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Self-organization of foraging behaviour: From simplicity to complexity without goals

  • Frederick D Provenza (a1), Juan J Villalba (a1), Carl D Cheney (a2) and Scott J Werner (a1)

A herbivore faces challenges while foraging—ongoing changes in its physiological condition along with variation in the nutrient and toxin concentrations of foods, spatially and temporally—that make selecting a nutritious diet a vital affair. Foraging behaviours arise from simple rules that operate across levels of resolution from cells and organs to individuals and their interactions with social and physical environments. At all these levels, behaviour is a function of its consequences: a behaviour operating on the environment to induce changes is itself changed by those events. Thus, behaviour emerges from its own functioning—behaviour self-organizes-not from that of its surroundings. This ostensible autonomy notwith-standing, no self-organizing system (cell, organ, or individual) is independent of its environs because existence consists of an ongoing exchange of energy and matter. According to this view, the notion of cause and effect is replaced with functional relationships between behaviours and environmental consequences. Changes in physical environments alter the distribution, abundance, nutritional, and toxicological characteristics of plants, which affect food preference. Social interactions early in life influence behaviour in various ways: animals prefer familiar foods and environments, and they prefer to be with companions. Animals in unfamiliar environments often walk farther, ingest less food, and suffer more from malnutrition and toxicity than animals in familiar environments. An individual's food preferences—and its ability to discriminate familiar from novel foods—arise from the functional integration of sensory (smell, taste, texture) and postingestive (effects of nutrients and toxins on chemo-, osmo-, and mechano-receptors) effects. The ability to discriminate among foods is critical for survival: all problems with poisonous plants are due to an inability to discriminate or a lack of alternatives. Animals eat a variety of foods as a result of nearing or exceeding tolerance limits for sensory and postingestive effects unique to each food. After eating any food too frequently or excessively, the likelihood increases that animals will eat alternative foods owing to exceeding sensory-, nutrient-, and toxin-specific tolerance limits. Cyclic patterns of intake of a variety of foods reflect seemingly chaotic interactions among flavours, nutrients, and toxins interacting along continua.

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This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

W. F. Andelt , D. L. Baker & K. P. Burnham (1992). Relative preference of captive cow elk for repellent-treated diets. Journal of Wildlife Management 56, 164173.

R. Andersen (1991). Habitat deterioration and the migratory behaviour of moose (Alces alces L.) in Norway. Journal of Applied Ecology 28, 102108.

D. R. Bazely (1989). Carnivorous herbivores: mineral nutrition and the balanced diet. Trends in Ecology and Evolution 4, 155156.

S. Biquand & V. Biquand-Guyot (1992). The influence of peers, lineage and environment on food selection of the criollo goat (Capra hircus). Applied Animal Behaviour Science 34, 231245.

N. Bond & E. Di Guisto (1975). Amount of solution drunk is a factor in the establishment of taste aversion. Animal Learning and Behavior 3, 8184.

J. P. Bryant , F. S. Chapin & D. R. Klein (1983). Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40, 357368.

J. P. Bryant , F. D. Provenza , J. Pastor , P. B. Reichardt , T. P. Clausen & J. T. Du Toit (1991). Interactions between woody plants and browsing mammals mediated by secondary metabolites. Annual Review of Ecology and Systematics 22, 431446.

E. A. Burritt & F. D. Provenza (1991). Ability of lambs to learn with a delay between food ingestion and consequences given meals containing novel and familiar foods. Applied Animal Behaviour Science 32, 179189.

E. A. Burritt & F. D. Provenza (1996). Amount of experience and prior illness affect the acquisition and persistence of conditioned food aversions in lambs. Applied Animal Behaviour Science 48, 7380.

E. A. Burritt & F. D. Provenza (1997). Effect of an unfamiliar location on the consumption of novel and familiar foods by sheep. Applied Animal Behaviour Science 54, 317325.

M. Cabanac (1971). Physiological role of pleasure. Science 173, 11031107.

T. Caraco , W. U. Blanckenhorn , G. M. Gregory , J. A. Newman , G. M. Recer & S. M. Zwicker (1990). Risk-sensitivity: ambient temperature affects foraging choice. Animal Behaviour 39, 338345.

L. E. Chase , P. J. Wangsness , J. F. Kavanaugh , L. C. Griel & J. H. Gahagan (1977). Changes in portal blood metabolites and insulin with feeding steers twice daily. Journal of Dairy Science 60, 403409.

