Hostname: page-component-669899f699-tzmfd Total loading time: 0 Render date: 2025-04-26T03:51:26.277Z Has data issue: false hasContentIssue false
  • English
  • Français

Diet selection is related to breeding status in two frugivorous hornbill species of Central Africa

Published online by Cambridge University Press:  23 June 2014

Aaron M. Lamperti ,
Aaron R. French ,
Ellen S. Dierenfeld ,
Mark K. Fogiel ,
Kenneth D. Whitney ,
Donald J. Stauffer ,
Kimberly M. Holbrook ,
Britta D. Hardesty ,
Connie J. Clark  and
John R. Poulsen
...Show all authors
Aaron M. Lamperti*
Affiliation:
Department of Biology, San Francisco State University, 1600 Holloway Avenue, San Francisco, CA 94132, USA
Aaron R. French
Affiliation:
Department of Biology, San Francisco State University, 1600 Holloway Avenue, San Francisco, CA 94132, USA
Ellen S. Dierenfeld*
Affiliation:
Department of Wildlife Nutrition, Wildlife Conservation Society, 2300 Southern Blvd., Bronx, NY 10460, USA
Mark K. Fogiel
Affiliation:
Department of Biology, San Francisco State University, 1600 Holloway Avenue, San Francisco, CA 94132, USA
Kenneth D. Whitney*
Affiliation:
Department of Biology, San Francisco State University, 1600 Holloway Avenue, San Francisco, CA 94132, USA
Donald J. Stauffer
Affiliation:
Department of Biology, San Francisco State University, 1600 Holloway Avenue, San Francisco, CA 94132, USA
Kimberly M. Holbrook
Affiliation:
The Nature Conservancy 4245 North Fairfax Drive, Suite 100 Arlington, VA 22203, USA
Britta D. Hardesty*
Affiliation:
Department of Biology, San Francisco State University, 1600 Holloway Avenue, San Francisco, CA 94132, USA
Connie J. Clark*
Affiliation:
Department of Biology, San Francisco State University, 1600 Holloway Avenue, San Francisco, CA 94132, USA
John R. Poulsen*
Affiliation:
Department of Biology, San Francisco State University, 1600 Holloway Avenue, San Francisco, CA 94132, USA
Benjamin C. Wang
Affiliation:
Department of Biology, San Francisco State University, 1600 Holloway Avenue, San Francisco, CA 94132, USA
Thomas B. Smith*
Affiliation:
Department of Biology, San Francisco State University, 1600 Holloway Avenue, San Francisco, CA 94132, USA
V. Thomas Parker
Affiliation:
Department of Biology, San Francisco State University, 1600 Holloway Avenue, San Francisco, CA 94132, USA
*
1Corresponding author. Current address: 557 New Boston Road, Norwich, Vermont 05055, USA. Email: aaron.lamperti@gmail.com
24736 Gatesbury Drive, St. Louis, MO 63128, USA
3Department of Biology, University of New Mexico, Albuquerque, NM 87131-0001, USA
4CSIRO Wealth from Oceans Flagship, Marine and Atmospheric Research, Hobart, TAS 7000, Australia
5Nicholas School of the Environment, Duke University, PO Box 90328, Durham, NC 27708, USA
5Nicholas School of the Environment, Duke University, PO Box 90328, Durham, NC 27708, USA
6Center for Tropical Research and Department of Ecology and Evolutionary Biology, University of California, Los Angeles, Box 951496, Los Angeles, CA 90095-1496, USA
Get access Rights & Permissions [Opens in a new window]

Abstract:

Avian diet selection is hypothesized to be sensitive to seasonal changes in breeding status, but few tests exist for frugivorous tropical birds. Frugivorous birds provide an interesting test case because fruits are relatively deficient in minerals critical for reproduction. Here, we quantify annual patterns of fruit availability and diet for two frugivorous hornbill (Bucerotidae) species over a 5.5-y period to test for patterns of diet selection. Data from the lowland tropical rain forest of the Dja Reserve, Cameroon, are used to generate two nutritional indices. One index estimates the nutrient concentration of the diet chosen by Ceratogymna atrata and Bycanistes albotibialis on a monthly basis using 3165 feeding observations combined with fruit pulp sample data. The second index is an estimate of nutrient concentration of a non-selective or neutral diet across the study area based on tree fruiting phenology, vegetation survey and fruit-pulp sample data. Fifty-nine fruit pulp samples representing 40 species were analysed for 16 nutrient categories to contribute to both indices. Pulp samples accounted for approximately 75% of the observed diets. The results support expected patterns of nutrient selection. The two hornbill species selected a diet rich in calcium during the early breeding season (significantly so for B. albotibialis in July and August). Through the brooding and fledging periods, they switched from a calcium-rich diet to one rich in iron and caloric content as well as supplemental protein in the form of invertebrates. Calcium, the calcium to phosphorus ratio and fat concentration were the strongest predictors of breeding success (significant for calcium and Ca:P for B. albotibialis in June). We conclude that hornbills actively select fruit based on nutritional concentration and mineral concentration and that the indices developed here are useful for assessing frugivore diet over time.

