The Landscape Ecology of Tropical Secondary Forest in Montane Costa Rica

Multinomial logistic models of land use/land cover in montane Costa Rica and landscape pattern analysis showed that relative to agriculture, secondary forest occurred closer to old-growth forest, further from roads, in forest reserves, and at higher elevations. Collinearity between explanatory variables yielded simple multivariate models; proportion of surrounding old growth predicted secondary forest most accurately. An old-growth matrix [mean patch size (MPS) 24.5 ha], located mainly within protected areas, dominated elevations greater than 2500 m. A matrix of agriculture (MPS 23.5 ha), with smaller patches (approximately 9 ha) of secondary forest and old growth, dominated elevations from 1500 to 2500 m. Combining secondary forest with old growth decreased forest patch number and increased MPS from 7.3 to 37.1 ha. I concluded that: (a) secondary forest pattern is nonrandom, so ancillary data will aid its mapping with satellite imagery. The variables elevation, agriculture distance, road distance, and population density distinguished secondary forest from old growth with 74% accuracy; (b) socioeconomic and biological forces probably interact to create these secondary forest patterns; and (c) the strong association between secondary forest and old growth supports the concept that tropical forest recovery depends on the landscape structure of remnant forest. Received 16 February 1999; accepted 20 August 1999.     

Tropical Montane Forest Restoration in Costa Rica: Overcoming Barriers to Dispersal and Establishment

Tropical forests are being cleared at an alarming rate although our understanding of their ecology is limited. It is therefore essential to design restoration experiments that both further our basic knowledge of tropical ecology and inform management strategies to facilitate recovery of these ecosystems. Here we synthesize the results of research on tropical montane forest recovery in abandoned pasture in Costa Rica to address the following questions: (1) What factors limit tropical forest recovery in abandoned pasture? and (2) How can we use this information to design strategies to facilitate ecosystem recovery? Our results indicate that a number of factors impede tropical forest recovery in abandoned pasture land. The most important barriers are lack of dispersal of forest seeds and seedling competition with pasture grasses. High seed predation, low seed germination, lack of nutrients, high light intensity, and rabbit herbivory also affect recovery. Successful strategies to facilitate recovery in abandoned pastures must simultaneously overcome numerous obstacles. Our research shows that establishment of woody species, either native tree seedlings or early‐successional shrubs, can be successful in facilitating recovery, by enhancing seed dispersal and shading out pasture grasses. On the contrary, bird perching structures alone are not an effective strategy, because they only serve to enhance seed dispersal but do not reduce grass cover. Remnant pasture trees can serve as foci of natural recovery and may enhance growth of planted seedlings. Our results highlight the importance of: (1) understanding the basic biology of an ecosystem to design effective restoration strategies; (2) comparing results across a range of sites to determine which restoration strategies are most generally useful; and (3) considering where best to allocate efforts in large‐scale restoration projects.     

Seed Availability as a Limiting Factor in Forest Recovery Processes in Costa Rica

Abandoned pastures and secondary forests are increasingly prominent features of tropical landscapes. Forest regrowth on abandoned pastures is generally slow and virtually limited to regeneration from seeds from external sources, since agricultural activities alter site conditions. We hypothesize that seed availability is a major limiting factor in forest recovery on abandoned pastures. This hypothesis was tested by studying the seed bank, seed rain, and seed predation in a small pasture (1 ha) situated in a forest‐pasture mosaic in northwestern Costa Rica. The tree seed density in the pasture seed bank was much lower (21/m²) than the density in the seed bank of a neighboring secondary forest (402/m²). Within a period of five weeks, 23 tree seeds entered the pasture by seed rain. This number is low compared to densities found in closed forests but higher than densities reported in other studies where virtually no seeds were found beyond 20 m from the forest edge. Possibly the small size of the pasture with seed sources nearby and the small‐scale landscape mosaic enhance seed dispersal. Predation limits the seed density in pastures, with 42% of the woody species consumed by predators. The low seed density in the seed bank, and hampered recruitment combined with significant losses, pose severe restrictions to forest recovery on abandoned pastures. Moderate land use, and small sized clearings with seed sources nearby may increase the pace of recovery. Nevertheless, forest establishment may still take a considerable time. Thus, enlarging the available pool of species may be a worthwhile management strategy.     

