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Can animals use foraging behaviour to combat parasites?

Published online by Cambridge University Press:  11 August 2008

Michael R. Hutchings ,
Spiridoula Athanasiadou ,
Ilias Kyriazakis  and
Iain J. Gordon
Michael R. Hutchings*
Affiliation:
Animal Nutrition and Health Department, Scottish Agricultural College, West Mains Road, Edinburgh, EH9 3JG, UK
Spiridoula Athanasiadou
Affiliation:
Animal Nutrition and Health Department, Scottish Agricultural College, West Mains Road, Edinburgh, EH9 3JG, UK
Ilias Kyriazakis
Affiliation:
Animal Nutrition and Health Department, Scottish Agricultural College, West Mains Road, Edinburgh, EH9 3JG, UK
Iain J. Gordon
Affiliation:
Macaulay Institute, Craigiebuckler, Aberdeen, AB15 8QH, UK
*
*Corresponding author: Dr M. Hutchings, fax +44 131 535 3121, M.Hutchings@ed.sac.ac.uk
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Abstract

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Host-parasite interactions are often seen as an arms race, with parasites attempting to overcome host resistance to infection. Herbivory is a common route of transmission of parasites that represents the most pervasive challenge to mammalian growth and reproduction. The present paper reviews the foraging skills of mammalian herbivores in relation to their ability to exploit plant properties to combat parasites. The starting point is that foraging behaviour may ameliorate the impact of parasitism in three ways; hosts could: (1) avoid foraging in areas contaminated with parasites; (2) select diets which increase their resistance to parasites; (3) select for foods containing anti-parasitic properties (self-medication). Details are given of the pre-requisite skills needed by herbivores if they are to combat parasitism via behaviour, i.e. herbivores are able to: (a) determine their parasitic state and alter their behaviour in relation to that state (behaviours 1, 2 and 3); (b) determine the environmental distribution of parasites (behaviour 1); (c) distinguish plant species or plant parts that increase their resistance to parasites (behaviour 2) or have anti-parasitic properties (behaviour 3). Mammalian herbivores cannot detect the presence of the parasites themselves and must rely on cues such as faeces. Despite the use of these cues contacting parasites may be inevitable and so mechanisms to combat parasitism are necessary. Mammalian herbivores have the foraging skills needed to exploit the heterogeneous distributions of nutrients and parasites in complex foraging environments in order to avoid, and increase their resistance to, parasites. Current evidence for the use of plant secondary metabolites (PSM) by herbivores for self-medication purposes remains equivocal. PSM have both positive (anti-parasitic) and negative (toxic) effects on herbivores. Here details are given of an experimental approach using tri-trophic (plant-herbivore-parasite) interactions that could be used to demonstrate self-medication in animals. There is strong evidence suggesting that herbivore hosts have developed the foraging skills needed to take advantage of plant properties to combat parasites and thus use behaviour as a weapon in the host-parasite arms race.

Keywords

Acquired immunityGrazing behaviourParasite controlParasite distributionSelf-medication
Type
Nutrition and Behaviour Group Symposium on ‘Exploitation of medicinal properties of plants by animals and man through food intake and foraging behaviour’
Information
Proceedings of the Nutrition Society , Volume 62 , Issue 2 , May 2003 , pp. 361 - 370
Copyright
Copyright © The Nutrition Society 2003

References

Abbott, EM, Parkins, JJ & Holmes, PH (1988) Influence of dietary protein on the pathophysiology of haemonchosis in lambs given continuous infections. Research in Veterinary Science 45, 41–49CrossRefGoogle ScholarPubMed
