Rodent suppression of seedling establishment in tropical pasture.

Grasses are recognized as a critical regeneration barrier in tropical pastures, yet the effects of rodents and rodent-grass interactions are not well understood. As selective foragers, rodents could shape tree communities, moderating biodiversity in regenerating tropical landscapes. We utilized a fully crossed two-way factorial design to examine the effect that grasses, rodents, and their interaction had on tree seedling establishment in pasture habitat. We followed two separate tree cohorts for 1 year each within the experimental framework. Multiple cohorts were used to better represent successional tree species variation and responses. Trees species were characterized by a gradient of seed masses and as pioneer or persistent successional type. Both cohort seedlings were altered when rodents were present compared to control treatments. In Cohort 1, rodents adversely affected seedlings of persistent tree species only in the absence of grass. In Cohort 2, seedlings of persistent tree species were decimated by rodents in the absence or presence of grass. In both cohorts, seedlings of persistent species established better in grass treatments, while seedlings of pioneer tree species were strongly suppressed. Tree species seed mass positively correlated with seedling establishment across all treatments except no grass-rodent treatments. Strong suppression of tree seedlings by rodents (Sigmodon toltecus) is a novel result in tropical land recently released from agriculture. One implication is that selective foraging by rodents on large-seeded persistent tree species may be facilitated by the removal of grass. Another implication is that temporary rodent control in pastures may permit higher establishment of deep-forest persistent species.

Restored connectivity facilitates recruitment by an endemic large-seeded tree in a fragmented tropical landscape.

Many large-seeded Neotropical trees depend on a limited guild of animals for seed dispersal. Fragmented landscapes reduce animal abundance and movement, limiting seed dispersal between distant forest remnants. In 2006, experimental plantings were established in pasture to determine whether plantings enhance seed dispersal and, ultimately, seedling recruitment. We examined patterns of naturally recruited seedlings of Ocotea uxpanapana, a large-seeded bird-dispersed tree endemic to southern Mexico that occurs in the surrounding landscape. We used GIS and least-cost path analysis to ask: (1) Do restoration efforts alter recruitment patterns? (2) What is the importance of canopy cover and likely dispersal pathways to establishment? Patterns of seedling establishment indicated that dispersal agents crossed open pastures to wooded plots. Recruitment was greatest under woody canopies. Also, by reducing movement cost or risk for seed dispersers, wooded canopies increased influx of large, animal-dispersed seeds, thereby restoring a degree of functional connectivity to the landscape. Together, canopy openness and path distance from potential parent trees in the surrounding landscape explained 73% of the variance in O. uxpanapana seedling distribution. Preliminary results suggest that strategic fenced plantings in pastures increase dispersal and establishment of large-seeded trees, thereby accelerating forest succession in restorations and contributing to greater connectivity among forest fragments.

Early recruitment dynamics in tropical restoration.

Unassisted secondary succession in abandoned tropical pastures often results in species-poor forests of pioneer trees that persist for decades. We characterize recruitment rates of woody vegetation in planting treatments during the first 60 months of experimental restoration on thin, eroded soils at Los Tuxtlas, southern Mexico. We test the hypothesis that recruitment of later-successional trees is greater in fenced plots planted with native trees than in fenced controls that simulate natural succession, and further that recruitment of such species would be greater in plots planted with animal-dispersed trees than in those planted with wind-dispersed trees. Results indicated much greater recruitment of later-successional animal-dispersed trees in planted plots as compared with controls. Three censuses per year recorded 960 recruited individuals of 44 species of trees and shrubs from 20-60 months after cattle exclusion. Ninety-six percent of recruits were not of planted species. Repeated-measures analyses of variance indicated that recruited communities included more species of pioneers than of later-successional trees and shrubs, with more individuals and species dispersed by animals than by wind. Recruitment of pioneers did not differ between control and planted plots. Later-successional recruits dispersed by animals accumulated > 10 times faster in planted than control plots, with apparent acceleration after planted Cecropia obtusifolia and Ficus yoponensis first produced fleshy fruits 48 months after cattle exclusion. Sparse later-successional wind-dispersed recruits did not differ by treatment. Our preliminary results over the first five years after cattle exclusion indicate that planted stands clearly accelerate succession through accumulation of later-successional trees and shrubs dispersed by animals.

