Threatened Peripheral Populations in Context: Geographical Variation in Population Frequency and Size and Sexual Reproduction in a Clonal Woody Shrub

Abstract:  Geographically peripheral populations of widespread species are often the focus of conservation because they are locally rare within political jurisdictions. Yet the ecology and genetics of these populations are rarely evaluated in a broader geographic context. Most expectations concerning the ecology and evolution of peripheral populations derive from the abundant-center model, which predicts that peripheral populations should be less frequent, smaller, less dense, and have a lower reproductive rate than central populations. We tested these predictions and in doing so evaluated the conservation value of peripheral populations for the clonal shrub Vaccinium stamineum L. (Ericaceae, deerberry), which is listed as threatened in Canada. Based on 51 populations sampled from the center to the northern range limits over 2 years, population frequency and size declined toward the range limit, but ramet density increased. Sexual reproductive output varied widely among populations and between years, with many populations producing very few seeds, but did not decline toward range margins. In fact seed mass increased steadily toward range limit, and this was associated with faster germination and seedling growth, which may be adaptive in seasonal northern environments. Our results did not support the prediction that clonal reproduction is more prevalent in peripheral populations or that it contributed antagonistically to the wide variation in seed production. Peripheral populations of V. stamineum are as productive as central populations and may be locally adapted to northern environments. This emphasizes the importance of a broad geographical perspective for evaluating the ecology, evolution, and conservation of peripheral populations.     

Bridging the generation gap in plants: pollination, parental fecundity, and offspring demography

Despite extensive study of pollination and plant reproduction on the one hand, and of plant demography on the other, we know remarkably little about links between seed production in successive generations, and hence about long-term population consequences of variation in pollination success. We bridged this "generation gap" in Ipomopsis aggregata, a long-lived semelparous wildflower that is pollinator limited, by adding varying densities of seeds to natural populations and following resulting plants through their entire life histories. To determine whether pollen limitation of seed production constrains rate of population growth in this species, we sowed seeds into replicated plots at a density that mimics typical pollination success and spacing of flowering plants in nature, and at twice that density to mimic full pollination. Per capita offspring survival, flower production, and contribution to population increase (lambda) did not decline with sowing density in this experiment, suggesting that typical I. aggregata populations freed from pollen limitation will grow over the short term. In a second experiment we addressed whether density dependence would eventually erase the growth benefits of full pollination, by sowing a 10-fold range of seed densities that falls within extremes estimated for the natural "seed rain" that reaches the soil surface. Per capita survival to flowering and age at flowering were again unaffected by sowing density, but offspring size, per capita flower production, and lambda declined with density. Such density dependence complicates efforts to predict population dynamics over the longer term, because it changes components of the life history (in this case fecundity) as a population grows. A complete understanding of how constraints on seed production affect long-term population growth will hinge on following offspring fates at least through flowering of the first offspring generation, and doing so for a realistic range of population densities.     

Are functional traits good predictors of demographic rates? Evidence from five neotropical forests

A central goal of comparative plant ecology is to understand how functional traits vary among species and to what extent this variation has adaptive value. Here we evaluate relationships between four functional traits (seed volume, specific leaf area, wood density, and adult stature) and two demographic attributes (diameter growth and tree mortality) for large trees of 240 tree species from five Neotropical forests. We evaluate how these key functional traits are related to survival and growth and whether similar relationships between traits and demography hold across different tropical forests. There was a tendency for a trade-off between growth and survival across rain forest tree species. Wood density, seed volume, and adult stature were significant predictors of growth and/or mortality. Both growth and mortality rates declined with an increase in wood density. This is consistent with greater construction costs and greater resistance to stem damage for denser wood. Growth and mortality rates also declined as seed volume increased. This is consistent with an adaptive syndrome in which species tolerant of low resource availability (in this case shade-tolerant species) have large seeds to establish successfully and low inherent growth and mortality rates. Growth increased and mortality decreased with an increase in adult stature, because taller species have a greater access to light and longer life spans. Specific leaf area was, surprisingly, only modestly informative for the performance of large trees and had ambiguous relationships with growth and survival. Single traits accounted for 9-55% of the interspecific variation in growth and mortality rates at individual sites. Significant correlations with demographic rates tended to be similar across forests and for phylogenetically independent contrasts as well as for cross-species analyses that treated each species as an independent observation. In combination, the morphological traits explained 41% of the variation in growth rate and 54% of the variation in mortality rate, with wood density being the best predictor of growth and mortality. Relationships between functional traits and demographic rates were statistically similar across a wide range of Neotropical forests. The consistency of these results strongly suggests that tropical rain forest species face similar trade-offs in different sites and converge on similar sets of solutions.     

