REVIEW published: 13 September 2019 doi: 10.3389/fvets.2019.00303 A Case for Eustress in Grazing Animals Juan J. Villalba 1* and Xavier Manteca 2 1 Department of Wildland Resources, Utah State University, Logan, UT, United States, 2 School of Veterinary Science, Universidad Autónoma de Barcelona, Barcelona, Spain Herbivores grazing in extensive systems are exposed to a series of challenges, rooted in the inherent spatial and temporal variability of their environment that potentially constrain their health, nutrition, and welfare. Nevertheless, in this review, we argue that challenges induced by some biotic (e.g., vegetation) and abiotic (e.g., terrain) factors may also be viewed as “positive” sources of stress or eustress, since they present complex problems, that when solved successfully elicit a greater degree of behavioral plasticity and adaptability in grazing animals. Chemically and structurally diverse landscapes require animals to display complex behaviors and exhibit adaptive capabilities, like building a balanced and safe diet or finding shelter, which ultimately lead to positive emotional states. Thus, maintaining or enhancing the diversity occurring in natural systems represent a management approach that can be used to improve welfare and prepare the animal for an efficient adaptation to future, and potentially unknown, environmental challenges. Edited by: Luiz Carlos Pinheiro Machado F◦ , Keywords: eustress, grazing, herbivore, animal health, adaptive behavior Federal University of Santa Catarina, Brazil Reviewed by: INTRODUCTION Manja Zupan, Biotechnical Faculty, University of Animal welfare is an essential element of modern animal production. First and foremost, animal Ljubljana, Slovenia welfare is grounded on ethical concerns that derive from the fact that animals are sentient beings, Ruan Rolnei Daros, i.e., able to suffer and experience emotions, but improving animal welfare may have additional University of British Columbia, Canada benefits. As many welfare problems have a detrimental effect on production, improving the welfare *Correspondence: of farm animals very often has positive effects on performance (1, 2). In addition, improving animal Juan J. Villalba welfare is one of the strategies that potentially contributes to reduce the use of antimicrobials in Juan.villalba@usu.edu farm animals (3). An in-depth discussion of the concept of animal welfare is well-beyond the scope of this review Specialty section: paper, and several reviews are available on the topic [e.g., (4–6)]. However, it is important to This article was submitted to mention that animal welfare encompasses not only the physical health of the animals (i.e., the Animal Behavior and Welfare, absence of diseases and injuries) but also their behavior and emotions (6–8). a section of the journal Frontiers in Veterinary Science For many years, the Five Freedoms (9) have provided a useful framework to identify the welfare problems of farm animals. These freedoms, which represent ideal states rather than actual standards Received: 08 April 2019 for animal welfare are (a) freedom from thirst, hunger and malnutrition, (b) freedom form thermal Accepted: 27 August 2019 Published: 13 September 2019 and physical discomfort, (c) freedom from pain, injury and disease, (d) freedom to express most patterns of normal behavior, and (e) freedom from fear and distress. Citation: Villalba JJ and Manteca X (2019) A More recently, the Five Freedoms have been criticized since they can be misunderstood as Case for Eustress in Grazing Animals. aiming at eliminating all negative experiences (which is not realistic or even desirable, as we argue Front. Vet. Sci. 6:303. in this review), but also because they fail to capture our current understanding of the biological doi: 10.3389/fvets.2019.00303 processes underlying animal welfare (5). As an alternative to the Five Freedoms, the so-called Five Frontiers in Veterinary Science | www.frontiersin.org 1 September 2019 | Volume 6 | Article 303 Villalba and Manteca Eustress and Grazing Domains Model for assessing animal welfare was developed to with different environmental challenges such that if they are address these problems. The Model incorporates four physical to survive and reproduce, they should maintain a fitness level domains of “nutrition,” “environment,” “health,” and “behavior,” >0. Innate behavioral strategies and learning play a key role in and a fifth “mental” domain. Each physical domain has an impact the ability of animals to cope and adapt to stressful situations on the affective state of the animal (i.e., on the fifth domain), imposed by an ever-changing environment (21). and the net outcome in the mental domain resulting from the combination of the four physical domains represents the animals’ overall welfare state. STRESS AND EUSTRESS IN EXTENSIVE It is clear that the Five Domains Model applies to animals kept SYSTEMS in confinement under intensive livestock production systems, but the approach is equally relevant to herbivores grazing in The concepts of “animal welfare” and “stress” are closely linked, extensive systems, as all states identified in the model are partially because many welfare problems cause stress (22). The crucial for the maintenance of their welfare, even when animals term “stress” has been widely used in biology to describe a set of evolved and are presumably adapted to their “natural” grazing physiological and behavioral changes elicited by aversive stimuli. environments. In several instances, the natural environment Cannon (23) described stress as the