Elsevier

Small Ruminant Research

Volume 49, Issue 3, September 2003, Pages 257-274
Small Ruminant Research

Review
Linking herbivore experience, varied diets, and plant biochemical diversity

https://doi.org/10.1016/S0921-4488(03)00143-3Get rights and content

Abstract

We contend diets and habitats that allow animals to select among alternatives enable individuals to better meet needs for nutrients and to better cope with toxins. All plants contain toxins, and the amount of toxin an animal can ingest depends on the kinds and amounts of nutrients and toxins in the forages on offer. Nutrients and toxins both cause animals to satiate, and excesses of nutrients, nutrient imbalances, and toxins all limit food intake. Thus, individuals can better meet their needs for nutrients and regulate their intake of toxins when offered a variety of foods that differ in nutrients and toxins than when constrained to a single food, even if the food is “nutritionally balanced”. Food intake and preference also depend on differences in how individual animals are built morphologically and how they function physiologically, and marked variation is common even among closely related animals in needs for nutrients and abilities to cope with toxins. Transient food aversions compound the inefficiency of single-food diets—whether in confinement, on pastures, or on rangelands—by depressing intake among individual animals, even if they are suited “on average” to that nutrient or toxin profile. Thus, feeding and grazing practices that allow producers to capitalize on the individuality of animals are likely to improve performance of the herd by enabling the uniqueness of individuals to become manifest. Finally, past experiences play a crucial role in an animal’s propensity to learn to eat different foods. When herbivores are allowed to eat only the most preferred plants, they are not likely to learn to mix foods high in nutrients with foods that contain toxins. Conversely, herbivores encouraged to eat all plants in an area are more likely to learn to eat mixes of plants that mitigate toxicity. Experienced animals who have learned to eat a variety of foods that differ in nutrients and toxins do so even when nutritious alternatives are available, whereas naive animals familiar only with the nutritious alternatives eat only that subset of familiar foods. Different systems of management alter how animals forage. Continuous grazing at low stock densities encourages selectivity and reduces diet and habitat breadth, whereas short-duration grazing at high stock densities increases diet and habitat breadth. Thus, what was traditionally considered proper grazing management—rotational grazing at low stock densities—may have trained generations of livestock to “eat the best and leave the rest” thus inadvertently accelerating a decline in biodiversity and an increase in the abundance of less desirable plant species.

Introduction

It is widely purported that ecosystem function depends on biological diversity. Nonetheless, the issue is controversial (Kaiser, 2000), in part because little is known about the biochemical links associated with plant diversity. While we have much to learn about biochemical interactions among plants, and about how herbivores learn to mix their diets to optimize intake of biochemicals, we submit that biochemical diversity increases the potential for resiliency, adaptability, and productivity of ecosystems by increasing options for plants, herbivores, and people. Furthermore, people interested in managing ecosystems can use understanding of biochemical interactions among plants and herbivores to enhance and maintain the biodiversity of landscapes.

The kinds and amounts of nutrients and toxins in a plant or its neighbors determine the effectiveness of a toxin and influence the probability of a plant being eaten (Provenza et al., 2002). All plants contain some levels of toxins so complete avoidance is not feasible. Rather, herbivores must regulate intake of toxins (Foley et al., 1999). Intake of toxic plants depends on the kinds and concentrations of nutrients and toxins; some interactions increase intake, others do not (Burritt and Provenza, 2000, Villalba et al., 2003). How herbivores learn to mix their diets from an array of biochemically diverse plants in turn influences plant biochemical diversity. Associational effects involving plant chemistry and herbivore learning influence coexistence of plants and animals, and can either enhance or diminish biodiversity (Provenza et al., 2002, Villalba et al., 2002c, Villalba et al., 2003).

In this paper, we discuss how plant biochemical diversity interacts with an herbivore’s experiences mixing foods with different flavors, nutrients, and toxins, and the implications for managing animals in confinement, on pastures, and on rangelands.