Invasive insect abundance varies across the biogeographic distribution of a native host plant.

Studies of biogeographic variation in species abundances are fundamental to understanding and predicting the impacts of invasive exotic species. We quantified the abundance of the introduced and now invasive biocontrol weevil, Rhinocyllus conicus, on a newly adopted native host plant, Cirsium canescens (Platte thistle), across the plant's distributional range. We used regression and structural equation analyses to examine variation in weevil abundance at 92-108 sites over three years in relation to variation in abiotic and biotic parameters hypothesized to be important in insect or plant dynamics and distribution. We found that R. conicus now occurs throughout the majority of the range of C. canescens, even in the center of the native plant's distribution where its coevolved, targeted weed host (Carduus nutans, musk thistle) is absent. In fact, weevil densities were greater in the center of the native plant's distribution in the Sand Hills formation than in peripheral sand patches closer to areas where the targeted 'exotic thistle is common. None of the macroclimatic variables examined were consistent predictors of the large-scale variation in weevil abundance on C. canescens. In addition to biogeographic position, the only other consistent predictor of weevil densities across sites was the number of flower heads per C. canescens plant. These results exclude the "spillover" hypothesis to explain nontarget feeding on this newly adopted native host species. Instead, the results are consistent with the alternative hypothesis that exotic weevil abundance on C. canescens is related to the local availability of native floral resources. Because C. canescens densities have declined with increases in R. conicus at sites central in the plant's distribution, these results suggest that isolated, peripheral populations of C. canescens are likely to be critical for persistence of Platte thistle. More generally, this study suggests that the persistence of a native species that is impacted by an exotic natural enemy may require preservation of populations in habitats outside the optimal portion of the native species' distribution.     

Reproductive Success Increases with Local Density of Conspecif ics in a Desert Mustard (Lesquerella fendleri)

We investigated the effects of plant density on reproduction for an insect-pollinated desert mustard (Lesquerella fendleri [Brassicaceae]). Individual reproductive success, as measured by seeds per fruit, proportion of flowers setting fruit, and total seed production, increased with the density of conspecifics within 1 m. However, including the density of conspecifics at greater distances (1–3 m) did not significantly increase the amount of variation in reproductive success explained by the regression model. This implies that processes occurring on a scale of 1 m or less have important effects on reproduction. Total seed production also was greater for high-density plants than for otherwise similar plants with a low-density of conspecifics. We argue that increased pollinator visitation is the most likely cause of this facilitation and that investigations of the effects of rarity on reproductive success should directly consider density along with more commonly used attributes such as population size and fragmentation.     

Recovery Patterns of Understory Herbs and Their Use as Indicators of Deciduous Forest Regeneration

Abstract: Habitat fragmentation has reduced the richness of native species of forests in northeastern North America. Despite recent large-scale increases in forest cover, studies indicate that understory herbaceous plant communities may take many decades to recover. We studied recovery patterns of vegetation following up to 35 years of forest regeneration in restored former cottage and road sites at Point Pelée National Park, Ontario, Canada, to assess the vulnerability of the understory herbaceous species. Overall, there were no significant differences in the diversity of native species between restored and relatively undisturbed reference sites. There was, however, significant among-site variation in the composition of the native species component of these plant communities. When only restored sites were examined, variation in native species composition was associated with time since site restoration, soil moisture, canopy cover, and distance to continuous forest. Native species were assigned vulnerability rankings according to their relative occurrence in reference and restored sites. Spring-flowering herbs, with ant- or gravity-dispersed seeds, were absent from restored sites and were defined as highly vulnerable. In contrast, summer- and fall-flowering herbs, with vertebrate- and wind-dispersed seeds, dominated restored sites and were less vulnerable. Species of low and intermediate vulnerability had colonized restored sites successfully, and the latter should function as indicators of recovery. In contrast, species with high vulnerability rankings had not recovered at all and, because of their limited dispersal ranges, may recolonize restored sites only if they are actively reintroduced.     

