Different strokes: Can managing behavioral types increase post-release success?

Applied Animal Behaviour Science 102 (2007) 364–379 www.elsevier.com/locate/applanim

Different strokes: Can managing behavioral types increase post-release success?§ Jason V. Watters a,*, Cheryl L. Meehan b a

Department of Environmental Science and Policy, University of California, One Shields Avenue Davis, CA 95616, United States b Center for Animal Welfare, University of California, One Shields Avenue Davis, CA 95616, United States Available online 30 June 2006

Abstract Re-introduction programs for endangered animals operate under the hope that protected habitats can sustain viable populations that rely little on humans. The goal of these programs is to supply animals with the resources and skills they need to succeed in the modern wild. However, predicting the set of skills necessary to respond to unpredictable selection events is difficult and efforts sometimes fail as animals respond inappropriately to environmental variation because they lack behavioral flexibility. Population resilience to environmental change may be enhanced if all members of a population do not exhibit the same response when selection pressures change. In many species individual animals express behavioral types that exhibit alternative responses to the same stimuli. Yet when animals are prepared for release to the wild, there is rarely consideration of consistent behavioral variation between individuals. Since experience influences both behavioral and physiological responses to varied stimuli and can shape the future behavioral type of captive animals, pre-release environmental enrichment may be successful in facilitating the expression of varied behavioral types in populations slated for release. This approach to environmental enrichment requires a departure from a ‘one size fits all’ strategy and may also involve exposure to increased challenge and competition. In addition, there is a need for empirical evidence to better understand the role of environmental enrichment and behavioral types on post-release success. The zoo environment provides an excellent arena for examining the development and expression of behavioral types and for taking a novel functional approach to environmental enrichment research that may prove to be very important to re-introduction efforts. # 2006 Elsevier B.V. All rights reserved. Keywords: Behavioral types; Competition; Environmental enrichment; Re-introduction; Phenotype management

§ This paper is a part of the special issue entitled ‘‘Conservation, Enrichment and Animal Behaviour’’, Guest Edited by Dr. Ronald R. Swaisgood. * Corresponding author. Tel.: +1 530 754 9307; fax: +1 530 752 3350. E-mail address: [email protected] (J.V. Watters).

0168-1591/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2006.05.036

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1. Introduction Captive rearing programs that aim to re-introduce animals to the wild frequently meet with failure (Beck et al., 1994; Lyles and May, 1987; Snyder et al., 1996). One common reason for failures of these programs is that animals are not behaviorally equipped to deal with environmental stressors (Beck, 1995). For example, released animals might respond ineffectively to natural predators (Griffin et al., 2000) or forage inefficiently in the release habitat (Frantzen et al., 2001). Thus, managers try to prepare animals to act appropriately in their new habitats. This preparation is an attempt to mimic specific selection pressures that are relevant to the population of concern. For instance, prior to release animals may be trained in anti-predator responses and feeding skills (Ellis et al., 1977; Biggins et al., 1993). The goal of this training is to promote the development of individuals that express behaviors that fall within a ‘‘target-trait range’’ of responses to environmental stressors (McPhee and Silverman, 2004). The target-trait range is the range of values of a single trait (behavioral, morphological, etc.) that confers a high probability of survival in the natural environment (McPhee and Silverman, 2004). While the target-trait range concept is a useful construct for managers because it suggests a clear goal by which the readiness of animals for release can be assessed, expanding the concept to a multi-trait range may be useful. This is because, in the natural setting there are many contexts (i.e. foraging, avoiding predators, mating, etc.) in which fitness is determined. Ideally, managers seek to release animals that fall within the target-trait range in all contexts (see Alberts, this issue). However, limited behavioral plasticity prevents animals from altering their behavior in certain circumstances. Thus, animals may excel at some tasks, but be unable to perform others effectively. In this light, a multi-trait range perspective may account for the fact that animals express some behaviors that fall outside of the target-trait range for a specific context and some behaviors that fall inside the range for another context. It is possible that those animals that perform poorly in one context, such as foraging, may excel in others, such as avoiding predators and that these differences in performance are related to the generalized behavioral style of each animal. In fact, recent studies with a variety of species have documented the expression of ‘‘behavioral types’’ in animals (reviewed in Sih et al., 2004), which are likened to personalities or temperaments. Behavioral types are indicated if an animal’s behavior is consistent over time in the same context (i.e. foraging, anti-predator response, etc.) or correlates across contexts (e.g. Gosling, 1998; Reale et al., 2000; Sih et al., 2003; Sih and Watters, 2005). For example, some individuals may be ‘‘shy’’ while others are ‘‘bold’’ (Coleman and Wilson, 1998; Wilson et al., 1994). Bold individuals may be more likely to sample novel foods (Kelley et al., 2005) or they may maintain a high activity schedule, even in the presence of predators. On the other hand, shy individuals might maintain low activity levels and feed less but simultaneously have a lower overall predation risk. Additionally, shy individuals may be more likely to notice and react appropriately to environmental change (Verbeek et al., 1996). Apparently these individuals rely more on external cues to determine their responses to the environment while bold individuals act in a manner more intrinsically driven and routine-like (Marchetti and Drent, 2000). Because individuals that express behavioral types are likely to act in consistent ways across contexts, they are sometimes likely to behave in a manner that is not appropriate for a specific context. If the bold individual is unable to completely reduce its activity level in the presence of predators, it may be more likely to suffer predation than individuals that are less active across contexts. This inappropriate behavior is a result of limited behavioral plasticity that leads to the consistent expression of behaviors across contexts and the subsequent determination of a behavioral type. It should be noted that behavioral plasticity may be limited