sympatho-adrenomedullary negatively impacts animal welfare due to its inherent temporal (SAM) system’s attempt to regulate homeostasis when threatened and spatial variability, which may lead to unsuccessful coping by a variety of aversive stimuli or stressors. Later, Selye (24) responses to unpredictable and ever-changing challenges (10, conducted some of his classic studies on the response of the 11). With regards to the grazing process, climate variability hypothalamic-pituitary-adrenal (HPA) axis to noxious stimuli has significant negative effects on herbivores, particularly for and suggested that the organism reacted in a non-specific manner dryland regions with low and variable precipitation and high to a wide variety of aversive stimuli, mainly with an increase temperatures in the growing season (12). Under these conditions, in the HPA axis activity. Some forms of stress such as the forage abundance and quality may be limited during certain chronic activation of the HPA axis caused by long-term factors periods, negatively affecting the nutrition domain, which in are typically viewed as impinging deleterious effects on natural turn compromises animal welfare. Clear seasonal patterns have populations, inevitably resulting in maladaptation and pathology been observed for fecal cortisol levels (an indicator of chronic (25). Both the HPA axis and the SAM system are generally stress) in Pyrenean chamois (Rupicapra pyrenaica) grazing in considered to be the two main elements of the stress response rangelands of northeastern Spain (13). Concentration of fecal and levels of glucocorticoids in different animal tissues (e.g., cortisol tracked the levels of nutrient and other environmental blood, hair, saliva) and excretions (e.g., feces) have been widely stresses experienced by these animals throughout the year (13). used as measures of stress. The problem with this approach, The effects of season are compounded with the impacts of however, is that the HPA axis and the SAM system have a thermal stress on ruminants in the face of future heat and cold crucial function in energy mobilization and redistribution of waves of greater frequency, intensity and duration (14). As an nutrients to active tissues and both aversive (e.g., fighting) example, heat stress reduces feed intake in ruminants while and rewarding situations (e.g., play and mating) may elicit a increasing maintenance requirements, a trend that is aggravated similar physiological stress response (26). Therefore, if stress by the predicted decrease in the quality and productivity of is perceived as potentially negative, it may be misleading to feed resources available to herbivores grazing in rangelands (15). consider stress as a synonymous of the HPA axis activation. All these effects have the potential to promote reductions in On the other hand, there is now enough evidence showing that animal welfare and productivity given that long-term declines in it is not the physical nature of an aversive stimulus that has food availability lead to poor nutrition and stress (16). Another negative consequences on the animal but rather the degree to response related to the unpredictability observed in rangelands which the stimulus can be predicted and controlled (26). As a involves fear to predation and the indirect effects that predators result, it has been suggested that the term “stress” should be impinge on prey by negatively affecting foraging patterns (i.e., restricted to conditions where an environmental demand exceeds reduced grazing time, increased vigilance), and as a consequence the regulatory capacity of the organism, mainly when such animal nutrition and reproduction rates (17, 18). conditions include unpredictability and uncontrollability (26). The aforementioned inherent variability of rangelands and Thus, when animals have available the conditions or “tools” to the potential negative impacts on the nutrition and welfare of control or predict their environment, a challenge may represent a herbivores has been extensively reviewed elsewhere [e.g., (19) and stimulus that results in improvements to their welfare, provided papers in that book]. This review was developed with the aim of that the animal overcomes the challenge. Interestingly, research looking at variability in rangelands from a different angle, i.e., in zoo animals has shown that giving animals the opportunity to as a force that may potentially bring about greater adaptation choose between two different environments (which presumably and resiliency for animals grazing in the complex chemical and increases the animals’ perception of control) reduces several structural realm of rangelands. It is clear that welfare depends behavioral and physiological indicators of stress and poor welfare not only on whether the animal succeeds at coping with the (27, 28). challenges emerging from its environment, but also on whether The coping process to a stressful situation (i.e., an animal coping attempts lead to negative consequences for the animal being exposed to a certain uncomfortable environment) may (20). On this regard, animals have evolved mechanisms to cope lead to fitness costs (i.e., searching activities that increase energy Frontiers in Veterinary Science | www.frontiersin.org 2 September 2019 | Volume 6 | Article 303 Villalba and Manteca Eustress and Grazing expenditure). Nevertheless, the net result of this response needs When herbivores engage in the process of building a diet to be adaptive (i.e., finding a more comfortable environment) if from an array of different foods from a