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.     

Population size affects vital rates but not population growth rate of a perennial plant

Negative effects of habitat fragmentation on individual performance have been widely documented, but relatively little is known about how simultaneous effects on multiple vital rates translate into effects on population viability in long-lived species. In this study, we examined relationships between population size, individual growth, survival and reproduction, and population growth rate in the perennial plant Phyteuma spicatum. Population size positively affected the growth of seedlings, the survival of juveniles, the proportion of adults flowering, and potential seed production. Analyses with integral projection models, however, showed no relationship between population size and population growth rate. This was due to the fact that herbivores and pathogens eliminated the relationship between population size and seed production, and that population growth rate was not sensitive to changes in the vital rates that varied with population size. We conclude that effects of population size on vital rates must not translate into effects on population growth rate, and that populations of long-lived organisms may partly be able to buffer negative effects of small population size on vital rates that have a relatively small influence on population growth rate. Our study illustrates that we need to be cautious when assessing the consequences of habitat fragmentation for population viability based on effects on only one or a few vital rates.     

Habitat-specific impacts of multiple consumers on plant population dynamics

Multiple consumers often attack seeds, seedlings, and adult plants, but their population-level consequences remain uncertain. We examined how insect and small mammal consumers influenced the demography and abundance of the perennial shrub, bush lupine (Lupinus arboreus). In grassland and dune habitats we established replicate experimental lupine populations in 81-m2 plots that were either protected from, or exposed to, herbivorous voles and granivorous mice (via fencing) and/or root feeding insects (via insecticide treatment). Populations were initiated with transplanted seedlings in 1999 and 2000. We followed the demography of these cohorts, subsequent generations, and the seed bank for 5.5 years. Voles and insects killed many seedlings in dune (1999 only) and grassland (1999 and 2000) habitats. After 2000, insects and voles had minimal effects on seedling or adult survival. Seed predation by granivorous mice, however, greatly depressed seedling recruitment, resulting in lower adult lupine abundance in control plots vs. those protected from rodents. In grasslands, initial effects of voles and insects on seedling survival produced large differences among treatments in adult plant density and the cumulative number of seeds produced throughout the experiment. Differences among grassland populations in seed rain, however, had little influence on the magnitude of seedling recruitment into this habitat. Instead, recruitment out of a preexisting seed bank compensated for the lack of seed production in populations exposed to consumers. Shading by dense adults in plots protected from consumers limited seedling establishment within these populations. Although differences among populations in cumulative seed rain did not influence adult establishment, populations protected from consumers accumulated substantially larger seed banks than controls. These results illustrate how density dependence, habitat-specific seed dynamics, and particular demographic impacts of consumers interact to shape plant population responses to consumers.     

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.     

Biotic resistance via granivory: establishment by invasive, naturalized, and native asters reflects generalist preference

Escape from specialist natural enemies is frequently invoked to explain exotic plant invasions, but little attention has been paid to how generalist consumers in the recipient range may influence invasion. We examined how seed preferences of the widespread generalist granivore Peromyscus maniculatus related to recruitment of the strongly invasive exotic Centaurea stoebe and several weakly invasive exotics and natives by conducting laboratory feeding trials and seed addition experiments in the field. Laboratory feeding trials showed that P. maniculatus avoided consuming seeds of C. stoebe relative to the 12 other species tested, even when seeds of alternative species were 53-94% smaller than those of C. stoebe. Seed addition experiments conducted in and out of rodent exclosures revealed that weakly invasive exotics experienced relatively greater release from seed predation than C. stoebe, although this was not the case for natives. Seed mass explained 81% of the variation in recruitment associated with rodent exclusion for natives and weak invaders, with larger-seeded species benefiting most from protection from granivores. However, recruitment of C. stoebe was unaffected by rodent exclusion, even though the regression model predicted seeds of correspondingly large mass should experience substantial predation. These combined laboratory and field results suggest that generalist granivores can be an important biological filter in plant communities and that species-specific seed attributes that determine seed predation may help to explain variation in native plant recruitment and the success of exotic species invasions.     

