Resource Availability and Quality Influence Patterns of Diet Mixing by Sheep
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- Shaw, R.A., Villalba, J.J. & Provenza, F.D. J Chem Ecol (2006) 32: 1267. doi:10.1007/s10886-006-9083-2
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In grazing systems, forage availability is a function of herbivore density, which can influence an animal's ability to be selective. In turn, the influence of food availability on selectivity has the potential to influence plant biodiversity. We hypothesized that the ability of herbivores to mix toxin-containing foods in their diets is a function of the availability of nontoxic foods and the nutritional characteristics of the toxin-containing foods. We evaluated this hypothesis in two trials simulating different diet qualities (high-quality foods in trial 1, low-quality foods in trial 2). Within each trial, the four treatment groups were offered with different amounts of nutritious, familiar foods—10, 30, 50, and 70% of ad libitum intake—but were offered with ad libitum access to toxin-containing foods. Each lamb was presented with five foods, including three toxin-containing unfamiliar foods (terpenes, tannins, and oxalates) and two nutritious familiar foods (alfalfa and barley). In trial 1, as the availability of nutritious familiar foods decreased, animals ate more of all three toxin-containing foods. As the availability of nutritious alternatives increased, the pattern of selection shifted from terpenes to tannins and oxalates. In trial 2, animals also ate more toxins as the availability of nutritious alternatives decreased, but their pattern of diet mixing changed. Low availability of nutritious alternatives resulted in the animals eating more oxalates. During preference tests when all five foods were offered ad libitum, animals fed with 10, 30, 50, and 70% of ad libitum intake from trial 1 ate 49, 47, 41, and 38% of the three toxin-containing foods, respectively. The lower diet quality in trial 2 affected intake of the toxin-containing foods such that animals fed with 10, 30, 50, and 70% of ad libitum intake ate 37, 36, 29, and 27%, respectively, of the three toxin-containing foods. Thus, the quality of toxin-containing foods and the availability of nutritious alternatives interacted to modify the pattern of diet mixing by lambs.
Herbivores modify environments by selectively consuming foods (Palo and Robbins, 1991), and the process of diet selection is shaped by intricate interactions between nutrients, toxins, and animal experience (Hanley, 1997; Provenza et al., 2003a; Villalba et al., 2004). Nutrients and toxins both influence the kinds and amounts of foods eaten as animals strive to meet nutritional needs (Westoby, 1978), and regulate their intake of toxins (Freeland and Janzen, 1974; Villalba et al., 2002a). Experiences early in life, of both the social and physical environments, shape behavior, influence gene expression (McCormick et al., 2000; Duffy et al., 2002), and improve performance by inducing neurological, morphological, and physiological changes in animals (Piersma and Lindstrom, 1997; Schlichting and Pigliucci, 1998). Such plasticity enables adaptation to different environmental conditions and implies that different conditions influence how an animal perceives diet and habitat quality (Davis and Stamps, 2004). These dynamics influence the structure and diversity of plant communities (Provenza et al., 2003a,b).
Herbivores learn to forage (goats, Distel and Provenza, 1991; lambs, Green et al., 1984; and cattle, Wiedmeier et al., 2002), but how they learn to mix their diets given a variety of alternatives is poorly understood (Provenza et al., 2003b). The availability of alternative plants likely increases the difficulty of distinguishing beneficial or deleterious relationships involving toxin–toxin, nutrient–toxin, and nutrient–nutrient interactions. Such interactions influence the amount of nutrients and toxins an animal can ingest (Freeland and Janzen, 1974; Illius and Jessop, 1995; Banner et al., 2000), as well as preferences for foods that differ in nutrients and toxins (Villalba et al., 2002a,b). In addition, interactions among toxins can either increase or decrease consumption of combinations of foods that contain toxins (Schmidt et al., 1998; Dearing and Cook, 1999; Burritt and Provenza, 2000; Provenza et al., 2003a; Villalba et al., 2004).