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within an individual for a number of reasons. One such reason is a lack of ecologically relevant stimuli during ontogeny. This circumstance may result in an individual that lacks a fully developed range of species-typical behaviors. Another, and potentially more important mechanism is that individuals develop in the presence of a fully appropriate set of stimuli but there are many sets of ecologically relevant stimuli that promote alternative developmental trajectories. Each trajectory may lead to the development of phenotypic variants that express a full complement of species-typical behaviors. Such conditions may arise when there is variation in the suitable habitat for a population, when social group composition varies across the population or when there are different resources available that require different skill sets to utilize. When these conditions exist, it may be difficult for individuals who have followed a specific developmental trajectory to express the behaviors that might develop along an alternative trajectory. In such cases, environmental variation at the population level is important in the expression of individual behavioral types. The literature on animal personality has demonstrated the occurrence of behavioral types in many species. For example, Gosling (1998) noted the occurrence of different personalities in captive hyenas. These personalities could not be attributed to dominance status, age or sex. A point of interest is that hyenas with different personalities responded differently to similar situations. This association between behavioral type and response to the environment is also illustrated in a recent study of three-spined stickleback (Gasterosteus aculeatus). This study found that bold fish foraged at higher rates and inspected predators more than shy fish, while shy fish were generally less active whether a predator was present or not (Bell and Stamps, 2004). Even when placed in a novel environment, bold stickleback maintained higher activity schedules than shy fish. Thus, it is plausible that different types (high versus low activity) experience different fitness consequences in different conditions (predators present versus predators not present). In addition to different behavioral responses to similar situations, animals expressing variant behavioral types are also likely to have varying physiological responses to environmental stressors. These different physiological responses mean that animals with different behavioral types are vulnerable to different types of pathogens (Koolhaas et al., 1999; Hessing et al., 1995; Kavelaars et al., 1999). For example, individuals that are more proactive or bold appear to be more susceptible to autoimmune disease than reactive, shy individuals (Hessing et al., 1995). Since individuals with different behavioral types have different behavioral and physiological responses to the same environmental scenarios, behavioral types must be considered in constructing populations that will be resilient to environmental change (Watters et al., 2003). This is due to the fact that when behavioral types are expressed, no one individual is likely to express a phenotype that fully encompasses a multi-trait target range of response in the new environment, and instead the target range is achieved by promoting population structure that encompasses a diversity of behavioral types. In this paper, we suggest that behavioral types are common and that groups composed of individuals that express different behavioral types are likely to be more stable than those where individuals express similar behavioral types. In creating release groups where individuals express different behavioral types, managers may hedge their bets against environmental uncertainty because the strength of natural selection acting on individuals with different behavioral types varies (Watters et al., 2003). To manage behavioral types, we must understand their causes, determine effective means of assaying individuals for their behavioral type, and develop protocols for directing the expression of behavioral types in animals. We suggest a means of using environmental enrichment in the captive setting to determine and promote the expression of individuals’ behavioral types. Since many of the