A spatial gradient in the potential reproductive output of the sea mussel <Emphasis Type="Italic">Mytilus californianus</Emphasis>

Spatial variation in reproductive output from different populations within a region could have important consequences for recruitment, and cascading effects on populations and communities of marine species, but is rarely examined over meso-scales (i.e., tens to hundreds of kilometers). In this study, reproduction in the dominant mid-intertidal mussel, Mytilus californianus, was examined from sites spanning Point Conception, California over a 6-month period (March–August 2000). There was a dramatic geographic pattern in the relationship between size and potential reproductive output that was qualitatively similar across all 6 months sampled. Increases in allocation to reproductive tissue with increasing body size occurred at all sites, but the slope nearly doubled at sites south of Point Conception compared to northern sites. The spatial variation in size-specific reproductive output, coupled with additional spatial gradients in mussel density and size distributions, combined to increase total reproductive output by over eightfold at southern relative to northern sites. This study highlights the need to explicitly examine spatial patterns of reproductive output at these meso-scales, in order to better understand connectivity and source–sink dynamics in marine systems.     

Dispersal Can Limit Local Plant Distribution

The ability of species to establish new populations at unoccupied sites is a critical feature in the maintenance of biological diversity, and it has taken on new importance as a result of global climate change and expected changes in species distribution. To examine the dispersal potential of plant species, seeds of four annual plant species were experimentally dispersed 40 to 600 m from existing populations in Massachusetts (U.S.A.) to 34 nearby unoccupied but apparently suitable sites. At three of these sites new populations were established that persisted for four generations and expanded slowly in area. At seven sites, a small initial population eventually died out. At the 24 other sites, new populations did not become established, indicating that the sites were in some way unsuitable, that not enough seeds arrived, or that conditions suitable for seed germination do not occur every year. These results suggest that some species may be unable to disperse naturally out of their existing ranges in response to global climate change, particularly if habitat fragmentation creates barriers to dispersal. These species may have to be assisted to reach suitable sites nearby to prevent their extinction in the wild.     

Recruitment limitation constrains local species richness and productivity in dry grassland

Species coexistence and local-scale species richness are limited by the availability of seeds and microsites for germination and establishment. We conducted a seed addition experiment in seminatural grassland at three sites in southern Switzerland and repeated the experiment in two successive years to evaluate various circumstances under which seed limitation and establishment success affect community functioning. A collection of 144,000 seeds of 22 meadow species including grasses and forbs of local provenance was gathered, and seeds were individually sown in a density that resembled natural seed rain. The three communities were seed limited. Three years after sowing, single species varied in emergence (0-50%), survival (0-69%), and establishment rates (0-27%). One annual and 13 perennial species reached reproductive stage. Low establishment at one site and reduced growth at another site indicated stronger microsite limitation compared to the third site. Recruitment was influenced by differences in abiotic environmental conditions between sites (water availability, soil minerals) and by within-site differences in biotic interaction (competition). At the least water-limited site, sowing resulted in an increase in phytomass due to establishment of short-lived perennials in the second and third years after sowing. This increase persisted over the following two years due to establishment of longer-lived perennials. After sowing in a wetter year with higher phytomass, however, productivity did not increase, because higher intensity of competition in an early phase of establishment resulted in less vigorous plants later on. Due to the generally favorable weather conditions during this study, sowing year had a small effect on numbers of established individuals over all species. Recruitment limitation can thus constrain local-scale species richness and productivity, either by a lack of seeds or by reduced seedling growth, likely due to competition from the established vegetation.     

Genetic Structure of Fragmented Populations of the Endangered Daisy Rutidosis leptorrhynchoides