P. D. Coley , J. P. Bryant & F. S. Chapin (1985). Resource availability and plant antiherbivore defense. Science 230, 895899.

R. Coppersmith & M. Leon (1984). Enhanced neural response to familiar olfactory cues. Science 225, 849851.

D. F. Cottrell & A. Iggo (1984). Mucosal enteroceptors with vagal afferent fibers in the proximal duodenum of sheep. Journal of Physiology 354, 497522.

R. A. Distel & F. D. Provenza (1991). Experience early in life affects voluntary intake of blackbrush by goats. Journal of Chemical Ecology 17, 431450.

A. Drewnowski , J. A. Grinker & J. Hirsch (1982). Obesity and flavor perception: multidimensional scaling of soft drinks. Appetite 3, 361368.

M. L. Dudzinski , W. J. Müller , W. A. Low & H.-J. Schuh (1982). Relationship between dispersion behaviour of free-ranging cattle and forage conditions. Applied Animal Ethology 8, 225241.

M. L. Dudzinski , H.-J. Schuh , D. G. Wilcox , H. G. Gardiner & J. G. Morrissey (1978). Statistical and probabilistic estimators of forage conditions from grazing behaviour of merino sheep in a semi-arid environment. Applied Animal Ethology 4, 357368.

G. English-Loeb , M. J. Stout & S. S. Duffey (1997). Drought stress in tomatoes: changes in plant chemistry and potential nonlinear consequences for insect herbivores. Oikos 79, 456468.

E. R. Flores , F. D. Provenza & D. F. Balph (1989). Role of experience in the development of foraging skills of lambs browsing the shrub serviceberry. Applied Animal Behaviour Science 23, 271278.

W. J. Freeman (1991). The physiology of perception. Scientific American 264(2), 7885.

E. L. Gibson & D. A. Booth (1989). Dependence of carbohydrate-conditioned flavor preference on internal state in rats. Learning and Motivation 20, 3647.

L. Glass & C. P. Malta (1990). Chaos in multi-looped negative feedback systems. Journal of Theoretical Biology 145, 217223.

E. A. Gluesing & D. F. Balph (1980). An aspect of feeding behavior and its importance to grazing systems. Journal of Range Management 33, 426427.

I. J. Gordon , A. W. Illius & J. D. Milne (1996). Sources of variation in the foraging efficiency of grazing ruminants. Functional Ecology 10, 219226.

B. Griffith , J. M. Scott , J. W. Carpenter & C. Reed (1989). Translocation as a species conservation tool: status and strategy. Science 245, 477480.

N. T. Hobbs (1996). Modification of ecosystems by ungulates. Journal of Wildlife Management 60, 695713.

M. Hollick (1993). Self-organizing systems and environmental management. Environmental Management 17, 621628.

L. D. Howery , F. D. Provenza , R. E. Banner & C. B. Scott (1996). Differences in home range and habitat use among individuals in a cattle herd. Applied Animal Behaviour Science 49, 305320.

L. D. Howery , F. D. Provenza , R. E. Banner & C. B. Scott (1998). Social and environmental factors influence cattle distribution on rangeland. Applied Animal Behaviour Science 55, 231244.

R. F. Hunter & C. Milner (1963). The behaviour of individual, related and groups of south country Cheviot hill sheep. Animal Behaviour 11, 507513.

J. W. Kalat (1974). Taste salience depends on novelty, not concentration, in taste-aversion learning in the rat. Journal of Comparative and Physiological Psychology 86, 4750.

J. W. Kalat & P. Rozin (1970). ‘Salience’: A factor which can override temporal contiguity in taste-aversion learning. Journal of Comparative and Physiological Psychology 71, 192197.

A. C. Kamil , R. L. Misthal & D. W. Stephens (1993). Failure of simple optimal foraging models to predict residence time when patch quality is uncertain. Behavioral Ecology 4, 350363.

M. L. Kaplan & N. R. Kaplan (1991). The self-organization of human psychological functioning. Behavioral Science 36, 161178.

M. Kennedy & R. D. Gray (1993). Can ecological theory predict the distribution of foraging animals? A critical analysis of experiments on the Ideal Free Distribution. Oikos 68, 158166.

C. Key & R. M. Maclver (1980). The effects of maternal influences on sheep: breed differences in grazing, resting and courtship behaviour. Applied Animal Ethology 6, 3348.

