Pollen digestion by new world bats: effects of processing time and feeding habits

INTRODUCTION

Pollen grains are included in the diet of several vertebrate and invertebrate flower visitors (Howell 1974a, Turner 1984, Peng et al. 1986, Richardson et al. 1986, Wooller et al. 1988, Law 1992a, b, Grant 1996). Although pollen can be an important source of proteins, vitamins, and minerals, its exine coat is highly resistant to degradation by digestive enzymes (Stanley and Linskens 1974). Several studies have estimated the efficiency and rate at which vertebrate digestive systems process pollen grains under experimental and natural conditions (Turner 1984, Richardson et al. 1986, Wooller et al. 1988, Brice et al. 1989). Extraction efficiencies of pollen contents in these studies ranged from 7% to 100%, whereas pollen transit through the gut took from 30 min to several hours.

Comparative studies of pollen digestive processing in animals that have different diets do not yet provide a satisfactory picture of the digestive adaptations of flower visitors. Wooller et al. (1988) concluded that pollen digestion in specialized avian pollen feeders did not differ from the digestive performance of birds that do not include pollen in their natural diets. However, their work did not have a standard methodology for comparing the different species they studied. Some bat species regularly include pollen in their diet (Gardner 1977) and are able to extract its contents (Howell 1974a, Law 1992a). Because of the broad dietary spectrum showed by its members (Gardner 1977), the family Phyllostomidae offers a unique opportunity to compare pollen extraction efficiencies among animals with different feeding habits. In this study, we compared the efficiency with which phyllostomid bats with different degrees of flower specialization extract the contents of three species of pollen. We hypothesized that bat species that regularly include pollen in their diet should be more efficient at extracting pollen contents than species that ingest pollen only seasonally.

METHODS

We conducted this study with nonreproductive adults of four species of phyllostomids: Anoura geoffroyi (Glossophaginae), Leptonycteris curasoae (Glossophaginae), Artibeus jamaicensis (Stenodermatinae), and Sturnira lilium (Stenodermatinae). Artibeus jamaicensis, S. lilium, and A. geoffroyi are species resident to the study site, whereas L, curasoae is present only during late spring and summer. L. curasoae is considered a derived nectarivorous species (Koopman 1981); its diet includes pollen, nectar, fruit, and a small amount of insects (Gardner 1977). Pollen constitutes an important part of the diet of this species throughout the year (Alvarez and Gonzalez 1970, Fleming 1995, Valiente-Banuet et al. 1996). Fleming et al. (1993) postulate that migratory populations of the subspecies L. c. yerbabuenae move north from central Mexico along a nectar corridor of blooming columnar cacti in the spring, and then move south following blooming paniculate agaves in the fall. Members of this subspecies spend the winter and fall in central and southern Mexico, where they feed on nectar and pollen from flowers in the Bombacaceae, Convolvulaceae, Leguminosae, Agavaceae, and Cactaceae. Similarly, nonmigratory populations of L. c. yerbabuenae in northern and central Mexico feed on flowers year-round (Fleming 1995). According to Alvarez and Gonzalez (1970) and Howell (1974b), insects account for a very small fraction of the diet of L. curasoae.

According to Koopman (1981), Anoura geoffroyi is a more primitive and more generalized nectarivore than L. curasoae; its diet includes pollen, nectar, fruits, and insects (Gardner 1977). Alvarez and Gonzalez (1970) considered this species to be a facultative pollen eater. Stomachs and feces of A. geoffroyi have been reported to contain pollen as well as large amounts of insect remains (Alvarez and Gonzalez 1970, Howell 1974b, Sazima 1976, Willig et al. 1993).

Artibeus jamaicensis feeds on fruits, insects, pollen, and nectar (Gardner 1977). Heithaus et al. (1975) considered it to be primarily a frugivore that feeds heavily on nectar and pollen during the dry season in tropical dry forests. During the wet season, when flower resources are scarce and fruits are more abundant, this species switches back to a diet of mostly fruit. The importance of fruits with respect to pollen during the dry season, however, is probably underestimated. Pollen consumption was inferred from samples obtained from bat fur, whereas fruit ingestion was determined by examining fecal samples; the absence of fruit remains in most (92%) fecal samples of A. jamaicensis probably reflects either short fruit retention times in the gut, or the fact that large, single seeds of some fruits are not ingested (Heithaus et al. 1975). In a central Mexico desert, A. jamaicensis feeds occasionally on the pollen and nectar of Neobuxbaumia tetetzo, a species of columnar cactus, but it is a much more common visitor to this plant when fruit is available (Valiente-Banuet et al. 1996). Insects are a secondary part of the diet of A. jamaicensis (Fleming et al. 1972).