Reproductive Ecology of Understory Species in a Tropical Montane Forest in Costa Rica1

The reproductive ecology of nine hermaphroditic understory species in a tropical montane Quercus forest was studied at two sites (2300 and 2600 m elev.) in the Cordillera de Talamanca, Costa Rica. Flower life span, studied in six species, averaged 4.4 d. This is longer than flower life spans found in the Monteverde cloud forest (2.7 d) and comparable to flower life spans found for arctic and alpine species. We studied the breeding system in five species and found no self-incompatible species. Four species proved self-compatible, and three of these showed autogamy. The main diurnal insect pollinator was the bumblebee Bombus ephippiatus. Natural fruit set was low (8-32%) in six species with few seeds per fruit, while two many-seeded species showed a high rate of fruit set (90 and 96%). The incidence of pre–dispersal seed predation was high; the percentage of seeds infested in four species ranged from 8 to 56 percent.     

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.     

Seed Dynamics in Relation to Gaps in a Tropical Montane Rainforest of Hainan Island, South China： （I） Seed Rain

Seed dynamics is an important part of stand dynamics in forest ecosystems. In this paper, 26 gaps were randomly selected to study the influence of gaps on the spatial and temporal patterns of seed rains in a tropical montane rainforest of Hainan Island, South China. Three zones for each gap, including outside gap zone （Non-gap）, transitional gap zone （EG-CG）, and central gap zone （CG）, were designed, and fourseed traps （each lm x lm in size） were placed in each zone. Seed rains were collected by these traps every 10 days from June 2001 to May 2002. Seed rain varied greatly with season and generally exhibited a pattern of unimodal change during the study period： seed abundance and species richness were both greater in the wet season than in the dry season. Gaps significantly influenced the temporal patterns of both species richness and density of seed rains. Gaps had no significant influences on the spatial distribution patterns of seed rain species richness, but significantly affected the spatial distribution pattern of seed rain densities. Among the three different zones of gaps, the outside gap zone generally received more seeds inputs than the two other gap zones.     

Composition and Dynamics of Functional Groups of Trees During Tropical Forest Succession in Northeastern Costa Rica

We compared the functional type composition of trees ≥10 cm dbh in eight secondary forest monitoring plots with logged and unlogged mature forest plots in lowland wet forests of Northeastern Costa Rica. Five plant functional types were delimited based on diameter growth rates and canopy height of 293 tree species. Mature forests had significantly higher relative abundance of understory trees and slow-growing canopy/emergent trees, but lower relative abundance of fast-growing canopy/emergent trees than secondary forests. Fast-growing subcanopy and canopy trees reached peak densities early in succession. Density of fast-growing canopy/emergent trees increased during the first 20 yr of succession, whereas basal area continued to increase beyond 40 yr. We also assigned canopy tree species to one of three colonization groups, based on the presence of seedlings, saplings, and trees in four secondary forest plots. Among 93 species evaluated, 68 percent were classified as regenerating pioneers (both trees and regeneration present), whereas only 6 percent were classified as nonregenerating pioneers (trees only) and 26 percent as forest colonizers (regeneration only). Slow-growing trees composed 72 percent of the seedling and sapling regeneration for forest colonizers, whereas fast-growing trees composed 63 percent of the seedlings and saplings of regenerating pioneers. Tree stature and growth rates capture much of the functional variation that appears to drive successional dynamics. Results further suggest strong linkages between functional types defined based on adult height and growth rates of large trees and abundance of seedling and sapling regeneration during secondary succession.
Abstract in Spanish is available at http://www.blackwell-synergy.com/loi/btp     

