Vertebrate herbivory impacts seedling recruitment more than niche partitioning or density-dependent mortality.

In tropical forests, resource-based niches and density-dependent mortality are mutually compatible mechanisms that can act simultaneously to limit seedling populations. Differences in the strengths of these mechanisms will determine their roles in maintaining species coexistence. In the first assessment of these mechanisms in a Congo Basin forest, we quantified their relative strengths and tested the extent to which density-dependent mortality is driven by the distance-dependent behavior of seed and seedling predators predicted by the Janzen-Connell hypothesis. We conducted a large-scale seed addition experiment for five randomly selected tropical tree species, caging a subset of seed addition quadrats against vertebrate predators. We then developed models to assess the mechanisms that determine seedling emergence (three months after seed addition) and survival (two years after seed addition). As predicted, both niche differentiation and density-dependent mortality limited seedling recruitment, but predation had the strongest effects on seedling emergence and survival. Seedling species responded differently to naturally occurring environmental variation among sites, including variation in light levels and soil characteristics, supporting predictions of niche-based theories of tropical tree species coexistence. The addition of higher densities of seeds into quadrats initially led to greater seedling emergence, but survival to two years decreased with seed density. Seed and seedling predation reduced recruitment below levels maintained by density-dependent mortality, an indication that predators largely determine the population size of tree seedlings. Seedling recruitment was unrelated to the distance to or density of conspecific adult trees, suggesting that recruitment patterns are generated by generalist vertebrate herbivores rather than the specialized predators predicted by the Janzen-Connell hypothesis. If the role of seed and seedling predation in limiting seedling recruitment is a general phenomenon, then the relative abundances of tree species might largely depend on species-specific adaptations to avoid, survive, and recover from damage induced by vertebrate herbivores. Likewise, population declines of herbivorous vertebrate species (many of which are large and hunted) may trigger shifts in species composition of tropical forests.

Plants as reef fish: fitting the functional form of seedling recruitment.

The life histories of many species depend first on dispersal to local sites and then on establishment. After dispersal, density-independent and density-dependent mortalities modify propagule supply, determining the number of individuals that establish. Because multiple factors influence recruitment, the dichotomy of propagule versus establishment limitation is best viewed as a continuum along which the strength of propagule or establishment limitation changes with propagule input. To evaluate the relative importance of seed and establishment limitation for plants, we (1) describe the shape of the recruitment function and (2) use limitation and elasticity analyses to quantify the sensitivity of recruitment to perturbations in seed limitation and density-independent and density-dependent mortality. Using 36 seed augmentation studies for 18 species, we tested four recruitment functions against one another. Although the linear model (accounting for seed limitation and density-independent mortality) fitted the largest number of studies, the nonlinear Beverton-Holt model (accounting for density-dependent mortality) performed better at high densities of seed augmentation. For the 18 species, seed limitation constrained population size more than other sources of limitation at ambient conditions. Seedling density reached saturation with increasing seed density in many studies, but at such high densities that seedling density was primarily limited by seed availability rather than microsite availability or density dependence.

Are plant populations seed limited? A critique and meta-analysis of seed addition experiments.

We examine the relative importance of processes that underlie plant population abundance and distribution. Two opposing views dominate the field. One posits that the ability to establish at a site is determined by the availability of suitable microsites (establishment limitation), while the second asserts that recruitment is limited by the availability of seeds (seed limitation). An underlying problem is that establishment and seed limitation are typically viewed as mutually exclusive. We conducted a meta-analysis of seed addition experiments to assess the relative strength of establishment and seed limitation to seedling recruitment. We asked (1) To what degree are populations seed and establishment limited? (2) Under what conditions (e.g., habitats and life-history traits) are species more or less limited by each? (3) How can seed addition studies be better designed to enhance our understanding of plant recruitment? We found that, in keeping with previous studies, most species are seed limited. However, the effects of seed addition are typically small, and most added seeds fail to recruit to the seedling stage. As a result, establishment limitation is stronger than seed limitation. Seed limitation was greater for large-seeded species, species in disturbed microsites, and species with relatively short-lived seed banks. Most seed addition experiments cannot assess the relationship between number of seeds added and number of subsequent recruits. This shortcoming can be overcome by increasing the number and range of seed addition treatments.

An experimental test of dietary enzyme modulation in pine warblers Dendroica pinus.

Modulation of gut function is important in an ecological and evolutionary context because it likely determines what food items an animal can and cannot eat. We examined how diet affects activity of digestive enzymes in an omnivorous bird, the pine warbler (Dendroica pinus). Pine warblers were fed insect-based, fruit-based, and seed-based diets for approximately 54 d. We then measured activity of amylase, maltase, sucrase, aminopeptidase-N, trypsin, chymotrypsin, carboxypeptidase A, carboxypeptidase B, pancreatic lipase, and carboxyl ester lipase. We predicted that carbohydrase activities would be highest in birds fed the diet highest in carbohydrates (fruit based), protease activities would be highest in those fed the diet highest in protein (insect based), and lipase activities would be highest in those fed the diets highest in lipid (insect based and seed based). Also, we predicted that pine warblers would exhibit greater dietary modulation of enzyme activity than reported for a less omnivorous congener, the yellow-rumped warbler (Dendroica coronata). All predictions were upheld, supporting the hypothesis that pine warblers modulate the activity of digestive enzymes in proportion to demand from substrates in the diet.

Test, rejection, and reformulation of a chemical reactor-based model of gut function in a fruit-eating bird.

