Juan J. Villalba

Linking herbivore experience, varied diets, and plant biochemical diversity

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.

Preference for wheat straw by lambs conditioned with intraruminal infusions of starch

We hypothesized that feed preference depends on the interplay between flavour and postingestive effects, and we tested two predictions based on this hypothesis: (1) lambs acquire preferences for poorly nutritious feeds paired with starch; and (2) preferences persist when starch is no longer administered. Twenty lambs were randomly allocated to two groups and conditioned as follows: on odd-numbered days, lambs in group 1 received onion-flavoured wheat straw and lambs in group 2 received oregano-flavoured wheat straw. On even-numbered days, the flavours were switched and starch (2.5-9.4% of the digestible energy received/d) was infused into the rumen of all animals during straw consumption. Four periods of 8 d of conditioning were performed and on the 9th day of each period all animals were offered a choice between onion- and oregano-flavoured straw. After conditioning, starch administration was suspended and lambs were offered onion- and oregano-flavoured straw at weekly intervals for 8 weeks (extinction). Lambs strongly preferred the flavoured straw paired with starch, and this preference persisted during extinction. Thus, these results suggest that the postingestive effects of energy play an important role in the development of feed preferences of ruminants.

Preference for flavoured foods by lambs conditioned with intraruminal administration of nitrogen

We suggested that food preference depends on the interplay between flavour and post-ingestive effects, and we predicted that protein-restricted lambs would acquire preferences for foods paired with supplemental sources of N, including urea (Expts 1 and 2), casein (Expt 3), and gluten (Expt 4). In each experiment, twenty lambs, in two groups of ten, were conditioned as follows: on odd-numbered days, lambs in group 1 received wheat straw (Expts 1, 3, and 4) or ground barley (Expt 2) flavoured with a distinctive flavour, and lambs in group 2 received the same food but with a different flavour. On even-numbered days, flavours were switched and lambs received capsules containing different amounts of urea (ranging from 0.12 to 0.92 g N/d), casein (ranging from 0.23 to 0.69 g N/d), or gluten (ranging from 0.23 to 0.69 g N/d). After conditioning period of 8 d, lambs were given a two-choice test to determine preference for flavours paired with N. In Expts 1 and 2, lambs preferred the flavours conditioned with urea at lower doses (0.12 g N/d in Expt 1, 0.23 and 0.46 g N/d in Expt 2), but they avoided the flavour associated with urea at the highest dose (0.23 g N/d in Expt 1 and 0.92 g N/d in Expt 2). In Expts 3 and 4, lambs avoided the flavours associated with the lowest doses of casein or gluten (0.23 g N/d), but they preferred the flavours paired with casein or gluten at higher doses (0.46 and 0.69 g N/d). After conditioning, N administrations were suspended and lambs in Expts 3 and 4 were offered a choice of the two flavours at weekly intervals for 2 weeks (extinction); preferences persisted during extinction. Collectively, these results suggest that the post-ingestive effects of N in different forms and concentrations influenced the development of food preferences by lambs.

Self-Organization of Foraging Behaviour: From Simplicity to Complexity without Goals

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 individuals 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.

FORAGING IN CHEMICALLY DIVERSE ENVIRONMENTS: ENERGY, PROTEIN, AND ALTERNATIVE FOODS INFLUENCE INGESTION OF PLANT SECONDARY METABOLITES BY LAMBS

Interactions among nutrients and plant secondary metabolites (PSM) may influence how herbivores mix their diets and use food resources. We determined intake of a food containing a mix of terpenoids identified in sagebrush (Artemisia tridentata) when present in isoenergetic diets of increasing concentrations of protein (6, 9, 15, or 21% CP) or in isonitrogenous diets of increasing concentrations of energy (2.17, 2.55, 3.30, or 3.53 Mcal/kg). Lambs were offered choices between those diets with or without terpenes or between diets with terpenes and alfalfa hay. Intake of the diets with terpenes was lowest with the lowest concentrations of protein (6%) and energy (2.17 Mcal/kg) in the diets, and highest with diets of 15% CP and 3.53~Mcal/kg. In contrast, when terpenes were absent from the diets, lambs consumed similar amounts of all four diets with different concentrations of protein, and more of the diets with intermediate amounts of energy. When given a choice between the diet with or without terpenes, lambs preferred the diet without terpenes. When lambs were offered choices between terpene-containing diets and alfalfa, energy and protein concentrations influenced the amount of terpenes animals ingested. Energy densities higher than alfalfa, and protein concentrations higher than 6%, increased intake of the terpene-containing diet. Thus, the nutritional environment interacted with terpenes to influence preference such that lambs offered diets of higher energy or protein concentration ate more terpenes when forced, but not when offered alternative food without terpenes. The nutrients supplied by a plant and its neighbors likely influence how much PSM an animal can ingest, which in turn may affect the dynamics of plant communities, and the distribution of herbivores in a landscape. We discuss implications of these findings for traditional views of grazing refuges and varied diets in herbivores.

Tannins and Self-medication:Implications for Sustainable Parasite Control in Herbivores

Animals adapt to the variability of the external environment and to their changing internal needs not only by generating homeostatic physiological responses, but also by operating in the external environment. In this study, we determined whether sheep with a gastrointestinal parasite infection increased intake of a low-quality food containing a natural antiparasitic agent (tannins) relative to non-parasitized sheep. Four groups of lambs (n=8 lambs/group) were assigned to a 2 x 2 factorial design with parasitic burden (P=parasites; NP=no parasites) and the offer of a supplement containing tannins (yes, no) as the main factors. Parasitized lambs ate more of the tannin-containing food than non-parasitized lambs for the first 12 days of the study, when parasite burdens were high, but differences became smaller and disappeared toward the end of the study when parasite burdens decreased. This result suggests the lambs detected the presence of internal parasites or associated symptoms and modified their ingestion of an antiparasitic agent as a function of need.

