E. Raymond Heithaus

Foraging Patterns and Resource Utilization in Seven Species of Bats in a Seasonal Tropical Forest

Many tropical bats eat fruit, nectar, and pollen, and many tropical plants are pollinated or dispersed by bats. These groups make up a coevolved system that illustrates the effects plants can have on animal populations, and conversely, the effects animals can have on plant populations. This paper reports a 2—yr intensivie study of one bat—plant community in a seasonal Costa Rican forest. Seven common phyllostomatid bat species visited flowers or fruits. These were Glossophaga soricina, Phyllostomus discolor, Artibeus jamaicensis, Artibeus lituratus, Sturnira lilium, and Carollia perspecillata. The incidence of nectar ivory was high among these species, even among the species previously considered to be frugivores. Flora resources were seasonally abundant and competition for these resources appeared minimal during the period of peak abundance, but only G. ssoricina was nectarivorous during the period of low flower abundance. Fruit resources were more evenly available through the year and were more finely divided among the species of bats. There was a correlation between size of bat and the average size of fruits eaten. To the extent that competition for food has influenced the structure of this bat community, competition for fruits was more important than competition for nectar and pollen in determining species diversity. Resource distributions through space and time also infuenced bat foraging and reproductive behaviors. Small species of bats feed on resources of high abundance, whereas large species utilize resources that are patchy in time and space. The latter species probably forage in groups to maximize foraging efficiency. Reproductive behavior is seasonal and correlated with resource abundance. The flowering periods of plant species tend to be displaced, suggesting competition among plants for bat—pollinator services. A combination of the timing of plant—reproductive behavior and bat foraging characteristics promotes long—distance outcrossing and seed dispersal. These are critical factors in determining the low—density propulations characteristic of many tropical plant species.

Seed Predation by Rodents on Three Ant-Dispersed Plants

Seed predation by small mammals has been proposed as one selective force in the evolution of ant-dispersal (myrmecochory) in many herbaceous plants of mesic deciduous forests. Three myrmecochorous species, Asarum canadense, Jeffersonia diphylla, and Sanguinaria cana- densis, were studied in the Monongahela National Forest, West Virginia, USA, to (a) assess the impact of seed predators on seed mortality, (b) compare seed removal rates when ants were present vs. absent, and (c) evaluate the effects of elaiosome removal, seed burial, and doubling seed number per depot on rates of seed predation. Seed predators, especially rodents, cause more mortality among these woodland herbs than pre- viously thought. Predispersal seed predation by rodents destroyed 24% and 47% of the seed crops of A. canadense and J. diphylla, respectively. The proportions of A. canadense seeds lost to predators varied among sites. Sanguinaria canadensis also suffered seed predation before capsules dehisced. Peromyscus leucopus was the most common seed predator. In exclosure experiments, seed predators removed 70% of the A. canadense seeds when dispersal by ants was prevented, but only 24-39o of the seeds suffered predation when ants were allowed access. Seed predators removed 84% of the S. canadensis seeds when ants were excluded, but 13- 43% were lost when also exposed to ants. These estimated minimal proportions of seeds lost to predators when ants were allowed access differed between two study sites, but myrmecochory clearly reduced seed predation at parent plants. In laboratory experiments, P. leucopus located buried A. canadense and S. canadensis seeds less frequently than seeds on the surface (67.5% vs. 100%). Consumption of buried seeds by rodents was reduced when elaiosomes were removed, as would be done by ants in natural conditions. Increasing the delectability of seeds through adding olfactory cues or doubling seed number per depot did not increase the frequency of predation, because mice were able to locate depots without these additional cues.

Bat Activity and Pollination of Bauhinia Pauletia: Plant-Pollinator Coevolution

The relationship between the pollination biology of a tropical plant, Bauhinia pauletia, and the foraging strategies of the nectarivorous bats visiting it was studied. At least two bat species are pollen vectors, Plyllostomus discolor and Glossophaga soricina. Artibeus jamaicensis and Sturnira lilium were also captured near Bauhinia flowers. Larger bats (P. discolor) drain flowers of nectar and forage in groups, while smaller bats (G. soricina) make brief visits and forage independently. These foraging strategies should optimize energetic gain for the bats and promote outcrossing for the plant. Bauhinia pauletia is self-compatible, but is found where conditions favor outcrossing. Andromonoecism (the presence of hermaphrodite and male flowers) in this species appears to be an adaptation to pollination by large pollinators that also promotes outcrossing.

Coevolution between Bats and Plants

More than 250 species of bats eat some fruit, nectar, or pollen. In doing so, bats often provide dispersal and pollination services to at least 130 plant genera (Howell and Hodgkin, 1976). These interactions have profoundly influenced the evolution of some bats and plants. For example, the leaf-nosed bat, Leptonycteris sanborni, has morphological and physiological traits that allow it to subsist entirely on flowers and fruits, whereas the same traits apparently preclude the extensive use of insects (Howell and Hodgkin, 1976). On the other side of the interaction, plants such as Crescentia alata (the calabash tree) are so efficiently pollinated by bats that they are unable to reproduce without bat assistance. The structure of its flowers and the timing of nectar presentation preclude pollination by other animals.