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.     

Evidence for life history changes in high-altitude populations of three perennial forbs

Relatively little is known about how the life histories of perennial forb species, and especially their lifetime patterns of growth, vary across environmental gradients. We used a post hoc approach (herb-chronology) to determine plant age and previous growth (width of successive annual rings in roots) in three species of perennial forb (two long-lived species [Penstemon venustus, Lupinus laxiflorus] and one short-lived [Rudbeckia occidentalis]) along a 1000-m altitudinal gradient in the Wallowa Mountains (northeast Oregon, USA). Plants from the highest altitude tended to be considerably older and produced up to five times as many flowering shoots as lowland plants. In addition, mean ring widths of high-altitude plants were about half those of lowland plants. In plants from low and intermediate altitudes, ring width either decreased linearly or varied inconsistently during the life of the plant. In contrast, ring widths of high-altitude plants increased at first and later decreased, resulting in curvilinear growth trajectories that were highly consistent among species. Together, these data for three ecologically distinct forb species provide evidence of a consistent shift toward more conservative and strongly constrained life histories at higher altitudes. More generally, the results indicate the possible importance of changes in selection pressures across strong environmental gradients on life history strategies within a single species.     

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.     

Accelerating Forest Succession in a Fragmented Landscape: The Role of Birds and Perches

Previous research suggests that in highly fragmented forest landscapes ecological succession can be arrested by lack of seeds, but that seed deposition abundance and diversity of bird-dispersed plants can be enhanced by bird-attracting structures such as snags. Consequently, bird perches remain a potential tool for accelerating ecological succession and reforesting disturbed land. Consequently, in order to determine the effectiveness of bird perches in reclaiming forested landscapes, seed dispersal, seedbank storage, and recruitment of bird-dispersed plants was studied on a central Florida mined site with clay-rich soil undergoing primary succession over a seven-year period. Data collection included 20 continuous months of seed dispersal data, an analysis of the total and germinable seedbanks, and plant recruitment at one and two years after a fire destroyed perches and burnt vegetation. Seed dispersal to perches reached a peak seedfall by weight in August, which was attributable to nonmigratory birds. Myrica cerifera, the most abundant species dispersed to the sites, was the only species dispersed during the winter and spring months, and it may be a keystone species for the frugivorous bird guild in central Florida. Seedfall beneath perches had a higher diversity of seed genera, and seed numbers (340 seeds m⁻² yr⁻¹) were 150 times greater than in sites without perches. Seeds of bird-dispersed plants in the seedbank under perches numbered 77 ± 33 (m⁻²) in total and 17 ± 5 for the viable seedbank. The population density of bird-dispersed plants was 1.4 and 2.0 plants m⁻² at one and two years afler the fire. Less than 0.06% of the dispersed seeds survived to become seedlings. Species composition shifted from seedfall to seedlings, with small-seeded, early-successional (r-selected) shrubs and herbs becoming relatively more common than the desired large-seeded, late-successional (K-selected) tree species. Perches attracted birds and associated seeds, but the physically harsh conditions created by primary succession and/or high predation on seeds appeared to reduce the success of the desired late-successional plant species. Nonetheless, there was a higher abundance and diversity of bird-dispersed plants under perches, suggesting that perch structures have a limited ability to enhance plant diversity under conditions of primary succession.     

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.     

Conserving Slow-Growing, Long-Lived Tree Species: Input from the Demography of a Rare Understory Conifer, Taxus floridana