Abstract: The endangered grassland daisy Rutidosis leptorrhynchoides has been subject to severe habitat destruction and fragmentation over the past century. Using allozyme markers, we examined the genetic diversity and structure of 16 fragmented populations. The species had high genetic variation compared to other plant species, and both polymorphism and allelic richness showed strong positive relationships with log reproductive population size, reflecting a loss of rare alleles (frequency of q < 0.1) in smaller populations. Fixation coefficients were positively related to size, due either to a lack of rare homozygotes in small populations or to Wahlund effects (owing to spatial genetic structure) in large ones. Neither gene diversity nor heterozygosity was related to population size, and other population parameters such as density, spatial contagion, and isolation had no apparent effect on genetic variation. Genetic divergence among populations was low , despite a large north-to-south break in the species' current distribution. To preserve maximum genetic variation, conservation strategies should aim to maintain the five populations larger than 5000 reproductive plants, all of which occur in the north of the range, as well as the largest southern population of 626 plants at Truganina. Only one of these is currently under formal protection. High heterozygosity in smaller populations suggests that they are unlikely to be suffering from inbreeding depression and so are also valuable for conservation. Erosion of allelic richness at self-incompatibility loci, however, may limit the reproductive capacity of populations numbering less than 20 flowering plants.     

Individual- and population-level responses of a keystone predator to geographic variation in prey

Investigating how food supply regulates the behavior and population structure of predators remains a central focus of population and community ecology. These responses will determine the strength of bottom-up processes through the food web, which can potentially lead to coupled top-down regulation of local communities. However, characterizing the bottom-up effects of prey is difficult in the case of generalist predators and particularly with predators that have large dispersal scales, attributes that characterize most marine top predators. Here we use long-term data on mussel, barnacle, limpet, and other adult prey abundance and recruitment at sites spread over 970 km to investigate individual- and population-level responses of the keystone intertidal sunstar Heliaster helianthus on the coast of Chile. Our results show that this generalist predator responds to changes in the supply of an apparently preferred prey, the competitively dominant mussel Perumytilus purpuratus. Individual-level parameters (diet composition, per capita prey consumption, predator size) positively responded to increased mussel abundance and recruitment, whereas population-level parameters (density, biomass, size structure) did not respond to bottom-up prey variation among sites separated by a few kilometers. No other intertidal prey elicited positive individual predator responses in this species, even though a large number of other prey species was always included in the diet. Moreover, examining predator-prey correlations at approximately 80, 160, and 200 km did not change this pattern, suggesting that positive prey feedback could occur over even larger spatial scales or as a geographically unstructured process. Thus individual-level responses were not transferred to population changes over the range of spatial scales examined here, highlighting the need to examine community regulation processes over multiple spatial scales.     

Strong population differentiation of softshell clams (Mya arenaria) sampled across seven biogeographic marine ecoregions: possible selection and isolation by distance

Twenty-two Mya arenaria samples spanning seven marine ecoregions mostly situated in the Cold Temperate Northwest Atlantic (CTNA) biogeographic province were collected between 2001 and 2010 and genotyped at seven highly polymorphic microsatellite loci to test for population differentiation. Results showed strong regional differentiation with six genetic clusters: (1) Northern Gulf of St. Lawrence (GSL), (2) Magdalen Archipelago, (3) Southern GSL, (4) Lower Atlantic Canada, (5) US Coasts and (6) Northern Europe. Population structure was supported no matter the statistical approach and generally does not reflect the geographical limits of marine ecoregions. A latitudinal cline in allelic richness provides evidence for a northward post-glacial expansion range for this species. While geographical distance explains the genetic variation detected in southern CTNA, increased heterogeneity observed in northern CTNA can be explained by isolation by distance, marine landscaping and presumable selective processes acting at the Mar5 locus. Exclusion of Mar5 from analyses resulted in the detection of three genetic clusters instead of six.     

Integrating quality and quantity of mutualistic service to contrast ant species protecting Ferocactus wislizeni

Generalized, facultative mutualisms are often characterized by great variation in the benefits provided by different partner species. This variation may be due to differences among species in the quality and quantity of their interactions, as well as their phenology. Many plant species produce extrafloral nectar, a carbohydrate-rich resource, to attract ant species that can act as "bodyguards" against a plant's natural enemies. Here, we explore differences in the quality and quantity of protective service that ants can provide a plant by contrasting the four most common ant visitors to Ferocactus wislizeni, an extrafloral nectary-bearing cactus in southern Arizona. The four species differ in abundance when tending plants, and in the frequency at which they visit plants. By adding surrogate herbivores (Manduca sexta caterpillars) to plants, we demonstrate that all four species recruit to and attack potential herbivores. However, their per capita effectiveness in deterring herbivores (measured as the inverse of the number of workers needed to remove half of the experimentally added caterpillars) differs. Using these among-species differences in quality (per capita effectiveness) and quantity (number of workers that visit a plant and frequency of visitation), we accurately predicted the variation in fruit production among plants with different histories of ant tending. We found that plant benefits (herbivore removal and maturation of buds and fruits) typically saturated at high levels of ant protection, although plants could be "well defended" via different combinations of interaction frequency, numbers of ant workers per interaction, and per capita effects. Our study documents variation among prospective mutualists, distinguishes the components of this variation, and integrates these components into a predictive measure of protection benefit to the plant. The method we used to average saturating benefits over time could prove useful for quantifying overall service in other mutualisms.     

