (1-10 m) and temporal (within season) scales led to qualitative differences in the outcome of disturbance colonization such that native species dominated disturbances when exotic seed supply was low but failed to establish when exotic seed supply was high. Local dispersal and spatial heterogeneity in species composition promoted coexistence of native and exotic species by creating refuges from high exotic seed supply within native dominated patches. Despite this, copious exotic seed production strongly limited recruitment of native species in exotic dominated patches. Most grasslands in California are presently dominated by exotic species, suggesting that competition at the seedling stage is a major barrier to native species restoration.     

Modeling seed dispersal distances: implications for transgenic Pinus taeda.

Predicting forest-tree seed dispersal across a landscape is useful for estimating gene flow from genetically engineered (GE) or transgenic trees. The question of biocontainment has yet to be resolved, although field-trial permits for transgenic forest trees are on the rise. Most current field trials in the United States occur in the Southeast where Pinus taeda L., an indigenous species, is the major timber commodity. Seed dispersal distances were simulated using a model where the major determinants were: (1) forest canopy height at seed release, (2) terminal velocity of the seeds, (3) absolute seed release, and (4) turbulent-flow statistics, all of which were measured or determined within a P. taeda plantation established from seeds collected from wild forest-tree stands at the Duke Forest near Durham, North Carolina, USA. In plantations aged 16 and 25 years our model results showed that most of the seeds fell within local-neighborhood dispersal distances, with estimates ranging from 0.05 to 0.14 km from the source. A fraction of seeds was uplifted above the forest canopy and moved via the long-distance dispersal (LDD) process as far as 11.9-33.7 km. Out of 10(5) seeds produced per hectare per year, roughly 440 seeds were predicted to be uplifted by vertical eddies above the forest canopy and transported via LDD. Of these, 70 seeds/ha traveled distances in excess of 1 km from the source, a distance too great to serve as a biocontainment zone. The probability of LDD occurrence of transgenic conifer seeds at distances exceeding 1 km approached 100%.     

The effects of plant distribution and frugivore density on the scale and shape of dispersal kernels

For many plant species, seed dispersal is one of the most important spatial demographic processes. We used a diffusion approximation and a spatially explicit simulation model to explore the mechanisms generating seed dispersal kernels for plants dispersed by frugivores. The simulation model combined simple movement and foraging rules with seed gut passage time, plant distribution, and fruit production. A simulation experiment using plant spatial aggregation and frugivore density as factors showed that seed dispersal scale was largely determined by the degree of plant aggregation, whereas kernel shape was mostly dominated by frugivore density. Kernel shapes ranged from fat tailed to thin tailed, but most shapes were between an exponential and that of the solution of a diffusion equation. The proportion of dispersal kernels with fat tails was highest for landscapes with clumped plant distributions and increased with increasing number of dispersers. The diffusion model provides a basis for models including more behavioral details but can also be used to approximate dispersal kernels once a diffusion rate is estimated from animal movement data. Our results suggest that important characteristics of dispersal kernels will depend on the spatial pattern of plant distribution and on disperser density when frugivores mediate seed dispersal.     

Introduced Birds and the Fate of Hawaiian Rainforests

Abstract:  The Hawaiian Islands have lost nearly all their native seed dispersers, but have gained many frugivorous birds and fleshy-fruited plants through introductions. Introduced birds may not only aid invasions of exotic plants but also may be the sole dispersers of native plants. We assessed seed dispersal at the ecotone between native- and exotic-dominated forests and quantified bird diets, seed rain from defecated seeds, and plant distributions. Introduced birds were the primary dispersers of native seeds into exotic-dominated forests, which may have enabled six native understory plant species to become reestablished. Some native plant species are now as common in exotic forest understory as they are in native forest. Introduced birds also dispersed seeds of two exotic plants into native forest, but dispersal was localized or establishment minimal. Seed rain of bird-dispersed seeds was extensive in both forests, totaling 724 seeds of 9 native species and 2 exotics with over 85% of the seeds coming from native plants. Without suitable native dispersers, most common understory plants in Hawaiian rainforests now depend on introduced birds for dispersal, and these introduced species may actually facilitate perpetuation, and perhaps in some cases restoration, of native forests. We emphasize, however, that restoration of native forests by seed dispersal from introduced birds, as seen in this study, depends on the existence of native forests to provide a source of seeds and protection from the effects of ungulates. Our results further suggest that aggressive control of patches of non-native plants within otherwise native-dominated forests may be an important and effective conservation strategy.     

