Seed predation by Neotropical rain forest mammals increases diversity in seedling recruitment

Seed dispersal and seedling recruitment (the transition of seeds to seedlings) set the spatiotemporal distribution of new individuals in plant communities. Many terrestrial rain forest mammals consume post-dispersal seeds and seedlings, often inflicting density-dependent mortality. In part because of density-dependent mortality, diversity often increases during seedling recruitment, making it a critical stage for species coexistence. We determined how mammalian predators, adult tree abundance, and seed mass interact to affect seedling recruitment in a western Amazonian rain forest. We used exclosures that were selectively permeable to three size classes of mammals: mice and spiny rats (weighing <1 kg), medium-sized rodents (1-12 kg), and large mammals (20-200 kg). Into each exclosure, we placed seeds of 13 tree species and one canopy liana, which varied by an order of magnitude in adult abundance and seed mass. We followed the fates of the seeds and resulting seedlings for at least 17 months. We assessed the effect of each mammalian size class on seed survival, seedling survival and growth, and the density and diversity of the seedlings that survived to the end of the experiment. Surprisingly, large mammals had no detectable effect at any stage of seedling recruitment. In contrast, small- and medium-sized mammals significantly reduced seed survival, seedling survival, and seedling density. Furthermore, predation by small mammals increased species richness on a per-stem basis. This increase in diversity resulted from their disproportionately intense predation on common species and large-seeded species. Small mammals thereby generated a rare-species advantage in seedling recruitment, the critical ingredient for frequency dependence. Predation by small (and to a lesser extent, medium-sized) mammals on seeds and seedlings significantly increases tree species diversity in tropical forests. This is the first long-term study to dissect the effects of various mammalian predators on the recruitment of a diverse set of tree species.     

Herbivores on a dominant understory shrub increase local plant diversity in rain forest communities

Indirect effects of trophic interactions on biodiversity can be large and common, even in complex communities. Previous experiments with dominant understory Piper shrubs in a Costa Rican rain forest revealed that increases in herbivore densities on these shrubs caused widespread seedling mortality as a result of herbivores moving from Piper to seedlings of many different plant genera. We tested components of the Janzen-Connell hypothesis by conducting focused studies on the effects of specialist and generalist Piper herbivores on local seedling diversity. Whereas specialist herbivores are predicted to increase mortality to neighboring seedlings that are closely related to the source plant, true generalists moving from source plants may cause density-dependent mortality of many species, and possibly increase richness if new species replace abundant species that have been thinned by herbivores. Therefore, we hypothesized that seedling richness would be greater in understory control plots created in patches of Piper that had normal densities of generalist herbivores compared to plots from which we removed generalist herbivores manually from all Piper shrubs. After 15 months, generalist-herbivore-removal plots had > 40% fewer seedlings, > 40% fewer species, and 40% greater seedling evenness, on average, than control plots with generalist herbivores intact. Using a complementary approach in unmanipulated plots in four forests, we used path analysis to test for a positive association between seedling diversity and herbivore damage on Piper species. In unmanipulated plots, for both generalist and specialist herbivores, our data were significant fits to the causal model that Piper herbivores decrease evenness and increase plant species richness, corroborating the experimental results. Because herbivores changed how individuals were apportioned among the species and families present (lower evenness), one interpretation of these associations between herbivores on Piper shrubs and local seedling richness is that high seedling mortality in dominant families allowed the colonization or survival of less common species. If interspecific or apparent competition allowed for a relative increase in species richness, then the Janzen-Connell hypothesis may extend its predictions to generalist seedling predators. We speculate that apparent competition may explain some of the deviations from neutral model predictions, especially at small scales.     

Mutualism as reciprocal exploitation: African plant-ants defend foliar but not reproductive structures

The foundation of many plant-ant mutualisms is ant protection of plants from herbivores in exchange for food and/or shelter. While the role of symbiotic ants in protecting plants from stem- and leaf-feeding herbivores has been intensively studied, the relationship between ant defense and measures of plant fitness has seldom been quantified. We studied ant aggression, damage by herbivores and seed predators, and fruit production among Acacia drepanolobium trees occupied by four different acacia-ant species in an East African savanna. Levels of ant aggression in response to experimental disturbance differed strongly among the four species. All four ant species recruited more strongly to new leaf growth on host plants following disturbance, while recruitment to developing fruits was on average an order of magnitude lower. Host plants occupied by more aggressive ant species suffered significantly less vegetative damage from leaf-feeding insects, stem-boring beetles, and vertebrate browsers than host plants occupied by less aggressive ant species. However, there were no differences among fruiting host plants occupied by different ant species in levels of seed predation by bruchid seed predators. Fruit production on host trees was significantly correlated with tree stem diameter but not with the identity of resident ants. Our results demonstrate that defense of host plants may differ substantially among ant species and between vegetative and reproductive structures and that fruit production is not necessarily correlated with high levels of aggression by resident ants.     