Section snippets

Uniqueness of the individual

With the advent of statistics in the 20th century, great emphasis has been placed on assessing the response of the “average” animal to a treatment. While the discipline of statistics has advanced our ability to conduct experiments, it also has made variation among individuals a foe to counter rather than a friend to embrace (Provenza et al., 1999). Today, we emphasize means and populations, rather than individuals and variation, while nature and evolutionary processes do the opposite.

Roles of nutrients and toxins

Interactions among nutrients and toxins influence food and habitat selection and mediate plant–herbivore interactions, but they do so in ways we are just beginning to understand. Most studies of nutrient–toxin interactions have been done with rodents and humans. Although many of the principles derived from these investigations apply across species, care must be taken when extrapolating the influence of specific compounds on different species and individuals, both of which respond uniquely to

Theoretical considerations regarding experience and diet mixing

Optimal foraging theory assumes that herbivores forage to maximize energy intake per unit effort (Stephens and Krebs, 1986). According to this theory, foods vary with respect to their intrinsic quality, and an herbivore should either eat or ignore a type of food (the zero-one rule). In other words, a ‘high quality’ food is always better than a ‘low quality’ food. Accordingly, herbivores should not exhibit partial preferences for “poorer” quality foods.

Nevertheless, partial preferences have been

Feeding animals in confinement

Dairy cows, beef cattle, and sheep maximize energy intakes when their diets consist of a mixture of concentrates and roughages, especially when the concentrate portion of the ration greatly exceeds needs. The amount of roughage needed to maximize energy intake depends on the individual, as well as the species, age, and level of production (reviewed by Grovum (1988)). Lactating cows consume less energy from an extremely high energy diet containing mainly grain than they do when the mixture of

Conclusions

We contend that plant biochemical diversity increases the resiliency, adaptability, and productivity of systems by increasing options for plants, herbivores, and people. Biochemical diversity enables the neurological, morphological, physiological uniqueness of each individual in a group to be manifest by selecting diets that optimize its intake of nutrients and toxins. Feeding practices that permit animals to choose among foods create opportunities to reduce costs and enhance performance in

Acknowledgements

This effort was supported by the Utah Agricultural Experiment Station (Project No. 4-20526), and the United States Department of Agriculture Cooperative State Research, Education and Extension Service (Agreement No. 2001-52103-11215).

References (161)

  • S.N. Mirza et al.

    Effects of age and conditions of exposure on maternally mediated food selection in lambs

    Appl. Anim. Behav. Sci.

    (1992)
  • H. Olff et al.

    Effects of herbivores on grassland plant diversity

    TREE

    (1998)
  • L. Ortega-Reyes et al.

    Amount of experience and age affect the development of foraging skills of goats browsing blackbrush (Coleogyne ramosissima)

    Appl. Anim. Behav. Sci.

    (1993)
  • C. Perez et al.

    Carbohydrate- and protein-conditioned flavor preferences: effects of nutrient preloads

    Phys. Behav.

    (1996)
  • T. Piersma et al.

    Rapid reversible changes in organ size as a component of adaptive behaviour

    TREE

    (1997)
  • P. Pliner

    The effects of mere exposure on liking for edible substances

    Appetite

    (1982)
  • C.G. Aldrich et al.

    The effects of endophyte-infected tall fescue consumption and use of a dopamine antagonist on intake, digestibility, body temperature, and blood constituents in sheep

    J. Anim. Sci.

    (1993)
  • S.B. Atwood et al.

    Changes in preferences of gestating heifers fed untreated or ammoniated straw in different flavors

    J. Anim. Sci.

    (2001)
  • S.B. Atwood et al.

    Influence of free-choice versus mixed-ration diets on food intake and performance of fattening calves

    J. Anim. Sci.

    (2001)
  • Bailey, A.W., 1996. Future role of fire in rangeland vegetation dynamics. In: West, N.E. (Ed.), Proceedings of the...
  • R.E. Banner et al.

    Supplemental barley and activated charcoal increase intake of sagebrush by lambs

    J. Range Manage.

    (2000)
  • Baraza, E., Villalba, J.J., Provenza, F.D., 2003. Nutritional context influences preferences of lambs for foods with...
  • Belovsky, G.E., Schmitz, O.J., 1991. Mammalian herbivore foraging and the role of plant defenses. In: Palo, R.T.,...
  • G.E. Belovsky et al.