Relative size of Aristotle's lantern in Echinometra mathaei occuring at different densities

Like species of sea urchins in Zanzibar and Oregon (USA), Echinometra mathaei (de Blainville) at Rottnest Island, Western Australia, displays variation in the size of Aristotle's lantern relative to the maximum diameter of the test. This variation was associated with local variations in density of urchins at each of two sites in each of two years (1980 and 1981); this association with density was consistent with the proposal that relatively larger lanterns are a response to decreased food availability. Furthermore, variation of relative lantern size associated with local density was similar in magnitude to the variation displayed between sites and between years. This temporal variation demonstrated the plasticity of the relative lantern size over periods as short as 12 mo. Further experimental studies are required before relative length of lanterns can be used as estimates of food availability.     

Setbacks to shoot growth are common in woody plants, so how are shoots of some species safer than others?

Tissue turnover is a critical facet of plant life history variation. This study quantifies losses from setbacks to growth of terminal woody shoots 1.2m long, across 83 species and seven sites in eastern Australia. Setbacks, where the leading meristem had been removed or died and a new leader had emerged, were common (median three per shoot). Shoots had lost an average of 0.25 m of lead-stem length for 1.2 m net shoot-length gain. Insects like girdlers and borers were prominent causes of large setbacks. The sites spanned tropical to temperate and humid to semiarid climates, but variation in stem loss was much greater across species than across sites. We measured 17 plant functional traits related to growth form, mechanics, hydraulics, and economics. Only four traits were correlated with variation across species in stem losses: stem diameter, stem nitrogen content, bark thickness, and maximum photosynthetic rate. The correlations were weak. Stem specific gravity (wood density) showed no correlation with risk. Our results suggest a pattern similar to the growth risk trade-off known for herbaceous plants, where traits associated with fast growth increase tissue turnover and herbivory, but the weak correlations leave ample scope for other influences that remain to be identified.     

Seed availability and insect herbivory limit recruitment and adult density of native tall thistle

Understanding spatial and temporal variation in factors influencing plant regeneration is critical to predicting plant population growth. We experimentally evaluated seed limitation, insect herbivory, and their interaction in the regeneration and density of tall thistle (Cirsium altissimum) across a topographic ecosystem productivity gradient in tallgrass prairie over two years. On ridges and in valleys, we used a factorial experiment manipulating seed availability and insect herbivory to quantify effects of: seed input on seedling density, insect herbivory on juvenile density, and cumulative impacts of both seed input and herbivory on reproductive adult density. Seed addition increased seedling densities at three of five sites in 2006 and all five sites in 2007. Insect herbivory reduced seedling survival across all sites in both years, as well as rosette survival from the previous year's seedlings. In both years, insecticide treatment of seed addition plots led to greater adult tall thistle densities in the following year, reflecting the increase in juvenile thistle densities in the experimental year. Seedling survival was not density dependent. Our analytical projection model predicts a significant long-term increase in adult densities from seed input, with a greater increase under experimentally reduced insect herbivory. While plant community biomass and water stress varied significantly between ridges and valleys, the effects of seed addition and insect herbivory did not vary with gradient position. These results support conceptual models that predict seedling and adult densities of short-lived monocarpic perennial plants should be seed limited. Further, the experiment demonstrates that even at high juvenile plant densities, at which density dependence potentially could have overridden herbivore effects on plant survival, insect herbivory strongly affected juvenile thistle performance and adult densities of this native prairie species.     