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ideas raised in this paper pertain to both social groups and populations (of either social or non-social species), we will simply use the term ‘‘group’’ when the point applies to either level. When our comments apply solely to either social groups or populations, we will state so. 2. Behavioral types and group stability When there are multiple behavioral types in a population, the population’s niche is partitioned between individuals (Bolnick et al., 2003). This niche partitioning means that individuals compete less with each other than they would if they were all making a living in exactly the same way. In addition, when the environment shifts such that some portion of this niche is unavailable, causing the individuals that utilize it to fail, those that utilize a portion of the niche that is still available are unaffected (Watters et al., 2003). Similarly, social groups composed of variant behavioral types are likely to be composed of individuals that perform different roles in the social group. Thus, the ability of social groups to persist, particularly in cases of environmental change, may be enhanced when they are composed of variant behavioral types. The notion that a group’s composition plays an important role in group persistence is not often investigated empirically. Nevertheless, a few studies suggest that the mix of behavioral types is important in determining a group’s stability. One study (Sih and Watters, 2005) demonstrates that at least some social groups composed of individuals expressing similar behavioral types do not fare well. These authors investigated the performance of social groups that were composed of males of similar behavioral type in the aquatic insect, the water strider (Aquarius remigis). Social groups that were made up of highly active and aggressive males were marked by a high degree of male–male aggression, which was associated with low mating rates because females responded to increased male aggression by leaving. Group composition is also important in animal production. Domestic pigs express active and reactive ‘‘coping styles’’ which can be likened to behavioral types. These types differ physiologically and behaviorally (Hessing et al., 1993) and individual pigs from groups composed of a mixture of types have higher weight gain and better carcass quality than single type groups (Hessing et al., 1994). It may also be the case that the behavior of individuals following an encounter with a predator varies with their behavioral type and the behavioral types of their social group members. A recent study on great tits demonstrates that the risk-taking behavior performed by individuals of different behavioral types depends on the behavior of their social partner (van Oers et al., 2005). In this study, the researchers classified birds as ‘‘fast explorers’’ and ‘‘slow explorers’’ and observed the time it took birds to return to feed following a simulated attack. The results were that slow exploring males paid attention to the behavior of companion males and returned to feed at a rate similar to the companion’s. Fast exploring males apparently paid no attention to the behavior of companion birds and returned at their own pace. The authors suggest that the fitness of different behavioral types is likely to be context dependent. Thus, under certain environmental conditions, it is possible that certain social group compositions will be associated with higher fitness than others. In another recent ecological study, Dingenmanse et al. (2004) found that the survival of great tits of different behavioral types within a population varied with annual changes in environmental conditions. In some years one type fared well while in other years another type had higher survival. While few, taken together, these studies suggest that the ability of groups to persist depends in part upon their composition in terms of behavioral types.

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3. Causes of behavioral types Given that behavioral types may be common and important in group function, the factors that cause behavioral types must be considered when managing captive animals as release candidates. Like most phenotypic characters, behavioral types are an expression of the interaction of an individual’s genes and its environment. Thus, it can be assumed that the largest diversity of behavioral types a population can express occurs when there is a large effective population size, and individuals from various genetic backgrounds develop in differing environmental conditions. While managers pursue maximum genetic diversity in captive populations through controlled breeding of animals of known pedigree (Ballou and Foose, 1996), the reality of the captive setting is most often that population sizes are small and thus realized genetic diversity is typically low. As a result, the few animals that are entered into captive rearing programs are a precious commodity because they represent the small potential to rebuild wild populations. If the goal is to build populations that are resilient to natural pressures because they are composed of individuals of various behavioral types, managers must consider environmental circumstances that lead to phenotypic diversity. Most genotypes have a ‘‘norm of reaction’’ in which variant phenotypes are expressed in different environmental conditions (Schlichting and Pigliucci, 1998). Just as reaction norms lead a genotype to express different morphological phenotypes under different conditions, various behavioral types can also be expressed (Stamps, 2003). Thus, variation of captive rearing environments and experiences is likely to promote the expression of variant behavioral types within the range possible for the genotypes in the captive population. As such, when manipulating environmental conditions to direct the development of behavioral types, caution should be exercised to ensure that rearing conditions remain ecologically-relevant. For most individuals, competition is a relevant component of developmental experience. As a result of this competition and the evolutionary need to survive and reproduce, individuals may adopt alternative developmental pathways that lead to variant behavioral and morphological phenotypes. For example, the quality of a parent’s territory may affect the expression of behavioral type in juveniles. This process occurs due to many factors, including the fact that territory quality can impact the social interactions that juveniles experience while growing, if for example, the distribution of food resources is unequal (i.e. clumped versus equally spread) across the territory or territories. When clumped, resources become easier to monopolize and this leads to variation in the physical condition of population members because some individuals acquire a disproportionate share. Those individuals that do not acquire the lion’s share of the resource must develop alternative means to maintain growth and body function or their expected fitness will ultimately go to zero. Often, such variation in growth rates results in variation in morphology that can constrain individuals to specific behavioral repertoires (Emlen, 1997). In a similar struggle for a different type of resource, mates, many alternative male phenotypes have evolved (Gross, 1996; Shuster and Wade, 2003). In these species, males express different behavioral and/or morphological phenotypes that lead to reproductive success for both types. For example, in many salmon species there are large, colorful males that actively fight for access to females and small, cryptic males that avoid conflict with large males but skirt by them stealthily to gain access to females. These alternative male types develop as a response to different social and environmental conditions in early development and cannot be reversed at maturity (Gross, 1996). Large and cryptic male salmon interact with their habitat and conspecifics in different ways, yet achieve equal fitness as a result of expressing different behavioral types (Gross, 1985; Watters, 2005). However, equivalent fitness of variant behavioral types is not necessarily the rule. In some species, such as the horned beetle, competition may cause certain individuals to adopt