M. Konarzewski & J. Diamond (1994). Peak sustained metabolic rate and its individual variation in cold-stressed mice. Physiological Zoology 67, 11861212.

R. Langvatn & T. A. Hanley (1993). Feeding-patch choice by red deer in relation to foraging efficiency-an experiment. Oecologia 95, 164170.

K. L. Launchbaugh , F. D. Provenza & M. J. Werkmeister (1997). Overcoming food neophobia in domestic ruminants through addition of a familiar flavor and repeated exposure to novel foods. Applied Animal Behaviour Science 54, 327334.

H. R. Maturana & F. J. Varela (1980). Autopoiesis and Cognition: the realization of the living. Dordrecht: Reidel.

R. M. May (1986). When two and two do not make four: nonlinear phenomena in ecology. Proceedings of the Royal Society of London B 228, 241266.

H. Mehansho , A. Hagerman , S. Clements , L. Butler , J. Rogler & D. M. Carlson (1983). Modulation of proline-rich protein biosynthesis in rat parotid glands by sorghums with high tannin levels. Proceedings of the National Academy of Sciences of the USA 80, 39483952.

M. M. Millonas (1992). A connectionist type model of self-organized foraging and emergent behaviour in ant swarms. Journal of Theoretical Biology 159, 529552.

S. N. Mirza & F. D. Provenza (1990). Preference of the mother affects selection and avoidance of foods by lambs differing in age. Applied Animal Behaviour Science 28, 255263.

S. N. Mirza & F. D. Provenza (1992). Effects of age and conditions of exposure on maternally mediated food selection by lambs. Applied Animal Behaviour Science 33, 3542.

M. Naim , J. G. Brand & M. R. Kare (1986). Role of variety of food flavor in fat deposition produced by ‘cafeteria’ feeding of nutritionally controlled diets. In Interaction of the Chemical Senses with Nutrition, pp. 269292 [M.R. Kare and J.G. Brand , editors]. New York: Academic Press.

D. L. Nolte & F. D. Provenza (1991). Food preferences in lambs after exposure to flavours in milk. Applied Animal Behaviour Science 32, 381389.

D. L. Nolte , & F. D. Provenza , R. Callan & K. E. Panter (1992). Garlic in the ovine fetal environment. Physiology & Behavior 52, 10911093.

L. Ortega-Reyes & F. D. Provenza (1993). Amount of experience and age affect the development of foraging skills of goats browsing blackbrush (Coleogyne ramosissima). Applied Animal Behaviour Science 36, 169183.

C. Perez , K. Ackroff & A. Sclafani (1996). Carbohydrate- and protein-conditioned flavor preferences: effects of nutrient preloads. Physiology and Behavior 59; 467474.

J. A. Pfister , F. D. Provenza , G. D. Manners , D. R. Gardner & M. H. Ralphs (1997). Tall larkspur ingestion: Can cattle regulate intake below toxic levels? Journal of Chemical Ecology 23, 759777.

F. D. Provenza (1995). Postingestive feedback as an elementary determinant of food preference and intake in ruminants. Journal of Range Management 48, 217.

F. D. Provenza & E. A. Burritt (1991). Socially-induced diet preference ameliorates conditioned food aversion in lambs. Applied Animal Behaviour Science 31, 229236.

F. D. Provenza , E. A. Burritt , T. P. Clausen , J. P. Bryant , P. B. Reichardt & R. A. Distel (1990). Conditioned flavor aversion: a mechanism for goats to avoid condensed tannins in blackbrush. American Naturalist 136, 810828.

F. D. Provenza , J. J. Lynch , E. A. Burritt & C. B. Scott (1994 a). How goats learn to distinguish between novel foods that differ in postingestive consequences. Journal of Chemical Ecology 20, 609624.

F. D. Provenza , J. J. Lynch & C. D. Cheney (1995). Effects of a flavor and food restriction on the response to novel foods by sheep. Applied Animal Behaviour Science 43, 8393.

F. D. Provenza , J. J. Lynch & J. V. Nolan (1993 a). The relative importance of mother and toxicosis in the selection of foods by lambs. Journal Chemical Ecology 19, 313323.

F. D. Provenza , J. J. Lynch , & J. V. Nolan (1994 b). Food aversion conditioned in anesthetized sheep. Physiology & Behavior 55, 429432.

F. D. Provenza , J. V Nolan & J. J. Lynch (1993 b). Temporal contiguity between food ingestion and toxicosis affects the acquisition of food aversions in sheep. Applied Animal Behaviour Science 38, 269281.