Response of two prairie forbs to repeated vole herbivory.

Vertebrate herbivores as diverse as ungulates, geese, and rabbits preferentially feed on plants that have previously experienced herbivory. Here, we ask whether smaller grassland "cryptic consumers" such as voles (Microtus ochrogaster and M. pennsylvanicus) preferentially clip (cut stems for access to leaves or seeds) or avoid previously clipped individuals of two tallgrass prairie species (Desmanthus illinoensis and Echinacea purpurea) within a growing season. Further, we ask how these plants respond to repeated clipping within a growing season, and whether the effects of this herbivory last into the subsequent growing season. Voles preferentially clipped stems of D. illinoensis and E. purpurea plants that had been previously clipped. The exception was indiscriminant clipping of stems of E. purpurea late in the growing season when its achenes, a favorite vole food, ripened. For D. illinoensis, repeated clipping resulted in a 59% reduction in biomass, 42% lower ratio of reproductive to vegetative biomass, and 57% fewer seeds produced per plant compared with unclipped plants. These effects lasted into the following growing season in which plants were protected from voles. In contrast, the only effect of repeated clipping for E. purpurea was that the number of achenes per plant was substantially reduced by three episodes of clipping. This effect did not carry over to the next growing season. Such differences in D. illinoensis and E. purpurea response to repeated stem clipping by voles offer insights into how these small rodents can effect major changes in composition and dominance in grassland communities.

Early seed fall and seedling emergence: precursors to tropical restoration.

We explore processes of seed immigration and seedling recruitment before an experimental rainforest restoration matures enough to affect either. Twenty-four 30 × 30-m plots were fenced in 12 ha of pasture in 2006. Seeds were collected in ninety-six 1-m(-2) seed traps; recruits were censused in ~12,000 m(2) in which establishment was allowed. We tested effects of distance from forest, living trees, and stumps of trees cut during site preparation on seed rain in 2007 and effects of these and soil depth on recruits through June 2008. Seed fall and recruitment were not correlated with distance to forest 90-400 m away, nor to living shade trees outside the 160 × 485-m experimental grid. Recruitment differed for animal- and wind-dispersed species in a topographically complex landscape. Recruitment of wind-dispersed species was random with respect to soil depth or distance to recent stumps. Recruitment of animal-dispersed species was multimodal; partial correlations with number of stumps within 30 m of plots were significant with soil depth held constant (P < 0.025), as were correlations of recruitment with soil depth with number of stumps held constant (P < 0.01). Animal-dispersed recruits were often not conspecifics of adults that had been cut, indicating a legacy of attraction by fruiting trees of animals bearing seeds from distant sources. Ecological implications are that recruitment in pastures released from grazing reflects a mix of widely scattered wind-dispersed pioneers and, where animal-dispersed trees exist, multi-modal and decidedly non-random recruitment of pioneer and later successional animal-dispersed trees from seed banks.

Prairie forb response to timing of vole herbivory.

The timing of herbivory can be an important factor in the strength and direction of plant response to herbivore damage. To determine the effect of vole herbivory timing within a growing season on tallgrass prairie forbs, we used individual plant enclosures to limit vole access to three species, Desmanthus illinoensis, Echinacea purpurea, and Heliopsis helianthoides, in an experimental restoration in northern Illinois, USA. As part of a long-term experiment, we implemented five vole access treatments in 2003: (1) vole access for the entire growing season, (2) early-season access, (3) mid-season access, (4) late-season access, and (5) no vole access. We protected all plants from herbivory in the following growing season (2004) to test whether the effects of herbivory in one growing season carried over to the next. We also tested how restoration planting design, including seeding time (June or December) and density (35 or 350 seeds/m2 of each species) affected patterns of herbivory and plant recovery. Vole access for the entire growing season was most detrimental for the growth and reproduction of all three species. In contrast, vole access for a portion of the growing season had different effects on the three species: Desmanthus growth and reproduction was negatively affected by early-season access, Echinacea reproductive output was reduced by late-season access, and Heliopsis was not affected by early-, mid-, or late-season vole access. Negative effects of continual vole access carried over to the following growing season for Desmanthus and Heliopsis, but not for Echinacea. Effects of herbivory did not carry over to the next season for Echinacea and Heliopsis when plants were accessible to voles for only part of the growing season. In contrast, Desmanthus plants exposed to early-season herbivory in one year continued to produce fewer seeds per plant after being protected from vole herbivory for a growing season. Planting density and planting season had mixed effects. Echinacea and Desmanthus were larger in plots planted in June, showing that restoration design continued to affect plant population dynamics seven years after seeding. However, there was no interaction between plant response to vole herbivory and restoration design.

