The role of nitrogen from fruit pulp in the nutrition of the frugivorous bat Carollia perspicillata.

Nutritional analyses were performed on several fruit species that are eaten by the neotropical frugivorous bat Carollia perspicillata. All essential amino acids assayed were found to be present in fruit pulp. Compared to the relative amounts of essential amino acids required for growth by laboratory rats, methionine and lysine were the most limiting amino acids in fruit protein. Captive bats were fed fruits of either Chlorophora tinctoria or Muntingia calabura so that the digestibilities of pulp nitrogen and gross energy could be determined. Digestibility estimates were lower than those found for Artibeus jamaicensis fed fruits of Ficus insipida, but this was probably caused by methodological differences. The measures of nutrient content and digestibility were used with estimates of daily nitrogen and energy requirements of bats to predict the amount of pulp needed to meet these requirements. Fruits were judged to be adequate nitrogen sources if the amount predicted to satisfy nitrogen requirements was less than that to satisfy energy requirements. By this criterion, most fruits were found to be adequate for maintenance metabolism; only fruit of Piper amalago was adequate for lactating bats. However, when amino acid deficiencies were considered, Piper amalago fruit was adequate only for maintenance metabolism, and no other fruits met this requirement. Insects found in fruit pulp were insufficient to constitute an important nitrogen source. Thus, if insects are important nitrogen sources they must be actively sought by bats. However, this analysis suggests that by selecting certain fruit species, frugivorous bats may not need to supplement their diets with insects. NEARLY ALL SPECIES OF NEOTROPICAL frugivorous bats (Phyllostomidae) studied include insects in their diets (Gardner 1977). The short-tailed fruit bat Carollia perspicillata also ingests insects (Arata et al. 1967, Fleming et al. 1972, Ayala & D'Alessandro 1973, Howell & Burch 1974), but their importance to the diet is unknown. Fleming et al. (1972) found that insects formed on average about 13 percent by volume of stomach contents in a sample of 272 bats whose stomachs contained food, but recently Thomas (1984a) has questioned some of the evidence for voluntary insect eating. An explanation for the inclusion of insects in the diet is that while fruits provide an often abundant and easily handled energy source, they do not provide sufficient nitrogen to meet the dietary requirements of bats (Morrison 1980, Thomas 1984b). Compared with insects, fruits contain very little nitrogen (Morton 1973, White 1974), however it is not clear that fruits are inadequate nitrogen sources. For example, Foster (1978) calculated that some fruits may be adequate nitrogen sources for nestling frugivorous birds. In this paper, I present the results of an investigation of the nutritional contents and digestibilities of some fruits eaten by Carollia perspicillata. The goal of this paper is to assess the value of fruit tissue as the only source of nitrogen for frugivorous bats. Specifically, I test the hypothesis that nitrogen requirements are met before energy requirements when bats ingest enough fruit to meet their energy requirements. MATERIALS AND METHODS The study was carried out from May to August, 1980 and 1981, in Parque Nacional Santa Rosa, Guanacaste Province, Costa Rica. This site was described in detail by Heithaus and Fleming (1978). Many fruit species that are available at this site during the wet season are eaten by Carollia perspicillata (Goodwin & Greenhall 1961, Gardner 1977). I collected sufficient fruit (>20 g dry pulp) for nutritional analyses from the following five plant species: Muntingia calabura (Eleocarpaceae), Chlorophora tinctoria (Moraceae), Cecropia peltata (Moraceae), Ficus ovalis (Moraceae), and Piper amalago (Piperaceae). These species represent roughly half of the wet season fruits reported to be eaten by Carollia in the park and account for about 60 percent of recorded fecal contents (Heithaus & Fleming 1978). Ripe fruits were collected daily and preserved in liquid nitrogen. Individual specimens were randomly sampled from the collected total and the following data were recorded: total fresh weight, seed number, total wet weight of seeds, and the number of insects present in the pulp. Pulp samples were prepared by removing seeds and insects from all fruit except Muntingia. Except for the skins of Muntingia, Ficus, and Cecropia, fruit parts not normally eaten by Carollia, such as the central stems of ' Received 12 November 1984, accepted 25 January 1985. 