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behavioral tactics that appear to ‘‘make the best of a bad job’’, resulting in reduced fitness relative to individuals that are superior competitors (Eberhard, 1982). Thus, basic competition for resources is a likely natural cause of variation in expression of behavioral types, and for the expansion of the population’s niche through the promotion of alternative behavioral strategies. In zoos and captive rearing settings, competition and other forms of selection are often relaxed. In fact, much zoo husbandry strives to eliminate selection from affecting captive animals. However, in natural settings, these selective pressures direct the development of behavioral repertoires in individuals. Thus, the elimination of selective pressures tends to increase the variance of behavioral responses seen in captive animals (McPhee, 2004) because developmental trajectories are not focused into specific paths that lead to the expression of adaptive behavior. The result is that many animals show behavioral responses that fall outside of the range of behaviors that confers fitness and would quickly fail in a wild setting (McPhee and Silverman, 2004). On the other hand, attempting to emulate only a specific set of conditions that are assumed to direct developmental trajectories (i.e. experience with specific predators or foraging tasks) is likely to produce individuals that are confined to a small set of responses. While these responses may fall within a specific target-trait range, husbandry that does not diversify developmental trajectories is likely to confine the range of behavioral responses expressed by release populations to only a small portion of the multi-trait range that confers population resilience in a wild setting. Thus, to prepare animals for release, consideration must be given to delivering a varied, relevant set of developmental circumstances that drive the expression of variant behavioral types (Watters et al., 2003). 4. Assessing behavioral type in zoo settings The captive environment provides excellent opportunity to observe animals and determine how behavioral types are expressed. Researchers in the zoo setting have recognized the importance of consistent behavioral characteristics of individual animals to the success of population management and ex situ species conservation (e.g. Carlstead et al., 1999). The ‘‘Methods of Behavioral Assessment’’ Project (MBA) was developed to improve the ability to maintain viable populations of endangered species by understanding individual behavioral differences and how they relate to the way animals cope with housing, husbandry and other environmental factors in captivity that may impact well-being and reproductive success (Carlstead et al., 1999). In a project involving black rhinoceros, an animal keeper questionnaire was used to describe behavioral profiles. The result was that ‘‘behavioral styles’’ of the individual rhinos became apparent. These styles were described with respect to six behavioral traits: Olfactory Behaviors, Chasing/Stereotypy/Mouthing, Fear, Friendly to Keeper, Dominant (to conspecifics) and Patrolling (Carlstead et al., 1999). Several of these traits were found to be related to captive breeding success. For example, the greater the breeding success of a male, the lower his score on Olfactory Behaviors and Dominant, while in females, lower scores on Chasing/Stereotypy/ Mouthing were associated with greater breeding success. In addition, breeding success was higher when the female was dominant to the male suggesting that sub-dominant individuals can obtain relatively high mating success when appropriate mates are available (Carlstead et al., 1999). These results indicate that assessment of behavioral types can be very useful in understanding the factors that promote the well-being and success of captive populations. Such data can be gathered via questionnaires, as in this example, or by more traditional observational techniques.

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These data would provide the basis for experiments which assess the success (in both controlled and wild contexts) of populations comprised of individuals with either similar or varied behavioral types. Such experiments would investigate the relative success of individuals with different behavioral styles in social and ecological contexts as well as various captive and postrelease environments. Their goal would be to predict the stability of groups with varied behavioral types in the face of environmental challenge. 5. Environmental enrichment in the context of behavioral types Environmental enrichment is generally thought of as a broad set of interventions that serve to improve both the physical and psychological well-being of captive animals. Unfortunately, the term ‘‘environmental enrichment’’ is used inconsistently across contexts and is often applied without clearly defined predictions or testable hypotheses (Newberry, 1995). A functional approach to defining enrichment has been suggested as a means of identifying specific objectives and methods for enrichment projects and grounding research in a sound theoretical framework (Newberry, 1995; Meehan & Mench, 2007). This approach places environmental enrichment within the context of biological principles thereby increasing both the integrity and the effectiveness of the work. For example, environmental enrichment work that serves the function of reducing or eliminating the performance of abnormal or self-injurious behaviors has been greatly enhanced by the guiding principles of motivational analysis (e.g. Hughes and Duncan, 1988). Theoretical work in this area has allowed researchers to effectively address the performance of abnormal behaviors in captive animals by designing enrichments that meet behavioral needs (e.g. Meehan et al., 2003a,b; Swaisgood et al., 2001; Huber-Eicher and Wechsler, 1998). Similarly, an understanding of the principles of learning has potential to enhance enrichment efforts for captive animals (Tarou and Bashaw, this issue; Bassett and Buchanan-Smith, this issue). The fields of learning and ontogeny have also improved pre-release environmental enrichment through the application of strategies that allow animals to develop the behavioral skills necessary for survival (e.g. Miller et al., 1998). However, the variability in success across re-introduction efforts (reviewed by Stamps and Swaisgood, this issue) has demonstrated the fact that there are a multitude of factors that can contribute to survival outcomes. These elements are both genetic and experiential in nature and can influence chances for post-release success as much as can a conscious program of pre-release training (Castro et al., 1998). Since an individual’s behavioral type is known to influence how it responds to different environmental scenarios (Sih et al., 2004; van Oers et al., 2005), examining the development and expression of behavioral types in animals destined for re-introduction into the wild presents a novel functional approach to environmental enrichment research that may prove to be very important to re-introduction efforts. As stated earlier, this importance arises because behavioral types are the expression of limited behavioral plasticity and most individuals are unable to express the population’s full range of phenotypes. When this is the case, populations composed of varied behavioral types are likely to be more resilient to varied selection pressures than those composed of a limited set of behavioral types. 6. Environmental enrichment as a means of assessing behavioral types It is possible that existing environmental enrichment programs can be used to assess the behavioral types of captive animals since a significant component of many enrichment programs is the introduction of novel stimuli into the captive environment. While the goal of many