Functional nonredundancy of elephants in a disturbed tropical forest

Conservation efforts are often motivated by the threat of global extinction. Yet if conservationists had more information suggesting that extirpation of individual species could lead to undesirable ecological effects, they might more frequently attempt to protect or restore such species across their ranges even if they were not globally endangered. Scientists have seldom measured or quantitatively predicted the functional consequences of species loss, even for large, extinction‐prone species that theory suggests should be functionally unique. We measured the contribution of Asian elephants (Elephas maximus) to the dispersal of 3 large‐fruited species in a disturbed tropical moist forest and predicted the extent to which alternative dispersers could compensate for elephants in their absence. We created an empirical probability model with data on frugivory and seed dispersal from Buxa Tiger Reserve, India. These data were used to estimate the proportion of seeds consumed by elephants and other frugivores that survive handling and density‐dependent processes (Janzen‐Connell effects and conspecific intradung competition) and germinate. Without compensation, the number of seeds dispersed and surviving density‐dependent effects decreased 26% (Artocarpus chaplasha), 42% (Careya arborea), and 72% (Dillenia indica) when elephants were absent from the ecosystem. Compensatory fruit removal by other animals substantially ameliorated these losses. For instance, reductions in successful dispersal of D. indica were as low as 23% when gaur (Bos gaurus) persisted, but median dispersal distance still declined from 30% (C. arborea) to 90% (A. chaplasha) without elephants. Our results support the theory that the largest animal species in an ecosystem have nonredundant ecological functionality and that their extirpation is likely to lead to the deterioration of ecosystem processes such as seed dispersal. This effect is likely accentuated by the overall defaunation of many tropical systems.     

Dispersal of seeds by the tropical sea breeze

Given the dependence of most wind-pollinated and wind-dispersed species on low relative humidity (RH) for abscission, and the minimization of RH in the early afternoon, there ought to be a marked directional bias in seed dispersal at sites with a strong local diurnal circulation. We filmed the abscission of seeds of five wind-dispersed tropical species near the coast of Mexico (Jalisco). We found that (1) most abscission occurred during the period from 10:00 to 17:00 hours; (2) there was a strong bias for landward dispersal due to the midday sea breeze; (3) the little nocturnal dispersal that occurred was toward the sea (due to the night land breeze); (4) there was no abscission in the absence of wind (i.e., indoors) except for one species; and (5) holding relative humidity constant, the proportion of seeds diurnally abscising is strongly correlated with horizontal wind speed. We predict that a similar bias (this time for upslope dispersal) for xerochastic dispersal will occur in complex terrain. We conclude that in coastal and mountainous terrain, dispersal models (and inverse modeling efforts) must include a directionality term.     

On the relative contributions of wind vs. animals to seed dispersal of four Sierra Nevada pines

Selective pressures that influence the form of seed dispersal syndromes are poorly understood. Morphology of plant propagules is often used to infer the means of dispersal, but morphology can be misleading. Several species of pines, for example, have winged seeds adapted for wind dispersal but owe much of their establishment to scatter-hoarding animals. Here the relative importance of wind vs. animal dispersal is assessed for four species of pines of the eastern Sierra Nevada that have winged seeds but differed in seed size: lodgepole pine (Pinus contorta murrayana, 8 mg); ponderosa pine (Pinus ponderosa ponderosa, 56 mg); Jeffrey pine (Pinus jeffreyi, 160 mg); and sugar pine (Pinus lambertiana, 231 mg). Pre-dispersal seed mortality eliminated much of the ponderosa pine seed crop (66%), but had much less effect on Jeffrey pine (32% of seeds destroyed), lodgepole pine (29%), and sugar pine (7%). When cones opened most filled seeds were dispersed by wind. Animals removed > 99% of wind-dispersed Jeffrey and sugar pine seeds from the ground within 60 days, but animals gathered only 93% of lodgepole pine seeds and 38% of ponderosa pine seeds during the same period. Animals gathered and scatter hoarded radioactively labeled ponderosa, Jeffrey, and sugar pine seeds, making a total of 2103 caches over three years of study. Only three lodgepole pine caches were found. Caches typically contained 1-4 seeds buried 5-20 mm deep, depths suitable for seedling emergence. Although Jeffrey and sugar pine seeds are initially wind dispersed, nearly all seedlings arise from animal caches. Lodgepole pine is almost exclusively wind dispersed, with animals acting as seed predators. Animals treated ponderosa pine in an intermediate fashion. Two-phased dispersal of large, winged pine seeds appears adaptive; initial wind dispersal helps to minimize pre-dispersal seed mortality whereas scatter hoarding by animals places seeds in sites with a higher probability of seedling establishment.     