Large Mammalian Herbivores and the Conservation of Arid Acacia Stands in the Middle East

Abstract: High mortality and poor recruitment in Acacia tree populations in many parts of the Middle East may result in loss of biodiversity. Human activities in recent decades have caused drastic changes in the water regime and the abundance of wild and domestic ungulates, which may negatively affect these trees. We studied the effects of large mammalian herbivores on the establishment of young Acacia raddiana and A. tortilis in the Arava Valley between the Red Sea and the Dead Sea, Israel. Seed accumulation under trees was high when large herbivores were excluded, and direct observations confirmed that ungulates were the main seed dispersers of these Acacia species. Insect seed predators (bruchid beetles) damaged more than 95% of seeds not consumed by ungulates. Seed germination was facilitated by gut passage through ungulates. Seedling survival was determined largely by water availability and was independent of herbivore density. Under present conditions, several years of high rainfall are necessary for successful establishment of young trees. Under severe browsing pressure by ungulates, growth in juvenile trees was delayed and smaller sizes were overrepresented. There was no evidence, however, of effects on the long-term demography of Acacia trees, perhaps because ungulates increased seedling densities by enhancing the viability and germination of seeds. We conclude that large mammalian herbivores are essential components of arid Acacia savannas and that wild and domestic ungulates must be included in future conservation plans.     

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.     

Invasive competitor and native seed predators contribute to rarity of the narrow endemic Astragalus sinuatus Piper

The conservation of rare plant species hinges on our ability to identify the underlying mechanisms that limit rare plant populations. Theory on rarity suggests that both predispersal seed predation and competition can be important mechanisms influencing abundance and/or distribution of rare plant populations. Yet few studies have tested these interactions, and those that have evaluated each mechanism independently. Astragalus sinuatus Piper (Whited's milkvetch) is a narrow endemic plant species restricted to eight populations within a 10-km2 area in eastern Washington. We used experimental and observational methods to test the effects of native insect predispersal seed predators and an invasive grass (Bromus tectorum L. [cheatgrass]) on seed set and population density of A. sinuatus. We quantified per capita seed production and pod predation rates across four sites and among four years. Seed predation rates were high across four sites (66-82%) and all years (65-82%). Experimental reduction of predispersal seed predators significantly increased per capita seed set of A. sinuatus (164-345%) at two experimental sites. Concurrently, two seed addition experiments demonstrated the effect of seed loss and presence of B. tectorum on seedling recruitment and establishment of A. sinuatus over four growing seasons. In the first seed addition experiment, we found no difference in recruitment and establishment between low (40) and high (120) seed addition levels. In the second addition experiment (one level of addition; 40 seeds), we found that recruitment and survivorship increased 200% in plots where B. tectorum was removed compared to plots where B. tectorum was present. Thus, seed addition had no impact in the presence of B. tectorum; conversely, in the absence of B. tectorum, seed addition was highly effective at increasing population numbers. Results suggest that, in areas where B. tectorum is present, recruitment is site limited, and it is seed limited when B. tectorum is absent. We recommend that managers reduce B. tectorum in an effort to increase population growth of A. sinuatus; in areas where B. tectorum is absent, short-term reduction of insect predators should be considered as a strategy to increase population growth of this rare species.     