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enrichment strategies which employ novel objects is to facilitate desirable behavior patterns such as those associated with exploration and play (Wood-Gush and Vestergaard, 1991; Wood-Gush and Vestergarrd, 1993), exposure to novelty can also elicit behaviors associated with fear including avoidance and retreat (Meehan and Mench, 2002). Responses to novel objects vary across individuals and may be attributable to factors such as maternal care (Fairbanks and McGuire, 1988), social context (Meehan et al., 2003a,b; Jones and Merry, 1988; Coe et al., 1982; Taylor, 1981) or previous experience (Meehan and Mench, 2002; Wood-Gush et al., 1990; Fox and Millam, 2004). However, given that reactivity to environmental elements is a central component used to distinguish behavioral types (e.g. Coleman and Wilson, 1998; Wilson et al., 1994; Boissy, 1995; Gosling, 2001), it would be predicted that individuals with different behavioral types would have divergent responses to novelty. As such, responses to novel objects in a captive setting are likely to be useful in evaluating an individual’s behavioral type. To assess behavioral type, many of the methods used to evaluate animals’ responses to novel objects in enrichment work could be applied. For example, latencies to inspect or interact with devices, duration of interaction with devices and the quality of interactions (vigorous, tentative, etc.) could be utilized. Even where animals’ responses to novel objects are assessed in the absence of an ecologically relevant context, it is possible to glean some notion of basic behavioral types. Such contexts occur, for example, when novel objects are placed into empty arenas or into the home cage of an individual test animal. However, because the expression of behavioral type will carry over across contexts, a complete evaluation should include observations in many circumstances. One circumstance that may provide excellent insight to behavioral types occurs when placing individuals in situations where they must respond to conflicting demands. For example, evaluating animal’s response to novelty when at risk for (simulated) predation, or when in competition with other individuals for access to a valued resource would require animals to prioritize behaviors or adopt varied strategies. In addition, if animals are presented with a wide variety of novel objects with different sensory qualities, similarities and distinctions between individual responses to varied stimuli could be recorded. Taken together, these methods would facilitate the development of multivariate behavioral profiles and allow for analyses which would demonstrate consistencies in behavior across contexts, thus revealing behavioral types 7. Environmental enrichment as a means of directing the development of behavioral types Producing populations of release candidates that are comprised of individuals with varied behavioral types is a novel context in which to apply the practices of environmental enrichment. The basic premise of our approach is that individuals of the same population that experience different environmental challenges during development tend to develop along different trajectories. The result is that there are variant behavioral types in the population. In addition (but equally important in our perspective), it is possible that individuals of dissimilar genetic composition that experience similar environmental conditions develop variant behavioral types. While individuals with different genetic backgrounds may express different phenotypes under similar environmental conditions, it is also possible that for some conditions there is a ‘‘best’’ behavioral response. Under these conditions, similar phenotypes are expected (Waddington, 1942). This is not to say that each individual will develop exactly the same phenotype under similar conditions, but that when there is no variation in the developmental environment experienced by individuals, the range of phenotypic expression is likely to be limited. Therefore, to ensure that a full range of behavioral types is expressed in captive populations, managers