    Plant defenses and optimal foraging by mammalian herbivores

    J. Mammal.

    (1994)
  • Belovsky, G.E., Fryxell, J., Schmitz, O.J., 1999. Natural selection and herbivore nutrition: optimal foraging theory...
  • D. Berteaux et al.

    Food choice by white-tailed deer in relation to protein and energy content of the diet: a field experiment

    Oecologia

    (1998)
  • E.W. Bork et al.

    Cover components on long-term seasonal sheep grazing treatments in three-tip sagebrush steppe

    J. Range Manage.

    (1998)
  • R. Boyle et al.

    Fate of the dietary terpene, p-cymene, in the male koala

    J. Chem. Ecol.

    (2000)
  • R.O. Bray et al.

    Influence of sagebrush terpenoids on mule deer preference

    J. Chem. Ecol.

    (1991)
  • Briske, D.D., Richards, J.H., 1995. Plant responses to defoliation: a physiological, morphological and demographic...
  • J.P. Bryant et al.

    Interactions between woody plants and browsing mammals mediated by secondary metabolites

    Annu. Rev. Ecol. Syst.

    (1991)
  • Bryant, J.P., Reichardt, P.B., Clausen, T.P., Provenza, F.D., Kuropat, P.J., 1992. Woody plant–mammal interactions. In:...
  • Burkhardt, J.W., 1996. Herbivory in the Intermountain West, Idaho Forest. Wildlife and Range Experiment Station...
  • E.A. Burritt et al.

    Role of toxins in intake of varied diets by sheep

    J. Chem. Ecol.

    (2000)
  • M.C. Calhoun et al.

    Experimental prevention of bitterweed (Hymenoxys odorata) poisoning of sheep

    Am. J. Vet. Res.

    (1989)
  • Cheeke, P.R., 1998. Natural Toxicants in Feeds, Forages, and Poisonous Plants. Interstate Publication Inc., Danville,...
  • Cheeke, P., Shull, L.R., 1985. Natural Toxicants in Feeds and Poisonous Plants. Avi Publishing, Westport,...
  • S.D.B. Cooper et al.

    The effect of physiological state (late pregnancy) on the diet selection of ewes

    Anim. Prod.

    (1993)
  • S.D.B. Cooper et al.

    Diet selection in sheep: the role of the rumen environment in the selection of a diet from two feeds that differ in their energy density

    Br. J. Nutr.

    (1995)
  • G.P. Cosgrove et al.

    Opportunities for enhancing the delivery of novel forage attributes

    Proc. N.Z. Soc. Anim. Prod.

    (2001)
  • H.D. Critchley et al.

    Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex

    J. Neurophysiol.

    (1996)
  • M.D. Dearing et al.

    Role of detoxification of plant secondary compounds on diet breadth in a mammalian herbivore, Trichosurus vulpecula

    J. Chem. Ecol.

    (1999)
  • R.A. Distel et al.

    Experience early in life affects voluntary intake of blackbrush by goats

    J. Chem. Ecol.

    (1991)
  • R.A. Distel et al.

    Effects of early experience on voluntary intake of low-quality roughage by sheep

    J. Anim. Sci.

    (1994)
  • R.A. Distel et al.

    Persistence of the effects of early experience on consumption of low-quality roughage by sheep

    J. Anim. Sci.

    (1996)
  • D. Early et al.

    Food flavor and nutritional characteristics alter dynamics of food preference in lambs

    J. Anim. Sci.

    (1998)
  • A.R. Egan

    Host animal–rumen relationships

    Proc. Nutr. Soc.

    (1980)
  • Engel, C., 2002. Wild Health: How Animals Keep Themselves Well and What We Can Learn from Them. Houghton Mifflin Co.,...
  • D.S. Fisher

    Modeling ruminant feed intake with protein, chemostatic, and distention feedbacks

    J. Anim. Sci.

    (1997)
  • W.J. Foley

    Nitrogen and energy retention and acid–base status in the common ringtail possum (Pseudocheirus peregrinus): evidence of the effects of absorbed allelochemicals

    Physiol. Zool.

    (1992)
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