Abstract:  Although land preservation and promotion of successful regeneration are important conservation actions, their ability to increase population growth rates of slow-growing, long-lived trees is limited. We investigated the demography of Taxus floridana Nutt., a rare understory conifer, in three populations in different ravine forests spanning its entire geographic range along the Apalachicola River Bluffs in northern Florida (U.S.A.). We examined spatial and temporal patterns in demographic parameters and projected population growth rates by using four years of data on the recruitment and survival of seedlings and established stems, and on diameter growth from cross-sections of dead stems. All populations experienced a roughly 10-fold increase in seedling recruitment in 1996 compared with other years. The fates of seedlings and stems between 8 and 16 mm differed among populations. The fates of stems in two other size classes (the 2- to 4-mm class and the 4- to 8-mm class) differed among both populations and years. Individual stems in all populations exhibited similarly slow growth rates. Stochastic matrix models projected declines in all populations. Stochastic matrix analysis revealed the high elasticity of a measure of stochastic population growth rate to perturbations in the stasis of large reproductive stems for all populations. Additional analyses also indicated that occasional episodes of high recruitment do not greatly affect population growth rates. Conservation efforts directed at long-lived, slow-growing rare plants like Taxus floridana should both protect established reproductive individuals and further enhance survival of individuals in other life-history stages, such as juveniles, that often do not appear to contribute greatly to population growth rates.     

The impact of invasive grasses on the population growth of Anemone patens, a long-lived native forb

Negative impacts of invasive plants on natives have been well documented, but much less is known about whether invasive plants can cause population level declines. We used demographic models to investigate the effects of two invasive grasses on the demography and population growth of Anemone patens, a long-lived native perennial of North American grasslands. Demographic data of A. patens growing in patches characterized by Bromus inermis, Poa pratensis, or native grasses were used to parameterize integral projection models. Models based on both average conditions and those allowing for environmental stochasticity indicate that A. patens is slowly increasing in patches of native grass (lambda = 1.02) and declining in patches of invasive grasses, particularly those dominated by B. inermis (lambda = 0.93). Extinction probabilities indicate that A. patens should persist in native grass patches, but has a much higher probability of extinction in Bromus patches compared to Poa patches. While sensitivity analyses showed that survival had the biggest effect on population growth rates in all habitats, results of a Life Table Response Experiment (LTRE) revealed that slower individual growth rates in patches of invasive grasses contributed the most to the observed reduction in population growth. These results suggest that invasive grasses may cause slow declines in A. patens, despite short-term coexistence, and that controlling B. inermis only would not be sufficient to ensure A. patens persistence.     

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.     

Importance of individual and environmental variation for invasive species spread: a spatial integral projection model

Plant survival, growth, and flowering are size dependent in many plant populations but also vary among individuals of the same size. This individual variation, along with variation in dispersal caused by differences in, e.g., seed release height, seed characteristics, and wind speed, is a key determinant of the spread rate of species through homogeneous landscapes. Here we develop spatial integral projection models (SIPMs) that include both demography and dispersal with continuous state variables. The advantage of this novel approach over discrete-stage spread models is that the effect of variation in plant size and size-dependent vital rates can be studied at much higher resolution. Comparing Neubert-Caswell matrix models to SIPMs allowed us to assess the importance of including individual variation in the models. As a test case we parameterized a SIPM with previously published data on the invasive monocarpic thistle Carduus nutans in New Zealand. Spread rate (c*) estimates were 34% lower than for standard spatial matrix models and stabilized with as few as seven evenly distributed size classes. The SIPM allowed us to calculate spread rate elasticities over the range of plant sizes, showing the size range of seedlings that contributed most to c* through their survival, growth and reproduction. The annual transitions of these seedlings were also the most important ones for local population growth (lambda). However, seedlings that reproduced within a year contributed relatively more to c* than to lambda. In contrast, plants that grow over several years to reach a large size and produce many more seeds, contributed relatively more to lambda than to c*. We show that matrix models pick up some of these details, while other details disappear within wide size classes. Our results show that SIPMs integrate various sources of variation much better than discrete-stage matrix models. Simpler, heuristic models, however, remain very valuable in studies where the main goal is to investigate the general impact of a life history stage on population dynamics. We conclude with a discussion of future extensions of SIPMs, including incorporation of continuous time and environmental drivers.     

