Biological Reviews

Review Article

Intake rates and the functional response in shorebirds (Charadriiformes) eating macro-invertebrates

John D. Goss-Custard a1c1, Andrew D. West a1, Michael G. Yates a1, Richard W. G. Caldow a1, Richard A. Stillman a1, Louise Bardsley a1, Juan Castilla a2, Macarena Castro a3, Volker Dierschke a4, Sarah. E. A. Le. V. dit Durell a1, Goetz Eichhorn a5, Bruno J. Ens a6, Klaus-Michael Exo a7, P. U. Udayangani-Fernando a8, Peter N. Ferns a9, Philip A. R. Hockey a10, Jennifer A. Gill a11, Ian Johnstone a12, Bozena Kalejta-Summers a13, Jose A. Masero a3, Francisco Moreira a14, Rajarathina Velu Nagarajan a15p1, Ian P. F. Owens a16, Cristian Pacheco a2, Alejandro Perez-Hurtado a3, Danny Rogers a17, Gregor Scheiffarth a7, Humphrey Sitters a18, William J. Sutherland a11, Patrick Triplet a19, Dave H. Worrall1 a20, Yuri Zharikov a21, Leo Zwarts a22 and Richard A. Pettifor a23
a1 Centre for Ecology and Hydrology, Winfrith Technology Centre, Dorchester DT2 8ZD, UK
a2 Departamento de Ecologia, Facultad de Ciencias Biologicas, Pontificia Universidad Catolica de Chile, Codigo Postal: 6513677, Santiago, Chile
a3 Departamento de Biologia, Facultad de Ciencias del Mar y Ambientals, E-11510 Puerto Real, Spain
a4 Research and Technology Centre, University of Kiel, Hafentörn, D-25671 Büsum, Germany
a5 Zoological Laboratory, University of Groningen, PO Box 14, 9750 AA Haren, The Netherlands
a6 Alterra, P.O. Box 167, NL-1790 AD Den Burg (Texel), The Netherlands
a7 Institut für Vogelforschung “Vogelwarte Helgoland”, An der Vogelwarte 21, D-26386 Wilhelmshaven, Germany
a8 29 Askam Road, Bramley, Rotherham, South Yorkshire S66 3YR, UK
a9 School of Biosciences, Cardiff University, Cardiff CF10 3TL, UK
a10 DST/NRF Centre of Excellence at the Percy FitzPatrick Institute of African Ornithology, University of Cape Town, Rondebosch 7701, South Africa
a11 Schools of Biological and Environmental Sciences, University of East Anglia, Norwich NR4 7TJ, UK
a12 RSPB North Wales Office, Maes y Ffynnon, Penrhosgarnedd, Bangor LL57 2DW, UK
a13 7 Mill Crescent, N. Kessock, Inverness IV1 3XY, UK
a14 Centro de Ecologia Aplicada ‘Prof. Baeta Neves’, Instituto Superior de Agraonomia, Tapada da Ajuda, 1349-017 Lisboa, Portugal
a15 Department of Psychology, University of Exeter, Exeter EX4 4QG, UK
a16 Department of Biological Sciences, and NERC Centre for Population Biology, Imperial College London, Silwood Park, Ascot, Berkshire SL5 7PY, UK
a17 Johnstone Centre, Charles Stuart University, PO Box 789, Albury NSW 2640, Australia
a18 Limosa, Old Ebford Lane, Ebford, Exeter EX3 0QR, UK
a19 SMACOPI, 1 place de l'Amiral Courbet, 80 100 Abbeville, France
a20 Countryside Council for Wales, Haverfordwest, Pembrokeshire SA67 8TB, UK
a21 SOLS, University of Queensland, Brisbane, QLD 4072, Australia
a22 RIZA, P.O. Box 17, Lelystad, The Netherlands
a23 Institute of Zoology, Zoological Society of London, Regents Park, London NW1 4RY, UK

