Hypocrealean (Hypocreales,Ascomycota) Fungal Diversity in Different Stages of Tropical Forest Succession in Costa Rica1

The relationship between forest succession and microfungal diversity has been poorly studied. Fungi provide important ecosystem services that may deteriorate in deforested or highly disturbed forests. To determine the possible effects of deforestation and forest succession on microfungi, species diversity of hypocrealean fungi (Ascomycota) was compared in forest stands in Eastern Costa Rica representing three stages of succession: 1–2, 25–27 yr old, and an old growth forest. Species diversity in a second‐growth forest fragment surrounded by timber plantations and second‐growth forest was also compared to that of a stand surrounded by old growth forest. The results show that the overall diversity of hypocrealean fungi was inversely proportional to the age of the forest stand, and each family showed different successional trends. Clavicipitaceae was more diverse in the old‐growth forest and was positively related to the age of the forest stand. Nectriaceae was highly diverse in the 1‐ to 2‐yr‐old stand and less diverse in the old‐growth stand. Saprobic and plant pathogenic fungal species were more diverse in the 1‐ to 2‐yr‐old stand and their diversity was inversely proportional to the age of the forest stand. The diversity of insect pathogens was positively related to the age of the forest stand. The 20‐ to 22‐yr‐old forest fragment had the lowest number of species overall. Based on the data gathered in this study, hypocrealean fungal species diversity is related to the successional stage and fragmentation of tropical forest.     

Species Richness,Spatial Variation,and Abundance of the Soil Seed Bank of a Secondary Tropical Rain Forest1

Despite the importance of the soil seed bank in tropical forest regeneration, little is known about spatial variability in species composition and abundance of seeds stored in the soil. To develop sampling methods for comparative studies, we examined species richness, spatial variation, and abundance of germinants from the soil seed bank in a 16 year old secondary, tropical wet forest at La Selva Biological Station, Costa Rica. Surface soil (10 cm deep, 4.7 cm diameter) was collected at the intersection points of a gridded 1 ha plot (10 × 10-m grid, 121 samples) and in a nested 100 m² subplot (2 × 2-m grid, 36 samples). The 1 ha plot had a density of 4535 seeds/m² with 34 species observed. Based on a series of 100 randomized species accumulation curves, a Michaelis-Menten fit predicted a mean species richness of 36.3 species; the number of observed species was close to the predicted asymptote. A nonparametric, first-order jackknife species richness estimator predicted a species richness of 37.0 species. Eighty-five and 95 percent of the observed species richness is contained, on average, within 41 and 74 pooled samples, respectively. Within the 100 m² nested subplot, a density of 5476 seeds/m² was observed, comprising 26 species with an estimated species richness (Michaelis-Menten fit) of 29.1 species. The jackknife species richness estimator predicted a species richness of 36.7 species. For species richness and abundance of both plots, spatial autocorrelation statistics (Moran's I) were not significantly different from zero at lag distances from 2 to 100 m, indicating a random distribution at these spatial scales. For this site, accurate estimates of species composition depend upon the number of samples collected as well as the spatial distribution of sampling effort. Many small samples distributed over a large area provide greater accuracy and precision for estimating species richness of the soil seed bank.     

Planting Design Effects on Avian Seed Dispersers in a Tropical Forest Restoration Experiment