We explored modulation of retention time in cedar waxwings (Bombycilla cedrorum) by feeding them diets varying in hexose concentration. Our goals were to (1) test three predictions of a chemical reactor-based model of how guts might respond optimally to diet shifts; (2) determine whether modulation of retention time can occur quickly, thereby facilitating rapid changes in diet; (3) tease apart the relative influence of ingestion rate and nutrient concentration on retention time; and (4) examine the degree of axial mixing in the intestine and its relationship with retention time. The model's predictions were rejected: mean retention time did not decrease, ingestion rate did not increase, and glucose assimilation efficiency did not decrease with increased hexose concentration of the diet. Instead, birds displayed maximal intake rate at intermediate sugar concentration, and mouth to cloaca mean retention times increased with hexose concentration. Significant modulation of retention time occurred quickly, within 3 h of exposure to a different diet. Birds did equally well in terms of total energy assimilated on diets differing 3.3-fold in hexose concentration (from 500 mmol/L to 1660 mmol/L) but showed reduced intake when fed food with low hexose concentration (110 mmol/L). Far more variation in retention time was explained by direct effects of ingestion rate than by direct effects of hexose concentration. Finally, a gut dispersion index that measured degree of axial mixing was positively correlated with mean retention time, indicating that higher retention times are accompanied by increased axial mixing. We propose a modification of the assumptions of the original model. The resulting "osmotic constraint" model better captures the interaction between feeding rate and digestive function in fruit-eating birds.

Directed seed dispersal by bellbirds in a tropical cloud forest.

A fundamental goal of plant population ecology is to understand the consequences for plant fitness of seed dispersal by animals. Theories of seed dispersal and tropical forest regeneration suggest that the advantages of seed dispersal for most plants are escape from seed predation near the parent tree and colonization of vacant sites, the locations of which are unpredictable in space and time. Some plants may gain in fitness as a fortuitous consequence of disperser behavior if certain species of dispersers nonrandomly place seeds in sites predictably favorable for seedling establishment. Such patterns of directed dispersal by vertebrates long have been suggested but never demonstrated for tropical forest trees. Here we report the pattern of seed distribution and 1-year seedling survival generated by five species of birds for a neotropical, shade-tolerant tree. Four of the species dispersed seeds to sites near the parent trees with microhabitat characteristics similar to those at random locations, whereas the fifth species, a bellbird, predictably dispersed seeds under song perches in canopy gaps. The pattern of seedling recruitment was bimodal, with a peak near parent trees and a second peak, corresponding to bellbird song perches, far (>40 m) from parent trees. Seedling survival was higher for seeds dispersed by bellbirds than by the other species, because of a reduction in seedling mortality by fungal pathogens in gaps. Thus, bellbirds play a significant role in seed dispersal by providing directed dispersal to favorable sites and therefore may influence plant recruitment patterns and species diversity in Neotropical forests.

Secondary metabolites of fleshy vertebrate-dispersed fruits: adaptive hypotheses and implications for seed dispersal.

We discuss seven hypotheses to explain the adaptive significance of secondary metabolites in ripe fleshy fruits and their implications for seed dispersal. These hypotheses are the attraction/association, seed germination inhibition, attraction/repulsion, protein assimilation, gut retention time, directed toxicity, and defense trade-off hypotheses. We examine evidence that supports or refutes these hypotheses and suggest further tests of each. In addition, we summarize recent work with Solanum fruit pulp glycoalkaloids that bears directly on three of these hypotheses (directed toxicity, gut retention time, and defense trade-off). We conclude that evidence addressing many of these hypotheses is either observational or indirect, but most hypotheses find at least some level of support. Because many of the hypotheses are not mutually exclusive, we also conclude that synergistic interactions and multifunctionality in secondary metabolites may provide economical evolutionary solutions for plants facing disparate and temporally variable selective pressures that impinge on fruits and seeds.

Digestive modulation in a seasonal frugivore, the American robin (Turdus migratorius).

American robins (Turdus migratorius) switch from eating fruits in the fall to insects in the spring. Our objective was to determine the physiological and morphological changes associated with such a switch. Three nonexclusive hypotheses addressed possible mechanisms operating on different levels. First, we hypothesized that birds on the two diets would differ in intestinal absorption rates of sugars and amino acids. We predicted that individuals on a high-protein low-carbohydrate insect diet would exhibit higher proline and lower glucose absorption than individuals on a low-protein high-carbohydrate fruit-based diet. Uptake rates of glucose and proline were measured in vitro, using an everted sleeve technique. We found no significant differences in uptake between the two groups and so rejected the hypothesis. The second hypothesis, that retention time of digesta in the gut changes with diet, was tested using an inert marker (polyethylene glycol) injected into insects or fruit and fed to birds. We predicted and found that the marker was excreted significantly faster in birds eating fruit rather than insects. Thus this hypothesis is supported. The third hypothesis focused on changes in gut morphology as a basis for shifts in digestive processing. We found no differences in gut length, nominal surface area, or volume and so rejected this hypothesis. Note that hypotheses two and three are closely related, because retention time is proportional to gut volume/digesta flow. Because gut volume did not differ between the two groups, the difference in retention time must have been due to a change in flow. Taken together, these results suggest that short retention times are likely an important adaptation to frugivory.

Facultative ripening in Hamelia patens (Rubiaceae): effects of fruit removal and rotting.

In Costa Rica individual Hamelia patens trees produce fruit throughout the year and experience dramatic changes in rates of fruit removal and rotting. During some moths, most fruits rot because they are not removed. Rotting fruits increase the probability that other fruits on the same infructescence will rot. When removal rates are high, fruits are taken as soon as their seeds become viable but before the fruit is completely ripe. Experimental removal of fruits produced significantly higher ripening rates than on control infructescences. This response allows Hamelia to ripen more fruit and increase the number of fruits taken when dispersers are abundant (e.g., during migration). The proximate mechanism of this response probably includes reallocation of energy conserved when partially ripe fruits are removed. Responding to fluctuating disperser populations likely increases dispersal success and may function as the ultimate cause.