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Nitrogen and Energy Requirements of Fruit

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Nitrogen and Energy Requirements of Fruit J Comp Physiol B (1996) 166:427 434 © Springer-Verlag 1996 M. Delorme • D. W. Thomas Nitrogen and energy requirements of the short-tailed fruit bat (Carollia perspicillata): fruit bats are not nitrogen constrained Accepted: 23 June 1996 Abstract Nitrogen (IN) and energy (E) requirements N nitrogen • MR metabolic rate • were measured in adult Carollia perspicillata which DMD dry matter digestibility were fed on four experimental diets. Bats ate 1.3-1.8 times their body mass- day-1 and ingested 1339.5-1941.4kJ-kg-°75-day -1. Despite a rapid Introduction transit time, dry matter digestibility and metabolizable E coefficient were high (83.3% and 82.4%, respectively), Owing to its low nitrogen (N) content, fruit has long but true N digestibility was low (67.0%). Mass change been considered a low-quality diet, and birds and mam- was not correlated with E intake, indicating that bats mals that eat only fruit are thought to have difficulty adjusted their metabolic rate to maintain constant meeting their N requirements (Morton 1973; McKey mass. Bats were able to maintain constant mass with 1975; Howe and Estabrook 1977; Foster 1978). Nitro digestible E intake as low as 1168.7 kJ" kg -°75" day- * limitation has been invoked to explain why (1) few bird or 58.6 kJ'. Metabolic fecal N and endogenous urinary species feed exclusively on fruit (Snow 1976, 1981; Howe N losses were 0.87 mg N-g- ~ dry matter intake and and Estabrook 1977), (2) even apparently specialized 172.5 mg N.kg -°'7s- day -1, respectively, and bats re- frugivorous birds feed their nestlings animal tissue (Mor- quired 442 mg N.kg -°'Ts" day- 1 (total nitrogen) or ton 1973), (3) frugivorous bats and birds have low 292.8 mg N. kg- o.75. day- 1 (truly digestible nitrogen) growth rates (Snow 1962, 1971; Thomas and Marshall for N balance. Based on E and N requirements and 1984; but Ricklefs 1976), and (4) is specialized frugivor- digestibilities, it was calculated that non-reproductive ous oilbirds (Steatornis caripensis) select fruit that is fruit bats were able to meet their N requirements with- unusually rich in protein (Snow 1962; Thomas et al. 1993). out resorting to folivory and without over-ingesting Thomas (1984) suggested that a fruit diet posed an energy. It was demonstrated that low metabolic fecal additional problem in terms of the balance between requirements allowed bats to survive on low-N diets. energy (E) and N. He argued that because fruit has a low- N content, obligate frugivorous bats such as the Key words Energy • Fruit bat • Nitrogen pteropodids, Epomops buettikoferi and Micropteropus pusillus, are obliged to ingest large quantities of fruit to Abbreviations E energy. EUN endogenous satisfy their N requirements, and in so doing they over- urinary nitrogen • MFN metabolic fecal nitrogen • ingest E as an unavoidable consequence of the high E/N ratio. Thomas et al. (1993) concluded that the storage of large fat reserves during development of nestling oilbirds was consistent with this over-ingestion hypothesis. M. Delorme (~) Recherche et d6veloppement scientifique, Biod6me de Montr6al, The N-limitation in frugivorous bats is not univer- 4777, ave Pierre-De Coubertin, Montr6al, Qu6bec, sally accepted. Law (1992) and Kunz and Diaz (1995) Canada H1V IB3 argued that specialized frugivorous bats are not N- D.W. Thomas limited (and so are not forced to over-ingest E) because D6partement de Biologie, Universit6 de Sherbrooke, Sherbrooke, some species ingest N-rich supplements in the form of Qu6bec, Canada J1 K 2R1 pollen or leaves. However, these two studies do not D.W. Thomas resolve the key problems relating to the nutrition and Mus~e du Seminaire de Sherbrooke, Sherbrooke, Qu6bec Canada, ecology of fruit bats and other specialized frugivores. J1H 1J9 The important question is not whether frugivorous 428 M. Delorme and D.W. Thomas: Nitrogen and energy requirements of fruit bats bats do incorporate N-rich supplements into their diet, but rather (1) are they forced to supplement their diets Materials and methods because they are unable to balance N requirements We conducted this study at the Biod6me de Montr~at using C. without an additional source of N, and (2) does the perspicillata that had been born and raised in captivity. Prior to fruit intake needed to satisfy N requirements necessar- feeding trials bats were able to fly freely in a large cave exhibit where ily result in the over-ingestion of E? the ambient temperature was 23-26°C and the light cycle was The only studies that directly address these questions 12L: 12D. For each feeding trial, we confined five C. perspicillata (2-3 males