diverse plant community the animal is to survive and reproduce, and if improvements in they are faced with solving a problem. This is because they animal welfare are expected. Thus, under circumstances when need to balance the ingestion of required nutrients and potential the animal is able to fully cope to a challenge, this may have a medicines (35) from an array of nutritionally unbalanced positive impact on animal welfare. Under this context, the word and potentially toxic foods. The solution is achieved by the “eustress” was coined (24) to refer to the idea that there is a application of a suite of complex behaviors that require cognitive “correct or optimal stress level” that is adaptive (29). For instance, and non-cognitive mechanisms for their efficient execution in problems that emerge during the grazing process such as building time and space (35, 36). For instance, locomotion activities a nutritious and safe diet may be stressful (e.g., overcoming food position the individual in space, within the preferred patch neophobia, or preventing the ingestion toxic plants or excessive and feeding station (36), followed by handling and ingestive amounts of nutrients), like the example described above in zoo activities that consummate a preference for particular plants and animals exposed to a choice between different environments, parts. Such preference is triggered by learning mechanisms that but ultimately beneficial if the individual possesses the skills integrate the plant’s orosensorial characteristics with its post- and resources needed to meet such challenge. Problem-solving ingestive consequences (37, 38). The challenge of building a opportunities presented during enrichment programs for captive balanced diet from a diverse array of alternatives may “breed” animals potentially enhances welfare, as individuals may be innovation and exploratory behaviors in herbivores that when motivated to participate in problem-solving activities when there successful, foster positive emotional responses and allow for is an optimal level of challenge, which depends on the individual’s better adaptations to future unpredictable conditions of the cognitive and behavioral skills to solve the presented problem environment (30). Good welfare is not simply the absence of (30). Contrafreeloading, the choice to work for resources when negative experiences; positive affective states play a significant identical resources are simultaneously available in free form, also role in providing animals a better quality of life (39). Under this entails an enrichment of the captive animal’s environment as analysis, forage diversity could be interpreted as an “eustressor” it provides opportunities for general exploration and cognitive that gives individuals the challenge but also the opportunity to challenge that may result in a positive outcome (i.e., “earning execute behaviors efficiently across contexts and solve problems food”), even when such activities represent departures from with potential to improve their welfare. In support of this optimal foraging strategies (31). idea, lambs faced with the problem of building a diet from a Our thesis in this review is that the inherent variability diverse array of food items with or without PSC, showed greater in structure, taxonomy, and chemistry provided by rangelands acceptance of novel foods and flavors in familiar (40) and novel represent stimuli that enhance the adaptability and resiliency (41) environments, and showed lower levels of stress-induced of herbivores grazing in these dynamic environments. This is hyperthermia and ambulation scores in open field tests than a novel approach to managing animals in rangelands as it animals exposed early in life to a single ration (41). Although suggests that preserving and promoting rangeland diversity is the initial reaction to novel feeds in all treatments was similar crucial for “providing the training grounds” that will prepare (i.e., low food intake; neophobia), neophobia was attenuated at a animals to better respond and adapt to future challenges that quicker rate in animals that had the task of building a diet from compromise their welfare. We also submit that management single foods relative to those previously exposed to a single ration interventions can contribute to foster flexibility in animals (40). In another study, lambs challenged to build a diet from grazing in variable environments by providing the means and an array of foods with different energy to protein ratios showed facilitating the acquisition of skills that optimize the prediction lower blood cortisol levels and neutrophil to lymphocyte ratios and control of the coping response to the problems presented in than lambs fed a single ration (42). Additionally, lambs under the the context of a changing world. diet-building task also spent a lower proportion of time eating and showed greater intake rates and greater proportion of time lying and greater activity than lambs under a single diet (42). FORAGE DIVERSITY AND EUSTRESS Heifers grazing 2- or 3-way choices of different legumes showed greater body weight gains, forage intake (43) and hair cortisol It is known that a variety of plant species enhances the nutrition levels than heifers grazing monocultures of these species. Some of mammalian herbivores because no single plant provides non-overwhelming challenges that increase cortisol levels, with all the nutrients or proportions needed by the animal (32). the subsequent decline when the task is mastered or the stimulus In addition, plant secondary compounds (PSC) ingested as a removed, have been linked to the development of resilience and dilute mixture of plants are less toxic to herbivores because the fostering of adaptations that enhance emotional processing, they are less concentrated and potentially detoxified by different cognitive control, and curiosity in monkeys (44). pathways [i.e., the Toxin Dilution Hypothesis; (33)]. Anatomical, Being able to solve a foraging problem, in addition to the physiological and experiential differences among individuals lead reward provided by the nutrients harvested in the process to specific needs, and thus individual animals can best meet their (nutrition and behavior domains in the Five Domains Model), needs for nutrients and medicines when offered a multiplicity of represents an intrinsic reward and positive emotional state forages, instead of receiving a single food, even if that food is (mental domain in the Five Domains Model) inherent to being balanced to meet the “average” needs of the “average” animal (34). successful at solving the task performed (30). Thus, the process Frontiers in Veterinary Science | www.frontiersin.org 3 September 2019 | Volume 6 | Article 303 Villalba and Manteca Eustress and Grazing of building a balanced and safe diet from a diverse array of innovation, and exploration that allow individuals to better nutritionally unbalanced alternatives may be interpreted as an adapt to the unpredictable conditions of their environment (52). achievement [a sense of “victory;” (24)] that leads to a positive Environmental enrichment programs that allow farm animals emotional state that improves welfare. More research is clearly show a more flexible foraging behavior lead to reductions in needed to better understand the effects of forage diversity chronic stress due to confinement (53). Sheep have been found and diet building on positive emotions in grazing animals. to predict and form expectations about the amounts of food Nevertheless, since the display of behaviors concerning essential that they are receiving, and to control an aversive event in activities such as foraging are considered self-rewarding (39), it order to access food, showing problem-solving abilities that allow is plausible to speculate that successful diet building activities for adjustments to new situations stemming from challenges are also linked to positive emotional states. Food seeking experienced and solutions achieved in previous tasks (46). This (motivational states of wanting) and consummatory behaviors plasticity acquired by the appraisal of novel situations relative (liking or the hedonic pleasure felt during food consumption) to the individual’s abilities and past experiences suggests that have rewarding properties (45) and they are clearly involved in animals challenged by less predictable environments may be the process of diet selection in mammalian herbivores (35, 37). more likely to show a broader range of coping strategies in In addition, it has been shown that controlling an event per response to changing environmental conditions than animals se can be perceived as rewarding or at least as less stressful living in more stable and predictable conditions (54). Behavioral (46). In contrast, foragers may experience negative states (i.e., flexibility may be also influenced by early life conditions as frustration) when exposed to monotonous rations that may not individually housed calves had learning deficits relative to calves satisfy all their individual and specific nutritional and medicinal housed in a dynamic group with access to their mothers (55). requirements, as well as the need to experience a diverse array of flavors during the foraging process (47, 48). Under the context of single feeds or rations, foraging opportunities are limited since VARIABLE LANDSCAPES AND EUSTRESS the only responses possible are to eat or to stop eating. Single foods/plants may elicit frustration as the animal’s response does Access to pasture for animals kept in confinement provides not lead to a solution, i.e., there are no single plants/forages some health-related welfare benefits to cows, even when diets that provide all the nutrients and proportions required by the in confinement are nutritionally balanced and cover all of animal (32, 34) and generalist herbivores evolved consuming a the animals’ physiological needs (health domain in the Five diversity of flavors from diverse plant communities instead of Domains Model). For example, at least in some circumstances, single flavors in monotonous foods. In addition, the initial stress cows on pasture have a lower incidence of lameness (56) and (i.e., neophobia) promoted by exposing animals to diverse novel mastitis (57) than cows kept indoors. If given the choice, foods may be attenuated by the presence of a familiar model such cows will spend a significant proportion of time on pasture, as mother (35) or experienced companions (49), which allow for mainly at night (58). Moreover, by using operant responses to a prompt selection of a diversity of food items from the array assess motivation, it has been shown that cows value access of novel foods presented. Finally, forage diversity allows for the to pasture as highly as fresh feed (59). It might be suggested expression of foraging preferences that may not be able to be that access to pasture provides an opportunity to experience a expressed under monotonous diets resulting in some animals more diverse, stimulus-rich environment than indoor housing. expressing abnormal and stereotyped behaviors, considered an Although boredom