Seed dispersal often limits tropical forest regeneration and animals disperse most rainforest tree seeds. This presents two important questions for restoration ecologists: (1) which animals are common seed dispersers? and (2) which restoration techniques attract them? Fourteen restoration sites were planted with four tree species in three designs, (1) controls (no planting, natural regeneration) (2) islands (trees planted in small patches), and (3) plantations (trees planted continuously over a large patch). We sampled birds in November, February, and April 2007–2008 with mist nets, in February and July 2009 with observations, and in July 2008 with both techniques. We documented 30 seed species from fecal samples of captured birds. All identified seed species were early‐successional forms. Four tanager species, three thrushes, two saltators, two flycatchers, and one finch were categorized as common seed dispersers, based on their high likelihood of dispersing seeds. Common dispersers were generalist species with small gape widths (<15 mm). Common dispersers were captured significantly more often in plantations than controls in most seasons and more often in plantations than islands during one season. Common disperser observations were significantly greater in plantations than controls during two periods and in plantations compared with islands in one period. Results indicate that plantation‐style planting is the conservative strategy to maximize attractiveness to common dispersers in tropical restoration sites. Island planting is an alternative when resources are limited although disperser activity may be lower in some seasons than in plantations. Additional research should investigate how to attract large, forest‐associated dispersers.     

Forest Succession and Distance from Forest Edge in an Afro‐Tropical Grassland1

Forest succession on degraded tropical lands often is slowed by impoverished seed banks and low rates of seed dispersal. Within degraded landscapes, remnant forests are potential seed sources that could enhance nearby forest succession. The spatial extent that forest can influence succession, however, remains largely unstudied. In abandoned agricultural lands in Kibale National Park, Uganda, recurrent fires have helped perpetuate the dominance of tall (2–3 m) grasses. We examined the effects of distance from forest and grassland vegetation structure on succession in a grassland having several years of fire exclusion. At 10 and 25 m from forest edge, we quantified vegetation patterns, seed predation, and survival of planted tree seedlings. Natural vegetation was similar at both distances, as was seed (eight species) and seedling (six species) survival; however, distance may be important at spatial or temporal scales not examined in this study. Our results offer insight into forest succession on degraded tropical grasslands following fire exclusion. Naturally recruited trees and tree seedlings were scarce, and seed survival was low (20% after 7 mo). While seedling survival was high (95% after 6 to 8 mo), seedling shoot growth was very slow (x?= 0.5 cm/100 d), suggesting that survivorship eventually may decline. Recurrent fires often impede forest succession in degraded tropical grasslands; however, even with fire exclusion, our study suggests that forest succession can be very slow, even in close proximity to forest.     

Small Tent-Roosting Bats Promote Dispersal of Large-Seeded Plants in a Neotropical Forest

In Neotropical regions, fruit bats are among the most important components of the remaining fauna in disturbed landscapes. These relatively small-bodied bats are well-known dispersal agents for many small-seeded plant species, but are assumed to play a negligible role in the dispersal of large-seeded plants. We investigated the importance of the small tent-roosting bat Artibeus watsoni for dispersal of large seeds in the Sarapiquí Basin, Costa Rica. We registered at least 43 seed species > 8 mm beneath bat roosts, but a species accumulation curve suggests that this number would increase with further sampling. Samples collected beneath bat feeding roosts had, on average, 10 times more seeds and species than samples collected 5 m away from bat feeding roosts. This difference was generally smaller in small, disturbed forest patches. Species-specific abundance of seeds found beneath bat roosts was positively correlated with abundance of seedlings, suggesting that bat dispersal may influence seedling recruitment. Our study demonstrates a greater role of small frugivorous bats as dispersers of large seeds than previously thought, particularly in regions where populations of large-bodied seed dispersers have been reduced or extirpated by hunting.     

Spatial and Temporal Variation of Seed Rain in the Canopy and on the Ground of a Tropical Cloud Forest

Spatial and temporal patterns of seed rain impact plant fitness, genetic and demographic structure of plant populations, and species' interactions. Because plants are sessile, they rely on biotic and abiotic dispersal agents to move their seeds. The relative importance of these dispersal agents may shift throughout the year. In tropical forests, seed dispersal of epiphytes constitutes a major but hitherto unknown portion of seed rain ecology. For the first time, we report on patterns of seed rain for both epiphytic and terrestrial plants across an entire year in a Neotropical montane forest. To examine seed rain, we placed traps in the canopy and on the ground. We analyzed seed dispersal syndrome (bird, mammal, wind) and plant habit (epiphyte, liana, shrub, small tree, large tree) across all seasons of the year (dry, misty, wet). We found that the community of species collected in canopy traps was significantly different from the community in ground traps. Epiphytes were the most common plant habit found in canopy traps, while large trees were most common in ground traps. Species with bird‐dispersed seeds dominated all traps. Species richness was significantly higher during the dry season in ground traps, but did not vary across seasons in canopy traps. Our results highlight the distinct seed rain found in the canopy and on the ground and underscore the importance of frugivores for dispersing both arboreal and terrestrial plants in tropical ecosystems.     