We hypothesized that the ability of herbivores to mix toxin-containing foods in their diets is a function of the availability of nontoxic foods and the nutritional characteristics of toxin-containing foods. Based on these hypotheses, we predicted that young animals exposed to high availability of nutritious alternatives would consume less novel toxin-containing foods, thus impeding their acquisition of diet-mixing behavior. In contrast, we predicted that young animals exposed to low availability of nutritious alternatives would learn to consume more of the novel toxin-containing foods.
Methods and Materials
The objective of these studies was to determine the degree to which sheep mix an array of unfamiliar toxin-containing foods with familiar high-quality foods when the familiar foods were available in different amounts: 10, 30, 50, and 70% of the animal's intake capacity. The toxins were present in a high-quality (trial 1) or a low-quality (trial 2) base food. Trial 1 was conducted from June 24, 2002 to July 31, 2002, and trial 2 from August 6, 2002 to September 12, 2002. The studies were conducted at the Green Canyon Ecology Center, located at Utah State University in Logan, UT, USA, and were approved by the Animal Care and Use Committee at Utah State University.
We used a different set of 32 lambs in each trial. Lambs were commercial crossbreds of both sexes, 4–5 mo old. In trial 1, they averaged 40 kg (SE = 0.73) body mass, and in trial 2, they averaged 37 kg (SE = 1.03) body mass. They were inexperienced with the toxins at the start of each trial, as well as with the ingredients of the base food that contained the toxins. Lambs were individually penned with free access to trace mineral salt blocks and freshwater. They were individually penned 10 d prior to initial exposure, during which they received alfalfa pellets ad libitum and barley (300 g/lamb/d).
We used five foods in this study: three unfamiliar and two familiar to the lambs. The three unfamiliar, high-quality test foods were formulated with the same ingredients, but 0 isoenergetic (2.9 ± 0 Mcal/kg, NRC 1985) and isonitrogenous (126 g CP/kg; NRC, 1985). The ingredients and compositions of the diets were as follows: (1) tannin diet (76% beet pulp, 9% soybean meal, and 15% quebracho tannin); (2) terpene diet (52.8% beet pulp, 26% grape pomace, 14% soybean meal, 1.82% camphor, 1.1% 1-8-cineole, 0.12% methacrolein, 0.06% p-cymene, and 4.1% vegetable oil); and (3) oxalate diet (67.5% beet pulp, 20% grape pomace, 11% soybean meal, and 1.5% oxalic acid). The remaining two familiar, high-quality foods were (4) a 50:50 mix of ground alfalfa and ground barley (3.2 Mcal/kg and 14% crude protein) and (5) ground alfalfa (2.5 Mcal/kg and 15% crude protein).
Three low-quality foods also were formulated to be isoenergetic (2.3 ± 0 Mcal/kg; NRC, 1985) and isonitrogenous (63 g CP/kg; NRC, 1985), with the same ingredients and different concentrations and types of toxins. The ingredients and compositions of the diets were as follows: (1) tannin diet (58.5% beet pulp, 25% grape pomace, 1.5% soybean meal, and 15% quebracho tannin); (2) terpene diet (35.8% beet pulp, 51% grape pomace, 6% soybean meal, 1.82% camphor, 1.1% 1-8-cineole, 0.12% methacrolein, 0.06% p-cymene, and 4.1% vegetable oil); (3) oxalate diet (50.5% beet pulp, 45% grape pomace, 3% soybean meal, and 1.5% oxalic acid). The other two foods were the same familiar foods (alfalfa/barley; alfalfa) offered in the previous trial.
Food ingredients in both test diets were ground to 2- to 3-mm particle size to facilitate mixing. Toxins were in crystalline (oxalic acid, camphor), powder (tannin), or liquid (1,8-cineole, methacrolein, p-cymene) form. Volatilization of the terpenoids was minimized by daily mixing in vegetable oil prior to mixing them with the remaining ingredients. The concentrations of toxins in the test diets were selected according to the amount of toxins sheep can ingest in 1–4 hr (Villalba et al., 2004).
