Tomás A. Carlo

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.

Avian fruit preferences across a Puerto Rican forested landscape: pattern consistency and implications for seed removal

Abstract. Avian fruit consumption may ensure plant reproductive success when frugivores show consistent preference patterns and effectively remove and disperse seeds. In this study we examined avian fruit preferences and their seed-removal services at five study sites in north-central Puerto Rico. At each site, we documented the diet of seven common fruit-eating avian species from February to September 1998. Using foraging observations and area-based estimates of fruit abundance, we examined preference patterns of birds. We found that 7 out of 68 fleshy-fruited plant species were responsible for most of the fruit diet of birds. Seventeen plant species were preferred and four of them were repeatedly preferred across several study sites and times by at least one avian species. Preferred plant species comprised a small percentage of fleshy fruits at each site (<15% in four out of five study sites), but showed extended phenology patterns. The quantity of seeds removed by frugivore species was not strictly related to preferences. Some frugivores showing no preference could effectively remove more seeds from plants at some locations than species exhibiting constancy in their patterns of preference. Only two frugivores, Euphonia musica and Vireo altiloquous, removed most of the seeds of plants for which they exhibited repeated preference across the landscape. Preference patterns, particularly those exhibiting consistency in space and time for plant species having prolonged fruiting periods, may have important mechanistic consequences for the persistence, succession, and regeneration of tropical plant communities.

Evolutionary ecology of pungency in wild chilies.

The primary function of fruit is to attract animals that disperse viable seeds, but the nutritional rewards that attract beneficial consumers also attract consumers that kill seeds instead of dispersing them. Many of these unwanted consumers are microbes, and microbial defense is commonly invoked to explain the bitter, distasteful, occasionally toxic chemicals found in many ripe fruits. This explanation has been criticized, however, due to a lack of evidence that microbial consumers influence fruit chemistry in wild populations. In the present study, we use wild chilies to show that chemical defense of ripe fruit reflects variation in the risk of microbial attack. Capsaicinoids are the chemicals responsible for the well known pungency of chili fruits. Capsicum chacoense is naturally polymorphic for the production of capsaicinoids and displays geographic variation in the proportion of individual plants in a population that produce capsaicinoids. We show that this variation is directly linked to variation in the damage caused by a fungal pathogen of chili seeds. We find that Fusarium fungus is the primary cause of predispersal chili seed mortality, and we experimentally demonstrate that capsaicinoids protect chili seeds from Fusarium. Further, foraging by hemipteran insects facilitates the entry of Fusarium into fruits, and we show that variation in hemipteran foraging pressure among chili populations predicts the proportion of plants in a population producing capsaicinoids. These results suggest that the pungency in chilies may be an adaptive response to selection by a microbial pathogen, supporting the influence of microbial consumers on fruit chemistry.

Where do seeds go when they go far? Distance and directionality of avian seed dispersal in heterogeneous landscapes

Seed dispersal at large scales strongly influences plant population dynamics. Still, ecologists have rarely measured seed dispersal at relevant scales, and the role of habitat types in affecting seed dispersal at long distances remains unexplored. We studied seed dispersal of Ilex aquifolium and Crataegus monogyna in northern Spain, hypothesizing that seeds would be recovered at higher rates and at longer distances (LDD) at habitats with fleshy-fruited trees, compared to habitats with other tree types or at open habitats. We tracked seeds in eight landscapes by enriching trees with 15N isotopes at the center of landscapes, and then detected 15N-marked seeds by sampling at distances of up to 700 m. We found that seeds arrive in greater densities and at longer distances in habitats with trees, particularly fleshy-fruited types, producing different LDD probabilities for each habitat. Results also show a disproportional arrival of seeds in habitats similar to those of mother plants, which should affect seed establishment and the genetic diversity of plant neighborhoods. Findings reveal the strong dependence of seed dispersal on the existing templates that guide the movements of avian dispersers in heterogeneous landscapes and also suggest that LDD above tree lines and beyond hard habitat edges can be difficult.

INTERSPECIFIC NEIGHBORS CHANGE SEED DISPERSAL PATTERN OF AN AVIAN‐DISPERSED PLANT

Ecologists increasingly recognize that plant–plant facilitation can influence plant community structure. However, seed dispersal facilitation among plant neighbors that share seed dispersal agents has received little study. Seed dispersal facilitation among neighboring plants can be defined as an increase in the number, distances, and/or places reached by a plants seeds that is due to the presence of co-fruiting-plant neighbors with which it shares frugivore seed dispersers. I experimentally tested the potential for seed dispersal facilitation and competition among co-fruiting-plant neighbors using Solanum americanum and Cestrum diurnum, two plant species that co-occur in open habitats of Puerto Rico and whose seeds are dispersed by the same bird species. I constructed S. americanum neighborhoods with and without C. diurnum (i.e., mixed and non-mixed) while controlling plant ripe-fruit crop and surrounding fruiting landscape in six replicate fields. I quantified seed dispersal using a grid of seed-collec...