Disperser limitation and recruitment of an endemic African tree in a fragmented landscape.

Forest fragmentation may have positive or negative effects on tropical tree populations. Our earlier study of an endemic African tree, Leptonychia usambarensis (Sterculiaceae), in the East Usambara Mountains of Tanzania, found poorer recruitment of seedlings and juveniles in small fragments compared to continuous forest, and concomitant reduction of seed-dispersal agents and seed dispersal. However, the possibility that other biotic or abiotic consequences of the fragmentation process contribute to diminished recruitment in fragments was left open. Here we test whether excessive seed predation, diminished fecundity, low seed quality, or adverse abiotic effects acted independently or in concert with reduced seed dispersal to limit seedling and juvenile recruitment in fragments. Extended observations of disperser activity, a seed placement experiment, seed predator censuses, and reciprocal seedling transplants from forest and fragment sources failed to support the alternative hypotheses for poorer seedling and juvenile recruitment in fragments, leaving reduced seed dispersal as the most plausible mechanism. Poorer recruitment of this species in forest fragments, where high edge-to-area ratios admit more light than in continuous forest, is particularly striking because the tree is an early successional species that might be expected to thrive in disturbed microhabitats.

Recruitment of hornbill-dispersed trees in hunted and logged forests of the Indian Eastern Himalaya.

Hunting of hornbills by tribal communities is widespread in logged foothill forests of the Indian Eastern Himalaya. We investigated whether the decline of hornbills has affected the dispersal and recruitment of 3 large-seeded tree species. We hypothesized that 2 low-fecundity tree species, Chisocheton paniculatus and Dysoxylum binectariferum (Meliaceae) bearing arillate fruits, are more dispersal limited than a prolifically fruiting drupaceous tree Polyalthia simiarum (Annonaceae), which has potential dispersers other than hornbills. We estimated the abundance of large avian frugivores during the fruiting season along transects in 2 protected and 2 disturbed forests. We compared recruitment of the tree species near (<10 m) and far (10-40 m) from parent trees at protected and disturbed sites. Median abundance of Great (Buceros bicornis), Wreathed (Aceros undulatus), and Oriental Pied Hornbills (Anthracoceros albirostris) were significantly lower in disturbed forests, but sites did not differ in abundances of the Mountain Imperial Pigeon (Ducula badia). Overall, tree species showed more severely depressed recruitment of seedlings (77% fewer) and juveniles (69% fewer) in disturbed than in protected forests. In disturbed forests, 93% fewer seedlings of C. paniculatus were beyond parental crowns, and a high number of all seedlings (42%) accumulated directly under reproductive adults. In contrast, D. binectariferum and P. simiarum were recruitment rather than dispersal limited, with fewer dispersed seedlings surviving in disturbed than in protected forests. Results are consistent with the idea that disturbance disrupts mutualisms between hornbills and some large-seeded food plants, with the caveat that role redundancy within even small and specialized disperser assemblages renders other tree species less vulnerable to loss of regular dispersal agents.

The anomalous Kentucky coffeetree: megafaunal fruit sinking to extinction?

The Kentucky coffeetree (Gymnocladus dioicus, Fabaceae) is an ecological paradox. A rare tree in nature in eastern and central North America, G. dioicus produces legumes that are only known to be dispersed by water, but appear similar to fruits consumed and dispersed by elephants and rhinoceros. One would expect the pods to be consumed by livestock, but the pulp and seeds are toxic to cattle and sheep. We examine the puzzle of G. dioicus dispersal in light of its other reproductive and life history characteristics and find that it probably is a botanical anachronism, in terms of both a set of dispersal agents long extinct and habitats, including what we term megafaunal disclimaxes, which have disappeared. Large seeds, the megafaunal gestault of the fruit, a dioecious mating system, and shade-intolerance combined with vigorous cloning suggest a widely dispersed pioneer of Miocene through Pleistocene habitats profoundly altered by large-mammal herbivory. As to what ate it, we can only say there were once many candidates. We hypothesize that the plant is an ecological anachronism, sinking to extinction in the wild.