Retention of Inorganic Nitrogen by Epiphytic Bryophytes in a Tropical Montane Forest1

We developed and evaluated a model of the canopy of a tropical montane forest at Monteverde, Costa Rica, to estimate inorganic nitrogen (N) retention by epiphytes from atmospheric deposition. We first estimated net retention of inorganic N by samples of epiphytic bryophytes, epiphyte assemblages, vascular epiphyte foliage, and host tree foliage that we exposed to cloud water and precipitation solutions. Results were then scaled up to the ecosystem level using a multilayered model of the canopy derived from measurements of forest structure and epiphyte mass. The model was driven with hourly meteorological and event‐based atmospheric deposition data, and model predictions were evaluated against measurements of throughfall collected at the site. Model predictions were similar to field measurements for both event‐based and annual hydrologic and inorganic N fluxes in throughfall. Simulation of individual events indicated that epiphytic bryophytes and epiphyte assemblages retained 33–67 percent of the inorganic N deposited in cloud water and precipitation. On an annual basis, the model predicted that epiphytic components retained 3.4 kg N ha/yr, equivalent to 50 percent of the inorganic N in atmospheric deposition (6.8 kg N ha/yr). Our results indicate that epiphytic bryophytes play a major role in N retention and cycling in this canopy by transforming highly mobile inorganic N (ca. 50% of atmospheric deposition is NO^?₃) to less mobile (exchangeable NH⁺₄) and recalcitrant forms in biomass and remaining litter and humus.     

Seed Dispersal of a High Quality Fruit by Specialized Frugivores: High Quality Dispersal?1

Dispersal quality, as estimated by the cumulative effects of dispersal, germination, seed predation, and seedling survival, was examined for Beilschmiedia pendula (Lauraceae) in Monteverde, Costa Rica. I determined the pattern of dispersal by finding seeds deposited by birds, protected the seeds from seed predators with cages to assess germination and seedling survival, and examined seed predation rates with marked seeds. Seed predation, germination, and seedling survival were compared between seeds naturally dispersed by birds and seeds placed at randomly located sites. Approximately 70 percent of seeds dispersed by birds (N= 244) were deposited <10 m from crown edges of fruiting B. pendula trees, although some seeds were dispersed at least 70 m away. Larger seeds were more likely to be dispersed under or close to the parent trees, and larger seeds produced larger seedlings. Seed size was not correlated directly with seedling survival, but larger seedlings at three months were most likely to survive one year. Seed predation by mammals and insects and seedling mortality due to fungal pathogens were concentrated beneath the crowns of parent trees. Seedlings and saplings were more abundant beneath fruiting B. pendula trees, but individuals farther away were taller on average. Thus, dispersal is beneficial for B. pendula, but such benefits appear most pronounced at a small spatial scale; seeds dispersed >30 m from the crown edges actually had a lower probability of survival than those dispersed 10–20 m. Only 10 percent of B. pendula. seeds received high‐quality dispersal in terms of landing in the zone with the highest per seed probability of seedling survival 10–20 m from parental crowns.     