FEMALE‐DIRECTED DISPERSAL AND FACILITATION BETWEEN A TROPICAL MISTLETOE AND A DIOECIOUS HOST

Phoradendron hexastichum is a bird-dispersed mistletoe that infects the dioecious tree Cecropia schreberiana. Because both species share frugivore seed dispersers, we hypothesized that female Cecropia would have a greater probability and intensity of mistletoe infection than males due to more frequent visitation by shared frugivores. Over 50% of female Cecropia were infected, in contrast with 25% of males. On average, female trees had twice as many mistletoes as male trees. Infection probability and intensity increased with basal area in females but not in males, suggesting that lifetime reinfection was also female biased. We found mistletoe frugivores visiting uninfected fruiting females twice as often as males. Although mistletoes were mostly consumed by the mistletoe specialist Euphonia musica, we did not record Euphonia visiting uninfected Cecropia trees. Uninfected Cecropia trees were frequently visited by generalist frugivores (such as Spindalis portoricensis) that used both mistletoes and Cecropia fruits. The Cecropia–frugivores– Phoradendron network of interactions seems to have led to the spatial linkage of the two plant species through directional dispersal, to plant–plant facilitation through shared frugivores, and to bird–bird facilitation in which generalist frugivores start new foci of infection that specialist frugivores can use.

A field test of the directed deterrence hypothesis in two species of wild chili

The directed deterrence hypothesis posits that secondary metabolites in ripe fruit function to deter fruit consumption by vertebrates that do not disperse seeds, while not impacting consumption by those that do. We tested this hypothesis in two species of wild chilies (Capsicum spp.). Both produce fruits that contain capsaicinoids, the compounds responsible for the pungency of chilies. Previous work suggests seed-dispersing birds but not seed-destroying rodents consume chili fruits, presumably because rodents are deterred by capsaicin. However, fruit removal from chili plants by rodents and other mammals has not been previously explored. Because laboratory rodents can develop a preference for capsaicin, it is quite possible that wild rodents are natural consumers of chili fruits. We monitored the fate of 125 marked fruits of Capsicum chacoense and 291 fruits of Capsicum annuum. For both species, essentially all fruit removal occurred during the day, when rodents are inactive. Video monitoring revealed fruit removal only by birds, mostly by species known to disperse chili seeds in viable condition. Furthermore, these species are from taxonomic groups that tend to specialize on lipid-rich fruits. Both species of chili produce fruits that are unusually high in lipids (35% in C. chacoense, 24% in C. annuum). These results support the directed deterrence hypothesis and suggest that fruiting plants distinguish between seed predators and seed dispersers by producing fruits that repel the former and attract the latter.

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.

A new method to track seed dispersal and recruitment using 15N isotope enrichment

Seed dispersal has a powerful influence on population dynamics, genetic structuring, evolutionary rates, and community ecology. Yet, patterns of seed dispersal are difficult to measure due to methodological shortcomings in tracking dispersed seeds from sources of interest. Here we introduce a new method to track seed dispersal: stable isotope enrichment. It consists of leaf-feeding plants with sprays of 15N-urea during the flowering stage such that seeds developed after applications are isotopically enriched. We conducted a greenhouse experiment with Solanum americanum and two field experiments with wild Capsicum annuum in southern Arizona, USA, to field-validate the method. First, we show that plants sprayed with 15N-urea reliably produce isotopically enriched progeny, and that delta 15N (i.e., the isotopic ratio) of seeds and seedlings is a linear function of the 15N-urea concentration sprayed on mothers. We demonstrate that three urea dosages can be used to distinctly enrich plants and unambiguously differentiate their offspring after seeds are dispersed by birds. We found that, with high urea dosages, the resulting delta 15N values in seedlings are 10(3) - 10(4) times higher than the delta 15N values of normal plants. This feature allows tracking not only where seeds arrive, but in locations where seeds germinate and recruit, because delta 15N enrichment is detectable in seedlings that have increased in mass by at least two orders of magnitude before fading to normal delta 15N values. Last, we tested a mixing model to analyze seed samples in bulk. We used the delta 15N values of batches (i.e., combined seedlings or seeds captured in seed traps) to estimate the number of enriched seeds coming from isotopically enriched plants in the field. We confirm that isotope enrichment, combined with batch-sampling, is a cheap, reliable, and user-friendly method for bulk-processing seeds and is thus excellent for the detection of rare dispersal events. This method could further the study of dispersal biology, including the elusive, but critically important, estimation of long-distance seed dispersal.

When condition trumps location: seed consumption by fruit-eating birds removes pathogens and predator attractants.

Seed ingestion by frugivorous vertebrates commonly benefits plants by moving seeds to locations with fewer predators and pathogens than under the parent. For plants with high local population densities, however, movement from the parent plant is unlikely to result in ‘escape’ from predators and pathogens. Changes to seed condition caused by gut passage may also provide benefits, yet are rarely evaluated as an alternative. Here, we use a common bird-dispersed chilli pepper (Capsicum chacoense) to conduct the first experimental comparison of escape-related benefits to condition-related benefits of animal-mediated seed dispersal. Within chilli populations, seeds dispersed far from parent plants gained no advantage from escape alone, but seed consumption by birds increased seed survival by 370% – regardless of dispersal distance – due to removal during gut passage of fungal pathogens and chemical attractants to granivores. These results call into question the pre-eminence of escape as the primary advantage of dispersal within populations and document two overlooked mechanisms by which frugivores can benefit fruiting plants.