Effects of life history and reproduction on recruitment time lags in reintroductions of rare plants

Reintroductions are important components of conservation and recovery programs for rare plant species, but their long-term success rates are poorly understood. Previous reviews of plant reintroductions focused on short-term (e.g., ≤3 years) survival and flowering of founder individuals rather than on benchmarks of intergenerational persistence, such as seedling recruitment. However, short-term metrics may obscure outcomes because the unique demographic properties of reintroductions, including small size and unstable stage structure, could create lags in population growth. We used time-to-event analysis on a database of unusually well-monitored and long-term (4–28 years) reintroductions of 27 rare plant species to test whether life-history traits and population characteristics of reintroductions create time-lagged responses in seedling recruitment (i.e., recruitment time lags [RTLs]), an important benchmark of success and indicator of persistence in reintroduced populations. Recruitment time lags were highly variable among reintroductions, ranging from <1 to 17 years after installation. Recruitment patterns matched predictions from life-history theory with short-lived species (fast species) exhibiting consistently shorter and less variable RTLs than long-lived species (slow species). Long RTLs occurred in long-lived herbs, especially in grasslands, whereas short RTLs occurred in short-lived subtropical woody plants and annual herbs. Across plant life histories, as reproductive adult abundance increased, RTLs decreased. Highly variable RTLs were observed in species with multiple reintroduction events, suggesting local processes are just as important as life-history strategy in determining reintroduction outcomes. Time lags in restoration outcomes highlight the need to scale success benchmarks in reintroduction monitoring programs with plant life-history strategies and the unique demographic properties of restored populations. Drawing conclusions on the long-term success of plant reintroduction programs is premature given that demographic processes in species with slow life-histories take decades to unfold.     

Seed and establishment limitation contribute to long-term native forb declines in California grasslands

The effects of exotic species invasions on biodiversity vary with spatial scale, and documentation of local-scale changes in biodiversity following invasion is generally lacking. Coupling long-term observations of local community dynamics with experiments to determine the role played by exotic species in recruitment limitation of native species would inform both our understanding of exotic impacts on natives at local scales and regional-scale management efforts to promote native persistence. We used field experimentation to quantify propagule and establishment limitation in a suite of native annual forbs in a California reserve, and compared these findings to species abundance trends within the same sites over the past 48 years. Observations at 11 paired sites (inside and outside the reserve) indicated that exotic annual plants have continued to increase in abundance over the past 48 years. This trend suggests the system has not reached equilibrium > 250 years after exotic species began to spread, and 70 years after livestock grazing ceased within the reserve. Long-term monitoring observations also indicated that six native annual forb species went extinct from more local populations than were colonized. To determine the potential role of exotic species in these native plant declines, we added seed of these species into plots adjacent to monitoring sites where plant litter and live grass competition were removed. Experimental results suggest both propagule and establishment limitation have contributed to local declines observed for these native forbs. Recruitment was highest at sites that had current or historical occurrences of the seeded species, and in plots where litter was removed. Grazing history (i.e., location within or outside the reserve) interacted with exotic competition removal, such that removal of live grass competition increased recruitment in more recently grazed sites. Abundance of forbs was positively related to recruitment, while abundance of exotic forbs was negatively related. Thus, exotic competition is likely only one factor contributing to local declines of native species in invaded ecosystems, with a combination of propagule limitation, site quality, and land use history also playing important and interactive roles in native plant recruitment.     

Disentangling the drivers of reduced long-distance seed dispersal by birds in an experimentally fragmented landscape