Can forest fragmentation disrupt a conditional mutualism? A case from central Amazon.

This is the first study to investigate whether scatter-hoarding behavior, a conditional mutualism, can be disrupted by forest fragmentation. We examined whether acouchies (Myoprocta acouchy, Rodentia) and agoutis (Dasyprocta leporina, Rodentia) changed scatter-hoarding behavior toward seeds of Astrocaryum aculeatum (Arecaceae) as a consequence of a decrease in forest-patch area. Our study was conducted at the 30-year-old Biological Dynamics of Forest Fragments Project, in central Amazon, Brazil. We tested whether forest size affected the number of Astrocaryum seeds removed and scatter-hoarded (and likely dispersed) by acouchies and agoutis, as well as the distance that the seeds were hoarded. The study extended over three seasons: the peak of the rainy season (March-April), the transition between the rainy and the dry season (May-June), and the peak of the dry season (August-September). Our results revealed that the number of seeds removed was larger in smaller fragments, but that the percentage of seeds hoarded was much lower, and seeds eaten much higher, in 1-ha fragments. Moreover, fewer seeds were taken longer distances in fragments than in the continuous forest. Site affected the number of seeds removed and season affected the percentage of seeds hoarded: more seeds were removed from stations in one site than in two others, and hoarding was more important in April and September than in June. Our study reveals that scatter-hoarding behavior is affected by forest fragmentation, with the most important disruption in very small fragments. Fragmentation converts a largely mutualistic relationship between the rodents and this palm in large forest patches into seed predation in small fragments.

The paradox of forest fragmentation genetics.

Theory predicts widespread loss of genetic diversity from drift and inbreeding in trees subjected to habitat fragmentation, yet empirical support of this theory is scarce. We argue that population genetics theory may be misapplied in light of ecological realities that, when recognized, require scrutiny of underlying evolutionary assumptions. One ecological reality is that fragment boundaries often do not represent boundaries for mating populations of trees that benefit from long-distance pollination, sometimes abetted by long-distance seed dispersal. Where fragments do not delineate populations, genetic theory of small populations does not apply. Even in spatially isolated populations, where genetic theory may eventually apply, evolutionary arguments assume that samples from fragmented populations represent trees that have had sufficient time to experience drift, inbreeding, and ultimately inbreeding depression, an unwarranted assumption where stands in fragments are living relicts of largely unrelated predisturbance populations. Genetic degradation may not be as important as ecological degradation for many decades following habitat fragmentation.

Episodic death across species of desert shrubs.

Extreme events shape population and community trajectories. We report episodic mortality across common species of thousands of long-lived perennials individually tagged and monitored for 20 years in the Colorado Desert of California following severe regional drought. Demographic records from 1984 to 2004 show 15 years of virtual stasis in populations of adult shrubs and cacti, punctuated by a 55-100% die-off of six of the seven most common perennial species. In this episode, adults that experienced reduced growth in a lesser drought during 1984-1989 failed to survive the drought of 2002. The significance of this event is potentially profound because population dynamics of long-lived plants can be far more strongly affected by deaths of adults, which in deserts potentially live for centuries, than by seedling births or deaths. Differential mortality and rates of recovery during and after extreme climatic events quite likely determine the species composition of plant and associated animal communities for at least decades. The die-off recorded in this closely monitored community provides a unique window into the mechanics of this process of species decline and replacement.

Massive and distinctive effects of meadow voles on grassland vegetation.

We ask whether vole herbivory in experimental grassland plots is sufficient to create an unpalatable community. In a six-year experiment, meadow voles (Microtus pennsylvanicus) reduced plant standing crop between 30% and 72%, well within the range of ungulate effects. Moreover, meadow voles reduced their available forage species by changing the plant community composition: four grass species and a legume upon which they foraged declined sharply in cover and/or number of individuals, five forbs avoided by voles increased, and two forbs neither declined nor increased with either measure. Reductions of diversity occurred when voles first defoliated the plots in 2000 but disappeared as plant species avoided by voles replaced vulnerable plants. Within six years, meadow voles created plant communities dominated by species that they did not eat.

