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Can fruit pulp meet the calcium needs of tropical frugivorous passerines during reproduction?

Published online by Cambridge University Press:  11 November 2013

Mercedes S. Foster
Mercedes S. Foster*
Affiliation:
Biological Survey Division, USGS Patuxent Wildlife Research Center, National Museum of Natural History, PO Box 37012, Washington, DC 20013–7012, USA
*
1Corresponding author. Email: fosterm@si.edu
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Abstract:

Calcium is an important nutrient for birds, especially for eggshell production and the mineralization of the skeleton of developing young. In temperate regions insects and seeds that form the bulk of the diet of breeding passerines do not contain sufficient calcium to meet the needs of breeding females and young; these birds obtain their calcium by eating snails, woodlice and millipedes. Little is known about the way tropical frugivorous passerines meet their calcium needs. The calcium contents of fruits of 34 species eaten by birds during the breeding season in mature floodplain forest in south-eastern Peru were determined. The suitability of these fruits as calcium sources for hypothetical 10-g and 25-g birds and for 26 species of frugivore that breed at the study site was evaluated based on bird body weight and on the rictal width of the bill, which influences feeding. Fruits of five species in the study area appear to be suitable sources of calcium for birds ≤25 g, although those of Ficus killipii (Moraceae) are likely optimal. The latter contain a lot of calcium (2.48% dry weight of pulp or c. 4.15 mg per pulp per fruit) and are small enough (mean diam. = 9 mm) for most birds to swallow whole, and trees produce large crops. Snails, woodlice and millipedes are common in the area and also contain sufficient calcium to meet birds’ needs. In addition, birds could likely meet their calcium needs through geophagy at natural mineral licks.

Keywords

avian reproductioncalciumeggshellfigfruitmillipedemineral lickPerusnailwoodlice
Type
Research Article
Information
Journal of Tropical Ecology , Volume 30 , Issue 1 , January 2014 , pp. 79 - 88
Copyright
Copyright © Cambridge University Press 2013 