Reproduction of the Bat Glossophaga commissarisi (Phyllostomidae: Glossophaginae) in the Costa Rican Rain Forest During Frugivorous and Nectarivorous Periods1

I studied the reproduction of the 9 g nectarivorous bat Glossophaga commissarisi (Phyllostomidae: Glossophaginae) in relation to its food choice in a Costa Rican lowland rain forest over more than 2 yr. Reproduction was bimodal with birth peaks in April/May and October/November. The first birth peak coincided with a period of frugivory, whereas the second occurred during a period of almost exclusive nectarivory. All adult females recaptured in consecutive reproductive periods were reproductively active on both occasions, indicating that individual G. commissarisi females regularly reproduce twice per year at the study site. Throughout the annual cycle the mean testis length of the males correlated best with the proportion of females lactating, suggesting a post partum estrous pattern. Animals became reproductively active at about 1 yr of age. Fecal samples showed that females consumed significantly more insects than males.     

Postdispersal Seed Fate of Tropical Montane Trees in an Agricultural Landscape, Southern Costa Rica

Variation in postdispersal seed fate is an important factor driving patterns of forest regeneration. Because most previous studies have not tracked final seed fate and have commonly equated seed removal with predation without considering the possibility of secondary dispersal, little is known about individual seed mortality factors in successional and degraded habitats. This study tracked the postdispersal fate of large-seeded tropical montane trees in abandoned pasture, young secondary forests, and small forest fragments during two consecutive years in an agricultural landscape in southern Costa Rica. The incidence of secondary dispersal by animals, scatterhoarding in particular, and the effects of seed burial on germination were measured. Overall, seeds survived through germination more often in secondary forests with high levels of mortality occurring in abandoned pastures and forest fragments. The majority of seed mortality was caused by rodent predation in forest fragments, insects and fungal pathogens in secondary forests, and a combination of desiccation, insects, and fungal pathogens in pastures. Seeds were frequently secondarily dispersed in larger forest fragments, whereas they were only rarely moved in pastures and secondary forests. Burial tended to improve germination in pastures and was important for an often scatterhoarded species, Otoba novogranatensis, in all habitats. The results of this study suggest that: (1) seed mortality factors differ in response to the type of habitat degradation; (2) large-seeded species have high potential for survival when dispersed to young secondary forests; and (3) seed removal is not a reliable proxy for seed predation, particularly in less degraded forest fragments.     

Phosphorus Limits Tropical Rain Forest Litter Fauna

The stoichiometry of resources may explain bottom-up regulation of higher trophic levels. We tested the effects of soil and litter nutrient stoichiometry on the invertebrate litter fauna of a Costa Rican tropical rain forest. Animal densities were estimated from 15 sites across a phosphorus gradient. The density of the invertebrate litter fauna varied considerably, and was strongly tied to soil and litter phosphorus concentrations. An increase in phosphorus concentrations corresponded with an equally proportionate increase in animal densities. Natural variation in nutrient levels can thus serve as a predictor of density in a highly diverse tropical animal community.     

Factors Limiting Tropical Rain Forest Regeneration in Abandoned Pasture: Seed Rain,Seed Germination,Microclimate, and Soil1

Vegetation, seed rain, seed germination, microclimate, and soil physical and chemical parameters were measured in a recently abandoned pasture and adjacent primary rain forest in southern Costa Rica. The goal of this study was to assess the importance of these factors in limiting forest regeneration in abandoned pastures. Seed rain of animal dispersed species decreased dramatically in the pasture >5 m from the forest/pasture edge; fewer wind dispersed seeds fell in the pasture than in the forest, but the difference was much less than for animal dispersed seeds. Percent seed germination of most species studied was similar in the forest and in pasture with grasses; seed germination was lower during the dry season in areas of pasture cleared of grasses. Air temperature, vapor pressure deficit (VPD), and photon flux density (PFD) were much higher in the pasture than in the forest at 1 m above the ground. VPD and PFD at ground level and soil temperature were similar in the pasture and the forest, indicating that pasture grasses strongly modify microclimatic conditions near the soil surface. The lowest gravimetric water content recorded in the pasture during the dry season was 0.5 and leaf relative water contents of the two species measured in the forest and pasture were identical, suggesting that plants in the pasture were not water stressed. Levels of most soil nutrients were lower in the pasture as compared to the forest; however, aboveground and root biomass for seedlings grown in pasture and forest soils did not differ significantly. Although a number of factors impede forest recovery in abandoned pastures, these results suggest that the most imporrant limitation is lack of seed dispersal.     