Terrestrial vertebrates alter seedling composition and richness but not diversity in an Australian tropical rain forest

Although birds and mammals play important roles in several mechanisms hypothesized to maintain plant diversity in species-rich habitats, there have been few long-term, community-level tests of their importance. We excluded terrestrial birds and mammals from fourteen 6 x 7.5 m plots in Australian primary tropical rain forest and compared recruitment and survival of tree seedlings annually over the subsequent seven years to that on nearby open plots. We re-censused a subset of the plots after 13 years of vertebrate exclusion to test for longer-term effects. After two years of exclusion, seedling abundance was significantly higher (74%) on exclosure plots and remained so at each subsequent census. Richness was significantly higher on exclosure plots from 1998 to 2003, but in 2009 richness no longer differed, and rarefied species richness was higher in the presence of vertebrates. Shannon's diversity and Pielou's evenness did not differ in any year. Vertebrates marginally increased density-dependent mortality and recruitment limitation, but neither effect was great enough to increase richness or diversity on open plots relative to exclosure plots. Terrestrial vertebrates significantly altered seedling community composition, having particularly strong impacts on members of the Lauraceae. Overall, our results highlight that interactions between terrestrial vertebrates and tropical tree recruitment may not translate into strong community-level effects on diversity, especially over the short-term, despite significant impacts on individual species that result in altered species composition.     

Plant-Mammal Interactions in Tropical Bolivian Forests with Different Hunting Pressures

Abstract: We studied plant-animal interactions and vegetation structure in two geographically close tropical Bolivian forests subjected to different hunting intensities. We hypothesized that reduction of mammals openface> 1 kg in an "intensively hunted forest," compared with an "occasionally hunted forest," should correlate with decreased seed predation and seedling trampling, increased seedling survival and density, and decreased tree-species diversity at the seedling stage in relation to the adult stage. The occasionally hunted forest held 1.7 times as many mammalian species as the intensively hunted forest. As predicted, predation of Astrocaryum murumuru seeds was 34.2% lower in the intensively hunted forest. Similarly, trampling of model seedlings was 5.4 times lower and seedling survival was 1.15 times greater in the intensively hunted forest than that in the occasionally hunted forest. But the intensively hunted forest displayed lower seedling densities and a higher ratio of seedling diversity to tree diversity than did the occasionally hunted forest. Reduction of peccaries from the intensively hunted forest may explain much of the between-site differences in seed predation, trampling, and seedling survival. Lack of consistent differences in seedling density and diversity could mean that reduced granivory and trampling may be counteracted by reduced seed dispersal. The reduction of mammalian populations may produce a complex mosaic of forest patches with distinct degrees of structural change, depending on the intensity of defaunation.     

Predicting how defaunation-induced changes in seed predation and dispersal will affect tropical tree populations

The loss of large animals due to overhunting and habitat loss potentially affects tropical tree populations and carbon cycling. Trees reliant on large-bodied seed dispersers are thought to be particularly negatively affected by defaunation. But besides seed dispersal, defaunation can also increase or decrease seed predation. It remains unclear how these different defaunation effects on early life stages ultimately affect tree population dynamics. We reviewed the literature on how tropical animal loss affects different plant life stages, and we conducted a meta-analysis of how defaunation affects seed predation. We used this information to parameterize models that altered matrix projection models from a suite of tree species to simulate defaunation-caused changes in seed dispersal and predation. We assessed how applying these defaunation effects affected population growth rates. On average, population-level effects of defaunation were negligible, suggesting that defaunation may not cause the massive reductions in forest carbon storage that have been predicted. In contrast to previous hypotheses, we did not detect an effect of seed size on changes in seed predation rates. The change in seed predation did not differ significantly between exclosure experiments and observational studies, although the results of observational studies were far more variable. Although defaunation surely affects certain tree taxa, species that benefit or are harmed by it and net changes in forest carbon storage cannot currently be predicted based on available data. Further research on how factors such as seed predation vary across tree species and defaunation scenarios is necessary for understanding cascading changes in species composition and diversity.     

Widespread density-dependent seedling mortality promotes species coexistence in a highly diverse Amazonian rain forest