in animals has received little empirical study, indicator of poor welfare (20). research done in several species suggests that monotonous environments caused an increased motivation for diverse stimuli, consistent with the hypothesis that animals kept in barren FORAGE DIVERSITY AND environments may experience boredom or something like it (60). GENERALIZATION TO OTHER CONTEXTS Cattle in pens with ad libitum access to a monotonous forage displayed contrafreeloading, spending energy (they pushed a As expected from an evolutionary point of view, the ability gate) to obtain a forage which was simultaneously available of animals to compensate for the variability imposed by their in a feeder and in abundance (61). This behavior could be environment will be a function of the individuals’ phenotypic interpreted as a form of environmental enrichment, given that plasticity (50). Such plasticity may also be interpreted as the housing environment was barren and the animals had limited behavioral flexibility, allowing for a rapid pathway for adjusting social contact (61). Alternatively, pushing a gate may have been to environmental changes that exceeds the rate of evolutionary perceived as rewarding if this behavior attenuated boredom, genetic change (51). Behavioral flexibility may be acquired created a sense of control over the environment or allowed the when animals become familiar with solving foraging problems, animals to experience “a sense of victory” by handling a doable generalizing their problem-solving abilities to other contexts, challenge (61). and situations imposed by a changing environment. There is Consistent with the research described for cows in evidence for this process to occur under natural and artificial confinement, and for zoo animals exposed to a choice between settings. For instance, models with hummingbirds suggest that different environments (27, 28), the welfare of ruminants grazing environmental heterogeneity (e.g., changes in temperature, water in extensive systems may benefit from the opportunity to and food availability) are linked to problem-solving abilities, choose across different locations in the landscape. Nevertheless, Frontiers in Veterinary Science | www.frontiersin.org 4 September 2019 | Volume 6 | Article 303 Villalba and Manteca Eustress and Grazing preference in dominant animals within a social group may location, but born and raised in a humid environment with overcome spatial preferences by subordinate animals, which may gentle topography and lush vegetation (68). During winter and lead to frustration. Food preferences and social interactions both early summer (drought conditions), naïve cows selected diets influence choice of foraging location by sheep (62), although with lower crude protein content than cows born and raised in when animals experienced toxicosis after eating certain foods, the desert (68). No welfare parameters were measured in this dietary preferences overrode social influences (62). study, but it is likely that “desert cows” experienced a sustained Access to locations that require complex tasks like moving cognitive enrichment by the association of successful coping with across rugged terrain or uphill may represent challenges that a demanding behavioral task (i.e., moving in rugged terrain, elicit a higher degree of behavioral diversity in grazing animals uphill and away from water in a dry environment) rewarded by (environmental domain in the Five Domains Model). Foraging food. Interestingly, cows born and raised in the desert, moved enrichments in confinement are in general designed to facilitate to lush pastures for 3 years and then returned to the desert, the physical expression of feeding behaviors such as food- displayed behavioral patterns similar to cows that spent their searching and food consumption, but not to facilitate complex whole life at the desert (68). tasks related to food acquisition (30), although recent research on cognitive enrichment shows positive effects on animal VARIABLE LANDSCAPES AND THE welfare (63). We propose that the equivalent of complex task- solving processes for animals grazing in extensive systems THERMAL ENVIRONMENT entails building a diet from a diverse and complex landscape Trees, shrubs, or long grass, as well as abiotic factors such as with different biotic (e.g., plants with diverse chemistries and topography also provide a diversity of structural arrangements in structures) and abiotic (e.g., slope, rough terrain, rocky outcrops) the landscape that contribute to reduce the incidence of thermal challenges. Foraging across different spatial scales, from regions stress in animals living under natural conditions. Thermal stress and landscapes to plant communities and patches could be is a direct welfare problem, as it causes discomfort and it can viewed a “natural cognitive enrichment program” that enhances significantly reduce access to pasture in grazing animals (58). animal welfare by providing a form of enrichment, creating Use of shade is likely to be the most feasible strategy for grazing a sense of control over the environment, or allowing for the ruminants. Depending on the quality of shade, provision of shade realization of a task that leads to a positive emotional state. In will reduce radiant heat load by 30–70% (69). Even in temperate contrast, lack of biotic and/or abiotic challenges, similar to those climates, provision of shade has positive effects on heat load and observed in barren environments lead to boredom, frustration, production in grazing ruminants (70). The thermal environment