2 Current address: Department of Ecology and Behavioral Biology, University of Minnesota, Minneapolis, Minnesota 55455, U.S.A. BIOTROPICA 18(1): 39-44 1986 39 This content downloaded from 40.77.167.28 on Fri, 27 May 2016 05:46:25 UTC All use subject to http://about.jstor.org/terms TABLE 1. Physical characteristics of five fruit species. Fresh weight (g) Water content Pulp: seed Fruit species Mean SD N Percenta dry weight ratioa Muntingia calabura 1.41 0.36 120 81.8 (20) 2.33b Chlorophora tinctoria 4.76 1.01 60 79.6 (20) 6.00 (20) Cecropia peltata 4.87 1.61 22 78.1 (22) 0.87 (10) Ficus ovalis 0.82 0.20 130 78.5 (22) 6.53 (22) Piper amalago 1.25 0.69 48 73.0 (20) 0.83 (20) a Overall mean of (N) samples. b Calculated from mean no. of seeds per fruit, mean seed dry weight, and mean whole fruit dry weight. Cecropia and Piper, were also removed (based on personal observations of bats' feeding in captivity and examinations of fruits dropped under night roosts). Samples of Muntingia seeds and skins were analyzed separately and used to correct results from analyses of whole fruits. Pulp and seed samples were dried in an oven to constant weight at 5 5?C. Dried pulp samples were pooled for each species, ground through size 20 mesh in a Wiley mill and analyzed by standard techniques (Association of Official Analytical Chemists 1980). Analyses included: gross caloric content, ash, total nitrogen (Kjeldahl), and neutral detergent fiber. In addition, subsamples (1 g) of all fruit except Muntingia were hydrolyzed and run through an automatic amino acid analyzer using an internal standard of n-leucine. This technique provided quantitative determinations of 17 of the 20 common amino acids. I used the amino acid analyses to calculate the proportion of total nitrogen that is actually in the form of amino acids by summing the amounts of nitrogen present in each amino acid quantity and dividing this by the total (Kjeldahl) nitrogen content. Results of amino acid analyses were also used to assess the quality of fruit protein by comparing the amounts of essential amino acids present (except tryptophan, which was not measured) with the amounts required for a balanced diet. Because no data exist on the amino acid requirements of bats, I used the levels recommended for growth in laboratory rats (Maynard et al. 1979). I conducted digestibility studies on captive bats in order to estimate the efficiency with which bats extract energy and nitrogen from fruit pulp. Eight male bats were captured and held in captivity for 4 days. Six bats were fed fresh fruits of Chlorophora tinctoria and two were fed fruits of Muntingia calabura ad libitum. Each bat was housed in a hardware cloth cage measuring 30 x 30 x 30 cm. To minimize contamination of food by feces, a food dish was suspended on a wire shelf about 15 cm above the cage bottom. Cages were set on aluminum baking pans for the collection of all feces and urine produced each night. The first day of captivity was used as an adjustment period and no feces were collected. On the following three mornings, the feces-urine mixture was collected, weighed to the nearest 0.1 g, and stored in airtight vials in liquid nitrogen. To estimate the wet weight of fruit ingested, uneaten portions of fruit were also weighed and subtracted from the weight of fruit offered. Feces samples were dried to constant weight at 5 50C, pooled for each bat, ground through a size 20 mesh, and subsampled for nitrogen and gross caloric content determinations. The remaining material was pooled among individuals to produce a sample large enough to complete the analysis. Seeds were either removed from the feces before drying (Chlorophora) or were included in analyses and corrected for in later calculations (Muntingia). Dry matter digestibility (DMD) was calculated (on a non-ash-free basis) using the ash tracer method (Johnson & Maxell 1966). Because urine was collected with the feces, corrections for urinary loss of minerals were not necessary. An assumption of this method is that the animals are in mineral balance. This method gave a lower, more conservative estimate than dividing the difference between ingested fruit and feces weights by ingested fruit weight. The partial apparent digestibility (PAD) of a nutritional component was calculated as follows: PD=A, (1 DMD)Af PAD Al(1A, )A (1) A, where A, and Af are the relative amounts of a nutrient in ingesta and feces respectively. These estimates do not yield digestibility per se because urinary losses are included in the feces. Because urinary loss of nitrogen is related to basal metabolic rate rather than intake rate (Pike & Brown 1967), the estimates of nitrogen partial apparent digestibility were corrected as follows: PADcorrected= PAD + EUN/I(N), (2) where PAD = estimated partial apparent digestibility of nitrogen, EUN = endogenous urinary nitrogen loss (g/ Kcal basal metabolic rate), I = observed intake of dry fruit pulp, and N, = the nitrogen content of fruit pulp. These digestibility estimates were used in conjunction with estimated requirements to predict minimum food intake levels for normal and lactating bats.