Trial 1: Toxins in a High-Quality Food
This trial consisted of 7 d of preconditioning and 21 d of conditioning. During the 7 d of preconditioning, lambs were offered with the two familiar foods ad libitum from 0800 to 1200 hr, after which refusals were collected and weighed. Animals then were stratified into four groups of eight animals according to their individual total intake of the two familiar foods. Animals from these groups were then randomly allocated to one of the four treatments. For the next 21 d, animals in treatments 1, 2, 3, and 4 received, respectively, 10, 30, 50, and 70% of the average total intake during preconditioning. The proportions of these two familiar foods were based on the average intakes of each animal during the pretrial. For example, a lamb in treatment 1 that ate on average 1000 g of ground alfalfa/barley and 500 g of ground alfalfa received 100 g of the alfalfa/barley mix and 50 g of the ground alfalfa during the trial. Lambs were offered with the three unfamiliar (toxin-containing) foods ad libitum.
During the 21 d of conditioning, all five foods were offered from 0800 to 1200 hr. No other foods were offered for the remainder of the day. At 1200 hr, refusals were gathered and weighed, and intake of each of the five foods was recorded for each animal. Lambs were weighed individually at the beginning and end of the 21-d conditioning period.
Trial 2: Toxins in a Low-Quality Food
Trial 2 occurred immediately after trial 1 with a new set of 32 lambs. Conditioning for trial 2 followed the same protocol as for trial 1, the only difference being the reduced quality of the test diets that contained the toxins.
Preference Tests for Trials 1 and 2
For 2 d immediately after conditioning in each trial, animals had ad libitum access to all five foods from 0800 to 1200 hr. Refusals were collected and weighed, and individual intake was recorded. Following that preference test, animals were fed with alfalfa pellets (ad libitum) and barley (300 g/lamb/d) for 7 d. This period allowed all animals to be on a comparable plane of nutrition. Following this period, another 2-d preference test was conducted.
The statistical design for the analysis of variance (ANOVA) during the conditioning period and the preference tests was a split-plot with day as a repeated measure. At the whole-plot level, there were four treatments (10, 30, 50, and 70% restriction) with eight lambs nested within each of the four treatments. At the subplot level, there were five foods and their interaction with treatment. Day (N = 21 during conditioning and 2 during preference tests) was the repeated measure. Intake was converted to grams of food ingested/kg MBW (kg0.75) to account for differences in body mass within and between trials. When F values were significant (P < 0.05), differences in means were analyzed with the least significant difference test. ANOVA was performed using the MIXED procedure in SAS (SAS; Littell et al., 1996).
Trial 1 Conditioning
The availability of alternatives influenced the diet selection of lambs. The total amount of toxin-containing foods ingested by lambs in treatments 1 and 2 (61 and 59 g/kg0.75) was greater than for treatments 3 and 4 (43 and 46 g/kg0.75; P < 0.005). As the availability of nutritious alternatives—alfalfa and barley—increased, the total amount of toxin-containing foods consumed decreased.
The average daily weight gain did not differ among treatments as the availability of alternatives increased (P > 0.05). The trial average increase was 0.102 kg/lamb/d.
Trial 1 Preference
Restriction during conditioning increased preference for the toxin-containing foods. Given ad libitum access to all five foods, lambs showed higher preference for the three toxin-containing foods in treatments 1 (49%) and 2 (47%) than in treatments 3 (41%) and 4 (38%; P < 0.05). Total intake of the toxin-containing foods did not differ from that of the nutritious familiar alternatives for any of the groups (P > 0.05).
Preference was greater in all treatments for the tannin-containing food than for the terpene or oxalate-containing foods (P < 0.05; Fig. 2). In treatments 1 and 4, intake was greater for the oxalate than the terpene-containing food (P < 0.05; Fig. 2). The alfalfa/barley mix was preferred by all treatments (P < 0.005), whereas the intake of alfalfa was less than the tannin-containing food in treatments 1, 2, and 4 (P < 0.005).