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should seek to provide an array of relevant and varied developmental circumstances under which different individuals will be reared. Thus, when planning to produce populations with varied behavioral types, managers must create the unique environmental circumstances that will drive the developmental pathways of sub-groups or individuals through the application of a suite of environmental enrichment strategies. These strategies may very well incorporate existing methods of environmental enrichment such as foraging tasks, habitat manipulation and social groupings. However, the manner in which these techniques are chosen, applied and assessed may vary from traditional methods so as to be appropriate to the theoretical framework of behavioral types. Generally, the enrichment techniques applied to zoo populations focus on the interaction of the individual and its environment with broad goals for behavioral outcomes. Examples of these behavioral outcomes include: reducing abnormal behaviors (Grindrod and Cleaver, 2001; Markowitz et al., 1995; Carlstead et al., 1991); increasing space utilization (Williams et al., 1996); or meeting behavioral needs (Swaisgood et al., 2001). Traditional methods of implementing and assessing environmental enrichment strategies rely on the comparison of individuals exposed to control or standard environments with those exposed to environments that have been modified to address the specific behavioral goals. Alternatively, animals can serve as their own controls whereby their behavior in a standard environment is compared to their behavior in the modified environment. Mean levels of the behaviors of interest are then compared across environmental treatments to determine the impact of the intervention. This methodology has proven to be very useful in the development, refinement and assessment of environmental enrichment techniques as it can highlight the environmental features which have the greatest impact on specific behavioral outcomes. However, this approach is not sensitive to the differential effects of environmental interventions on individual animals, or the variation in behavior that may exist between individuals who have experienced identical environmental intervention (Swaisgood and Shepherdson, 2005). Essentially, by looking at treatment level effects of environmental enrichment we ignore the range of variation that may occur within groups of animals. This variation in behavioral expression within groups of individuals experiencing identical (or what appear to be identical) environmental conditions is central to the concept of behavioral types. Thus, in considering behavioral types, we must look at the variation of responses of animals both within and across treatments designed to elicit differential development. Such considerations must pay attention to the possibility that the ‘same environment’ may affect different individuals in different ways. Such differential effects will lead to the development of dissimilar phenotypes. These effects can occur for a number of reasons including differences in the way various genotypes respond to similar environmental cues and differences in the experiences of individuals that are reared in the same environment. The provision of various enrichment challenges to different individuals is central to the concept of fostering the development of varied behavioral types. For example, many enrichment protocols are designed to provide foraging tasks for captive animals. Such tasks may engage the animal in a type of problem solving and often animals quickly become proficient at completing foraging tasks to obtain food items. By providing an array of foraging tasks to members of captive populations and observing the response of individual animals, managers can assess the range of behavioral responses within the group. For example, it may be the case that certain individuals are more likely to try novel foods while others become proficient at utilizing a known food source and avoid novelty. Alternatively, some individuals may vigorously interact with foraging devices and learn to access food items through repeated trial and error, while others play a more observant role. In addition, certain individuals might display greater proficiency at foraging tasks that

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present a cognitive challenge, while others excel at tasks that require physical skills. From these data, managers might determine how best to train individual animals slated for release such that their relative innate abilities are used advantageously. In so doing, managers can direct the skill set of the captive population such that some individuals are adept at certain tasks while others excel in solving different types of problems. Thus, through the use of varied foraging enrichments, managers can both assay for the expression of behavioral types and diversify the types of foraging styles that release groups express. In addition to finding food, release animals must also avoid predation. Captive animals slated for release are often exposed to potential predators as a means of preparing them to survive outside of captivity (Griffin et al., 2000). In this case, observers should determine the manner in which each individual avoids specific predators and whether individuals respond differently to the same predator (Stapley and Keogh, 2004). While it may be the goal of managers to produce animals that respond effectively against a wide array of predators, the reality might be that individuals with different behavioral types respond more effectively against certain predators than against others. If individual animals within a group slated for release show consistent, yet differential responses to varied types of predators, then the development of these innate skills can be fostered through pre-release training tailored to each behavioral type. Skills such as vigilance, warning, evasion and fighting might be developed to different levels of proficiency in individuals who show a propensity to utilize each strategy by exposure to relevant predatory stimuli. This type of training may facilitate the creation of social groups where individuals with different behavioral types are represented. In this case, even if no individual responds perfectly to all types of predators, social groups composed of individuals that vary in their response to specific predators should fare better than social groups composed of a single behavioral type. Variation in developmental trajectories may also be managed by creating variation in the ‘‘habitats’’ in which captive animals are reared. Such variation can come about in terms of easily manipulated housing components such as the density of particular substrates (arboreal perches, bare ground, etc.). While there may be species preferences for certain types of substrate, individuals experienced with alternative substrates may more readily move into habitats that vary with respect to their physical composition. For captive reared fishes, differences in developmental trajectories can be promoted by creating habitats that vary with respect to water flow dynamics. In this case, some individuals may hold territories that are less energetically costly to maintain because they have low water velocity relative to others. Here, it is easy to produce variation in growth rates, even among individuals of the same cohort (Watters, 2003). For some species such as coho salmon, this variation in juvenile growth rate is a key factor in the expression of alternative behavioral types (Watters, 2003). Differences in the experience of individuals reared in the same environment can come about as a result of interactions among social group members or population members that only occasionally meet. Even in the simplest social group composed of only two members, each individual is likely to play a different role. For example, one individual may be dominant and the other subordinate. Thus, because of these different roles for social group members, each member experiences a somewhat different environment. As a result, the social milieu can be a determinant in behavioral development. For example, vervet monkeys reared by mothers with different styles (protectiveness versus rejection) showed long lasting differences in their behavioral type. Monkeys reared by protective mothers were less responsive to novel environments than monkeys reared by mothers who were less protective (Fairbanks and McGuire, 1988). While mothering style can promote the expression of behavioral types, larger social groups, which contain nonrelatives, should also be a component of the expression of behavioral types. Captive animals are