Negative density-dependent mortality can promote species coexistence through a spacing mechanism that prevents species from becoming too locally abundant. Negative density-dependent seedling mortality can be caused by interactions among seedlings or between seedlings and neighboring adults if the density of neighbors affects the strength of competition or facilitates the attack of natural enemies. We investigated the effects of seedling and adult neighborhoods on the survival of newly recruited seedlings for multiple cohorts of known age from 163 species in Yasuni National Park, Ecuador, an ever-wet, hyper-diverse lowland Amazonian rain forest. At local scales, we found a strong negative impact on first-year survival of conspecific seedling densities and adult abundance in multiple neighborhood sizes and a beneficial effect of a local tree neighborhood that is distantly related to the focal seedling. Once seedlings have survived their first year, they also benefit from a more phylogenetically dispersed seedling neighborhood. Across species, we did not find evidence that rare species have an advantage relative to more common species, or a community compensatory trend. These results suggest that the local biotic neighborhood is a strong influence on early seedling survival for species that range widely in their abundance and life history. These patterns in seedling survival demonstrate the role of density-dependent seedling dynamics in promoting and maintaining diversity in understory seedling assemblages. The assemblage-wide impacts of species abundance distributions may multiply with repeated cycles of recruitment and density-dependent seedling mortality and impact forest diversity or the abundance of individual species over longer time scales.     

Linking fruit traits to variation in predispersal vertebrate seed predation, insect seed predation, and pathogen attack

The importance of vertebrates, invertebrates, and pathogens for plant communities has long been recognized, but their absolute and relative importance in early recruitment of multiple coexisting tropical plant species has not been quantified. Further, little is known about the relationship of fruit traits to seed mortality due to natural enemies in tropical plants. To investigate the influences of vertebrates, invertebrates, and pathogens on reproduction of seven canopy plant species varying in fruit traits, we quantified reductions in fruit development and seed germination due to vertebrates, invertebrates, and fungal pathogens through experimental removal of these enemies using canopy exclosures, insecticide, and fungicide, respectively. We also measured morphological fruit traits hypothesized to mediate interactions of plants with natural enemies of seeds. Vertebrates, invertebrates, and fungi differentially affected predispersal seed mortality depending on the plant species. Fruit morphology explained some variation among species; species with larger fruit and less physical protection surrounding seeds exhibited greater negative effects of fungi on fruit development and germination and experienced reduced seed survival integrated over fruit development and germination in response to vertebrates. Within species, variation in seed size also contributed to variation in natural enemy effects on seed viability. Further, seedling growth was higher for seeds that developed in vertebrate exclosures for Anacardium excelsum and under the fungicide treatment for Castilla elastica, suggesting that predispersal effects of natural enemies may carry through to the seedling stage. This is the first experimental test of the relative effects of vertebrates, invertebrates, and pathogens on seed survival in the canopy. This study motivates further investigation to determine the generality of our results for plant communities. If there is strong variation in natural enemy attack among species related to differences in fruit morphology, then quantification of fruit traits will aid in predicting the outcomes of interactions between plants and their natural enemies. This is particularly important in tropical forests, where high species diversity makes it logistically impossible to study every plant life history stage of every species.     

Neutral theory and the evolution of ecological equivalence

Since the publication of the unified neutral theory in 2001, there has been much discussion of the theory, pro and con. The hypothesis of ecological equivalence is the fundamental yet controversial idea behind neutral theory. Assuming trophically similar species are demographically alike (symmetric) on a per capita basis is only an approximation, but it is equivalent to asking: How many of the patterns of ecological communities are the result of species similarities, rather than of species differences? The strategy behind neutral theory is to see how far one can get with the simplification of assuming ecological equivalence before introducing more complexity. In another paper, I review the empirical evidence that led me to hypothesize ecological equivalence among many of the tree species in the species-rich tropical forest on Barro Colorado Island (BCI). In this paper, I develop a simple model for the evolution of ecological equivalence or niche convergence, using as an example evolution of the suite of life history traits characteristic of shade tolerant tropical tree species. Although the model is simple, the conclusions from it seem likely to be robust. I conclude that ecological equivalence for resource use are likely to evolve easily and often, especially in species-rich communities that are dispersal and recruitment limited. In the case of the BCI forest, tree species are strongly dispersal- and recruitment-limited, not only because of restricted seed dispersal, but also because of low recruitment success due to heavy losses of the seedling stages to predators and pathogens and other abiotic stresses such as drought. These factors and the high species richness of the community strongly reduce the potential for competitive exclusion of functionally equivalent or nearly equivalent species.     

