Hostname: page-component-7c8c6479df-xxrs7 Total loading time: 0 Render date: 2024-03-27T15:13:55.670Z Has data issue: false hasContentIssue false

Frugivorous bats drink nutrient- and clay-enriched water in the Amazon rain forest: support for a dual function of mineral-lick visits

Published online by Cambridge University Press:  21 January 2013

Simon J. Ghanem*
Affiliation:
Leibniz Institute for Zoo and Wildlife Research, Evolutionary Ecology Research Group, Alfred-Kowalke-Str. 17, 10315 Berlin, Germany Freie Universität Berlin, Verhaltensbiologie, Takustr. 6, Berlin, Germany
Hans Ruppert
Affiliation:
Geosciences Center, Department of Sedimentology and Environmental Geosciences, University of Göttingen, Goldschmidtstr. 3, 37077 Göttingen, Germany
Thomas H. Kunz
Affiliation:
Center for Ecology and Conservation Biology, Department of Biology, Boston University, 5 Cummington Str., 02115 Boston, USA
Christian C. Voigt
Affiliation:
Leibniz Institute for Zoo and Wildlife Research, Evolutionary Ecology Research Group, Alfred-Kowalke-Str. 17, 10315 Berlin, Germany Freie Universität Berlin, Verhaltensbiologie, Takustr. 6, Berlin, Germany
*
1Corresponding author. Email: sghanem@gmx.de

Abstract:

In Central Amazonia, large mammals create water-filled puddles when consuming soil. These mineral licks are visited by pregnant and lactating frugivorous bats; possibly for two reasons. Frugivorous bats could supplement their mineral-depleted fruit diet by drinking salty water, or they could buffer dietary plant secondary compounds by consuming soil. We analysed bat fruits from Ecuador and showed that they are depleted in elemental concentrations (Na, K, P) compared with similar fruits collected from Costa Rica, where no mineral licks occur (n = 32). Analyses of water from Ecuador revealed that water samples from six mineral licks contained more physiologically relevant elements (Na, K, Mg, Ca) than four samples from river and stream water control sites (Mann–Whitney U-test). In support of the nutrient supplement hypothesis, we observed bats drinking mineral-enriched water at these licks (video observation). Furthermore, blood collected from 68 bats differed in composition with respect to physiologically relevant minerals (Na, K, Mg, Fe) from that of frugivorous bats captured at control sites. To test whether frugivorous bats also consumed clay for detoxification, we checked for soil tracer elements in 31 faecal samples. Soil tracers are insoluble in water and, thus, are not included in a strict fruit diet. Bats from mineral licks showed higher aluminium soil tracer concentrations in their faeces than bat species that never visit licks, suggesting that frugivorous bats take up clay material at mineral licks. Our results provide evidence that frugivorous bats ingest soluble mineral nutrients and insoluble soil by consuming soil-enriched water at mineral licks, thus supporting the hypothesis that frugivorous bats of western Amazonia may derive a dual benefit from drinking water from mineral licks.

Resumen:

En la Amazonia Central, los mamíferos grandes construyen charcos de agua durante el consumo del suelo. Estos saladeros son frecuentemente visitados por murciélagos frugívoros por dos posibles razones: suplementar su dieta baja en minerales por medio de beber agua con alto contenido de sales o amortiguar compuestos secundarios provenientes de plantas. Hemos analizado frutos consumidos por murciélagos en Ecuador y observamos una reducción en el contenido de minerales (Na, K, P) en comparación con frutos similares colectados en Costa Rica, donde no existen saladeros (n = 32). Los análisis de agua de seis saladeros en Ecuador revelaron un mayor contenido de minerales con relevancia fisiológica (Na, K, Mg, Ca) a cuatro muestras de puntos de control de ríos y afluentes. Con el uso de cámaras infrarrojas grabamos murciélagos tomando agua en saladeros. Determinamos si los murciélagos ingieren minerales al tomar agua rica en nutrientes en los saladeros comparando el contenido de minerales con relevancia fisiológica (Na, K, Mg, Fe) en la sangre de 68 murciélagos que visitan los saladeros con murciélagos capturados en sitios de control. La sangre de murciélagos frugívoros capturados en los saladeros difiere en su composición de minerales de la de murciélagos capturados en otros sitios. También examinamos si los murciélagos consumían arcilla buscando trazas de suelo en 31 muestras de heces. Dichas trazas son insolubles en agua y, por lo tanto, no incluidas en una dieta frugívora. Los murciélagos frugívoros que visitan los saladeros mostraron una mayor concentración de trazas de suelo en las heces que murciélagos insectívoros que nunca los visitan. Nuestros resultados proveen evidencia que los murciélagos frugívoros ingieren nutrientes minerales solubles y arcilla insoluble al consumir agua enriquecida con arcilla en los saladeros. Esto apoya la hipótesis que los murciélagos frugívoros de la Amazonia occidental obtienen un doble beneficio al visitar dichos saladeros.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ABRAHAMS, P. W. & PARSONS, J. A. 1996. Geophagy in the tropics: a literature review. The Geographical Journal 162:6372.CrossRefGoogle Scholar
BLAKE, J. G., GUERRA, J., MOSQUERA, D., TORRES, R., LOISELLE, B. A. & ROMO, D. 2010. Use of mineral licks by white-bellied spider monkeys (Ateles belzebuth) and red howler monkeys (Alouatta seniculus) in eastern Ecuador. International Journal of Primatology 31:471483.CrossRefGoogle Scholar
BRAVO, A., HARMS, K. E., STEVENS, R. D. & EMMONS, L. H. 2008. Collpas: activity hotspots for frugivorous bats (Phyllostomidae) in the Peruvian Amazon. Biotropica 40:203210.CrossRefGoogle Scholar
BRAVO, A., HARMS, K. E. & EMMONS, L. H. 2010. Puddles created by geophagous mammals are potential mineral sources for frugivorous bats (Stenodermatinae) in the Peruvian Amazon. Journal of Tropical Ecology 26:173184.CrossRefGoogle Scholar
BRIGHTSMITH, D. J. & MUÑOZ-NAJAR, R. A. 2004. Avian geophagy and soil characteristics in southeastern Peru. Biotropica 36:534543.Google Scholar
BRIGHTSMITH, D. J., TAYLOR, J. & PHILLIPS, T. D. 2008. The roles of soil characteristics and toxin adsorption in avian geophagy. Biotropica 40:766774.CrossRefGoogle Scholar
CALABRESE, E. J. & STANEK, E. J. 1995. A dog's tale – soil ingestion by a canine. Ecotoxicology and Environmental Safety 32:9395.CrossRefGoogle ScholarPubMed
CALABRESE, E. J., STANEK, E. J., PEKOW, P. & BARNES, R. M. 1997. Soil ingestion estimates for children residing on a superfund site. Ecotoxicology and Environmental Safety 36:258268.CrossRefGoogle ScholarPubMed
CLARKE, K. R. & WARWICK, R. M. 1994. Change in marine communities: an approach to statistical analysis and interpretation. Natural Environment Research Council, London. 144 pp.Google Scholar
DEMPSEY, J. L. 2004. Fruit bats: nutrition and dietary husbandry. Nutrition Advisory Group Handbook 14:117.Google Scholar
DIAMOND, J. M. 1999. Evolutionary biology: dirty eating for healthy living. Nature 400:120121.CrossRefGoogle ScholarPubMed
DIAMOND, J., BISHOP, K. D. & GILARDI, J. D. 1999. Geophagy in New Guinea birds. Ibis 141:181193.CrossRefGoogle Scholar
DUDLEY, R., KASPARI, M. & YANOVIAK, S. P. 2012. Lust for salt in the Western Amazon. Biotropica 44:69.CrossRefGoogle Scholar
EMMONS, L. H. & STARK, N. M. 1979. Elemental composition of a natural mineral lick in Amazonia. Biotropica 11:311313.CrossRefGoogle Scholar
GILARDI, J. D., DUFFEY, S. S., MUNN, C. A. & TELL, L. A. 1999. Biochemical functions of geophagy in parrots: detoxification of dietary toxins and cytoprotective effects. Journal of Chemical Ecology 25:897922.CrossRefGoogle Scholar
HANDLEY, C. O., WILSON, D. E. & GARDNER, A. L. 1991. Demography and natural history of the common fruit bat, Artibeus jamaicensis, on Barro Colorado Island, Panama. Smithsonian Institution Press, Baltimore.Google Scholar
HEISER, C. B. 1969. The wonderberry. Pp. 62105 in Nightshades: the paradoxical plants. W. H. Freeman & Co., San Francisco.Google Scholar