Trial 2 Conditioning
Lambs were influenced by the availability of alternatives and the poorer diet quality. The amount of total toxin-containing foods ingested decreased as the availability of alternatives increased, such that lambs in treatments 1–3 (61, 56, and 54 g/kg0.75, respectively) ate more total toxin-containing foods than lambs in treatment 4 (44 g/kg0.75; P < 0.005). Lambs in treatment 1 also consumed more total toxin-containing foods than those in treatment 3 (P < 0.05).
Consumption of individual toxin-containing foods also varied among treatments (Fig. 1). The intake of the oxalate-containing food was greater for lambs in treatment 1 than treatments 2–4 (P < 0.05) and greater in treatments 2 and 3 than in treatment 4 (P < 0.05). Lambs in treatment 1 also consumed more terpene-containing food than lambs in treatment 4 (P < 0.05), whereas those in treatment 3 ingested higher amounts of the tannin-containing food than lambs in treatment 1 (P < 0.05).
The intake of individual toxin-containing foods also varied (Fig. 1). Lambs ate the least of the terpene-containing food (P < 0.005). In treatment 1, intake of the oxalate-containing food was highest, whereas in treatments 3 and 4, consumption of the tannin-containing food was highest (P < 0.005). Lambs in treatment 2 ate similar amounts of the tannin and oxalate-containing foods (P > 0.05).
Patterns of use of toxin-containing foods varied between trials 1 and 2 (Fig. 1). Animals in trial 1 ate large amounts of tannins, whereas those in trial 2 ate large amounts of tannins and oxalates. Lambs in treatments 1–3 all ate more oxalates in trial 2 than in trial 1 (P < 0.005). All lambs ate more oxalates than terpenes in trial 2, and this pattern was most pronounced in lambs in treatment 1 that ate more oxalates than tannins or terpenes (P < 0.005; Fig. 1). Finally, intake of terpenes by treatments 1, 3, and 4 decreased from trials 1 to 2 (P < 0.05).
The average daily weight gain in trial 2 did not differ among treatments (P > 0.05). However, lambs gained less in trial 2 (0.015 kg/lamb/d) than in trial 1 (0.102 kg/lamb/d; P < 0.005).
Trial 2 Preference
While preference continued to be influenced by the availability of alternatives, the lower diet quality in trial 2 affected intake of the toxin-containing foods. Lambs in treatments 1 (37%) and 2 (36%) showed higher preference for the toxin-containing foods than lambs in treatments 3 (29%) and 4 (27%; P < 0.05). The total amount of toxin-containing foods consumed and the total amount of safe foods consumed during the preference tests did not differ (P > 0.05).
Intake of individual toxin-containing foods varied among treatments. Lambs in treatment 1 consumed more oxalate than those in treatments 3 and 4 (P < 0.05), and lambs in treatment 2 consumed more oxalates than those in treatment 4 (P < 0.05; Fig. 2). Preferences did not differ among treatments for the terpene and tannin-containing foods (P > 0.05; Fig. 2). Preference for the alfalfa/barley mix was lower in treatment 1 than treatments 3 and 4 and lower in treatment 2 than in treatments 1, 3, and 4 (P < 0.05; Fig. 2).
Within each of the four treatments, preference for the terpene-containing food was lower than for the other two toxin-containing foods (P < 0.005). Within treatment 1, preference was higher for the oxalate-containing food than for the tannin-containing food (P < 0.005; Fig. 2). As in trial 1, all lambs preferred the alfalfa/barley mix to other foods (P < 0.005). Alfalfa intake was higher than the tannin-containing food in treatment 2 (P < 0.05), higher than the oxalate-containing food in treatment 3 (P < 0.05), and higher than both tannin and oxalate-containing foods in treatment 4 (P < 0.05).