Consequences of patch reef spacing for density-dependent mortality of coral-reef fishes

The spatial configuration of habitat patches can profoundly affect a number of ecological interactions, including those between predators and prey. I examined the effects of reef spacing on predator-prey interactions within coral-reef fish assemblages in the Bahamas. Using manipulative field experiments, I determined that reef spacing influences whether and how density-dependent predation occurs. Mortality rates of juveniles of two ecologically dissimilar species (beaugregory damselfish and yellowhead wrasse) were similarly affected by reef spacing; for both species, mortality was density dependent on reef patches that were spatially isolated (separated by 50 m), and density independent on reef patches that were aggregated (separated by 5 m). A subsequent experiment with the damselfish demonstrated that a common resident predator (coney) caused a substantial proportion of the observed mortality, independent of reef spacing. Compared to isolated reefs, aggregated reefs were much more likely to be visited by transient predators (mostly yellowtail snappers), regardless of prey density, and on these reefs, mortality rates approached 100% for both prey species. Transient predators exhibited neither an aggregative response nor a type 3 functional response, and consequently were not the source of density dependence observed on the isolated reefs. These patterns suggest that resident predators caused density-dependent mortality in their prey through type 3 functional responses on all reefs, but on aggregated reefs, this density dependence was overwhelmed by high, density-independent mortality caused by transient predators. Thus, the spatial configuration of reef habitat affected both the magnitude of total predation and the existence of density-dependent mortality. The combined effects of the increasing fragmentation of coral reef habitats at numerous scales and global declines in predatory fish may have important consequences for the regulation of resident fish populations.     

Effects of Forest Fragmentation on Seed Dispersal and Seedling Establishment in Ornithochorous Trees

Abstract: Habitat fragmentation increases seed dispersal limitation across the landscape and may also affect subsequent demographic stages such as seedling establishment. Thus, the development of adequate plans for forest restoration requires an understanding of mechanisms by which fragmentation hampers seed delivery to deforested areas and knowledge of how fragmentation affects the relationship between seed‐deposition patterns and seedling establishment. We evaluated the dispersal and recruitment of two bird‐dispersed, fleshy‐fruited tree species (Crataegus monogyna and Ilex aquifolium) in fragmented secondary forests of northern Spain. Forest fragmentation reduced the probability of seed deposition for both trees because of decreased availability of woody perches and fruit‐rich neighborhoods for seed dispersers, rather than because of reductions in tree cover by itself. The effects of fragmentation went beyond effects on the dispersal stage in Crataegus because seedling establishment was proportional to the quantities of bird‐dispersed seeds arriving at microsites. In contrast, postdispersal mortality in Ilex was so high that it obscured the seed‐to‐seedling transition. These results suggest that the effects of fragmentation are not necessarily consistent across stages of recruitment across species. Habitat management seeking to overcome barriers to forest recovery must include the preservation, and even the planting, of fleshy‐fruited trees in the unforested matrix as a measure to encourage frugivorous birds to enter into open and degraded areas. An integrative management strategy should also explicitly consider seed‐survival expectancies at microhabitats to preserve plant‐population dynamics and community structure in fragmented landscapes.     

Weed-biocontrol insects reduce native-plant recruitment through second-order apparent competition

Small-mammal seed predation is an important force structuring native-plant communities that may also influence exotic-plant invasions. In the intermountain West, deer mice (Peromyscus maniculatus) are prominent predators of native-plant seeds, but they avoid consuming seeds of certain widespread invasives like spotted knapweed (Centaurea maculosa). These mice also consume the biological-control insects Urophora spp. introduced to control C. maculosa, and this food resource substantially increases deer mouse populations. Thus, mice may play an important role in the invasion and management of C. maculosa through food-web interactions. We examined deer mouse seed predation and its effects on seedling emergence and establishment of a dominant native grass, Pseudoroegneria spicata, and forb, Balsamorhiza sagittata, in C. maculosa-invaded grasslands that were treated with herbicide to suppress C. maculosa or left untreated as controls. Deer mice readily took seeds of both native plants but removed 2-20 times more of the larger B. sagittata seeds than the smaller P. spicata seeds. Seed predation reduced emergence and establishment of both species but had greater impacts on B. sagittata. The intensity of seed predation corresponded with annual and seasonal changes in deer mouse abundance, suggesting that abundance largely determined mouse impacts on native-plant seeds. Accordingly, herbicide treatments that reduced mouse abundance by suppressing C. maculosa and its associated biocontrol food subsidies to mice also reduced seed predation and decreased the impact of deer mice on B. sagittata establishment. These results provide evidence that Urophora biocontrol agents may exacerbate the negative effects of C. maculosa on native plants through a form of second-order apparent competition-a biocontrol indirect effect that has not been previously documented. Herbicide suppressed C. maculosa and Urophora, reducing mouse populations and moderating seed predation on native plants, but the herbicide's direct negative effects on native forb seedlings overwhelmed the indirect positive effect of reducing deer mouse seed predation. By manipulating this four-level food chain, we illustrate that host-specific biological control agents may impact nontarget plant species through food-web interactions, and herbicides may influence management outcomes through indirect trophic interactions in addition to their direct effects on plants.     