Adewunmi, CO, Agbedahunsi, JM, Adebajo, AC, Aladesanmi, AJ, Murphy, N & Wando, J (2001) Ethno-veterinary medicine: screening of Nigerian medicinal plants for trypanocidal properties. Journal of Ethnopharmacology 77, 19–24CrossRefGoogle ScholarPubMed
Akhtar, MS & Ahmad, I (1992) Comparative efficacy of Mallotus philippinensis fruit (Kamala) or Nilzan drug against gastrointestinal cestodes in Beetal goats. Small Ruminant Research 8, 121–128CrossRefGoogle Scholar
Athanasiadou, S, Kyriazakis, I, Jackson, F & Coop, RL (2000) Effects of short-term exposure to condensed tannins on adult Trichostrongylus colubriformis. Veterinary Record 146, 728–732CrossRefGoogle ScholarPubMed
Baker, JR, Muller, R & Rollinson, D (2001) Antiparasitic properties of medicinal plants and other naturally occurring products. Advances in Parasitology 50, 199–295Google Scholar
Bao, J, Giller, PS & Stakelum, G (1998) Selective grazing by dairy cows in the presence of dung and the defoliation of tall grass dung patches. Animal Science 66, 65–73CrossRefGoogle Scholar
Barnard, CJ & Behnke, JM (1990) Parasitism and Host Behaviour London Taylor and FrancisCrossRefGoogle Scholar
Barry, TN & McNabb, WC (1999) The implications of condensed tannins on the nutritive value of temperate forages fed to ruminants. British Journal of Nutrition 81, 263–272CrossRefGoogle ScholarPubMed
Basset, A, Fedele, M & DeAngelis, DL (2002) Optimal exploitation of spatially distributed trophic resources and population stability. Ecological Modelling 151, 245–260CrossRefGoogle Scholar
Bate-Smith, EC & Metcalf, CR (1957) Leucoanthocyanins. 3. The nature and systematic distribution of tannins in dicotyledoneous plants. Journal of the Linnaean Society 55, 669–705Google Scholar
Bazely, DR (1990) Rules and cues used by sheep foraging in monocultures Behavioural Mechanisms of Food Selection 343–367 Hughes RN London Springer VerlagCrossRefGoogle Scholar
Bazely, DR & Ensor, CV (1989) Discrimination learning in sheep with cues varying in brightness and hue. Applied Animal Behaviour Science 23, 293–299CrossRefGoogle Scholar
Black, JL & Kenney, PA (1984) Factors affecting diet selection by sheep. II. Height and density of pasture. Australian Journal of Agricultural Research 35, 565–578CrossRefGoogle Scholar
Bown, MD, Poppi, DP & Sykes, AR (1991) The effect of post-ruminal infusion of protein or energy on the pathophysiology of Trichostrongylus colubriformis infection and body composition in lambs. Australian Journal of Agriculture 42, 253–267Google Scholar
Coop, RL, Huntley, JF & Smith, WD (1995) Effect of dietary protein supplementation on the development of immunity to Ostertagia circumcincta in growing lambs. Research in Veterinary Science 59, 24–29CrossRefGoogle ScholarPubMed
Coop, RL & Kyriazakis, I (1999) Nutrition-parasite interaction. Veterinary Parasitology 84, 187–204CrossRefGoogle ScholarPubMed
Coop, RL & Kyriazakis, I (2001) Influence of host nutrition on the development and consequences of nematode parasitism in ruminants. Trends in Parasitology 17, 325–330CrossRefGoogle ScholarPubMed
Coop, RL, Sykes, AR & Angus, KW (1982) The effect of three levels of intake of Ostertagia circumcincta larvae on growth rate, food intake and body composition of growing lambs Journal of Agricultural Science, Cambridge 98, 247–255CrossRefGoogle Scholar
Cooper, J, Gordon, IJ & Pike, AW (2000) Strategies for the avoidance of faeces by grazing sheep. Applied Animal Behaviour Science 69, 15–33CrossRefGoogle ScholarPubMed
Cosgrove, GP & Niezen, JH (2000) Intake and selection for white clover by grazing lambs in response to gastrointestinal parasitism. Applied Animal Behaviour Science 66, 71–85CrossRefGoogle Scholar
Courchamp, F, Rasmussen, GSA & Macdonald, DW (2002) Small pack size imposes a trade-off between hunting and pup guarding in the painted hunting dog Lycaon pictus. Behavioural Ecology 13, 20–27CrossRefGoogle Scholar
Dantzer, R, Konsman, JP, Bluthe, RM & Kelley, KW (2000) Neural and humoral pathways of communication from the immune system to the brain: parallel or convergent?. Autonomic Neuroscience 85, 60–65CrossRefGoogle ScholarPubMed