Effects of seed size on seedling size in Virola surinamensis; a within and between tree analysis.

We conducted a greenhouse study of the effects of initial seed mass on seedling characteristics in a Panamanian population of Virola surinamensis, a canopy tree in which mean seed mass of different individuals ranges from 1.34 to 4.04g. The system is of particular interest because birds preferentially eat fruits of small-seeded plants, leaving seedlings of large-seeded individuals under conditions of potentially severe sibling competition (Howe and Vande Kerckhove 1980).Effects of differences of mean seed mass between trees are explored using an analysis of variance, while effects of seed-mass variation within crops are demonstrated with a regression analysis. A two-way analysis of variance decisively shows effects of parental source and light condition on seedling height, leaf length, and dry shoot mass (all P<0.0001). A posteriori tests show that differences in seedling characteristics reflect differences in initial seed mass, with especially strong differences apparent in shoot mass. Regression of seedling characteristics on initial seed mass shows that variation of seed size within a crop is sufficient to influence shoot mass at 15 weeks (P<0.0001).Effects of size differences of seeds that land adjacent to each other, either under the parent or in monkey droppings, are documented with growth of pairs of seedlings in pots. Differences in shoot height and mass at 15 weeks are evident when seeds of average size differ by only 0.2 g, and dramatic differences are evident when paired seeds differ by an average of 1.5 g. Seedlings grow more when isolated than when planted with conspecifics.These experimental results offer indirect support for the hypothesis that small-seeded Virola parents secure an advantage in reproduction through differential dispersal, while large-seeded plants produce more competitive seedlings under their own crowns - an advantage most likely to be of importance when frugivores are scarce.

Competition for dispersal agents among tropical trees: influences of neighbors.

We distinguish factors influencing seed dispersal that are potentially under the control of parent plants from those that are not in a Panamanian population of the neotropical nutmeg, Virola surinamensis (Myristicaceae).In the first category, we find that individual variation in crop size and nutritional components of the aril failed to explain any variation in the proportion of fruits taken from fruiting trees. The ratio of edible aril to indigestible seed explained a significant but small (13%) portion of variation in the fraction of fruits taken by tropical birds. These results suggest that the potential for ongoing natural selection on fruit and crop characteristics by dispersal agents exists, but is periodic or weak. On the other hand, the number of fruits available to birds within 50 m of any given Virola tree profoundly influenced the extent to which it secured dispersal. More than three times as much variation (42%) in relative dispersal could be explained by the number of "competing" Virola fruits during the peak of an individual tree's fruiting season. When isolated plants are eliminated from the analysis, the depressive effect of competition with neighbors explains 72% of the variation in individual dispersal. These results suggest that birds seek out clumps of fruiting trees, but that intraspecific competition for a limited disperser assemblage occurs within the clumps.Our results are a first step towards separating attributes of the plant that are potentially under the influence of natural selection by dispersal agents from emergent population effects that can override individual advantage in crop or fruit characteristics.

Fruit production, migrant bird visitation, and seed dispersal of Guarea glabra in Panama.

The relationship between bird visitation and the size of the available fruit crop was studied at an understory tree (Guarea glabra Vahl, Meliaceae) in the tropical wet forest of Barro Colorado Island, Panama Canal Zone. Twelve resident species and seven North American migrant species fed on the Bright orange arilloids (seeds with arils), which were not depleted during the normal fruiting period. The number of individual visitors, the number of visiting species, and the number of seeds removed increased linearly with the size of the available fruit crop. The proportion of seeds removed did not increase with the size of the available fruit crop, indicating that dispersal is a function of the number of fruit available and not a disproportionate function of large fruit displays. Four species of North American migrants (Myiarchus crinitus, Catharus ustulatus, Vireo olivaceus, and Vermivora peregrina) accounted for 70% of the visits and 60% of the seeds removed from the trees. No resident species visited Guarea as frequently as any one of these migrants. There was no indication that any single visitor was dependent on this tree for nutrition, nor that the tree was dependent upon any single species for dispersal. We hypothesize that the fruiting season of G. glabra is adaptively synchronized with northward migration of opportunistically frugivorous North American birds.