Spatial and temporal patterns of predation on seeds of the surfgrass Phyllospadix torreyi

Spatial and temporal patterns of predation on seeds of the seagrass Phyllospadix torreyi S. Watson were quantified at four sites near Santa Barbara, California, USA. Over a period of four flowering seasons during 1995 to 1998, monthly patterns of seed fall and intensity of seed predation were similar among sites, but were temporally quite variable. Abundance of dispersed seeds varied greatly both among seasons and years. Within any one year, seeds were present in the environment every month, but they peaked in abundance during the fall months following the annual flowering period. Seeds were more abundant during the earlier years of the study. The intensity of predation steadily increased throughout the study period, from a low of ≤10% seeds consumed during 1995 to ∼50% consumption by 1997, and it was not correlated with abundance of seeds in the environment. Pre-dispersal seed loss also was estimated in two flowering seasons by counting the numbers of seeds consumed prior to release from the plant, and was relatively low (<15%). No differences were detected among the four study sites in patterns of pre-dispersal loss. Field surveys were done at two sites to identify potential seed predators. Three of the most abundant species identified in these surveys were tested in the laboratory to determine size-specific patterns of feeding activity and to assess which early life stages of P. torreyi (fruits within spadices, dehisced fruits, seedlings) were most vulnerable to predation. All three of the early life stages were consumed. The crabs Pugettiaproducta (Randall) and Pachygrapsus crassipes Randall were much more voracious predators than the isopod Idotea resecata Stimpson. Received: 8 June 1999 / Accepted: 2 February 2000     

Seed trait changes in dispersers' guts and consequences for germination and seedling growth

The effectiveness of a frugivore as a disperser of a plant is greatly determined by how fruits and seeds are handled in its mouth and its digestive tract. Although a number of studies have investigated the effect of avian ingestion on germination, we still know very little about the modifications to seeds during ingestion and the specific consequences on plant fitness. Here we investigate for the first time the different mechanisms by which germination patterns of seeds are modified following ingestion by frugivores. Specifically, we examine changes in seed mass, water content, permeability, seed coat thickness, texture, and resistance in two common Mediterranean fleshy-fruited plants, Phillyrea angustifolia and Myrtus communis, after ingestion by Eurasian Blackbirds, Turdus merula. We found a number of differences between the plant species: Phillyrea seeds lost mass, mainly due to water loss, and had thinner coats after gut passage, but Myrtus seeds did not. Seeds of both species showed increased permeability, while Myrtus seeds in particular became less resistant to breakage. No quantifiable changes in seed coat texture were detected in either species, although this trait was partly associated with differences in germination rate in Phillyrea. High intraspecific plant variation was found for most seed traits measured. Seed passage through birds' guts sped up germination in both species, especially in Myrtus. Increased permeability in seeds of both species following ingestion resulted in a higher germination rate. Moreover, seeds with thick coats (and in the case of Phillyrea, harder coats) germinated at a slower rate and produced seedlings that also grew more slowly, indicating a cost of coat thickness and/or hardness for seedling emergence. Results obtained here contribute to explaining the great heterogeneity in germination responses among and within plant species and the large variety of factors, both intrinsic and extrinsic to the plants, that influence such responses.     

Demography of central and marginal populations of monkeyflowers (Mimulus cardinalis and M. lewisii)

Every species occupies a limited geographic area, but how spatiotemporal environmental variation affects individual and population fitness to create range limits is not well understood. Because range boundaries arise where, on average, populations are more likely to go extinct than to persist, range limits are an inherently population-level problem for which a demographic framework is useful. In this study, I compare demographic parameters and population dynamics between central and marginal populations of monkeyflowers, Mimulus cardinalis and M. lewisii, along an elevation gradient spanning both species' ranges. Central and marginal populations of both species differed in survival and fecundity. For M. lewisii, these components of fitness were higher in central than in marginal populations, but for M. cardinalis the converse was true. To assess spatiotemporal variation in population dynamics, I used transition matrix models to estimate asymptotic population growth rates (lambda) and found that population growth rates of M. lewisii were highest at the range center and reduced at the range margin. Population growth rates of M. cardinalis were highest at the range margin and greatly reduced at the range center. Life table response analysis decomposed spatiotemporal variation in lambda into contributions from each transition between life stages, finding that transitions from large nonreproductive and reproductive plants to the seed class and stasis in the reproductive class made the largest contributions to spatial differences in lambda. These transitions had only low to moderate sensitivities, indicating that differences in projected population growth rates resulted mainly from observed differences in transition matrix parameters and their underlying vital rates.     

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.