Avian Habitat Preference in Tropical Forest Restoration in Southern Costa Rica

An important question for tropical forest restoration is whether degraded lands can be actively managed to attract birds. We censused birds and measured vegetation structure at 27 stations in young (6–9‐yr old) actively and passively restored pasture and old growth forest at Las Cruces Biological Station in southern Costa Rica. During 481 10‐min point counts, we detected a high diversity—186 species—of birds using the restoration area. Surprisingly, species richness and detection frequency did not differ among habitats, and proportional similarity of bird assemblages to old growth forest did not differ between restoration treatments. Bird detection frequency was instead explained by exotic grass cover and understory stem density—vegetation structures that were not strongly impacted by active restoration. The similarity of bird assemblages in actively and passively restored forest may be attributed to differential habitat preferences within and among feeding guilds, low structural contrast between treatments, or the effect of nucleation from actively restored plots into passively restored areas. Rapid recovery of vegetation in this recently restored site is likely due to its proximity to old growth forest and the lack of barriers to effective seed dispersal. Previous restoration studies in highly binary environments (i.e., open pasture vs. tree plantation) have found strong differences in bird abundance and richness. Our data contradict this trend, and suggest that tropical restoration ecologists should carefully consider: (1) when the benefits of active restoration outweigh the cost of implementation; and (2) which avian guilds should be used to measure restoration success given differential responses to habitat structure.     

Establishment of Epiphytic Bromeliads in Successional Tropical Premontane Forests in Costa Rica

Plant community composition is the combined result of species-specific competitive abilities and the availability of propagules. For epiphytic plants, current hypotheses consider that dispersal-related factors are most important. By controlling seed dispersal constraints, we experimentally examined whether the community composition of epiphytic bromeliads in a tropical premontane area is determined during early phases of seedling recruitment. Also, we tested whether establishment success was related to eco-physiological traits of the species. A total of 7200 seeds were artificially affixed on several host trees in two secondary forest patches and in a mature forest stand. Four bromeliad species with differing physiological characteristics (CAM, C₃-CAM, and C₃) and habitat preference (secondary vs. primary forest) were selected. We found that differences in seed germination probability among habitats and species were not likely to influence community assembly. After 2 yr, seedling survival and plant development were relatively higher in the early-successional forest. Seedling establishment success was not associated with specific physiological and morphological adaptations or habitat preference of the studied species. Our results were not consistent with the described community composition and rates of population recruitment of the studied species in the same successional habitats. The results support the hypothesis that chance and historic events related to seed dispersal have an important influence on community assembly of epiphytic plants. In addition, differences in growth rates and reproductive turnover among species are expected to influence the relative abundance and recruitment rates in a particular habitat.     

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.     

Seed Dispersal by Monkeys and the Fate of Dispersed Seeds in a Peruvian Rain Forest1

Primary seed dispersal by two species of monkeys and the effects of rodents and dung beetles on the fate of dispersed seeds are described for a rain forest in southeastern Perú. During the six-month study period (June–November 1992) spider monkeys (Ateles paniscus) dispersed the seeds of 71 plant species, whereas howler monkeys (Alouatta seniculus) dispersed seeds of 14 species. Spider and howler monkeys also differed greatly in their ranging behavior and defecation patterns, and as a consequence, produced different seed rain patterns. Monkey defecations were visited by 27 species of dung beetles (Scarabaeidae). Dung beetles buried 41 percent of the seeds in the dung, but the number of seeds buried varied greatly, according to seed size. Removal rates of unburied seeds by rodents varied between 63–97 percent after 30 d for 8 plant species. The presence of fecal material increased the percentage of seeds removed by seed predators, but this effect became insignificant with time. Although seed predators found some seeds buried in dung balls (mimicking burial by dung beetles), depth of burial significantly affected the fate of these seeds. Less than 35 percent of Brosimum lactescens seeds buried inside dung balls at a depth of 1 cm remained undiscovered by rodents, whereas at least 75 percent of the seeds escaped rodent detection at a depth of 3 cm and 96 percent escaped at 5 cm. Both dung beetles and rodents greatly affected the fate of seeds dispersed by monkeys. It is thus important to consider postdispersal factors affecting the fate of seeds when assessing the effectiveness of frugivores as seed dispersers.     