Selection of Tannins by Sheep in Response to Gastrointestinal Nematode Infection

Herbivores learn to select compounds that attenuate the aversive effects of plant secondary metabolites (PSM), but can they increase intake of PSM they typically avoid when these PSM provide medicinal effects? We hypothesized that herbivores learn to increase intake of PSM-containing feeds when experiencing a gastrointestinal parasitic infection. Ten lambs with natural gastrointestinal parasitic burdens (PB) and 10 nonparasitized lambs (NP) were offered a choice of alfalfa (Medicago sativa) and alfalfa mixed with 10% quebracho tannin (Schinopsis quebracho-colorado; alfalfa:tannins) before and after they were conditioned with the postingestive effects of tannins. Preference for alfalfa:tannins did not differ between groups before experiencing the postingestive effects of tannins (P = 0.85) or when parasite loads were terminated due to the administration of ivermectin (P = 0.18). In contrast, when tested with a parasite burden, lambs in PB consumed more alfalfa:tannins (P = 0.08), showed greater preference for alfalfa:tannins (P = 0.07), and consumed less alfalfa than lambs in NP (P = 0.06). Ingestion of tannins by lambs in PB was followed by reduced fecal egg counts (FEC; P = 0.006), and there was a direct proportional relationship between preference for alfalfa:tannins and FEC (P = 0.07). In summary, parasitized lambs increased their intake of alfalfa:tannins when they experienced a parasite burden, which suggests they self-medicated with tannins against parasites. Self-selection of PSM has implications for the quest for alternatives to chemoprophylaxis in the treatment and well-being of parasitized wild and domestic animals grazing in pasturelands and in confinement.

Effects of food structure and nutritional quality and animal nutritional state on intake behaviour and food preferences of sheep

Abstract There is evidence of the independent effects of plant physical and chemical characteristics on foraging, but little has been done to determine how these traits interact to affect food selection. We determined if the nutritional state of lambs ( Ovis aries ) affected intake behavior and preference for foods with different ratios of protein/energy (alfalfa: high proportion protein/energy; barley: high proportion energy/protein), presented in different physical forms (whole or ground). Changes in nutritional state were induced by altering the nutritional composition of the basal diet (high [Ep] or low [eP] proportion of energy/protein). We determined preference for barley and alfalfa (whole or ground) when lambs were fed (1) a nutritionally balanced diet with a 15-h (overnight) fast (Period 1), (2) an unbalanced diet (Ep or eP) with a 15-h (overnight) fast (Period 2), and (3) an unbalanced diet without a fast (Period 3). Averaged across the three periods, all lambs preferred barley to alfalfa ( P P P P P P >0.05). These differences in intake of energy and protein by lambs fed the unbalanced diets led to a steady increase in the ratio of protein/energy selected by lambs fed the balanced basal diet and diet Ep during Periods 1, 2, and 3 (7.9, 11.7, 13.9 g CP/MJ), and a constant ratio of protein/energy selected by lambs fed the balanced basal diet and diet eP during Periods 1, 2, and 3 (7.6, 8.1, 8.1 g CP/MJ; P P

Learning and Dietary Choice in Herbivores

Abstract Herbivores select diets from an array of plant species that vary in nutrients and plant secondary metabolites (PSM). The outcome is a diet higher in nutrients and lower in PSM than the average available in the environment. Food preferences in herbivores are controlled by dietary cues (i.e., flavor) associatively conditioned by the foods postingestive actions. The senses of smell, taste, and sight enable animals to discriminate among foods. Postingestive feedback calibrates sensory experiences—like or dislike—in accord with past and present experiences with a foods utility to the body. Thus, food selection can be viewed as the quest for substances in the external environment that provide a homeostatic benefit to the internal environment. Livestock form preferences for foods that supply needed nutrients and medicines and avoid foods that provide excesses of PSM and nutrients. In order to manifest this plasticity, animals need a variety of foods instead of being constrained to a single food or monoculture. Under natural conditions where diversity of plants is the rule, not the exception, eating a variety of foods is how animals meet their nutrient requirements and cope with—and likely benefit from—PSM in their diets. At certain doses, PSM may provide beneficial effects to herbivores and favor plant persistence and adaptability. If herbivores learn to utilize multiple plants, the costs of consuming PSM on animal production and well-being could be minimized and the benefits of PSM enhanced. Once individuals learn about the contextual benefits of consuming diverse foods, social models (e.g., mothers) could train new generations of herbivores by observational learning. We propose that by combining the concepts of animal learning and food diversity, it will be possible to create sustainable grazing systems with less dependence on fossil fuels and with enhanced benefits for soils, plants, herbivores, and people.

A Theory of Associating Food Types with Their Postingestive Consequences

Animals often face complex and changing food environments. While such environments are challenging, an animal should make an association between a food type and its properties (such as the presence of a nutrient or toxin). We use information theory concepts, such as mutual information, to establish a theory for the development of these associations. In this theory, associations are assumed to maximize the mutual information between foods and their consequences. We show that associations are invariably imperfect. An association’s accuracy increases with the length of a feeding session and the relative frequency of a food type but decreases as time delay between consumption and postingestive consequence increases. Surprisingly, the accuracy of an association is independent of the number of additional food types in the environment. The rate of information transfer between novel foods and a forager depends on the forager’s diet. In light of this theory, an animal’s diet may have two competing goals: first, the provision of an appropriate balance of nutrients, and second, the ability to quickly and accurately learn the properties of novel foods. We discuss the ecological and behavioral implications of making associational errors and contrast the timescale and mechanisms of our theory with those of existing theory.