Keywords

avianCameroonDja Reservefrugivorymineral nutritionnutrition
Type
Research Article
Information
Journal of Tropical Ecology , Volume 30 , Issue 4 , July 2014 , pp. 273 - 290
Copyright
Copyright © Cambridge University Press 2014 

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.)

Article purchase

Temporarily unavailable

References

LITERATURE CITED

ANGGRAINI, K., KINNAIRD, M. & O’BRIEN, T. 2000. The effects of fruit availability and habitat disturbance on an assemblage of Sumatran hornbills. Bird Conservation International 10:189–202.Google Scholar
AOAC 1995. Official methods of analysis of AOAC International. (Sixteenth edition). AOAC International, Gaithersburg. 1200 pp.Google Scholar
BARCLAY, R. 1995. Does energy or calcium availability constrain reproduction by bats? Pp. 245–258 in Racey, P. A. & Swift, S. M. (eds.). Ecology, evolution and behaviour of bats. The Zoological Society of London. Clarendon Press, London.CrossRefGoogle Scholar
DATTA, A. & RAWAT, G. S. 2004. Nest-site selection and nesting success of three hornbill species in Arunachal Pradesh, north-east India: Great Hornbill Buceros bicornis, Wreathed Hornbill Aceros undulatus and Oriental Pied Hornbill Anthracoceros albirostris. Bird Conservation International 14.S1:S39–S52.Google Scholar
DHONDT, A. A. & HOCHACHKA, W. M. 2001. Variations in calcium use by birds during the breeding season. The Condor 103:592–598.CrossRefGoogle Scholar
DIERENFELD, E. S. 1996. Nutritional wisdom: adding the science to the art. Zoo Biology 15:447–448.Google Scholar
DUNN, E. H. 1980. On the variability in energy allocation of nestling birds. The Auk (1980):19–27.Google Scholar
FOEKEN, S. G., DE VRIES, M., HUDSON, E., SHEPPARD, C. D. & DIERENFELD, E. S. 2008. Determining nitrogen requirements of Aceros and Buceros hornbills. Zoo Biology 27:282–293.CrossRefGoogle ScholarPubMed
FOGIEL, M. F. 2007. An evaluation of fruit availability theory and measurement in an afrotropical rainforest. M.S. Thesis, San Francisco State University.Google Scholar
GARCÍA-NAVAS, V. & SANZ, J. J. 2011. The importance of a main dish: nestling diet and foraging behaviour in Mediterranean blue tits in relation to prey phenology. Oecologia 165:639–649.Google Scholar
GAUTIER-HION, A. & MICHALOUD, G. 1989. Are figs always keystone resources for tropical frugivorous vertebrates? A test in Gabon. Ecology 70:1826–1833.Google Scholar
GOERING, H. K. & VAN SOEST, P. J. 1970. Forage fiber analysis. Agricultural handbook #379. A.R.S., USDA Washington, DC. 24 pp.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.Google Scholar
GRAVELAND, J. & VANDERWAL, R. 1996. Decline in snail abundance due to soil acidification causes eggshell defects in forest passerines. Oecologia 105:351–360.CrossRefGoogle ScholarPubMed
HARDESTY, B. D. 1999. Seed rain and dispersal patterns in a lowland tropical rain forest. MA Thesis, San Francisco State University.Google Scholar
HARDESTY, B. D. & PARKER, V. T. 2003. Community seed rain patterns and a comparison to adult community structure in a West African tropical forest. Plant Ecology 164:49–64.Google Scholar
HERRERA, C. M. 1982. Seasonal variation in the quality of fruits and diffuse coevolution between plants and avian dispersers. Ecology 63:773–785.CrossRefGoogle Scholar
HOBSON, K. A., SHARP, C. M., JEFFERIES, R. L., ROCKWELL, R. F. & ABRAHAM, K. F. 2011. Nutrient allocation strategies to eggs by Lesser Snow Geese (Chen caerulescens) at a sub-Arctic colony. The Auk 128:156–165.Google Scholar