Datta, FU, Nolan, V, Rowe, JB & Gray, GD (1998) Protein supplementation improves the performance of parasitised sheep fed a straw-based diet. International Journal for Parasitology 28, 1269–1278CrossRefGoogle ScholarPubMed
Dawson, JM, Buttery, PJ, Jenkins, D, Wood, CD & Gill, M (1999) Effects of dietary Quebracho tannin on nutrient utilisation and tissue metabolism in sheep and rats. Journal of the Science of Food and Agriculture 79, 1423–14303.0.CO;2-8>CrossRefGoogle Scholar
Deharo, E, Bourdy, G, Quenevo, C, Munoz, V, Ruiz, G & Sauvain, M (2001) A search for natural bioactive compounds in Bolivia through a multidisciplinary approach. Part V. Evaluation of the antimalarial activity of plants used by the Tacana Indians. Journal of Ethnopharmacology 77, 91–98CrossRefGoogle ScholarPubMed
Elenkov, IJ, Wilder, RL, Chrousos, GP & Vizi, ES (2000) The sympathetic nerve – An integrative interface between two super-systems: the brain and the immune system. Pharmacological Reviews 52, 595–638Google Scholar
Engel, C (2002) Wild Health London Weidenfeld and NicolsonGoogle Scholar
Familton, AS & McAnulty, RW (1997) Life cycles and developments of nematode parasites of ruminants Sustainable Control of Internal Parasites in Ruminants 67–79 Barrell GK Lincoln Lincoln UniversityGoogle Scholar
Folstad, I, Nilssen, AC, Halvorsen, O & Andersen, J (1991) Parasite avoidance – the cause of post-calving migrations in rangifer. Canadian Journal of Zoology 69, 2423–2429CrossRefGoogle Scholar
Fox, MT (1997) Pathophysiology of infection with gastrointestinal nematodes in domestic ruminants: recent developments. Veterinary Parasitology 72, 285–308CrossRefGoogle ScholarPubMed
Gibb, MJ, Huckle, CA, Nuthall, R & Rook, AJ (1999) The effect of physiological state (lactating or dry) and sward surface height on grazing behaviour and intake by dairy cows. Applied Animal Behaviour Science 63, 269–287CrossRefGoogle Scholar
Gilbert, KA (1997) Red howling monkey use of specific defecation sites as a parasite avoidance strategy. Animal Behaviour 54, 451–455CrossRefGoogle ScholarPubMed
Goosens, B, Osaer, S & Kora, S (1997) Long term effects of an experimental infection with Trypanosoma congolense on reproductive performance of trypanotolerant Djallonke ewes and west African dwarf goats. Research in Veterinary Science 63, 169–173CrossRefGoogle Scholar
Grand, TC (2002) Foraging-predation risk trade-offs, habitat selection and the coexistence of predators. American Naturalist 159, 106–112CrossRefGoogle Scholar
Grenfell, BT & Dobson, AP (1995) Ecology of Infectious Diseases in Natural Populations Cambridge Cambridge University PressCrossRefGoogle Scholar
Guarrera, PM (1999) Traditional antihelmintic, antiparasitic and repellent uses of plants in Central Italy. Journal of Ethnopharmacology 68, 183–192CrossRefGoogle ScholarPubMed
Gulland, FMD (1992) The role of nematode parasites in Soay sheep ( Ovis aries L.) mortality during a population crash. Parasitology 105, 493–503CrossRefGoogle ScholarPubMed
Harborne, JB (1991) The chemical basis of plant defence Plant Defences Against Mammalian Herbivory 45–59 Palo RT Robbins CT Boca Raton, FL CRC PressGoogle Scholar
Hart, BL (1990) Behavioural adaptations to pathogens and parasites: five strategies. Neuroscience and Biobehavioural Reviews 14, 273–294CrossRefGoogle ScholarPubMed
Hassall, M, Tuck, JM, Smith, DW, Gilroy, JJ & Addison, RK (2002) Effects of spatial heterogeneity on feeding behaviour of Porcellio scaber (Isopoda: Oniscidea). European Journal of Soil Biology 38, 53–57CrossRefGoogle Scholar
Haynes, RJ & Williams, PH (1993) Nutrient cycling and soil fertility in the grazed pasture ecosystem. Advances in Agronomy 49, 119–199CrossRefGoogle Scholar
Herrera, CM & Pellmyr, O (2002) Plant-animal Interactions: An Evolutionary Approach Oxford Blackwell ScienceGoogle Scholar