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often maintained in variable social groups. In addition, manipulation of social group composition is relatively straightforward provided there is room available for more than one group. Paying attention to the behavioral types expressed in these groups may offer some insight to the role of social groups of varying composition in the expression of behavioral types. In addition, observing the relative well-being of different individuals within social groups of varied composition will be useful in determining the stability of these groups. 8. Integrating varied experience into pre-release environmental enrichment through competition Competition itself is a driving force in producing phenotypes that in turn minimize competition and lead to group stability. The reason for this is that competition forces the development of alternative solutions to the problem of acquiring resources. In this way, competition results in the development of varied skills and behaviors that are necessary for survival. Thus, the development of effective alternative behavioral strategies is an outcome of competition (Shuster and Wade, 2003). Environmental enrichment techniques can be used to bring about competition for resources among group members, thereby facilitating the expression of alternative behavioral types. Since many of the advancements in the field of environmental enrichment have focused on providing varied feeding and foraging opportunities, addressing competition through food availability is a likely candidate for the application of this principle. For example, providing a clumped food resource to a group of animals might lead to the situation where one or a few animals initially acquire a disproportionate share of the resource. Other animals may attempt to wrest the resource from animals holding it through agonistic encounters, or they may develop alternative means of acquiring the resource such as sneaking, stealing or banding together with other ‘‘losers’’. In general, competition for food resources increases with intensity when food is more clumped, and thus more easily defended (Chamove et al., 1982; Boccia et al., 1984). Thus, environmental enrichment devices which require animals to visit specific sites and perform foraging tasks to retrieve food items provide an excellent opportunity for researchers to observe individuals within the group as they adopt strategies to access the resource. While we are unaware of any research to date of this nature that has been implemented for the purpose of addressing the development or expression of behavioral types, there is precedence for utilizing foraging enrichment strategies to assess intra-group food competition. For example, Rappaport (1998), working with a group of golden lion tamarins in a large naturalistic enclosure at the National Zoological Park used a puzzle feeder to encourage food competition among group members. Despite the fact that the puzzle feeder was a highly defensible resource, all individuals obtained an equivalent number of items over the course of the experiment. However, the strategies by which individuals obtained their rations differed. Some tamarins obtained most of their food rewards directly from the device while others received their food rewards primarily through food transfer from other group members. In addition, the mode of food transfer had several forms including passive sharing, active sharing and stealing. Although individual level data were not reported in this study, the presence of alternative behavioral strategies in food acquisition presents the possibility that behavioral types emerged within the group as a result of the competition for food. Thus, this study demonstrates the feasibility of using foraging enrichment as a means of integrating varied experience into the pre-release environment through competition and as such, facilitating the development, expression and assessment of behavioral types.