Survival and growth of Virola surinamensis yearlings: Water augmentation in gap and understory.

Factors affecting seedling Virola surinamensis (Myristicaceae) survival and growth were investigated on Barro Colorado Island, Panama. Seedlings planted 3 months after germination were monitored in treefall gaps and understory using 2.25 ha irrigated and control plots through the first dry season. During the dry season, irrigated plants in gaps increased total leaf area significantly more than did irrigated plants in the shaded understory. Over the same dry season, control plants in gaps and in the shaded understory lost similar amounts of leaf area. Seedlings in understory were suppressed in stem height and biomass in both irrigated and control plots; these measures were greater in gaps and greatest in irrigated gaps (height). Roots were similar in length in all treatments, but greater in biomass in gaps than understory due to greater proliferation of secondary roots in control and irrigated gaps than in control and irrigated understory. This experiment demonstrates both water and light limitation during the first dry season after germination. V. surinamensis seedlings are capable of survival and modest growth of leaf area in the deep shade of the understory in moist locations; they are severely disadvantaged in shaded understory subject to drought, where most seeds fall and most seedlings establish. The broken canopy of a gap allows shoot and consequently root growth that permits seedlings to survive seasonal drought.

Roles of birds and bats in early tropical-forest restoration.

Restoration of tropical forest depended in large part on seed dispersal by fruit-eating animals that transported seeds into planted forest patches. We tested effectiveness of dispersal agents as revealed by established recruits of tree and shrub species that bore seeds dispersed by birds, bats, or both. We documented restoration of dispersal processes over the first 76 months of experimental restoration in southern Mexico. Mixed-model repeated-measures randomized-block ANOVAs of seedlings recruited into experimental controls and mixed-species plantings from late-secondary and mature forest indicated that bats and birds played different roles in the first years of a restoration process. Bats dispersed pioneer tree and shrub species to slowly regenerating grassy areas, while birds mediated recruitment of later-successional species into planted stands of trees and to a lesser extent into controls. Of species of pioneer trees and shrubs established in plots, seven were primarily dispersed by birds, three by bats and four by both birds and bats. Of later-successional species recruited past the seedling stage, 13 were of species primarily dispersed by birds, and six were of species dispersed by both birds and bats. No later-successional species primarily dispersed by bats established in control or planted plots. Establishment of recruited seedlings was ten-fold higher under cover of planted trees than in grassy controls. Even pre-reproductive trees drew fruit-eating birds and the seeds that they carried from nearby forest, and provided conditions for establishment of shade-tolerant tree species. Overall, after 76 months of cattle exclusion, 94% of the recruited shrubs and trees in experimental plots were of species that we did not plant.

Reversal of fortune: plant suppression and recovery after vole herbivory.

It is not clear how plant species preferred as forage by rodents persist in prairie vegetation. To test permanence of suppression of wet-mesic prairie vegetation by vole (Microtus pennsylvanicus) herbivory in synthetic experimental communities, access treatments were reversed after 9 years of vole exclusion or access. Between 1996 and 2004, rye grass Elymus virginicus (Poaceae) and tick-trefoil Desmodium canadense (Fabaceae) achieved mean cover of up to 30 and 25%, respectively, in plots where voles were excluded, but disappeared from plots where voles had access. To determine whether these species remained vulnerable to vole herbivory as established adults, and to determine whether the species could recover if vole herbivory were removed, access treatments were reversed at the end of the 2004 growing season and monitored through 2007. Repeated measures ANOVA demonstrated dramatic vole suppression of established E. virginicus, but not D. canadense, indicating continuing vulnerability of the grass but not of the adult legume. Release from vole herbivory resulted in re-growth of rye, but not tick-trefoil, which was apparently suppressed by established vegetation. Two additional common planted species did not respond to treatment reversal, nor did 11 much less common planted species that comprised a minor portion of the vegetation. Dominant perennial black-eyed Susan Rudbeckia subtomentosa (Asteraceae) did not change in plant numbers by year or treatment, but expanded or contracted in stems per plant and cover as E. virginicus was suppressed or released by vole herbivory or its absence. Results indicate that preferred food plants may persist through capacity to quickly recover during periods of relative vole scarcity, or reach a refuge in maturity.