Houdijk, JGM, Kyriazakis, I, Jackson, F & Coop, RL (2001) The expression of immunity to Teladorsagia circumcincta and its relationship to protein nutrition depend on body protein reserves. Parasitology 122, 661–672CrossRefGoogle ScholarPubMed
Houdijk, JGM, Kyriazakis, I, Jackson, F, Huntley, JF & Coop, RL (2000) Can an increased intake of metabolisable protein affect the periparturient relaxation in immunity against Teladorsagia circumcincta in sheep?. Veterinary Parasitology 91, 43–62CrossRefGoogle Scholar
Huffman, MA (2003) Animal self medication and ethnomedicine: exploration and exploitation of the medicinal properties of plants. Proceedings of the Nutrition Society 62, 371–381CrossRefGoogle ScholarPubMed
Hutchings, MR, Gordon, IJ, Kyriazakis, I & Jackson, F (2001a) Herbivore avoidance of faeces-contaminated patches leads to a trade-off between intake rate of forage and parasitism in subsequent foraging decisions Animal Behaviour 62, 955–964CrossRefGoogle Scholar
Hutchings, MR, Gordon, IJ, Kyriazakis, I, Robertson, E & Jackson, F (2002a) Grazing in heterogeneous environments: Infra- and supra-parasite populations determine herbivore grazing decisions. Oecologia 132, 453–460CrossRefGoogle ScholarPubMed
Hutchings, MR, Gordon, IJ, Robertson, E, Kyriazakis, I & Jackson, F (2000a) Effects of parasitic status and level of feeding motivation on the diet selected by sheep grazing grass/clover swards. Journal of Agricultural Science, Cambridge 135, 65–75CrossRefGoogle Scholar
Hutchings, MR & Harris, S (1997) The effects of farm management practices on cattle grazing behaviour and the potential for transmission of bovine tuberculosis from badgers to cattle. Veterinary Journal 153, 149–162CrossRefGoogle ScholarPubMed
Hutchings, MR, Kyriazakis, I, Anderson, DH, Gordon, IJ & Coop, RL (1998) Behavioural strategies used by parasitised and non-parasitised sheep to avoid ingestion of gastrointestinal nematodes. Animal Science 67, 97–106CrossRefGoogle Scholar
Hutchings, MR, Kyriazakis, I & Gordon, IJ (2001b) Herbivore physiological state affects foraging trade-off decisions between nutrient intake and parasite avoidance. Ecology 82, 1138–1150CrossRefGoogle Scholar
Hutchings, MR, Kyriazakis, I, Gordon, IJ & Jackson, F (1999) Trade-offs between nutrient intake and faecal avoidance in herbivore foraging decisions: the effect of parasitic status, level of feeding motivation and sward nitrogen content. Journal of Animal Ecology 68, 310–323CrossRefGoogle Scholar
Hutchings, MR, Kyriazakis, I, Papachristou, TG, Gordon, IJ & Jackson, F (2000b) The herbivore's dilemma: trade-offs between nutrition and parasitism in foraging decisions. Oecologia 124, 242–251CrossRefGoogle ScholarPubMed
Hutchings, MR, Milner, JM, Gordon, IJ, Kyriazakis, I & Jackson, F (2002b) Grazing decisions of Soay sheep ( Ovis aries ) on St Kilda: a consequence of parasite distribution?. Oikos 96, 235–244CrossRefGoogle Scholar
Ingrand, S, Agabriel, J, Dediey, B & Lassalas, J (2000) Effects of within-group homogeneity of physiological state on individual feeding behaviour of loose-housed Charolais cows. Annales de Zootechnie 49, 15–27CrossRefGoogle Scholar
Kahn, LP, Kyriazakis, I, Jackson, F & Coop, RL (2000) Temporal effects of protein nutrition on the growth and immunity of lambs infected with Trichostrongylus colubriformis. International Journal for Parasitology 30, 193–205CrossRefGoogle ScholarPubMed
Kambara, T, McFarlane, RG, Abell, TJ, McAnulty, RW & Sykes, AR (1993) The effect of age and dietary protein on immunity and resistance in lambs vaccinated with Trichostrongylus colubri-formis. International Journal of Parasitology 23, 411–416CrossRefGoogle Scholar
Keusch, GT, Wilson, CS & Waksal, SD (1983) Nutrition, host defences and the lymphoid system Advances in Host Defence Mechanisms, Vol. 2, 275–359 Gallin JI Fauci AS New York Plenum PressGoogle Scholar
Keymer, AE, Crompton, DW & Walters, DE (1983) Nippostrongylus (Nematoda) in protein malnourished rats: host mortality, morbidity and rehabilitation. Parasitology 86, 461–475CrossRefGoogle ScholarPubMed