helplessness, and depression (5). Supplying grazing animals plays an important role in determining livestock distribution with the opportunity to interact with a more sophisticated (71), and thus factors in the landscape such as aspect, slope, environment by challenging their cognitive abilities with chances type of terrain, type of vegetation also provide “tools” that allow to gain environmental control or to anticipate rewards represents animals gain environmental control or anticipate rewards (i.e., an appealing approach to enhance their welfare, supported by approach to their thermoneutral zone). Such tools are absent in the positive results observed for animals living in captivity (64). flat terrains without shelter. On sunny summer days, cows have These conditions at the spatial scale may facilitate the acquisition been observed spending considerable time (8 h) under shade trees of positive emotional states, induced by a successful coping with near water (72). Contrastingly, during winter cattle exhibited heat a complex cognitive challenge rewarded by the formation of seeking strategies of grazing south slopes during the day and not a balanced diet. Consistent with this idea, complex behavioral resting under shade trees and laying down at night on warmer tasks rewarded by food improve the welfare of intensively housed ridges (72). On cold days cattle would move to lower, sheltered pigs by providing adequate cognitive challenges that generated areas that were warmer (72), and on windy days cattle rest successful coping and positive emotional states (63, 65). In in sinkholes sheltered from the wind, possibly creating a more addition, structural (climbing racks) and cognitive enrichment thermally neutral microclimate (71). Effective shelter during cold (drinking water as a reward for a correct choice) improved weather may also entail dry grass or shrubs when sheep graze different aspects of behavioral competence (e.g., visual four- in areas with such structural diversity in the vegetation, leading choice discrimination tasks and reactions to external challenges) to substantial improvements in lamb survival under cold stress in goats exposed to stressful situations relative to animals exposed (73). Thus, biotic and abiotic factors that lead to successful coping to barren environments with easy access to water (64). It such as efficient thermoregulation could be viewed as “natural” has been hypothesized cows remain longer at feeding sites in enrichment elements with potential to enhance animal welfare. rugged heterogeneous pastures, with more diverse vegetation and nutrient profiles, than in homogeneous pastures as variability in biotic and abiotic factors reduce satiety and increase residence RANGELAND DIVERSITY, MANAGEMENT, time at the more complex feeding sites (66). In contrast, AND PREPAREDNESS TO THE UNKNOWN monotonous landscapes of uniform topography promote satiety and reduce the time spent at individual feeding sites (67). Cows Social and psychological research has placed emphasis in recent born and raised under the environmental challenges of the years on positive outcomes to stress-related experiences that Chihuahuan Desert were farther from water and spent less time breed resilience in organisms (74), instead of negative emotions at water than naïve cows of the same breed grazing at the same and chronic stress that promote illness. A similar approach could Frontiers in Veterinary Science | www.frontiersin.org 5 September 2019 | Volume 6 | Article 303 Villalba and Manteca Eustress and Grazing be followed in natural systems by maintaining or enhancing their vegetation such that animals are able to build “optimal diets” chemical and structural diversity, which in addition to services that provide an appropriate mix of nutrients and medicinal PSC. like improvements in the efficiency of resource capture, nutrient Environments of low nutritional quality reduce the fitness and cycling and stability (75, 76), may promote improvements in welfare of grazers and browsers (13), but the same is true when animal welfare. Providing new chemicals to the landscape like plants are high in nutrients (38). Non-complementary plant medicinal PSC (e.g., with the introduction of herbs, shrubs or species that provide excesses of nutrients (e.g., crude protein) trees) will benefit the nutrition and health of grazing animals lead to stress and food aversions because excessive or frequent (77, 78), thus addressing the nutrition and health dimensions ingestion of such foods produce high levels of byproducts of of the Five Domain Model. The benefits of plant diversity on fermentation that are toxic [e.g., ammonia or acid loads; (38, 83)]. animal welfare may also need to be pondered in relation to the Animals faced with the problem of building a diet from nature of the assemblage of plant species presented to herbivores. an array of diverse and complementary alternatives may be For instance, when subjects are offered a choice of foods more adapted to maintain their fitness and welfare in response under experimental settings to understand their specific nutrient to future challenges triggered by shifts in vegetation like requirements through their diet-building abilities [e.g., the the predicted reductions in crude protein content in grasses geometric framework of diet selection; (79)], the foods presented in response to increased ambient temperatures (15). It has are unbalanced but designed in such a way that allows for the been proposed that as climatic warming reduces grass protein construction of a mixed balanced