The preference for toxin-containing foods also varied between trials (Fig. 2). Lambs ate more oxalate and less terpene during conditioning in trial 1 than in trial 2, and this pattern persisted during the preference trial. Treatments 1 and 2 consumed more oxalate and less terpene than they did during trial 1 (P < 0.05). Additionally, lambs in treatments 1, 2, and 4 had a lower preference for tannin in trial 2 than in trial 1 (P < 0.05). Lambs in trial 2 also ate more alfalfa/barley mix (treatments 1, 3, and 4, P < 0.05) and more alfalfa (treatments 2 and 4, P < 0.05; and treatment 3, P < 0.05).
We hypothesized that the ability of herbivores to mix toxin-containing foods in their diets is a function of the availability of nontoxic foods and the nutritional characteristics of toxin-containing foods. Based on this hypothesis, we predicted that young lambs exposed to high availability of nutritious alternatives would consume less novel toxin-containing foods, thus impeding their acquisition of diet-mixing behavior. In contrast, we predicted that young lambs exposed to low availability of nutritious alternatives would learn to consume more of the novel toxin-containing foods.
In our studies, both the quality of the toxin-containing food and the availability of alternatives affected the acquisition and retention of diet-mixing behavior. Animals consistently ingested more of the three toxin-containing foods during both conditioning and preference trials, as the availability of high-quality foods decreased and the quality of the foods containing the toxins increased (Figs. 1 and 2). Given an adequate level of nutrition, the toxin-containing diets we used complement one another in that lambs eat much more when offered a meal of three foods (tannins, terpenes, and oxalates) than they do in a meal of two foods (tannins–terpenes, tannins–oxalates, or terpenes–oxalates), and they eat much more in a meal of two foods than when they are offered only one of the foods (Villalba et al., 2004). According to optimal foraging theory, herbivores should forage on plants that maximize energy intake per unit effort (Stephens and Krebs, 1986), and they should either eat or ignore food depending on the density of other more profitable foods (the zero–one rule, Stephens and Krebs, 1986; or the none-or-all rule, McNamara and Houston, 1987). According to this rule, animals should not exhibit partial preferences for poorer quality foods. However, generalist herbivores typically do exhibit partial preferences (Stephens and Krebs, 1986; Belovsky and Schmitz, 1991; Belovsky et al., 1999), and several explanations have been proposed (McNamara and Houston, 1987; Illius et al., 1999; Provenza et al., 2003b). Our study provides evidence that partial preferences depend on prior foraging experience and nutrient–toxin interactions.
Experience and the availability of alternative foods both influence diet mixing, as illustrated in trials where lambs with 3 mo of experience mixing tannin, terpene, and oxalate-containing foods were compared with lambs with no previous experience with the same foods (Villalba et al., 2004). As in the present study, all lambs were offered five foods, including the toxin-containing foods and two nutritious alternatives—ground alfalfa and barley. However, in contrast to this study, which limited the availability of familiar foods to 10, 30, 50, or 70%, that study provided half of the lambs with 200 g (restricted to approximately 20–25% of ad libitum) and half with ad libitum access to the familiar foods. Lambs lacking experience with the toxin-containing foods, and given the nutritious alternatives ad libitum, ate much less of the toxin-containing foods than lambs with restricted alternatives (66 vs. 549 g/d). Experienced lambs also ate less of the toxin-containing foods if they were given ad libitum rather than restricted access to alternatives (809 vs. 1497 g/d). In both cases, the availability of nutritious alternatives and previous mixing experience influenced how much of the toxin-containing foods were consumed. In both trials, animals learned to mix toxin-containing foods with nutritious alternatives if nutritious alternatives were heavily restricted.
