Kathryn E. Stoner

Effects of Forest Fragmentation on Pollinator Activity and Consequences for Plant Reproductive Success and Mating Patterns in Bat-pollinated Bombacaceous Trees1

ABSTRACT Forest fragmentation and the resulting spatial isolation of tree species can modify the activity of pollinators and may have important implications for the reproductive success and mating systems of the plants they pollinate. The objectives of this study were to (1) evaluate the effect of forest fragmentation on pollinator activity in bat-pollinated bombacaceous trees and (2) determine the effects of forest fragmentation on reproductive success and mating systems of bombacaceous trees. We studied these parameters in three bombacaceous tree species in tropical seasonal forest of Chamela, Jalisco, Mexico, and Osa and Guanacaste, Costa Rica. For Ceiba aesculifolia, more visits were observed in fragments by both Glossophaga soricina and Leptonycteris curasoae. For Ceiba grandiflora, Musonycteris harrisoni visited flowers exclusively in forest and G. soricina visited more flowers in forest than in fragments; no difference was shown by L. curasoae. For Ceiba pentandra in Chamela, no differences were found in visitation by G. soricina between forest and fragments; L. curasoae visited significantly more flowers in forest. Ceiba pentandra received more visits by Phyllostomus discolor than G. soricina in Guanacaste, whereas no bat visitors were observed in Osa. Total mean flower production was greater in fragments than forest for C. aesculifolia, whereas no difference was observed for C. grandiflora. Fruit set was greater in forest than in fragments for C. grandiflora, whereas no difference was observed for C. aesculifolia. Outcrossing rates were high for C. aesculifolia and C. grandiflora in Chamela, and for C. pentandra in Guanacaste, independent of tree habitat, while C. pentandra in Osa showed a mixed-mating system. The effects of forest fragmentation on bat pollinators, plant reproductive success, and mating patterns varied depending upon the bombacaceous species. This variability was associated with the effects that forest fragmentation may have on differences in flowering patterns, bat foraging behavior, and plant self-incompatibility systems.

Evolution and function of routine trichromatic vision in primates.

Abstract Evolution of the red-green visual subsystem in trichromatic primates has been linked to foraging advantages, namely the detection of either ripe fruits or young leaves amid mature foliage. We tested competing hypotheses globally for eight primate taxa: five with routine trichromatic vision, three without. Routinely trichromatic species ingested leaves that were “red shifted” compared to background foliage more frequently than species lacking this trait. Observed choices were not the reddest possible, suggesting a preference for optimal nutritive gain. There were no similar differences for fruits although red-greenness may sometimes be important in close-range fruit selection. These results suggest that routine trichromacy evolved in a context in which leaf consumption was critical.

Factors affecting phenological patterns of bombacaceous trees in seasonal forests in Costa Rica and Mexico

We compared phenological patterns of tree species of the family Bombacaceae in three seasonal forests in Mexico and Costa Rica whose dry seasons vary in duration and intensity. The objectives were to (1) determine intraspecific variation in phenology between sites in different geographic locations with different precipitation regimes, (2) compare interspecific phenological patterns within sites during one year, and (3) document seasonal pollinator use of floral resources at one site in relation to the flowering phenology of these species. To determine the sequence of phenological events in trees of the family Bombacaceae across three study sites, phenology of marked individuals was recorded every 2 wk from September 2000 through August 2001 for six species. To estimate the importance of bombacaceous species in the diet of nectarivorous bats, pollen samples were collected from the bodies or feces of bats once every 2 wk during flowering. Our study suggests that phenological patterns of the Bombacaceae family in Neotropical dry forests are mainly constrained by phylogenetic membership and adaptive selective pressures associated with competition for pollinators. Abiotic factors related to precipitation and soil water content appear to be regulating leaf flushing and abscission, but the principal causes of flowering are related to ultimate factors associated with competition for pollinators. This study is the first that evaluates the phenological pattern of species and genera of the same family at different latitudes in a similar life zone.

Diet of spider monkeys (Ateles geoffroyi) in Mesoamerica: current knowledge and future directions.