HOLBROOK, K. M. & SMITH, T. B. 2000. Seed dispersal and movement patterns in two species of Ceratogymna hornbills in West African tropical lowland forest. Oecologia 125:249–257.Google Scholar
HOLBROOK, K. M., SMITH, T. B. & HARDESTY, B. D. 2002. Long-distance movements of frugivorous rainforest hornbills. Ecography 25:745–749.Google Scholar
KANNAN, R. & JAMES, D. A. 1999. Fruiting phenology and the conservation of the Great Pied Hornbill (Buceros bicornis) in the Western Ghats of Southern India. Biotropica 31:167–177.Google Scholar
KARR, J. R. 1976. Seasonality, resource availability, and community diversity in tropical bird communities. American Naturalist 110:973–994.Google Scholar
KEMP, A. C. 2001. Family Bucerotidae (Hornbills). Pp. 436–523 in del Hoyo, J., Elliott, A., & Sargatal, J. (eds.). Handbook of the birds of the World. Vol. 6. Mousebirds to hornbills. Lynx Edicions, Barcelona.Google Scholar
KINNAIRD, M. F. & O’BRIEN, T. G. 1999. Breeding ecology of the Sulawesi Red-Knobbed Hornbill Aceros cassidix. Ibis 141:60–69.Google Scholar
KINNAIRD, M. F. & O’BRIEN, T. G. 2005. Fast foods of the forest: the influence of figs on primates and hornbills across Wallace's line. Pp. 155–184 in Dew, J. L. & Boubli, J. P. (eds.). Tropical fruits and frugivores. Springer, the Netherlands.Google Scholar
KINNAIRD, M. F. & O’BRIEN, T. G. 2008. The ecology and conservation of Asian hornbills: farmers of the forest. University of Chicago Press, Chicago. 315 pp.Google Scholar
KITAMURA, S., THONG-AREE, S., MADSRI, S. & POONSWAD, P. 2011. Characteristics of hornbill-dispersed fruits in lowland dipterocarp forests of southern Thailand. The Raffles Bulletin of Zoology 24:137–147.Google 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.Google Scholar
LAMPERTI, A. M. 2004. Aspects of the seed dispersal ecology of Ceratogymna hornbills in the Dja Reserve, Cameroon. MA Thesis, San Francisco State University.Google Scholar
LEIGHTON, M. & LEIGHTON, D. R. 1983. Vertebrate responses to fruiting seasonality within a Bornean rain forest. Pp. 181–196 in Sutton, S. L., Whitmore, T. C. & Chadwick, A. C. (eds.). Tropical rain forest: ecology and management. Blackwell Scientific Publications, Oxford.Google Scholar
MARTIN, T. E. 1987. Food as a limit on breeding birds: a life-history perspective. Annual Review of Ecology and Systematics 18:453–487.Google Scholar
MARTIN, T. E. 1993. Nest predation and nest sites. BioScience 43:523–532.CrossRefGoogle Scholar
MCDOWELL, L. R. 2003. Minerals in animal and human nutrition. (Second edition). Elsevier, Amsterdam. 660 pp.Google Scholar
MCKEY, D. 1975. The ecology of coevolved seed dispersal systems. Pp. 159–191 in Gilbert, L. E. & Austin, P. H. (eds.). Coevolution of animals and plants. University of Texas Press, Austin.Google Scholar
MUCHAAL, P. K. & NGANDJUI, G. 1995. Wildlife populations in the western Dja Reserve (Cameroon): an assessment of the impact of village hunting and alternatives for sustainable utilization. Republic of Cameroon Ministry of Environment and Forests and ECOFAC (Conservation and Sustainable Utilization of Forest Ecosystems in Central Africa). Yaoundé, Cameroon.Google Scholar
MUCHAAL, P. K. & NGANDJUI, G. 1999. Impact of village hunting on wildlife populations in the Western Dja Reserve, Cameroon. Conservation Biology 13:385–396.CrossRefGoogle Scholar
MURPHY, M. E. 1996. Nutrition and metabolism. Pp. 31–60 in Carey, C. (ed.). Avian energetics and nutritional ecology. Chapman & Hall, New York.Google Scholar
NAGER, R. G. 2006. The challenges of making eggs. Ardea-Wageningen 94.3:323.Google 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.Google Scholar