F. D. Provenza , J. A. Pfister & C. D. Cheney (1992). Mechanisms of learning in diet selection with reference to phytotoxicosis in herbivores. Journal of Range Management 45, 3645.

M. R. Ralphs (1997). Persistence of aversions to larkspur in naive and native cattle. Journal of Range Management 50, 367370.

I. Ramirez (1997). Intragastric carbohydrate exerts both intake-stimulating and intake-suppressing effects. Behavioral Neuroscience 111. 612622.

S. H. Revusky & E. W. Bedarf (1967). Association of illness and prior ingestion of novel foods. Science 155, 219220.

J. A. Ricardo & E. T. Koh (1978). Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala, and other forebrain structures in the rat. Brain Research 153, 126.

B. J. Rolls (1986 a). Sensory-specific satiety. Nutrition Reviews 44, 93101.

C. B. Scott , R. E. Banner & F. D. Provenza (1996). Observations of sheep foraging in familiar and unfamiliar environments: familiarity with the environment influences diet selection. Applied Animal Behaviour Science 49, 165171.

C. B. Scott , F. D. Provenza & R. E. Banner (1995). Dietary habits and social interactions affect choice of feeding location by sheep. Applied Animal Behaviour Science 45, 225237.

T. R. Scott (1990). Gustatory control of food selection. In Handbook of Behavioral Neurobiology, vol. 10. pp. 243263 [E.M. Stricker , editor]. New York: Plenum Press.

C. Seynaeve , P. H. M. De Mulder & J. Verweij (1991). Pathophysiology of cytotoxic drug-induced emesis: far from crystal-clear. Pharmaceutisch Weekblad, Scientific Edition 13, 16.

C. J. Shatz (1992). The developing brain. Scientific American 267 (3), 6167.

S. J. Simpson & D. Raubenheimer (1993). A multi-level analysis of feeding behaviour: the geometry of nutritional decisions. Philosophical Transactions of the Royal Society of London B Biological Sciences 342, 381402.

B. F. Skinner (1981). Selection by consequences. Science 213, 501504.

B. F. Skinner (1984).The evolution of behavior. Journal of the Experimental Analysis of Behavior 41, 217221.

R.V. Solé , O. Miramontes & B. C. Goodwin (1993). Oscillations and chaos in ant societies. Journal of Theoretical Biology 161, 343357.

G.L. Stebbins (1981). Coevolution of grasses and herbivores. Annals of the Missouri Botanical Garden 68, 7586.

T. R. Stickland , N. F. Britton & N. R. Franks (1995). Complex trails and simple algorithms in ant foraging. Proceedings of the Royal Society of London B 260, 5358.

S. E. Swithers & W. G. Hall (1994). Does oral experience terminate ingestion? Appetite 23, 113138.

R. J. Tausch , P. E. Wigand & J. W. Burkhardt (1993). Viewpoint. Plant community thresholds, multiple steady states, and multiple successional pathways: legacy of the Quaternary? Journal of Range Management 46, 439447.

A. G. Thorhallsdottir , F. D. Provenza & D. F. Balph (1990). Social influences on conditioned food aversions in sheep. Applied Animal Behaviour Science 25, 4550.

F. M. Toates (1997). Has pure ethology the right foundations for applied ethology? Applied Animal Behaviour Science 53, 113.

J. Wang & F. D. Provenza (1996 b). Food deprivation affects preference of sheep for foods varying in nutrients and a toxin. Journal of Chemical Ecology 22, 20112021.

J. T. Warren & I Mysterud . (1993). Extensive ranging by sheep released onto an unfamiliar range. Applied Animal Behaviour Science 38, 6773.

M. Westoby (1978). What are the biological bases of varied diets? American Naturalist 112, 627631.

J. F. Wilmshurst , J. M. Fryxell & R. J. Hudson (1995). Forage quality and patch choice by wapiti (Cervus elaphus). Behavioral Ecology 6, 209217.

O. W. Wooley , S. C. Wooley & R. B. Dunham (1972). Calories and sweet taste: effects on sucrose preference in the obese and nonobese. Physiology and Behavior 9, 765768.

J. Wu & O. L. Loucks (1995). From balance of nature to hierarchical patch dynamics: a paradigm shift in ecology. Quarterly Review of Biology 70, 439466.

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Nutrition Research Reviews
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