Bottom-up multitrophic effects in resprouting plants

Severe damage often provokes compensatory resprouting of plants, which commonly modify plant morphological and phenological traits. Rapid plant growth often results in poorly defended nutrient-rich foliage, which is more susceptible to foliar-chewing herbivores. It is less known how other guilds of arthropods are affected by plant regrowth. We tested the hypotheses that clipping-induced resprouting and nutrient availability, separately and in combination, would (1) influence plant traits, (2) benefit chewing herbivores, sap-suckers, gallers, and pre-dispersal seed predators, and (3) cascade up to the third trophic level by positively affecting herbivores. Resprouted plants were morphologically and phenologically different from undamaged plants; as a result, seed predation, infestation rate, richness, and diversity of seed predators increased, and species composition was altered. Leaf consumption by chewing herbivores was four times higher on resprouted plants. The number of galls decreased, whereas the abundance of sap-sucking and leaf-chewing insects was not affected. The incidence of predators and parasitoids was also higher on resprouted plants and on plants with nutrients added, but the increase was less pronounced compared to the herbivores they feed on. Thus, the effects of resprouting, contingent on nutrient availability, can propagate simultaneously through two independent tri-trophic level pathways.     

Indirect effects of prey swamping: differential seed predation during a bamboo masting event

Resource pulses often involve extraordinary increases in prey availability that "swamp" consumers and reverberate through indirect interactions affecting other community members. We developed a model that predicts predator-mediated indirect effects induced by an epidemic prey on co-occurring prey types differing in relative profitability/preference and validated our model by examining current-season and delayed effects of a bamboo mass seeding event on seed survival of canopy tree species in mixed Patagonian forests. The model shows that predator foraging behavior, prey profitability, and the scale of prey swamping influence the character and strength of short-term indirect effects on various alternative prey. When in large prey-swamped patches, nonselective predators decrease predation on all prey types. Selective predators, instead, only benefit prey of similar quality to the swamping species, while very low or high preference prey remain unaffected. Negative indirect effects (apparent competition) may override such positive effects (apparent mutualism), especially for highly preferred prey, when prey-swamped patches are small enough to allow predator aggregation and/or predators show a reproductive numerical response to elevated food supply. Seed predation patterns during bamboo (Chusquea culeou) masting were consistent with predicted short-term indirect effects mediated by a selective predator foraging in large prey-swamped patches. Bamboo seeds and similarly-sized Austrocedrus chilensis (ciprés) and Nothofagus obliqua (roble) seeds suffered lower predation in bamboo flowered than nonflowered patches. Predation rates on the small-seeded Nothofagus dombeyi (coihue) and the large-seeded Nothofagus alpina (rauli) were independent of bamboo flowering. Indirect positive effects were transient; three months after bamboo seeding, granivores preyed heavily upon all seed types, irrespective of patch flowering condition. Moreover, one year after bamboo seeding, predation rates on the most preferred seed (rauli) was higher in flowered than in nonflowered patches. Despite rapid predator numerical responses, short-term positive effects can still influence community recruitment dynamics because surviving seeds may find refuge beneath the litter produced by bamboo dieback. Together, our theoretical analysis and experiments indicate that indirect effects experienced by alternative prey during and after prey-swamping episodes need not be universal but can change across a prey quality spectrum, and they critically depend on predator-foraging rules and the spatial scale of swamping.     

Tropical forest restoration: tree islands as recruitment foci in degraded lands of Honduras.