Here we review all published articles and book chapters, as well as unpublished theses and data of Ateles geoffroyi diet to (1) summarize the literature; (2) synthesize general feeding patterns; (3) document plant taxonomic similarity in diet across study sites; and (4) suggest directions for future research and conservation priorities. We found 22 samples from five countries: Mexico, Guatemala, El Salvador, Costa Rica and Panama. Tropical wet forest is the most studied habitat (N=13 samples), followed by tropical dry forest (6) and tropical moist forest (3). Most samples have been carried out in large protected forests. In spite of showing an overall high dietetic diversity (364 species, 76 families), A. geoffroyi concentrated the majority of feeding time on a few species in the families Moraceae and Fabaceae. At all study sites fruits were the most common food item in the diet followed by leaves. Furthermore, a greater variety of food items and less fruit were consumed in forest fragments. These findings suggest that fruit shortage in fragments results in primates using foods of presumably lower energetic content such as leaves. Similarity in diet was higher among groups geographically closer to each other than among distant groups, showing that the floristic and phenological characteristics of the forest can influence diet composition. We conclude that several years of data are required to fully describe the dietary list of A. geoffroyi at any one site, as studies of the same group over different years shared as little as 56% of species. As most populations of A. geoffroyi live in highly fragmented landscapes, it is crucial to carry out studies in these areas to evaluate (1) changes in diet and activity patterns that may negatively affect survival; and (2) habitat attributes that may favor their persistence in altered landscapes. Am. J. Primatol. 71:8–20, 2009.

Effects of pollination by bats on the mating system of Ceiba pentandra (Bombacaceae) populations in two tropical life zones in Costa Rica

The identity and behavior of pollinators are among the main factors that determine the reproductive success and mating system of plants; however, few studies have directly evaluated the relationship between pollinators and the breeding system of the plants they pollinate. It is important to document this relationship because the global decline in pollinators may significantly affect the breeding systems of many animal-pollinated plants, particularly specialized systems. Ceiba pentandra is a tropical tree that has chiropterophilic flowers and a variable breeding system throughout its distribution, ranging from fully self-incompatible, to a mixed system with different degrees of selfing. To determine if regional differences in pollinators may result in regional differences in the outcrossing rate of this species, we used systematic observations of pollinator behavior in two tropical life zones and high-resolution genetic analysis of the breeding system of populations from these two regions using microsatellites. We found a predominantly self-incompatible system in regions with high pollinator visitation, while in environments with low pollinator visitation rates, C. pentandra changed to a mixed mating system with high levels of self-pollination.

Population dynamics, reproduction, and diet of the lesser long-nosed bat (Leptonycteris curasoae) in Jalisco, Mexico: implications for conservation

We estimate fluctuations in population size and sex ratio, documentbreeding behavior and reproduction, and determine the diet of a population ofthe lesser long-nosed bat, Leptonycteris curasoae, in anisland cave in Chamela Bay, Jalisco, Mexico, with monthly sampling during anannual cycle (October 1999–October 2000). Based on the area of thecaves ceiling and wall covered with L. curasoae inrelation to the potential roost area without them, in 1999 the abundanceincreased from 80% in October to 100% in November and December. In 2000 thepopulation decreased to 80% in January, 50% in February, 30% in March, 20% inApril, 10% in May, 5% in June and July, and less than 1% in August. Thepopulation rapidly increased to 60% in September and to 80% in October.Throughout the year there were significantly more males than females; however,there was significant heterogeneity over months. In September–Novemberthere were more females, but in December–August there were more malespresent. The majority of pregnant and lactating females were observed fromDecember to March and in July, while males were reproductive fromSeptember–January and in May–June. Breeding activity was observed inthe cave in November–December. Twenty-six species of plants were consumedduring the year, based on pollen identification from fecal samples. Bombacaceousspecies were the most important component of the diet from January to May andCactaceae were most important in June–September. Peak abundance and reproductive activitycoincided with peak flower resource availability, which occurred between Octoberand January and in June–July. The year-round presence and reproductiveactivity of L. curasoae at this site throughout the yeardemonstrate that many individuals are annual residents in this area and indicatethe importance of this roosting site. In order to develop a successfulconservation program for L. curasoae, in addition toprotecting migratory corridors and northern maternity roosts, it is equallyimportant to identify and protect areas that function as breeding colonies andyear-round sanctuaries for resident populations in the south.

Local and Landscape Factors Determining Occurrence of Phyllostomid Bats in Tropical Secondary Forests

Neotropical forests are being increasingly replaced by a mosaic of patches of different successional stages, agricultural fields and pasture lands. Consequently, the identification of factors shaping the performance of taxa in anthropogenic landscapes is gaining importance, especially for taxa playing critical roles in ecosystem functioning. As phyllostomid bats provide important ecological services through seed dispersal, pollination and control of animal populations, in this study we assessed the relationships between phyllostomid occurrence and the variation in local and landscape level habitat attributes caused by disturbance. We mist-netted phyllostomids in 12 sites representing 4 successional stages of a tropical dry forest (initial, early, intermediate and late). We also quantitatively characterized the habitat attributes at the local (vegetation structure complexity) and the landscape level (forest cover, area and diversity of patches). Two focal scales were considered for landscape characterization: 500 and 1000 m. During 142 sampling nights, we captured 606 individuals representing 15 species and 4 broad guilds. Variation in phyllostomid assemblages, ensembles and populations was associated with variation in local and landscape habitat attributes, and this association was scale-dependent. Specifically, we found a marked guild-specific response, where the abundance of nectarivores tended to be negatively associated with the mean area of dry forest patches, while the abundance of frugivores was positively associated with the percentage of riparian forest. These results are explained by the prevalence of chiropterophilic species in the dry forest and of chiropterochorous species in the riparian forest. Our results indicate that different vegetation classes, as well as a multi-spatial scale approach must be considered for evaluating bat response to variation in landscape attributes. Moreover, for the long-term conservation of phyllostomids in anthropogenic landscapes, we must realize that the management of the habitat at the landscape level is as important as the conservation of particular forest fragments.