ANTS REARRANGE THE VERTEBRATE-GENERATED SEED SHADOW OF A NEOTROPICAL FIG TREE

We studied the secondary movements of Ficus hondurensis seeds after their initial dispersal by vertebrates in Santa Rosa National Park, Costa Rica. Common vertebrate consumers of figs were various birds, bats, coatis, white-faced monkeys, and ctenosaurs. The ants Pheidole radosz- kowskii, P. fallax, and Atta cephalotes were common secondary disperers. Ants removed 25.2 to 97.7% of the seeds placed randomly in 275 groups (N = 13 700 seeds). Rodents did not attack these seeds. Ants removed seeds from vertebrate feces, but were more likely to remove seeds from fruit fragments. Ants found and depleted seed groups more rapidly in a late-successional forest site than under the fruiting tree. Some fig seeds that were discarded by ants germinated, indicating that such secondary movements of seeds may be beneficial to the parent plant.

FOOD FROM SEED-DISPERSAL MUTUALISM SHIFTS SEX RATIOS IN COLONIES OF THE ANT APHAENOGASTER RUDIS

Workers of Aphaenogaster rudis collect seeds of many species of spring-flowering, perennial herbs. This is part of a seed-dispersal system (myrmecochory) for which benefits to plants are documented, but consequences to ants have not been quantified. To test the predictions that colony size or reproductive output will be enhanced as a consequence of ants collecting seeds, we conducted a field experiment in a forest near Gambier, Ohio, in June and July 1993. Experimental colonies receiving seeds of Sanguinaria canadensis (N = 24 colonies) had ∼3.5 times as many gynes as control colonies (N = 27). Only 25% of control colonies produced any gynes, whereas 65% of experimental colonies did so. Control colonies produced as many males as experimental colonies. Access to seeds shifted the mass and numerical investment ratio in colony reproductive output toward female bias but did not affect the number of workers or queen size. These data support the hypothesis that myrmecochory is a true mutualism. Additionally, the experiment indicates that resource levels influence investment ratios in reproductive ants.

CUMULATIVE EFFECTS OF PLANT-ANIMAL INTERACTIONS ON SEED PRODUCTION BY BAUHINIA UNGULATA, A NEOTROPICAL LEGUME'

Seed production was studied in Bauhinia ungulata, a neotropical, perennial legume. Our goals were to identify the biotic factors influencing seed output, the magnitude and variability of their effects, and whether these effects were density dependent. We measured predispersal repro- ductive success in five stands, ranging in size from 18 to 175 ramets. Pollination success and flower herbivory were evaluated for 1375 flowers. Other sources decreasing seed output were observed by examining 1714 seedpods. Six factors led to reduction in potential seed-set. In order of the magnitude of their effects, these factors were lack of pollination, incomplete development of ovules in flowers that formed seedpods, herbivores that damaged flowers that could have been pollinated, bruchids that destroyed developing seeds, herbivores that damaged pistils, and herbivores that ate developing pods. Density dependence was observed for three of the factors: level of pollination success, seed predation, and herbivory on developing seedpods. There was significant variation among stands for the six factors that were measured in all stands. Key factor analysis was used to estimate the influence of these factors on variation among stands in seed-set. Seed predators and pollinators accounted for most of the observed variation. We conclude that pollinators and predators on seeds are potentially important to the population dynamics of this plant.

Seed dispersal mutualism and the population density of Asarum canadense, an ant-dispersed plant

The dispersal of seeds from Asarum canadense by ants was studied to quantify variation in mutualistic benefits and to test the hypothesis that this mutualism has effects on population density. Six populations of A. canadense were monitored in SE West Virginia, in the Monongahela National Forest. The rate of seed removal, dispersal distance, microhabitats of dispersed seeds and disperser species were determined in each study site. I measured ovule production and factors causing loss of ovules and the seeds resulting from them through the stage of dispersed seeds. The proportion of seeds removed from the area under the parent plant was the best indicator of dispersal benefits. Few components of dispersal varied among the six sites, but significant variation was observed for capsule formation, ovule development, and pre-dispersal seed predation. Key factor analysis showed pre-dispersal seed predation to be the major factor influencing spatial variation in seed production. Seedling density in 1984 was directly related to seed production in 1983. No population feedback for mutualism was detected.

Topics in Evolutionary Ecology

Mayhew, Peter J. 2006. Discovering evolutionary ecology: bringing together ecology and evolution. Oxford University Press, New York, New York. ix + 215 p.

Frugivorous Bats, Seed Shadows, and the Structure of Tropical Forests

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