Hunting Increases Dispersal Limitation in the Tree Carapa procera, a Nontimber Forest Product

Abstract:  The sustainability of seed extraction from natural populations has been questioned recently. Increased recruitment failure under intense seed harvesting suggests that seed extraction intensifies source limitation. Nevertheless, areas where more seeds are collected tend to also have more intense hunting of seed-dispersing animals. We studied whether such hunting, by limiting disperser activity, could cause quantitative dispersal limitation, especially for large crops and for crops in years of high seed abundance. In each of four Carapa procera (Meliaceae) populations in French Guiana and Surinam, two with hunting and two without, we compared seed fate for individual trees varying in crop size in years of high and low population-level seed abundance. Carapa seeds are a nontimber forest product and depend on dispersal by scatter-hoarding rodents for survival and seedling establishment. Hunting negatively affected the proportion of seeds dispersed and caused greater numbers of seeds to germinate or be infested by moths below parent trees, where they would likely die. Hunting of seed-dispersing animals disproportionally affected large seed crops, but we found no additional effect of population-level seed abundance on dispersal rates. Consistently lower rates of seed dispersal, especially for large seed crops, may translate to lower levels of seedling recruitment under hunting. Our results therefore suggest that the subsistence hunting that usually accompanies seed collection is at the cost of seed dispersal and may contribute to recruitment failure of these nontimber forest products. Seed extraction from natural populations may affect seedling recruitment less if accompanied by measures adequately incorporating and protecting seed dispersers.     

Soil vs. canopy seed storage and plant species coexistence in species-rich Australian shrublands

The fire-prone shrublands of southwestern Australia are renowned for their high plant species diversity and prominence of canopy seed storage (serotiny). We compared species richness, abundance, and life history attributes for soil and canopy seed banks in relation to extant vegetation among four sites with different substrate conditions and high species turnover (50-80%) to identify whether this unusual community-level organization of seed storage might contribute to maintenance of high species richness. Soil seed bank (SSB) densities were low to moderate (233-1435 seeds/m2) compared with densities for other Mediterranean-type vegetation and were lowest for sites with highest canopy seed bank (CSB) species richness and lowest nutrient availability, but not richness or abundance of resprouters. Annuals were infrequent in the lowest nutrient sites, but there was no evidence that small SSB size was due to low seed inputs or a trade-off between seed production/storage and seed size in response to low nutrient availability. Sorensen's similarity between SSB and extant vegetation was 26-43% but increased to 54-57% when the CSB was included, representing levels higher than reported for most other ecosystems. Resprouting species were well represented in both the SSB and CSB, and there was no evidence for lower seed production in resprouters than in non-sprouters overall. The SSB and CSB held no species in common and were characterized by markedly different seed dispersal attributes, with winged or small seeds in the CSB and seeds dispersed by ants, birds, and wind (though none with wings) in the SSB. There was no evidence of spatial differentiation in the distribution of seeds of SSB species between vegetated and open microsites that might facilitate species coexistence, but most woody non-sprouters showed aggregation at scales of 1-2 m, implying limited seed dispersal. High similarity between overall seed bank (SSB + CSB) and extant species composition, high number of resprouting species, and seed dispersal processes before (SSB) and after fire (CSB) leading to differential spatial aggregation of post-fire recruits from the two seed bank types may buffer species composition against rapid change and provide a mechanism for maintaining species coexistence at the local scale.     