Chimpanzee (Pan troglodytes) Seed Dispersal in an Afromontane Forest: Microhabitat Influences on the Postdispersal Fate of Large Seeds1

We examined the postdispersal fate of large seeds (≥5 mm) dispersed by chimpanzees in an afromontane forest to evaluate aspects of the effectiveness of seed dispersal by chimpanzees, Pan troglodytes. We assessed the influence of six microhabitat characteristics on seed persistence and germination in seeds dispersed in chimpanzee feces and “wadges.” A total of 257 fecal samples and 56 wadges were located over a 4‐mo period by tracking a semi‐habituated chimpanzee community on day follows. Forty‐nine (19.1%) of the fecal samples contained large seeds from five different tree species. The majority of fecal samples with seeds contained seeds from the mature forest tree Olea capensis (Oleaceae) (83.7%). Forty‐two wadges (75%) contained seeds from the mature forest tree Syzygium guineense (Myrtaceae). Seeds were monitored at their deposition site for removal and germination up to 49 d following deposition. We collected data on the microhabitat surrounding each fecal and wadge sample. Multivariate analyses indicated that while fecal and wadge samples were not clustered into particular microhabitats, there was little overlap in the microhabitats in which wadges and fecal samples were deposited. Significantly more seeds persisted over 49 d in wadges (67.9%) than in feces (30.3%). Elevation was the only microhabitat variable determined to have a significant influence on seed persistence, whereas slope was determined to have a significant influence on germination.     

The Effect of Dung and Dispersal on Postdispersal Seed Predation of Attalea phalerata (Arecaceae) by Bruchid Beetles1

Low postdispersal mortality of palm seeds in tapir dung is hypothesized to result from the mechanical barrier provided by dung against bruchid infestation and/or from the distance to adult palms at which seeds are dispersed. We tested these hypotheses by distributing endocarps of Attalea phalerata Mart. ex Spreng. in experimental dung piles in Beni, Bolivia. Predation rates were significantly lower for seeds covered by dung than for exposed or partially covered seeds, but did not differ between seeds placed below and 50 m away from palms. Thus, dung, not short‐distance dispersal, protects seeds against bruchid beetles, and may ultimately promote survival of palm seeds.     

The Role of Arboreal Seed Dispersal Groups on the Seed Rain of a Lowland Tropical Forest1

Most tropical plants produce fleshy fruits that are dispersed primarily by vertebrate frugivores. Behavioral disparities among vertebrate seed dispersers could influence patterns of seed distribution and thus forest structure. This study investigated the relative importance of arboreal seed dispersers and seed predators on the initial stage of forest organization–seed deposition. We asked the following questions: (1) To what degree do arboreal seed dispersers influence the species richness and abundance of the seed rain? and (2) Based on the plant species and strata of the forest for which they provide dispersal services, do arboreal seed dispersers represent similar or distinct functional groups? To answer these questions, seed rain was sampled for 12 months in the Dja Reserve, Cameroon. Seed traps representing five percent of the crown area were erected below the canopies of 90 trees belonging to nine focal tree species: 3 dispersed by monkeys, 3 dispersed by large frugivorous birds, and 3 wind‐dispersed species. Seeds disseminated by arboreal seed dispersers accounted for ca 12 percent of the seeds and 68 percent of the seed species identified in seed traps. Monkeys dispersed more than twice the number of seed species than large frugivorous birds, but birds dispersed more individual seeds. We identified two distinct functional dispersal groups, one composed of large frugivorous birds and one composed of monkeys, drop dispersers, and seed predators. These groups dispersed plants found in different canopy strata and exhibited low overlap in the seed species they disseminated. We conclude it is unlikely that seed dispersal services provided by monkeys could be compensated for by frugivorous birds in the event of their extirpation from Afrotropical forests.     