Article author query
goss-custard jd   [PubMed][Google Scholar] 
west ad   [PubMed][Google Scholar] 
yates mg   [PubMed][Google Scholar] 
caldow rw   [PubMed][Google Scholar] 
stillman ra   [PubMed][Google Scholar] 
bardsley l   [PubMed][Google Scholar] 
castilla j   [PubMed][Google Scholar] 
castro m   [PubMed][Google Scholar] 
dierschke v   [PubMed][Google Scholar] 
dit durell se   [PubMed][Google Scholar] 
eichhorn g   [PubMed][Google Scholar] 
ens bj   [PubMed][Google Scholar] 
exo km   [PubMed][Google Scholar] 
udayangani-fernando pu   [PubMed][Google Scholar] 
ferns pn   [PubMed][Google Scholar] 
hockey pa   [PubMed][Google Scholar] 
gill ja   [PubMed][Google Scholar] 
johnstone i   [PubMed][Google Scholar] 
kalejta-summers b   [PubMed][Google Scholar] 
masero ja   [PubMed][Google Scholar] 
moreira f   [PubMed][Google Scholar] 
nagarajan rv   [PubMed][Google Scholar] 
owens ip   [PubMed][Google Scholar] 
pacheco c   [PubMed][Google Scholar] 
perez-hurtado a   [PubMed][Google Scholar] 
rogers d   [PubMed][Google Scholar] 
scheiffarth g   [PubMed][Google Scholar] 
sitters h   [PubMed][Google Scholar] 
sutherland wj   [PubMed][Google Scholar] 
triplet p   [PubMed][Google Scholar] 
worrall1 dh   [PubMed][Google Scholar] 
zharikov y   [PubMed][Google Scholar] 
zwarts l   [PubMed][Google Scholar] 
pettifor ra   [PubMed][Google Scholar] 


As field determinations take much effort, it would be useful to be able to predict easily the coefficients describing the functional response of free-living predators, the function relating food intake rate to the abundance of food organisms in the environment. As a means easily to parameterise an individual-based model of shorebird Charadriiformes populations, we attempted this for shorebirds eating macro-invertebrates. Intake rate is measured as the ash-free dry mass (AFDM) per second of active foraging; i.e. excluding time spent on digestive pauses and other activities, such as preening. The present and previous studies show that the general shape of the functional response in shorebirds eating approximately the same size of prey across the full range of prey density is a decelerating rise to a plateau, thus approximating the Holling type II (‘disc equation’) formulation. But field studies confirmed that the asymptote was not set by handling time, as assumed by the disc equation, because only about half the foraging time was spent in successfully or unsuccessfully attacking and handling prey, the rest being devoted to searching.

A review of 30 functional responses showed that intake rate in free-living shorebirds varied independently of prey density over a wide range, with the asymptote being reached at very low prey densities (<150/m−2). Accordingly, most of the many studies of shorebird intake rate have probably been conducted at or near the asymptote of the functional response, suggesting that equations that predict intake rate should also predict the asymptote.

A multivariate analysis of 468 ‘spot’ estimates of intake rates from 26 shorebirds identified ten variables, representing prey and shorebird characteristics, that accounted for 81% of the variance in logarithm-transformed intake rate. But four-variables accounted for almost as much (77.3%), these being bird size, prey size, whether the bird was an oystercatcher Haematopus ostralegus eating mussels Mytilus edulis, or breeding. The four variable equation under-predicted, on average, the observed 30 estimates of the asymptote by 11.6%, but this discrepancy was reduced to 0.2% when two suspect estimates from one early study in the 1960s were removed. The equation therefore predicted the observed asymptote very successfully in 93% of cases.

We conclude that the asymptote can be reliably predicted from just four easily measured variables. Indeed, if the birds are not breeding and are not oystercatchers eating mussels, reliable predictions can be obtained using just two variables, bird and prey sizes. A multivariate analysis of 23 estimates of the half-asymptote constant suggested they were smaller when prey were small but greater when the birds were large, especially in oystercatchers. The resulting equation could be used to predict the half-asymptote constant, but its predictive power has yet to be tested.

As well as predicting the asymptote of the functional response, the equations will enable research workers engaged in many areas of shorebird ecology and behaviour to estimate intake rate without the need for conventional time-consuming field studies, including species for which it has not yet proved possible to measure intake rate in the field.

(Received November 1 2005)
(Revised May 19 2006)
(Accepted May 22 2006)
(Published Online July 24 2006)

Key Words: Charadriiformes; foraging behaviour; functional response; individual-based models; intake rate; predator-prey interactions; shorebirds.

c1 Havering, Church Road, Lympstone, Devon, EX8 5JT, UK. (E-mail:
p1 Present address: PG and Research Department of Zoology and Wildlife Biology, AVC College (Autonomous), Mannampandal-609305, India.