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References

LITERATURE CITED

BIDWELL, M. T. & DAWSON, R. D. 2005. Calcium availability limits reproductive output of tree swallows (Tachycineta bicolor) in a nonacidified landscape. Auk 122:246–254.CrossRefGoogle Scholar
BLEHER, B., POTGIETER, C. J., JOHNSON, D. N. & BÖHNING-GAESE, K. 2003. The importance of figs for frugivores in a South African coastal forest. Journal of Tropical Ecology 19:375–386.CrossRefGoogle Scholar
BLUM, J. D., TALIAFERRO, E. H. & HOLMES, R. T. 2001. Determining the sources of calcium for breeding migratory songbirds using stable strontium isotopes. Oecologia 126:569–574.CrossRefGoogle ScholarPubMed
BRAVO, A., HARMS, K. E. & EMMONS, L. H. 2010. Preference for collpa water by frugivorous bats (Artibeus): an experimental approach. Biotropica 42:276–280.CrossRefGoogle Scholar
BRIGHTSMITH, D. J. 2004. Effects of weather on parrot geophagy in Tambopata, Peru. Wilson Bulletin 116:134–145.CrossRefGoogle Scholar
BRIGHTSMITH, D. J. & ARAMBURÚ MUÑOZ-NAJAR, R. 2004. Avian geophagy and soil characteristics in southeastern Peru. Biotropica 36:534–543.Google Scholar
BRONSTEIN, J. L. & HOFFMANN, K. 1987. Spatial and temporal variation in frugivory at a Neotropical fig, Ficus pertusa. Oikos 49:261–268.CrossRefGoogle Scholar
BUREŠ, S. & WEIDINGER, K. 2000. Estimation of calcium intake by meadow pipit nestlings in an acidified area. Journal of Avian Biology 31:426–429.CrossRefGoogle Scholar
BUREŠ, S. & WEIDINGER, K. 2003. Sources and timing of calcium intake during reproduction in flycatchers. Oecologia 137:634–647.CrossRefGoogle ScholarPubMed
COLLAR, N. 2001. Family Trogonidae (trogons). Pp. 80–127 in del Hoyo, J., Elliott, A. & Sargatal, J. (eds.). Handbook of the birds of the World. Volume 6. Mousebirds to hornbills. Lynx, Barcelona.Google Scholar
COLLAR, N. 2005. Family Turdidae (thrushes). Pp. 514–808 in del Hoyo, J., Elliott, A. & Christie, D. A. (eds.). Handbook of the birds of the World. Volume 10. Cuckoo-shrikes to thrushes. Lynx, Barcelona.Google Scholar
DIAMOND, J., BISHOP, K. D. & GILARDI, J. D. 1999. Geophagy in New Guinea birds. Ibis 141:181–193.CrossRefGoogle Scholar
DICKINSON, E. C. (ed.). 2003. The Howard and Moore complete checklist of the birds of the World. (Third edition). Princeton University Press, Princeton. 1039 pp.Google Scholar
DUNNING, J. B. (ed.). 2008. CRC handbook of avian body masses. (Second edition). CRC Press, Boca Raton. 655 pp.Google Scholar
EMMONS, L. H. & STARK, N. M. 1979. Elemental composition of a natural mineral lick in Amazonia. Biotropica 11:331–333.CrossRefGoogle Scholar
FOSTER, M. S. 1976. Nesting biology of the long-tailed manakin. Wilson Bulletin 88:400–420.Google Scholar
FOSTER, M. S. 1978. Total frugivory in tropical passerines: a reappraisal. Tropical Ecology 19:131–154.Google Scholar
FOSTER, M. S. 1987. Feeding methods and efficiencies of selected frugivorous birds. Condor 89:566–580.CrossRefGoogle Scholar
FOSTER, M. S. 2008. Potential effects of arboreal and terrestrial avian dispersers on seed dormancy, seed germination and seedling establishment in Ormosia (Papilionoideae) species in Peru. Journal of Tropical Ecology 24:619–627.CrossRefGoogle Scholar
FRANCESCHI, V. R. & HORNER, H. T. 1980. Calcium oxalate crystals in plants. Botanical Review 46:361–427.CrossRefGoogle Scholar
GENTRY, A. H. & TERBORGH, J. 1990. Composition and dynamics of the Cocha Cashu “mature” floodplain forest. Pp. 542–564 in Gentry, A. H. (ed.). Four neotropical rainforests. Yale University Press, New Haven.Google Scholar
GILL, F. & WRIGHT, M. 2006. Birds of the World, recommended English names. Princeton University Press, Princeton. 259 pp.Google Scholar
GRAVELAND, J. 1996a. Calcium deficiency in wild birds. Veterinary Quarterly 18 (Suppl. 3):S136–S137.CrossRefGoogle ScholarPubMed
GRAVELAND, J. 1996b. Avian eggshell formation in calcium-rich and calcium-poor habitats: importance of snail shells and anthropogenic calcium sources. Canadian Journal of Zoology 74:1035–1044.CrossRefGoogle Scholar
GRAVELAND, J. & BERENDS, J. E. 1997. Timing of the calcium uptake and effect of calcium deficiency on behaviour and egg-laying in captive great tits, Parus major. Physiological Ecology 70:74–84.Google Scholar