Landscape and patch attributes impacting medium- and large-sized terrestrial mammals in a fragmented rain forest

Understanding the response of biodiversity to land-use changes is an important challenge for ecologists. We assessed the effects offive landscape metrics (forest cover, number of patches, edge density, mean inter-patch isolation distance and matrix quality) and three patch metrics (patch size, shape and isolation) on the number of species and patchoccupancyofmedium-andlarge-sizedterrestrialmammalsinthefragmentedLacandonarainforest,Mexico.We sampled mammal assemblages in 24 forest patches and four control areas within a continuous forest. The landscape metrics were measured within a 100-ha buffer, and within a 500-ha buffer from the centre of each sampling site. A total of 21 species from 13 families was recorded. The number of species increased with shape complexity and patch sizeatthepatchscale,andwithmatrixqualitywithin100-halandscapes.Whenconsidering500-halandscapes,only the number of patches (i.e. forest fragmentation level) tended to have a negative influence at the community level. Different landscape and patch metrics predicted the occurrence of each species within the sites. Our results indicate that there is a gradient of tolerance to forest cover change, from highly sensitive species to those tolerant of, or even benefited by, forest-cover change.

Effectiveness of Spider Monkeys (Ateles geoffroyi vellerosus) as Seed Dispersers in Continuous and Fragmented Rain Forests in Southern Mexico

Seed dispersal is considered a key process determining spatial structure and dynamics of plant populations, and has crucial implications for forest regeneration. We evaluated the effectiveness of spider monkeys (Ateles geoffroyi) as seed dispersers in continuous and fragmented habitats to test if this interaction is altered in forest fragments. We documented fruit and seed handling, defecation patterns, diversity and composition of seeds in feces, and seed germination of defecated and control seeds in the Lacandona rainforest, Mexico. For most species contributing to 80% of total fruit feeding time, monkeys swallowed and spat seeds, but swallowing was the most frequent seed handling category in continuous and fragmented forests. However, the proportion of feeding records of swallowed seeds was higher in continuous forest (0.59) than in fragments (0.46), whereas the opposite was true for proportion of dropped seeds (0.16 vs. 0.31). This pattern was reflected in the number of fecal samples containing seeds, which was greater in continuous (95.5%) than in fragmented forests (82.5%). Seeds in fecal samples included a total of 71 species from 23 plant families. The numbers of defecated seed species were similar between forest conditions, and in both cases most seeds (>86%) were undamaged. Defecated seeds showed greater germination percentages than control seeds in all of the five species evaluated. Although we identified some differences in seed handling and the percentage of feces with seeds between continuous forest and fragments, our results indicate that, in general terms, spider monkeys are effective seed dispersers in both forest conditions.

Effectiveness of bats as pollinators of Stenocereus stellatus (Cactaceae) in wild, managed in situ, and cultivated populations in La Mixteca Baja, central Mexico

Stenocereus stellatus is an endemic, self-incompatible, columnar cactus found in central Mexico where many of its wild populations have been fragmented. As an economically important species of fruit-producing cactus, S. stellatus occurs in wild, managed in situ, and cultivated populations. The objectives of this study were to determine the effective pollinators of S. stellatus, to compare pollinator visits and reproductive parameters among the three types of populations, and to determine if nectar feeding-bats are moving among populations. Effective pollinators were the nectarivorous bats Choeronycteris mexicana, Leptonycteris curasoae, and L. nivalis. Fewer total visits per flower per night and fewer visits by Choeronycteris were observed in cultivated populations, while the opposite pattern was observed for Leptonycteris. One aggressive interaction was filmed in which Choeronycteris was physically displaced by Leptonycteris, and Choeronycteris visits were significantly affected by Leptonycteris visits. Cultivated populations received more pollen grains and had more fruit set. Variation in pollinator visits between different populations and the consequent effects on reproductive success were likely a result of competition between bat species, and differences in foraging and in sensitivity of bat species to human populations. Three marked L. curasoae traveled 15 km from their roosting site to their foraging area, and one visited cultivated and managed populations, suggesting that this species may be particularly important in moving pollen among populations.