Seed dispersal is a crucial component of plant population dynamics. Human landscape modifications, such as habitat destruction and fragmentation, can alter the abundance of fruiting plants and animal dispersers, foraging rates, vector movement, and the composition of the disperser community, all of which can singly or in concert affect seed dispersal. Here, we quantify and tease apart the effects of landscape configuration, namely, fragmentation of primary forest and the composition of the surrounding forest matrix, on individual components of seed dispersal of Heliconia acuminata, an Amazonian understory herb. First we identified the effects of landscape configuration on the abundance of fruiting plants and six bird disperser species. Although highly variable in space and time, densities of fruiting plants were similar in continuous forest and fragments. However, the two largest-bodied avian dispersers were less common or absent in small fragments. Second, we determined whether fragmentation affected foraging rates. Fruit removal rates were similar and very high across the landscape, suggesting that Heliconia fruits are a key resource for small frugivores in this landscape. Third, we used radiotelemetry and statistical models to quantify how landscape configuration influences vector movement patterns. Bird dispersers flew farther and faster, and perched longer in primary relative to secondary forests. One species also altered its movement direction in response to habitat boundaries between primary and secondary forests. Finally, we parameterized a simulation model linking data on fruit density and disperser abundance and behavior with empirical estimates of seed retention times to generate seed dispersal patterns in two hypothetical landscapes. Despite clear changes in bird movement in response to landscape configuration, our simulations demonstrate that these differences had negligible effects on dispersal distances. However, small fragments had reduced densities of Turdus albicollis, the largest-bodied disperser and the only one to both regurgitate and defecate seeds. This change in Turdus abundance acted together with lower numbers of fruiting plants in small fragments to decrease the probability of long-distance dispersal events from small patches. These findings emphasize the importance of foraging style for seed dispersal and highlight the primacy of habitat size relative to spatial configuration in preserving biotic interactions.     

Habitat Change and Plant Demography: Assessing the Extinction Risk of a Formerly Common Grassland Perennial

Abstract:  An important aim of conservation biology is to understand how habitat change affects the dynamics and extinction risk of populations. We used matrix models to analyze the effect of habitat degradation on the demography of the declining perennial plant Trifolium montanum in 9 calcareous grasslands in Germany over 4 years and experimentally tested the effect of grassland management. Finite population growth rates (λ) decreased with light competition, measured as leaf-area index above T. montanum plants. At unmanaged sites λ was <1 due to lower recruitment and lower survival and flowering probability of large plants. Nevertheless, in stochastic simulations, extinction of unmanaged populations of 100 flowering plants was delayed for several decades. Clipping as a management technique rapidly increased population growth because of higher survival and flowering probability of large plants in managed than in unmanaged plots. Transition-matrix simulations from these plots indicated grazing or mowing every second year would be sufficient to ensure a growth rate ≥1 if conditions stayed the same. At frequently grazed sites, the finite growth rate was approximately 1 in most populations of T. montanum . In stochastic simulations, the extinction risk of even relatively small grazed populations was low, but about half the extant populations of T. montanum in central Germany are smaller than would be sufficient for a probability of survival of >95% over 100 years. We conclude that habitat change after cessation of management strongly reduces recruitment and survival of established individuals of this perennial plant. Nevertheless, our results suggest extinction processes may take a long time in perennial plants, resulting in an extinction debt. Even if management is frequent, many remnant populations of T. montanum may be at risk because of their small size, but even a slight increase in size could considerably reduce their extinction risk.     

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.     

Tracing impacts of partner abundance in facultative pollination mutualisms: from individuals to populations

Partner abundance affects costs and benefits in obligate mutualisms, but its role in facultative partnerships is less clear. We address this gap in a pollination web consisting of two clovers (Trifolium) that differ in specialization on a bumble bee pollinator Bombus balteatus. We examine how pollination niche breadth affects plant responses to pollinator abundance, comparing early-flowering (specialized) and late-flowering (generalized) cohorts of T. parryi and early T. parryi to T. dasyphyllum, a pollination generalist. Co-pollinators disrupt the link between B. halteatus visitation and pollination rate for both clovers. Only for early-flowering T. parryi do visitation, pollination, and seed set increase with density of B. balteatus. Bumble bee density also alters timing of seed germination in T. parryi, with seeds from plants receiving augmented B. balteatus germinating sooner than seeds of open-pollinated counterparts. Benefits saturate at intermediate bumble bee densities. Despite strong effects of B. balteatus density on individual plant fitness components, population models suggest little impact of B. balteatus density on lamda in T. parryi or T. dasyphyllum. Findings show that functional redundancy in a pollinator guild mediates host-plant responses to partner density. Unexpected effects of pollinator density on life history schedule have implications for recruitment under pollinator decline.