King, EJ, Lovell, DJ & Harris, S (1999) Effect of climate on the survival of Mycobacterium bovis and its transmission to cattle herds in south-west Britain Advances in Vertebrate Pest Management 147–162 Cowan DP Feare CJ Furth, Germany Filander VerlagGoogle Scholar
Kyriazakis, I, Anderson, DH, Oldham, JD, Coop, RL & Jackson, F (1996) Long-term subclinical infection with Trichostrongylus colubriformis: Effects on food intake, diet selection and performance of growing lambs. Veterinary Parasitology 61, 297–313CrossRefGoogle ScholarPubMed
Kyriazakis, I, Oldham, JD, Coop, RL & Jackson, F (1994) The effect of subclinical intestinal nematode infection on the diet selection of growing sheep. British Journal of Nutrition 72, 665–677CrossRefGoogle ScholarPubMed
Kyriazakis, I, Tolkamp, BJ & Hulchings, MR (1998) Towards a functional explanation for the occurrence of anorexia during parasitic infections. Animal Behaviour 56, 265–274CrossRefGoogle ScholarPubMed
Lankford, TE, Billerbeck, JM & Conover, DO (2001) Evolution of intrinsic growth and energy acquisition rates. II. Trade-offs with vulnerability to predation in Menidia menidia. Evolution 55, 1873–1881Google ScholarPubMed
Lewis, CE, Clark, TW & Derting, TL (2001) Food selection by the white-footed mouse ( Peromyscus leucopus ) on the basis of energy and protein contents. Canadian Journal of Zoology 79, 562–568CrossRefGoogle Scholar
Lochmiller, RL & Deerenberg, C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity?. Oikos 88, 87–98CrossRefGoogle Scholar
Lozano, GA (1991) Optimal foraging theory: a possible role for parasites. Oikos 60, 391–395CrossRefGoogle Scholar
Lozano, GA (1998) Parasitic stress and self-medication in wild animals. Advances in the Study of Behaviour 27, 291–317CrossRefGoogle Scholar
McFarlane, H (1976) Malnutrition and impaired immune response to infection. Proceedings of the Nutrition Society 35, 263–283CrossRefGoogle ScholarPubMed
Mansour, MM, Rowan, TG, Dixon, JB & Carter, SD (1991) Immune modulation by Ostertagia ostertagi and the effects of diet. Veterinary Parasitology 39, 321–332CrossRefGoogle ScholarPubMed
Niezen, JH, Robertson, HA, Waghorn, GC & Charleston, WAG (1998) Production, faecal egg counts and worm burdens of ewe lambs which grazed six contrasting forages. Veterinary Parasitology 80, 15–27CrossRefGoogle ScholarPubMed
Norris, K (1999) A trade-off between energy intake and exposure to parasites in oystercatchers feeding on a bivalve mollusc. Proceedings of the Royal Society of London 266 B 1703–1709CrossRefGoogle ScholarPubMed
Norris, K & Evans, MR (2000) Ecological immunology: life history trade-offs and immune defense in birds. Behavioural Ecology 11, 19–26CrossRefGoogle Scholar
Parsons, AJ, Newman, JA, Penning, PD, Harvey, A & Orr, RJ (1994) Diet preference of sheep – effects of recent diet, physiological state and species abundance. Journal of Animal Ecology 63, 465–478CrossRefGoogle Scholar
Penning, PD, Parasons, AJ, Orr, RJ, Harvey, A & Champion, RA (1995) Intake and behaviour responses by sheep, in different physiological states when grazing monocultures of grass or white clover. Applied Animal Behaviour Science 45, 63–78CrossRefGoogle Scholar
Pfenning, DW (2000) Effect of predator-prey phylogenetic similarity on the fitness consequences of predation: A trade-off between nutrition and disease?. American Naturalist 155, 335–345CrossRefGoogle Scholar
Poppi, DP, MacRae, JC, Brewer, A & Coop, RL (1986) Nitrogen transactions in the digestive tract of lambs exposed to the intestinal parasite, Trichostrongylus colubriformis. British Journal of Nutrition 55, 593–602CrossRefGoogle Scholar
Provenza, FD, Burritt, EA, Clausen, TP, Bryant, JP, Reichardt, PB & Distel, RA (1990) Conditioned flavour aversion: a mechanism for goats to avoid condensed tannins in blackbrush. American Naturalistic 136, 810–828CrossRefGoogle Scholar
Reed, JD (1995) Nutritional toxicology of tannins and related polyphenols in forage legumes. Journal of Animal Science 73, 1516–1528CrossRefGoogle ScholarPubMed