Experimental manipulation of seed shadows of an Afrotropical tree determines drivers of recruitment

The loss of animals in tropical forests may alter seed dispersal patterns and reduce seedling recruitment of tree species, but direct experimental evidence is scarce. We manipulated dispersal patterns of Manilkara mabokeensis, a monkey-dispersed tree, to assess the extent to which spatial distributions of seeds drive seedling recruitment. Based on the natural seed shadow, we created seed distributions with seeds deposited under the canopy ("no dispersal"), with declining density from the tree ("natural dispersal"), and at uniform densities ("good dispersal"). These distributions mimicked dispersal patterns that could occur with the extirpation of monkeys, low levels of hunting, and high rates of seed dispersal. We monitored seedling emergence and survival for 18 months and recorded the number of leaves and damage to leaves. "Good dispersal" increased seedling survival by 26%, and "no dispersal" decreased survival by 78%, relative to "natural dispersal." Using a mixed-effects survival model, we decoupled the distance and density components of the seed shadow: seedling survival depended on the seed density, but not on the distance from the tree. Although community seedling diversity tended to decrease with longer dispersal distances, we found no conclusive evidence that patterns of seed dispersal influence the diversity of the seedling community. Local seed dispersal does affect seedling recruitment and survival, with better dispersal resulting in higher seedling recruitment; hence the loss of dispersal services that comes with the reduction or extirpation of seed dispersers will decrease regeneration of some tree species.     

Release thresholds strongly determine the range of seed dispersal by wind

The effect of the seed abscission process on the dispersal distance of seeds has never been studied explicitly and is often ignored in studies that aim to estimate the seed shadows of species. To examine the importance of the abscission process for the seed shadow we used a seed trajectory model that keeps track of the release threshold dynamics of the individual seeds on mother plant. We defined the release threshold as the critical wind speed that induces a mechanical force that is just large enough to release a seed from its mother plant. The model used real wind speed sequences and seed appearance over time on the mother plant.Several calculations were performed to investigate the effect of release thresholds dynamics on seed shadow of two herbaceous species with contrasting terminal velocity values (V_t): Centaurea jacea (V_t = 4.1 m s⁻¹) and Hypochaeris radicata (V_t = 0.49 m s⁻¹).Release thresholds were responsible for a two-fold increase of median dispersal distances in both species. Tails of the seed shadows, the fraction of seeds that travel furthest, were even more sensitive and increased with a factor 4.5 for Centaurea and 7.0 for Hypochaeris. Our work indicates that the abscission process appears to be very important and suggests that dispersal distance of plants is currently severely underestimated, which, in turn, has major consequences for our current understanding of the distribution, metapopulation dynamics and survival of plant species.     

On the Estimation of Dispersal Kernels from Individual Mark-Recapture Data

We present a new method for estimating a distribution of dispersal displacements (a dispersal kernel) from mark-recapture data. One conventional method of calculating the dispersal kernel assumes that the distribution of displacements are Gaussian (e.g. resulting from a diffusion process) and that individuals remain within sampled areas. The first assumption prohibits an analysis of dispersal data that do not exhibit the Gaussian distribution (a common situation); the second assumption leads to underestimation of dispersal distance because individuals that disperse outside of sampling areas are never recaptured. Our method eliminates these two assumptions. In addition, the method can also accommodate mortality during a sampling period. This new method uses integrodifference equations to express the probability of spatial mark-recapture data; associated dispersal, survival, and recapture parameters are then estimated using a maximum likelihood method. We examined the accuracy of the estimators by applying the method to simulated data sets. Our method suggests designs for future mark-recapture experiments. Received: January 2004 / Revised: July 2005     

Worker size-related task partitioning in the foraging strategy of a seed-harvesting ant species

Messor bouvieri is a seed-harvesting ant species in which workers forage in trails from the nest to a search area. A previous observation of seed transfer events between workers returning to the nest suggested potential task partitioning. In this study, we describe seed transportation and analyze the role of task partitioning in the foraging strategy of this species in terms of seed intake efficiency in relation to costs and benefits based on transport speed and task reliability. We assess the harvesting efficiency of task partitioning by comparing cooperative seed transport (CST) and individual seed transport (IST) events. Our results show task partitioning in the form of a sequence of transfer events among workers going from the search area to the nest. Importantly, and despite the weak worker polymorphism of this species, this sequence involved workers of different sizes, with seeds usually being passed along from smaller to larger workers. In addition, we show that small workers are better at finding seeds (spend less time finding a seed), and large workers are better at transporting them (were faster when walking back to the nest and lost fewer seeds). However, we failed to demonstrate that workers of different sizes are specialized in performing the task in which they excel. Overall, sequential CST in M. bouvieri results in a greater seed intake because seed search time decreases and task reliability increases, compared to IST. The determinants and adaptive benefits of CST are discussed.     