GRAVELAND, J. & DRENT, R. H. 1997. Calcium availability limits breeding success of passerines on poor soils. Journal of Animal Ecology 66:279–288.CrossRefGoogle Scholar
GRAVELAND, J. & VAN DER WAL, R. 1996. Decline in snail abundance due to soil acidification causes eggshell defects in forest passerines. Oecologia 105:351–360.CrossRefGoogle ScholarPubMed
GRAVELAND, J. & VAN GIJZEN, T. 1994. Arthropods and seeds are not sufficient as calcium sources for shell formation and skeletal growth in passerines. Ardea 82:299–314.Google Scholar
GRAVELAND, J., VAN DER WAL, R., VAN BALEN, J. H. & VAN NOORDWIJK, A. J. 1994. Poor reproduction in forest passerines from decline in snail abundance on acidified soils. Nature 368:446–448.CrossRefGoogle Scholar
GREENBERG, R. & MARRA, P. P. 2005. Birds of two worlds: the ecology and evolution of migration. Johns Hopkins University Press, Baltimore. 466 pp.CrossRefGoogle Scholar
GUIMÃRES, C. T. 1981. Algumas observações de campo sobre biologia e ecologia de Pomacea haustrum (Reeve, 1856) (Mollusca, Pilidae). Memorias Instituto Oswaldo Cruz Rio de Janeiro 76:343–351.CrossRefGoogle Scholar
HOWE, H. F. 1979. Fear and frugivory. American Naturalist 114:925–931.CrossRefGoogle Scholar
JORDANO, P. 1983. Fig-seed predation and dispersal by birds. Biotropica 15:38–41.CrossRefGoogle Scholar
KARASOV, W. H. 1990. Digestion in birds: chemical and physiological determinants and ecological implications. Studies in Avian Biology 13:391–415.Google Scholar
KINNAIRD, M. F. & O'BRIEN, T. G. 2007. The ecology and conservation of Asian hornbills. University of Chicago Press, Chicago. 315 pp.Google Scholar
KINNAIRD, M. F., O'BRIEN, T. G. & SURYADI, S. 1996. Population fluctuation in Sulawesi red-knobbed hornbills: tracking figs in space and time. Auk 113:431–440.CrossRefGoogle Scholar
KREMENTZ, D. G. & ANKNEY, C. D. 1995. Changes in total body calcium and diet of breeding house sparrows. Journal of Avian Biology 26:162–167.CrossRefGoogle Scholar
LAMBERT, F. R. & MARSHALL, A. G. 1991. Keystone characteristics of bird-dispersed Ficus in a Malaysian lowland rain forest. Journal of Ecology 79:793–809.CrossRefGoogle Scholar
LYDEARD, C., COWIE, R. H., PONDER, W. F., BOGAN, A. E., BOUCHET, P., CLARK, S. A., CUMMINGS, K. S., FREST, T. J., GARGOMINY, O., HERBERT, D. G., HERSHLER, R., PEREZ, K. E., ROTH, B., SEDDON, M., STRONG, E. & THOMSON, F. G. 2004. The global decline of nonmarine mollusks. BioScience 54:321–330.CrossRefGoogle Scholar
MCWILLIAMS, S. R. & KARASOV, W. H. 1998a. Test of a digestion optimization model: effects of costs of feeding on digestive parameters. Physiological Zoology 71:168–178.CrossRefGoogle ScholarPubMed
MCWILLIAMS, S. R. & KARASOV, W. H. 1998b. Do variable-reward feeding schedules affect digestive performance of migratory birds? Oecologia 114:160–169.CrossRefGoogle Scholar
MCWILLIAMS, S. R., CAVIEDES-VIDAL, E. & KARASOV, W. H. 1999. Digestive adjustments in cedar waxwings to high feeding rate. Journal of Experimental Zoology 283:394–407.3.0.CO;2-0>CrossRefGoogle Scholar
MEDWAY, Lord & WELLS, D. R. 1976. The birds of the Malay Peninsula. Volume 5. Witherby (with Penerbit Universiti Malaya), London. 448 pp.Google Scholar
O'BRIEN, T. G. 1997. Behavioural ecology of the north Sulawesi tarictic hornbill Penelopides exarhatus exarhatus during the breeding season. Ibis 139:97–101.CrossRefGoogle Scholar
O'BRIEN, T. G., KINNAIRD, M. F., DIERENFELD, E. S., CONKLIN-BRITTAIN, N. L., WRANGHAM, R. W. & SILVER, S. C. 1998. What's so special about figs? Nature 392:668.CrossRefGoogle Scholar
PAHL, R., WINKLER, D. W., GRAVELAND, J. & BATTERMAN, B. W. 1997. Songbirds do not create long-term stores of calcium in their legs prior to laying: results from high-resolution radiography. Proceedings of the Royal Society of London B. 264:239–244.CrossRefGoogle Scholar
RAMSAY, S. L. & HOUSTON, D. C. 1999. Do acid rain and calcium supply limit eggshell formation for blue tits (Parus caeruleus) in the U.K.? Journal of Zoology (London) 247:121–125.CrossRefGoogle Scholar
REYNOLDS, S. J. 1997. Uptake of ingested calcium during egg production in the zebra finch (Taeniopygia guttata). Auk 114:562–569.CrossRefGoogle Scholar
REYNOLDS, S. J. & PERRINS, C. M. 2010. Dietary calcium availability and reproduction in birds. Current Ornithology 17:31–74.Google Scholar