Mammal Abundances and Seed Traits Control the Seed Dispersal and Predation Roles of Terrestrial Mammals in a Costa Rican Forest

In Neotropical forests, mammals act as seed dispersers and predators. To prevent seed predation and promote dispersal, seeds exhibit physical or chemical defenses. Collared peccaries (Pecari tajacu) cannot eat some hard seeds, but can digest chemically defended seeds. Central American agoutis (Dasyprocta punctata) gnaw through hard‐walled seeds, but cannot consume chemically defended seeds. The objectives of this study were to determine relative peccary and agouti abundances within a lowland forest in Costa Rica and to assess how these two mammals affect the survival of large seeds that have no defenses (Iriartea deltoidea, Socratea exorrhiza), physical defenses (Astrocaryum alatum, Dipteryx panamensis), or chemical defenses (Mucuna holtonii) against seed predators. Mammal abundances were determined over 3 yrs from open‐access motion‐detecting camera trap photos. Using semi‐permeable mammal exclosures and thread‐marked seeds, predation and dispersal by mammals for each seed species were quantified. Abundances of peccaries were up to six times higher than those of agoutis over 3 yrs, but neither peccary nor agouti abundances differed across years. Seeds of A. alatum were predominantly dispersed by peccaries, which did not eat A. alatum seeds, whereas non‐defended and chemically defended seeds suffered high levels of predation, mostly by peccaries. Agoutis did not eat M. holtonii seeds. Peccaries and agoutis did not differ in the distances they dispersed seeds. This study shows that seed fates are contingent upon many factors such as seed defenses, frugivore–granivore abundances, and seed‐handling capabilities. Mammal–seed interactions are complex; the outcomes of these interactions depend on the inherent characteristics of seeds and their potential dispersers.     

Size and Structure of Fine Root Systems in Old-growth and Secondary Tropical Montane Forests (Costa Rica)

The fine root systems of three tropical montane forests differing in age and history were investigated in the Cordillera Talamanca, Costa Rica. We analyzed abundance, vertical distribution, and morphology of fine roots in an early successional forest (10–15 years old, ESF), a mid‐successional forest (40 years old, MSP), and a nearby undisturbed old‐growth forest (OGF), and related the root data to soil morphological and chemical parameters. The OGF stand contained a 19 cm deep organic layer on the forest floor (i.e., 530 mol C/m²), which was two and five times thicker than that of the MSF (10 cm) and ESF stands (4 cm), respectively. There was a corresponding decrease in fine root biomass in this horizon from 1128 g dry matter/m² in the old‐growth forest to 337 (MSF) and 31 g/m² (ESF) in the secondary forests, although the stands had similar leaf areas. The organic layer was a preferred substrate for fine root growth in the old‐growth forest as indicated by more than four times higher fine root densities (root mass per soil volume) than in the mineral topsoil (0–10 cm); in the two secondary forests, root densities in the organic layer were equal to or lower than in the mineral soil. Specific fine root surface areas and specific root tip abundance (tips per unit root dry mass) were significantly greater in the roots of the ESF than the MSF and OGF stands. Most roots of the ESF trees (8 abundant species) were infected by VA mycorrhizal fungi; ectomycorrhizal species (Quercus copeyemis and Q. costaricensis) were dominant in the MSF and OGF stands. Replacement of tropical montane oak forest by secondary forest in Costa Rica has resulted in (1) a large reduction of tree fine root biomass; (2) a substantial decrease in depth of the organic layer (and thus in preferred rooting space); and (3) a great loss of soil carbon and nutrients. Whether old–growth Quercus forests maintain a very high fine root biomass because their ectomycorrhizal rootlets are less effective in nutrient absorption than those of VA mycorrhizal secondary forests, or if their nutrient demand is much higher than that of secondary forests (despite a similar leaf area and leaf mass production), remains unclear.