provide conflicting views. Thomas (1984) and Steller and 2-3 females per trial) separately in inverted 5-1 glass bottles. (1986) concluded that pteropodid bats could balance A wire mesh cylinder inside the bottle allowed bats to hang and N requirements on an all-fruit diet, but that they were climb, but not to fly. Food was presented at 1800 hours in a plastic forced to over-ingest E to do so. In contrast, Herbst feeder near the top of the chamber to avoid fecal contamination. (1986) and Korine et al. (1996) argued that the phyllos- Urine and feces drained through the neck into a polyethylene vial to which 1 ml of glacial acetic acid was added to avoid volatile ammo- tomid bat, Carollia perspicitlata, and the pteropodid bat, nia loss. Each morning, all feces and urine were scraped from the Rousettus aegyptiacus, could balance N requirements chamber, the walls were washed with a known volume of distilled without incurring an over-ingestion of E on most fruits. water, and the combined excreta were weighed and frozen. The bats The difference between these studies and the major were then weighed and transferred to a clean chamber. Each group of five bats was presented with one of four diets of weakness in all of them lie in the fact that there are no varying N and E content (Table 1). We formed the diets by adding accurate measures of urinary and fecal N losses for varying amounts of high protein monkey chow (Purina 5045 25.0% either pteropodid or phyllostomid bats. Urinary N and crude protein) and sucrose to unsweetened canned peaches and then fecal N are difficult to separate in feeding trials involv- blending to make a uniform pure. Thus, bats were not able to ing fruit bats and, as a result, N requirements have been eliminate the fiber portion of the fruit prior to ingestion. We desig- nated diets according to their N and E content as low N/low E, low estimated from Smuts' (1935) allometric equations for N/high E, high N/low E, and high N/high E. We presented bats with EUN losses (e.g. Thomas 1984; Herbst 1986; Stetler a given diet for a 3-day pre-triat adjustment period, and then 1986; Korine et al. 1996). Fruit intake required to collected feces and urine for the following 4 days. We calculated balance N requirements was based on crude estimates daily food intake from the mass loss of the feeder corrected for of biological value and MFN losses (e.g. Thomas 1984; evaporative losses from a control feeder. For analyses, excreta samples were thawed, homogenized, and Herbst 1986; Korine et al. 1996). subdivided into three aliquots for analyses of E, total N, and urinary Predictions based on allometric equations are often N. Duplicates were run only for E. For E content, we transferred in error. Thus, for non-ruminant eutherians, EUN a 6-ml sample into a pre-weighed filter paper and oven-dried the averages 160 mg N-kg -°'75-day -1 as compared to combined sample at 55 °C to constant mass. We then burned the Smuts' (1935) estimate of 140 mg N" kg -°'7s "day- 1, filter paper and excreta in a ballistic bomb calorimeter (Gallenkamp) and calculated the excreta E content after correcting for the E con- but marsupials, average EUN level is far lower tent of the filter paper. We measured the total N of the excreta in (53mgN.kg-°VS-day-1; Robbins 1993). Mainten- a Tecator Fiastar 5020 following digestion at 375 °C in sulphuric ance N requirements of frugivorous oitbirds (50 mg acid with a selenium catalyst. We estimated urinary N losses by N-kg-°'VS.day-1; Bosque and De Parra 1992) are centrifuging the sample to remove solids and successively running ammonia and urea analyses on the supernatant (Tecator 5020). Urea well below the allometric predictions for birds (430 mg was transtbrmed into ammonia by a urease digestion prior to N" kg -°'75" day- 1; Robbins 1993). Error in the estima- analysis. We also measured creatinine N in a Synchron CX5 using tion of N requirements or of required food intake Jaffe's kinetic method (Beckman Instruments 1989) with picric acid would lead to false conclusions regarding the ability of and a pH of 13.3. We consider that urinary N losses are the sum of fruit bats to balance their N requirements on all-fruit ammonia, urea, and creatinine N, while fecal N is the difference between N total and urinary N. diets and whether the over-ingestion of E is a necessary We calculated DMD, metabolizable E coefficient, and apparent consequence of an all-fruit diet. and true N digestibilities following Robbins (1993). Maintenance The purpose of this study was to measure the diges- N requirement was estimated by regressing N balance against di- tive efficiency and E and N requirements for the etary N intake and calculating the N intake required to achieve frugivorous phyllostomid bat, C.
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