REYNOLDS, S. J., MÄND, R. & TILGAR, V. 2004. Calcium supplementation of breeding birds: directions for future research. Ibis 146:601–614.CrossRefGoogle Scholar
RICKLEFS, R. E. 1974. Energetics of reproduction in birds. Pp. 152–202 in Paynter, R. E. (ed.). Avian energetics. Publications of the Nuttall Ornithological Club 15, Nuttall Ornithological Club, Cambridge.Google Scholar
RILEY, M. P. 1994. Soil chemical changes accompanying a primary riparian succession in Manu National Park, Madre de Dios, Peru. Unpubl. Master's project. School of the Environment, Duke University, Durham, North Carolina.Google Scholar
SEASTEDT, T. R. & MACLEAN, S. F. 1977. Calcium supplements in the diet of nestling Lapland longspurs Calcarius lapponicus near Barrow, Alaska. Ibis 119:531–533.CrossRefGoogle Scholar
SHORT, L. & HORNE, J. F. M. 2002. Family Capitonidae (barbets). Pp. 140–219 in del Hoyo, J., Elliott, A. & Sargatal, J. (eds.). Handbook of the birds of the World. Volume 7. Jacamars to woodpeckers. Lynx, Barcelona.Google Scholar
SIMKISS, K. 1967. Calcium in reproductive physiology. Chapman Hall, London. 254 pp.Google Scholar
SNOW, B. K. 1970. A field study of the bearded bellbird in Trinidad. Ibis 112:299–329.CrossRefGoogle Scholar
SNOW, D. W. 1961. The natural history of the oilbird, Steatornis caripensis, in Trinidad, W. I. Pt. 1. General behavior and breeding habits. Zoologica 46:27–48.Google Scholar
SNOW, D. W. 1962. The natural history of the oilbird, Steatornis caripensis, in Trinidad, W. I. Pt. 2. Population, breeding ecology and food. Zoologica 47:199–221.Google Scholar
SNOW, D. W. 2004. Family Cotingidae (cotingas). Pp. 80–127 in del Hoyo, J., Elliott, A. & Christie, D. A. (eds.). Handbook of the birds of the World. Volume 6. Cotingas to pipits and wagtails. Lynx, Barcelona.Google Scholar
SNYDER, N. F. R. & SNYDER, H. A. 1971. Defenses of the Florida apple snail Pomacea paludosa. Behaviour 40:175–214.CrossRefGoogle Scholar
SQUIRE, M. E., BRAGUE, J. C., SMITH, R. J. & OWEN, J. C. 2011. Evidence of medullary bone in two species of thrushes. Wilson Journal of Ornithology 123:831–835.CrossRefGoogle Scholar
SUMMERS, D. B. B. 1982. The survival of bullfinches on cultivated fruit buds. Journal of Applied Ecology 19:813–819.CrossRefGoogle Scholar
TALIAFERRO, E. H., HOLMES, R. T. & BLUM, J. D. 2001. Eggshell characteristics and calcium demands of a migratory songbird breeding in two New England forests. Wilson Bulletin 113:94–100.CrossRefGoogle Scholar
TELLO, J. G. 2003. Frugivores at a fruiting Ficus in south-eastern Peru. Journal of Tropical Ecology 19:717–721.CrossRefGoogle Scholar
TERBORGH, J. 1983. Five new world primates: a study in comparative ecology. Princeton University Press, Princeton. 260 pp.Google Scholar
TERBORGH, J. 1990. An overview of research at Cocha Cashu Biological Station. Pp. 48–59 in Gentry, A. H. (ed.). Four neotropical rainforests. Yale University Press, New Haven.Google Scholar
TERBORGH, J. W., FITZPATRICK, J. W. & EMMONS, L. 1984. Annotated checklist of bird and mammal species of Cocha Cashu Biological Station, Manu National Park, Peru. Fieldiana, Zoology 21:1–29.Google Scholar
TILGAR, V., MÄND, R. & LEIVITS, A. 1999. Effect of calcium availability and habitat quality on reproduction in pied flycatcher Ficedula hypoleuca and great tit Parus major. Journal of Avian Biology 30:383–391.CrossRefGoogle Scholar
TILGAR, V., MÄND, R. & MÄGI, M. 2002. Calcium shortage as a constraint on reproduction in great tits Parus major: a field experiment. Journal of Avian Biology 33:407–413.CrossRefGoogle Scholar
TILGAR, V., MÄND, R., OTS, I., MAGI, M., KILGAS, P. & REYNOLDS, S. J. 2004. Calcium availability affects bone growth in nestling of free-living great tits Parus major, as detected by plasma alkaline phosphatase. Journal of Zoology (London) 263:269–274.CrossRefGoogle Scholar
TILGAR, V., MÄND, R., KILGAS, P. & REYNOLDS, S. J. 2005. Chick development in free-living great tits Parus major in relation to calcium availability and egg composition. Physiological and Biochemical Zoology 78:590–598.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 32:489–501.CrossRefGoogle Scholar
WHEELWRIGHT, N. T. 1985. Fruit size, gape width, and the diets of fruit-eating birds. Ecology 66:808–818.CrossRefGoogle Scholar