OTTEN, B. A., OROSZ, S. E., AUGE, S. & FRAZIER, D. L. 2001. Mineral content of food items commonly ingested by keel-billed toucans (Ramphastos sulfuratus). Journal of Avian Medicine and Surgery 15:194–196.Google Scholar
ELMER, PERKIN. 1982. Analytical methods for atomic absorption spectrophotometry. Perkin Elmer, Norwalk. 300 pp.Google Scholar
POONSWAD, P., TSUJI, A. & JIRAWATKAVI, N. 2004. Estimation of nutrients delivered to nest inmates by four sympatric species of hornbills in Khao Yai National Park, Thailand. Ornithological Science 3:99–112.Google Scholar
POULIN, B., LEFEBVRE, G. & MCNEIL, R. 1992. Tropical avian phenology in relation to abundance and exploitation of food resources. Ecology 73:2295–2309.Google Scholar
POULSEN, J. R., CLARK, C. J. & SMITH, T. B. 2001. Seed dispersal by a diurnal primate community in the Dja Reserve, Cameroon. Journal of Tropical Ecology 17:787–808.Google Scholar
POULSEN, J. R., CLARK, C. J., CONNOR, E. F. & SMITH, T. B. 2002. Differential resource use by primates and hornbills: implications for seed dispersal. Ecology 83:228–240.Google Scholar
ROBBINS, C. T. 1993. Wildlife feeding and nutrition. Academic Press, New York. 352 pp.Google Scholar
RENDELL, W. B. & ROBERTSON, R. J. 1994. Cavity-entrance orientation and nest-site use by secondary hole-nesting birds. Journal of Field Ornithology 65:27–35.Google Scholar
RUBY, J., NATHAN, P. T., BALASINGH, J. & KUNZ, T. H. 2000. Chemical composition of fruits and leaves eaten by short-nosed fruit bat, Cynopterus sphinx. Journal of Chemical Ecology 26:2825–2841.Google Scholar
SCHOENER, T. W. 1968. The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology 49:704–726.CrossRefGoogle Scholar
SHANAHAN, M., SO, S., COMPTON, S. G. & CORLETT, R. 2001. Fig-eating by vertebrate frugivores: a global review. Biological Reviews 76:529–572.Google Scholar
SIBLY, R. M., WITT, C. C., WRIGHT, N. A., VENDITTI, C., JETZ, W. & BROWN, J. H. 2012. Energetics, lifestyle, and reproduction in birds. Proceedings of the National Academy of Sciences, USA 109:10937–10941.Google Scholar
STAUFFER, D. & SMITH, T. B. 2004. Breeding and nest site characteristics of the Black-casqued Hornbill Ceratogymna atrata and White-thighed Hornbill Ceratogymna cylindricus in south-central Cameroon. Ostrich 75:79–88.CrossRefGoogle Scholar
STILES, E. W. 1993. The influence of pulp lipids on fruit preference by birds. Vegetatio 107/108:227–235.Google Scholar
STRICKLAND, J. D. H. & PARSON, T. R. 1972. A practical handbook of seawater analysis. Fisheries Board of Canada, Ottawa. 310 pp.Google Scholar
TERBORGH, J. 1986. Keystone plant resources in the tropical forest. Pp. 330–344 in Soulé, M. E. (ed.). Conservation biology: the science of scarcity and diversity. Sinauer, Sunderland.Google 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.Google Scholar
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
WHITNEY, K. D. & SMITH, T. B. 1998. Habitat use and resource tracking by African Ceratogymna hornbills: implications for seed dispersal and forest conservation. Animal Conservaton 1:107–117.CrossRefGoogle Scholar
WHITNEY, K. D., FOGIEL, M. K., SMITH, T. B., PARKER, V. T. & STAUFFER, D. J. 1996. Dja Hornbill Project. EEP Hornbill Taxon Advisory Group Newsletter 2:25.Google Scholar
WHITNEY, K. D., FOGIEL, M. K., LAMPERTI, A. M., HOLBROOK, K. M., STAUFFER, D. J., HARDESTY, B. D., PARKER, V. T. & SMITH, T. B. 1998. Seed dispersal by Ceratogymna hornbills in the Dja Reserve, Cameroon. Journal of Tropical Ecology 14:351–371.Google Scholar