Tropical forest recovery in pastures is slowed by a number of biotic and abiotic factors, including a lack of adequate seed dispersal and harsh microclimatic extremes. Accordingly, methods to accelerate forest recovery must address multiple impediments. Here, we evaluated the ability of "tree islands" to serve as "recruitment foci" in a two-year study at three sites in northern Honduras. Islands of three sizes (64, 16, and 4 m2) and at two distances to secondary forest (20 and 50 m) were created by planting 2 m tall vegetative stakes of two native species: Gliricidia sepium (Fabaceae) and Bursera simaruba (Burseraceae), each in monoculture. Open-pasture "islands" of equal sizes served as controls. Tree islands reduced temperature and light (PAR) extremes as compared to open pasture, creating a microenvironment more favorable to seedling establishment. Seed-dispersing birds (quantified at one site only) showed an overwhelming preference for islands; 160 visits were recorded to islands compared with one visit to open pasture. Additionally, frugivores visited large islands more often, and for longer time periods, than small islands, thereby increasing the likelihood of a dispersal event there. In total, 144 140 seeds belonging to 186 species were collected in islands; more than 80% were grasses. Tree islands increased zoochorous tree seed rain; seed density and species richness were greater in tree islands than in open pasture, and large islands had greater seed density than smaller islands (Gliricidia only), suggesting that they are more effective for restoration. Distance to forest did not affect seed rain. A total of 543 seedlings and 41 species established in islands; > 85% were zoochorous. Seedling density did not differ among treatments (mean 0.2 seedlings/m2 for islands vs. 0.1 seedlings/m2 for pasture), although an increasing trend in tree islands over the course of two years suggests that seedling recruitment is accelerated there. Lastly, similar seedling densities were censused in the 1 m perimeter surrounding islands, suggesting that islands can expand outward into pasture. Planting vegetative stakes to create tree islands in pastures accelerates forest recovery by overcoming a number of impediments, and presents a simple, broadly applicable alternative for facilitating forest regeneration in abandoned pastures.     

Density dependence in marine fish populations revealed at small and large spatial scales

Experimental manipulation of population density has frequently been used to demonstrate demographic density dependence. However, such studies are usually small scale and typically provide evidence of spatial (within-generation) density dependence. It is often unclear whether small-scale, experimental tests of spatial density dependence will accurately describe temporal (between-generation) density dependence required for population regulation. Understanding the mechanisms generating density dependence may provide a link between spatial experiments and temporal regulation of populations. In this study, I manipulated the density of recently settled kelp rockfish (Sebastes atrovirens) in both the presence and absence of predators to test for density-dependent mortality and whether predation was the mechanism responsible. I also examined mortality of rockfish cohorts within kelp beds throughout central California to evaluate temporal (between-generation) density dependence in mortality. Experiments suggested that short-term behavioral responses of predators and/or a shortage of prey refuges caused spatial density dependence. Temporal density dependence in mortality was also detected at larger spatial scales for several species of rockfish. It is likely that short-term responses of predators generated both spatial and temporal density dependence in mortality. Spatial experiments that describe the causal mechanisms generating density dependence may therefore be valuable in describing temporal density dependence and population regulation.     

The disruption of an ant-aphid mutualism increases the effects of birds on pine herbivores

Predators affect herbivores directly and indirectly, by consumptive and nonconsumptive effects, and the combined influence of multiple predators is shaped by interactions among predators. I documented the individual and combined effects of birds (chickadees, nuthatches, warblers) and ants (Formica podzolica) on arthropods residing in pine (Pinus ponderosa) canopies in a factorial field experiment. Birds and ants removed herbivores but simultaneously benefited them by removing predatory arthropods. Birds and ants had net negative and positive effects, respectively, on the abundance of herbivore prey, supporting the notion that vertebrate predators have stronger negative effects on herbivores than do arthropod predators. Aphids (ant-tended and untended species) constituted three-quarters of herbivore biomass. The effect of birds on ant-tended aphids was twice that on untended aphid species or tended aphid species without ants. This was not due to there being more ant-tended aphids for birds to prey on; tended and untended aphid species were in similar abundances in the absence of birds. Instead, the effects of birds were strengthened by attributes of the mutualism that rendered tended aphids susceptible to predation. These dynamics led to nonadditive effects of birds and ants: birds only reduced tended aphid species and total herbivore abundances on trees with ants, while ants only increased tended aphid species and total herbivore abundances in the absence of birds. Consequently, top predators in this system only influenced total herbivore abundance when they disrupted an ant-aphid mutualism.