In this study, as diet quality decreased from trials 1 to 2, animals with the lowest availability of nutritious alternatives switched from tannin- to oxalate-containing foods (Fig. 1). This may be caused in part by detoxification processes, which impose nutritional costs by depleting the body of protein and glucose (Illius and Jessop, 1995, 1996) and inhibiting nitrogen utilization (Robbins et al., 1987a,b, 1991). These costs can deter feeding by herbivores (Dziba et al., 2006; Marsh et al., 2005). While knowledge of the effects of most toxin-containing foods in the body and their elimination pathways is incomplete (Foley et al., 1999; Villalba et al., 2002b), there is evidence that many terpenes are metabolized in the liver (Foley et al. 1999), that tannins bind to proteins in the diet (Robbins et al., 1991), and that oxalates are detoxified primarily by rumen microbes (Cheeke and Schull, 1985). Thus, we speculate that lambs may have relied more on hepatic and dietary mechanisms of detoxification when their diets were of higher quality, consuming more terpenes and tannins. Additionally, lambs may have been less sensitive to protein-binding tannins when they ate the higher diet quality. When diet quality was reduced, lambs consumed more food with oxalates, evidently relying more on ruminal detoxification and adaptation to consume oxalates (Cheeke and Schull, 1985). Finally, a decrease in diet quality reduced total intake of the three toxin-containing foods regardless of the availability of alternatives. Presumably, the low-quality diet reduced the supply of nutrients needed for both ruminal and hepatic detoxification processes, which, in turn, reduced the amount of toxin-containing foods the animals could ingest.
Our findings suggest that different grazing regimes may influence how animals forage. Herbivore density influences forage availability, which can influence the way animals select foods (Provenza et al., 2003a,b; Villalba et al., 2004). Animals in this study with greater access to nutritious alternatives ate less of the toxin-containing foods, regardless of diet quality (Figs. 1 and 2). These densities increased selective foraging and prevented animals from discovering complementarities among toxin-containing plants. In contrast, higher herbivore densities may decrease selectivity and facilitate the use of less palatable species, which can lead to herbivores learning about complementary relationships among toxin-containing species (Provenza et al., 2003a). During preference tests in these trials, animals restricted to the lowest levels of nutritious alternatives ate the toxin-containing foods despite having ad libitum access to the two safe familiar foods (Fig. 2). Use of chemically defended species could alter successional momentum, preventing less palatable species from increasing in dominance (Villalba et al., 2004) and potentially influencing plant biodiversity (Provenza et al., 2003a).
How animals learn about a foraging environment can influence diet breadth. Herbivores that experience toxin-containing foods while on a high plane of nutrition show a higher preference for them than animals on a low plane of nutrition (Baraza et al., 2004). Consequently, an animal's physiological state, which is influenced by biochemical diversity, including nutrient availability, is a context further shaping foraging behavior. This biochemical diversity, which includes less palatable species, may allow herbivores to discover and utilize suboptimal but complementary food alternatives, offering multiple foraging pathways from which to meet their nutritional requirements while consuming less palatable species (Singer et al., 2002; Villalba et al., 2004). In this study, animals conditioned with low levels of nutritious alternatives and high diet quality ate significantly more of the three toxin-containing foods than animals conditioned with high levels of nutritious alternatives and lower diet quality (Fig. 1).
Finally, diet-mixing behavior did not adversely influence animal performance. Animals that experienced the lightest restrictions ate more safe foods, but did not gain more weight than animals forced to consume higher amounts of toxin-containing foods (trials 1 and 2). Thus, above a threshold of restriction, animals did not eat other alternatives when the amounts of food were high enough to survive. In contrast, below a threshold of restriction, animals consumed toxin-containing foods. Possibly, because complementarities were present, they developed new foraging strategies. However, when the quality of the toxin-containing food declined (trial 2), the amount of nutrients ingested may not have been enough to allow for detoxification and growth. Thus, intake and preference for the toxin-containing foods declined as did animal performance.
This research was supported by grants from the Utah Agricultural Experiment Station and the United States Department of Agriculture Cooperative State Research, Education and Extension Service (Agreement No. 2001-52103-11215). This paper is published with the approval of the Director, Utah Agricultural Experiment Station, and Utah State University, as journal paper number 7647.