Long-Term Effects of Forest Regrowth and Selective Logging on the Seed Bank of Tropical Forests in NE Costa Rica1.

To investigate long-term effects of land use on the soil seed bank, we compared the abundance/density, species richness, life form distribution, and species composition of seeds stored in the soil of four 15–20 yr-old second-growth stands, two old-growth stands, and two previously selectively-logged stands in the Caribbean lowlands of Costa Rica. Surface soil (10 cm deep, 4.7 cm diameter) was collected at 10 m intervals along three 120–160 m long transects in each stand (44–48 soil cores, 22–24 combined seed bank samples per site). Seed density was highest but variable in second-growth stands (8331–14535 seeds/m²), low and homogeneous in old-growth stands (2258–2659 seeds/m²), and intermediate and highly variable in selectively-logged stands (1165–6854 seeds/m²), which also had contrasting logging intensities. Species richness was strongly dependent on seed density, but showed less variation. Life form distribution did not differ statistically among or within land-use categories. In each stand, herbs-forbs, shrubs, and vines dominated the seed bank (> 75% of the species richness and abundance), whereas trees were a minor component (< 20% of the species richness and < 5% of the abundance) and were predominandy early successional. Shrubs and vines were most abundant in second-growth stands where regrowth vegetation was repeatedly cut before abandonment, whereas grasses and sedges were most abundant in the only forest stand that was completely surrounded by pastures. In terms of species composition, old-growth stands were more similar to selectively-logged stands than to second-growth stands, but across stands, selectively-logged forests were most distinct from the other two forest types. An inventory of the standing woody vegetation in each site showed little representation of the woody taxa found in the seed bank. We discuss these results in the context of the main factors that have been postulated to influence the abundance, life form, and species composition of tropical forest seed banks, and explore the role of the latter during intermediate phases of tropical forest succession and regeneration.     

Effects of Selective Vegetation Thinning on Seed Removal in Secondary Forest Succession1

Seed removal was assessed for two tree species in three forest types: (1) secondary forest with and (2) without selective vegetation thinning, and (3) mature forest. Selective vegetation thinning meant the removal of all stems ≤3 cm in diameter of secondary‐forest species and was intended as a management technique to accelerate succession toward mature forest. Thinning did not have an effect on seed removal. One of the species showed lower seed removal in mature forest compared to secondary forest.     

Disperser- vs. Establishment-Limited Distribution of a Riparian Fig Tree (Ficus insipida) in a Costa Rican Tropical Rain Forest1

Studies were conducted at the La Selva Biological Station in Costa Rica and in a greenhouse in California to determine the factors accounting for the nonrandom distribution of the riparian fig tree Ficus insipida Willd. along streams in the La Selva Biological Reserve and adjacent deforested lands. We also evaluated the potential seed dispersers of this tree relative to the role of the fruit‐eating fish Brycon guatemalensis that previously was proposed to be an important disperser of F. insipida seeds in this system. At La Selva, we recorded the fig‐foraging activities of vertebrates at fruiting F. insipida trees, surveyed for the presence or absence of F. insipida along streams of different sizes, and determined the fate of fig seedlings transplanted in different riparian habitats. In the greenhouse, we measured seed germination and seedling survival and growth under different light and soil pH conditions mimicking natural conditions. The findings provided evidence that (1) the tree occurs along the larger streams running through forest habitat and only along smaller streams with relatively high light availability; (2) bats (Artibeus spp.) and fish are the major dispersers of F. insipida seeds; (3) the seedlings are subject to mortality not only from low light conditions but also from treefalls, frequent flooding, and bank erosion; and (4) high light levels and near neutral soil pH result in relatively better seed germination, faster growth, and higher survival rates of seedlings. Overall, our results suggest that this fig tree is dispersed mainly by bats and fish and is more establishment‐limited than disperser‐limited in its local distribution in the La Selva rain forest habitat.     