Richner, H (1998) Host-parasite interactions and life history evolution. Zoology Analysis of Complex Systems 101, 333–344Google Scholar
Rosenthal, GA & Berenbaum, MR (1991) Herbivores – Their Interaction with Secondary Plant Metabolites London Academic PressGoogle Scholar
Satrija, F, Nansen, P, Bjorn, H, Murtini, S & He, S (1994) Effect of Papaya latex against Ascaris suum in naturally infected pigs. Journal of Helminthology 68, 343–346CrossRefGoogle ScholarPubMed
Schetter, TA, Lochmiller, RL, Leslie, DM, Engle, DM & Payton, ME (1998) Examination of the nitrogen limitation hypothesis in non-cyclic populations of cotton rats ( Sigmodon hispidus ). Journal of Animal Ecology 67, 705–721CrossRefGoogle Scholar
Sheldon, BC & Verhulst, S (1996) Ecological immunology: costly parasite defenses and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317–321CrossRefGoogle ScholarPubMed
Sweitzer, RA (1996) Predation or starvation: Consequences of foraging decisions by porcupines ( Erethizon dorastum ). Journal of Mammalogy 77, 1068–1077CrossRefGoogle Scholar
Sykes, AR (1987) Endoparasites and herbivore nutrition Nutrition of Herbivores 211–232 Hacker JB Ternouth JH Sydney, NSW Academic PressGoogle Scholar
Tatar, M & Carey, JR (1995) Nutrition mediates reproductive trade-offs with age specific mortality in the beetle Callosobruchus-maculatus. Ecology 76, 2066–2073CrossRefGoogle Scholar
Tomaszewska, D & Przekop, F (1997) The immune-neuro-endocrine interactions. Journal of Physiology and Pharmacology 48, 139–158Google ScholarPubMed
Tveraa, T & Christensen, GN (2002) Body condition and parental decisions in the snow petrel ( Pagodroma nived ). Auk 119, 266–270CrossRefGoogle Scholar
van, der & Veen, IT (2002) Seeing is believing: information about predators influences yellowhammer behaviour. Behavioural Ecology and Sociobiology 51, 466–471Google Scholar
van, der, Wal, R, Irvine, J, Stien, A, Shepherd, N & Albon, SD (2000) Faecal avoidance and the risk of infection by nematodes in a natural population of reindeer. Oecologia 124, 19–25Google Scholar
van, Houtert, MFJ, van Barger, IA, Steel, JW, Windon, RG, Emery DL (1995) Effects of dietary protein intake on responses of young sheep to infection with Trichostrongylus colubriformis. Veterinary Parasitology 56, 163–180Google Scholar
Villalba, JJ & Provenza, FD (2002) Polyethylene glycol influences selection of foraging location by sheep consuming quebracho tannin. Journal of Animal Science 80, 1846–1851CrossRefGoogle ScholarPubMed
Waller, PJ, Bernes, G, Thamsborg, SM, Sukura, A, Richter, SH, Ingebrigsten, K & Hoglund, J (2001) Plants as de-worming agents of livestock in the Nordic countries: historical perspectives, popular beliefs and prospectives for the future. Acta Veterinaria Scandinavica 42, 31–44CrossRefGoogle ScholarPubMed
Walther, BA & Gosler, AG (2001) The effects of food availability and distance to protective cover on the winter foraging behaviour of tits ( Aves: Parssus ). Oecologia 129, 312–320CrossRefGoogle Scholar
Webb, JN, Szekely, T, Houston, AI & McNamara, JM (2002) A theoretical analysis of the energetic costs and consequences of parental care decisions. Philosophical Transactions of the Royal Society of London 357 B 331–340CrossRefGoogle ScholarPubMed
White, TCR (1993) The Inadequate Environment: Nitrogen and the Abundance of Animals New York Springer VerlagGoogle Scholar
Wilkins, RJ & Jones, R (2000) Alternative home-grown protein sources for ruminants in the United Kingdom. Animal Feed Science and Technology 85, 23–32CrossRefGoogle Scholar
Wright, J, Both, C, Cotton, PA & Brynant, D (1998) Quality vs. quantity: energetic and nutritional trade-offs in parental provisioning strategies. Journal of Animal Ecology 67, 620–634CrossRefGoogle Scholar
Zera, AJ & Harshman, LG (2001) The physiology of life history trade-offs in animals. Annual Review of Ecology and Systematics 32, 95–126CrossRefGoogle Scholar