diet that meets the specific concentrations, woody species increase in abundance and nutrient requirements of the individual. Extrapolating from this grassland habitats decline for growing populations of herbivores, controlled setting to natural systems, the foods presented in wild, and domestic species may need to compensate by relying the plant community should be such that different individuals less on grass and more on browse, which contains greater under different physiological states should be able to build a concentration of PSC (15, 84). In addition, the pattern of balanced diet. If mixing diverse foods does not lead to meeting protein reduction in grasses may also increase the reliance specific nutrient and medicinal needs, animals may experience on protein-richer eudicots, with greater potential for toxicity negative emotions such as frustration in response to suboptimal due to the greater concentration of PSC in these flowering diets, in addition to the direct negative impacts of unbalanced plants (85). Plant secondary toxicity may also be exacerbated diets on fitness. Thus, it is important to consider the herbivores’ with the predicted increases in ambient temperature because foraging preferences when managing grazing environments toxins interfere with thermoregulation (86, 87). Detoxification for improvements in animal welfare and productivity. As an pathways are thermogenic and toxins uncouple mitochondrial example, it has been shown that beef heifers grazing in natural oxidative phosphorylation, which also generates heat (88). The grasslands use low-quality tussocks in order to harvest strategic imbalanced nature of herbivore diets and the presence of amounts of dry matter during the day, given that the high toxins, which affect the thermal balance, may increase the productivity of these plants offer large intake rates (80). Intake likelihood of heat stress at high ambient temperatures (88). of tussocks is then complemented with the consumption of These emerging problems may require building diets of lower high-quality herbs and grasses (of lower productivity) present in PSC content in landscapes where the concentration of protein inter-tussock areas (80). Originally, farmers tended to eliminate is declining. Finding appropriate locations in the landscape low-quality tussocks, regardless of their abundance in the plant to dissipate heat under warmer conditions and the challenge community, as they were considered problematic for animal of temperature-dependent toxicity will be more relevant for production. After exploring the animals’ feeding preferences, future generations of herbivores. Adaptability in these predicted tussocks are now considered beneficial when present in the scenarios is expected to be greater for animals previously plant community below a certain frequency threshold such that exposed to solving the problem of building balanced diets animals build a diverse diet, where tussocks optimize the amount from complex arrays of unbalanced alternatives and complex of biomass harvested daily and herbs and grasses in the inter- landscapes with a diversity of biotic and abiotic factors that tussock areas provide the nutrients needed to optimize the foster cognitive enrichment. Trans-generational diet-building digestibility of tussocks in the rumen (81). Managers also offer abilities of offspring as observed in cattle (89) and sheep (90) proportions of grass and clover in the landscape that match the may also contribute to more efficient adaptations to future grazers’ preference for these forages in order to foster an optimal environmental challenges. use of food resources by herbivores (82); such arrangement may also contribute to animal welfare improvements as it offers the CONCLUSIONS conditions needed to successfully complete the task of building a balanced diet. Thus, fostering the “right” diversity, i.e., arrays of We submit that chemical and structural diversity breed animal complementary plants that when mixed lead to the realization of resiliency and adaptability to current and future challenges a balanced diet is essential. imposed by the inherent dynamic conditions of rangelands. Appropriate challenge is a key concept in environmental Positive outcomes to stress-related experiences may enhance enrichment, referring to the problem that is potentially solvable behavioral competence and lead to positive emotions that through the application of an animal’s cognitive and behavioral benefit animal welfare. Using this concept, managers should skills (30). Under this scenario, managers may be able to “enrich” promote resilience and plasticity in animals by enhancing a certain landscape by providing the supplements or plant chemical and structural diversity in rangelands (i.e., through species that complement the chemical composition of the existing targeted grazing treatments, revegetation efforts that increase Frontiers in Veterinary Science | www.frontiersin.org 6 September 2019 | Volume 6 | Article 303 Villalba and Manteca Eustress and Grazing plant species diversity, or by strategic distribution of water FUNDING points that enhance animal distribution in the landscape), thus creating “natural cognitive enrichment programs” that Utah State University provides funds for Open Access. This effort enhance animal welfare and better prepare animals for was supported by grants from the Utah Agricultural Experiment future challenges inherent of living in these dynamic and Station (Project UTAO 1321). variable landscapes. 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