Tree Seed Fate in a Logged and Fragmented Forest Landscape, Northeastern Costa Rica1

We compared the seed fate of two animal‐dispersed, large‐seeded timber species (Dipteryx panamensis [Fabaceae] and Carapa guianensis [Meliaceae]) in logged and fragmented forests with that for continuous forest in northeastern Costa Rica. For both species, we quantified rates of seed removal (an index of vertebrate predation) and the fate of dispersed seeds (those carried away from their original location that either germinated or were not subsequently removed within three months). We predicted that (1) fewer seeds would be dispersed by vertebrates in fragmented forest than in continuous forest due to low population abundances after hunting and/or loss of suitable habitat, and (2) seed predation rates would be higher in forest fragments than in continuous forest due to high abundance of small‐bodied seed consumers. We compared three forest fragments currently managed for timber (140–350 ha) and a large reserve of continuous forest (La Selva, 1500 ha and connected to a national park). An exclusion experiment was performed (seeds placed in the open vs. seeds within semipermeable wire cages; 5 cm mesh size) to evaluate the relative roles of large and small animals on seed removal. Seed germination capacity did not differ among all four sites for both species. Removal of Dipteryx seeds was higher in forest fragments (50% removal within 10 days and related to the activity of small rodents) compared to La Selva (50% removal after 50 days). Also, more Dipteryx seeds were dispersed at La Selva than in fragmented forests. Contrary to our predictions, removal of Carapa seeds was equally high among all four sites, and there was a trend for more seeds of Carapa to be dispersed in fragments than in La Selva. Our results suggest that fragmentation effects on tree seed fate may be specific to species in question and contingent on the animal biota involved, and that management strategies for timber production based on regeneration from seed may differ between forest patches and extensive forests.     

Explaining Legume Success in Tropical Dry Forests Based on Seed Germination Niches: A New Hypothesis

To test a new hypothesis explaining Fabaceae success in tropical dry forests, we compared seed germination of 34 species including legumes and non‐legumes. Legume seeds germinated twice as fast with higher final percentages compared to other taxa, which may afford them a competitive advantage in highly seasonal environments.     

Effects of Logging on the Diversity of Lianas in a Lowland Tropical Rain Forest in Hainan Island, South China

Lianas are an integral part of tropical forest ecosystems, which usually respond strongly to severe disturbances, such as logging. To compare the effect of different logging systems on the lianas diversity in tropical rain forest, we recorded all lianas and trees ≥1 cm dbh in two 40-year-old forest sites after clear cutting (CC) and selective cutting (SC) as well as in an old-growth (OG) lowland tropical rain forest on Hainan Island in south China. Results showed that OG contained fewer liana stems and lower species richness (stems: 261, richness: 42 in 1 ha) than CC (606, 52) and SC (727, 50). However, OG had the highest Fisher's α diversity index (17.3) and species richness per stem (0.184). Species composition and dbh class distribution of lianas varied significantly with different logging systems. The mean liana dbh in OG (22.1 cm) were higher than those in CC (7.0 cm) and SC (10.4 cm). Stem twining was the most frequent climbing mechanism represented in the forest, as shown by the greatest species richness, abundance, basal area, and host tree number with this mechanism. The percent of host tree stems ≥4 cm dbh hosting at least one liana individual in SC (39%) was higher than CC (23%) and OG (19.5%). Large host trees (dbh≥60 cm) were more likely to be infested by lianas in SC and OG. Our study demonstrated that logging disturbance could significantly change the composition and structure of liana communities in the lowland tropical rain forest of south China.