HOLDØ, R. M., DUDLEY, J. P., MCDOWELL, L. R. & TOMASI, T. E. 2002. Geophagy in the African elephant in relation to availability of dietary sodium. Journal of Mammalogy 83:652664.2.0.CO;2>CrossRefGoogle Scholar
JORDAN, C. F. & HERRERA, R. 1981. Tropical rain forests: are nutrients really critical? American Naturalist 117:167180.CrossRefGoogle Scholar
KAMCHAN, A., PUWASTIEN, P., SIRICHAKWAL, P. P. & KONGKACHUICHAI, R. 2004. In vitro calcium bioavailability of vegetables, legumes and seeds. Journal of Food Composition and Analysis 17:311320.CrossRefGoogle Scholar
KASPARI, M., YANOVIAK, S. P. & DUDLEY, R. 2008. On the biogeography of salt limitation: a study of ant communities. Proceedings of the National Academy of Sciences USA 105:1784817851.CrossRefGoogle ScholarPubMed
KLAUS, G. & SCHMID, D. B. 1998. Geophagy at natural licks and mammal ecology: a review. Mammalia 62:481497.CrossRefGoogle Scholar
KORINE, C., SPEAKMAN, J. & ARAD, Z. 2004. Reproductive energetics of captive and free-ranging Egyptian fruit bats (Rousettus aegyptiacus). Ecology 85:220230.CrossRefGoogle Scholar
KREULEN, D. 1985. Lick use by large herbivores: a review of benefits and banes of soil consumption. Mammal Review 15:107123.CrossRefGoogle Scholar
KRISHNAMANI, R. & MAHANEY, W. C. 2000. Geophagy among primates: adaptive significance and ecological consequences. Animal Behaviour 59:899915.CrossRefGoogle ScholarPubMed
KUNZ, T. H. & NAGY, K. A. 1988. Methods of energy budget analysis. Pp. 277302 in Kunz, T. H. (ed.) Ecological and behavioral methods for the study of bats. Smithsonian Institution Press, Washington, DC.Google Scholar
KUNZ, T. H., ADAMS, R. A. & HOOD, W. R. 2009. Methods for assessing postnatal growth and development of bats. Pp. 273324 in Kunz, T. H. & Parson, S. (eds.) Ecological and behavioral methods for the study of bats. (Second edition). Johns Hopkins University Press, Baltimore.CrossRefGoogle Scholar
MAHANEY, W. C. & KRISHNAMANI, R. 2003. Understanding geophagy in animals: standard procedures for sampling soils. Journal of Chemical Ecology 29:15031523.CrossRefGoogle ScholarPubMed
MONTENEGRO, O. L. 2004. Natural licks as keystone resources for wildlife and people in Amazonia. Ph.D. dissertation, University of Florida, Gainesville.Google Scholar
MORRISON, D. W. 1980. Efficiency of food utilization by fruit bats. Oecologia 45:270273.CrossRefGoogle ScholarPubMed
NATIONAL RESEARCH COUNCIL. 2005. Mineral tolerance of animals. National Academies Press, Washington, DC. 510 pp.Google Scholar
RACEY, P. A. & SPEAKMAN, J. R. 1987. The energy costs of pregnancy and lactation in heterothermic bats. Symposium of the Zoological Society of London 57:107125.Google Scholar
REX, K., KELM, D. H., WIESNER, K., MATT, F., KUNZ, T. H. & VOIGT, C. C. 2008. Structure of three Neotropical bat assemblages. Biological Journal of the Linnean Society 94:617629.CrossRefGoogle Scholar
RUBY, J., NATHAN, P. T., BALASINGH, J. & KUNZ, T. H. 2000. Chemical composition of leaves and fruits eaten by the short-nosed fruit bat, Cynopterus sphinx (Megachiroptera). Journal of Chemical Ecology 26:28252841.CrossRefGoogle Scholar
RUPPERT, H. 1987. Bestimmung von Schwermetallen im Boden sowie die ihr Verhalten beeinflussenden Bodeneigenschaften. Beilage zum GLA-Fachbericht 2, Munich. 11 pp.Google Scholar
STARK, N. 1970. The nutrient content of plant and soils from Brazil and Surinam. Biotropica 2:5160.CrossRefGoogle Scholar
TERBORGH, J. 1992. Diversity and the tropical rain forest. Scientific American Library, New York. 242 pp.Google Scholar
TIMM, R. M. & LAVAL, R. K. 1998. A field key to the bats of Costa Rica. Occasional Publication Series, Center of Latin American Studies, University of Kansas 22:130.Google Scholar
TIRIRA, S. D. 2007. Guía de Campo de los Mamíferos del Ecuador. Quito. 576 pp.Google Scholar
TUTTLE, M. D. 1974. Unusual drinking behavior of some stenodermine bats. Mammalia 38:141144.Google Scholar
VOIGT, C. C. 2003. Reproductive energetics of the nectar-feeding bat Glossophaga soricina (Phyllostomidae). Journal of Comparative Physiology B 173:7985.CrossRefGoogle ScholarPubMed
VOIGT, C. C., KELM, D. H. & VISSER, G. H. 2006. Field metabolic rates of phytophagous bats: do pollination strategies of plants make a life of nectar-feeders spin faster? Journal of Comparative Physiology B 176:213222.CrossRefGoogle ScholarPubMed
VOIGT, C. C., DECHMANN, D. K. N., BENDER, J., RINEHART, B. J., MICHENER, R. H. & KUNZ, T. H. 2007. Mineral licks attract neotropical seed-dispersing bats. Research Letters of Ecology 2007: Article ID 34212.CrossRefGoogle Scholar
VOIGT, C. C., CAPPS, K. A., DECHMANN, D. K. N., MICHENER, R. H. & KUNZ, T. H. 2008. Nutrition or detoxification: why bats visit mineral licks of the Amazonian rainforest. PLoS ONE 3:e2011.CrossRefGoogle ScholarPubMed
WENDELN, M. C., RUNKLE, J. R. & KALKO, E. K. V. 2000. Nutritional values of 14 fig species and bat feeding preferences in Panama. Biotropica 32:489501.CrossRefGoogle Scholar

Ghanem Supplementary Movie

Movie

Download Ghanem Supplementary Movie(Video)
Video 5.4 MB