Importance of species traits for species distribution in fragmented landscapes

Knowledge of the relationship between species traits and species distribution in fragmented landscapes is important for understanding current distribution patterns and as background information for predictive models of the effect of future landscape changes. The existing studies on the topic suffer from several drawbacks. First, they usually consider only traits related to dispersal ability and not growth. Furthermore, they do not apply phylogenetic corrections, and we thus do not know how considerations of phylogenetic relationships can alter the conclusions. Finally, they usually apply only one technique to calculate habitat isolation, and we do not know how other isolation measures would change the results. We studied the issues using 30 species forming congeneric pairs occurring in fragmented dry grasslands. We measured traits related to dispersal, survival, and growth in the species and recorded distribution of the species in 215 grassland fragments. We show many strong relationships between species traits related to both dispersal and growth and species distribution in the landscape, such as the positive relationship between habitat occupancy and anemochory and negative relationships between habitat occupancy and seed dormancy. The directions of these relationships, however, often change after application of phylogenetic correction. For example, more isolated habitats host species with smaller seeds. After phylogenetic correction, however, they turn out to host species with larger seeds. The conclusions also partly change depending on how we calculate habitat isolation. Specifically, habitat isolation calculated from occupied habitats only has the highest predictive power. This indicates slow dynamics of the species. All the results support the expectation that species traits have a high potential to explain patterns of species distribution in the landscape and that they can be used to build predictive models of species distribution. The specific conclusions are, however, dependent on the technique used, and we should carefully consider this when comparing among different studies. Since different techniques answer slightly different questions, we should attempt to use analyses both with and without phylogenetic correction and explore different isolation measures whenever possible and compare the results.     

Seed dispersal of desert annuals

We quantified seed dispersal in a guild of Sonoran Desert winter desert annuals at a protected natural field site in Tucson, Arizona, USA. Seed production was suppressed under shrub canopies, in the open areas between shrubs, or both by applying an herbicide prior to seed set in large, randomly assigned removal plots (10-30 m diameter). Seedlings were censused along transects crossing the reproductive suppression borders shortly after germination. Dispersal kernels were estimated for Pectocarya recurvata and Schismus barbatus from the change in seedling densities with distance from these borders via inverse modeling. Estimated dispersal distances were short, with most seeds traveling less than a meter. The adhesive seeds of P. recurvata went farther than the small S. barbatus seeds, which have no obvious dispersal adaptation. Seeds dispersed farther downslope than upslope and farther when dispersing into open areas than when dispersing into shrubs. Dispersal distances were short relative to the pattern of spatial heterogeneity created by the shrub and open space mosaic. This suggests that dispersal could contribute to local population buildup, possibly facilitating species coexistence. Overall, these results support the hypothesis that escape in time via delayed germination is likely to be more important for desert annuals than escape in space.     

Neighborhood effects on seed dispersal by frugivores: testing theory with a mistletoe-marsupial system in Patagonia

The outcome of the dispersal process in zoochorous plants is largely determined by the behavior of frugivorous animals. Recent simulation studies have found that fruit removal rates and mean dispersal distances are strongly affected by fruiting plant neighborhoods. We empirically tested the effects of conspecific fruiting plant neighborhoods, crop sizes, and plant accessibility on fruit removal rates and seed dispersal distances of a mistletoe species exclusively dispersed by an arboreal marsupial in Northern Patagonia. Moreover, in this study, we overcome technical limitations in the empirical estimation of seed dispersal by using a novel 15N stable isotope enrichment technique together with Bayesian mixing models that allowed us to identify dispersed seeds from focal plants without the need of extensive genotyping. We found that, as predicted by theory, plants in denser neighborhoods had greater fruit removal and shorter mean dispersal distances than more isolated plants. Furthermore, the probability of dispersing seeds farther away decreased with neighborhood density. Larger crop sizes resulted in larger fruit removal rates and smaller probabilities of longer distance dispersal. The interplay between frugivore behavioral decisions and the spatial distribution of plants could have important consequences for plant spatial dynamics.