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While facilitating competition may be desirable in groups of individuals being prepared for release, any intervention that could potentially increase the risk for injuries due to aggressive encounters must be approached with care. Since risk of injury is of particular concern when groups of release candidates are limited in size, competitive scenarios should be tested with species that have a similar social structure and ecological niche to the release candidates, before introducing them to groups of endangered animals. This testing will allow researchers to determine the factors that influence the intensity of aggressive interactions between individuals. For example, in the study cited above, rates of passive sharing were lower and aggression higher when the foraging task was more complex and time-consuming (Rappaport, 1998). However, neither this study, nor a study of food competition in groups of captive adult mangabeys (Stahl and Kaumanns, 2003) reported levels of agonistic interactions that were considered unacceptable. Thus, while protecting the health of release candidates should be of utmost concern, the introduction of competition into the captive environment through environmental enrichment should not compromise this goal provided it is approached conscientiously. Nevertheless, it has been suggested that, compared to animals that will remain in captivity, compromising the perceived comfort of release candidates may be necessary to fully prepare them for life in the wild (Beck, 1995). 9. Discussion Behavioral types appear to be common in many species. They are marked by limited behavioral plasticity and individuals of different types may utilize different portions of the species niche. As a result, different types may play different yet important roles in group function. Animals that make apparent mistakes in some situations may be those that perform best in yet other settings. In this way, groups composed of variable behavioral types have the potential to persist when environmental challenges affect some of their members. Further research is necessary to determine the potential of, and best methods for, application of phenotype management that focuses on behavioral types in the context of captive rearing programs. Assessment of captive animals to determine the behavioral types present and the responses of these types under different environmental conditions is a logical first step. In addition, managers should investigate the processes that lead to the expression of variant behavioral types in the species with which they work, and apply environmental intervention as necessary to encourage the development and expression of varied behavioral types within populations of release candidates. We have proposed that the application of environmental enrichment techniques to achieve these goals presents a novel, and potentially important approach to conservation research. Additional work should follow animals of different types after release and determine their survival and reproductive success in relation to multiple ecological contexts. Such contexts include varied predation risks, interaction with conspecifics, food availability, distribution and type, habitat characteristics, environmental perturbation, etc. Tracking several groups of animals consisting of different frequencies of variant behavioral types to determine how they respond to environmental pressures is a means of assessing their long-term stability. Data collection of this sort requires long-term monitoring of animals coupled with records of current environmental, social and ecological conditions. While time consuming and resource intensive, this type of postrelease monitoring has been cited as one of the key elements necessary to the advancement of re-introduction practices (Stoinski and Beck, 2004; Seddon, 1999). Thus, analyzing these data sets with respect to the performance of individuals with different behavioral types and groups

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with varying composition presents a feasible and potentially very useful opportunity to gain insight into the factors which impact re-introduction efforts. Here we have presented a suggestion for how re-introduction success might be improved. Our approach involves the diversification of captive rearing environments such that variant behavioral types are expressed in animals raised in captivity. While our focus has been on the release of captive reared animals, we believe that the basic tenets of the approach we suggest can be carried over to evaluate animals slated for translocation. Following evaluation, these animals might be selected so as to create groups that represent a variety of inherent behavioral types. This approach is as yet untested, and thus its validity remains to be seen. As such, it is not intended to replace other captive rearing programs. Indeed, many currently instituted programs such as antipredator training (Griffin et al., 2000), and developing specific locomotor (Stoinski and Beck, 2004) or foraging skills (Biggins et al., 1999) should be viewed as vital components of the phenotype management approach we suggest. Complimentary to our approach, Stamps and Swaisgood (this issue) suggest that managers pay particular attention to the habitat characteristics of release sites and more-or-less promote the expression of behavioral types that will fare well in the planned release area. These authors suggest that animals be reared such that they express preferences for the type of habitat found in the release area. In so doing, release animals may be initially more likely to remain in release areas and avoid the mortality risk of leaving to find an alternative habitat. While phenotype management approaches to reestablishing wild populations are likely to be important, we caution that predicting the precise developmental conditions that lead to specific phenotypes is difficult. Such prediction is likely to come about only through experimentation and observation that considers both the environmental conditions experienced by individuals as well as their genotypic condition. Furthermore, we caution that environmental change is often unpredictable, and even when tailoring the phenotypes of individuals to perform well in specific habitats, releasees should not be limited to a very few behavioral types. We also urge managers of wild lands to remember that habitat variation is a key component in the expression of behavioral types (Watters et al., 2003). Thus, the maintenance of behavioral types in wild populations is dependent upon the maintenance of habitat complexity. Acknowledgements We thank Jeremy Davis and Shay Redfield for comments and discussion. We also thank Ron Swaisgood and two anonymous reviewers for insightful comments and suggestions. References Ballou, J.D., Foose, T.J., 1996. Demographic and genetic management of captive populations. In: Kleiman, D.G., Allen, M.E., Thompson, K.V., Lumpkin, S. (Eds.), Wild Mammals in Captivity: Principles and Techniques. University of Chicago Press, Chicago, pp. 263–283. Beck, B.B., Rapaport, L.G., Stanley Price, M.R., Wilson, A.C., 1994. Reintroduction of captive born animals. In: Olney, P.J.S., Mace, G.M., Feistner, A.T.C. (Eds.), Creative Conservation: Interactive Management of Wild and Captive Animals. Chapman and Hall, London, UK, pp. 265–286. Beck, B.B., 1995. Reintroduction, zoos, conservation and animal welfare. In: Norton, B.G., Hutchins, M., Maple, T.L. (Eds.), Ethics on the Ark: Zoos, Animal Welfare and Wildlife Conservation. Smithsonian Institution Press, Washington D.C., USA, pp. 155–163. Bell, A.M., Stamps, J.A., 2004. Development of behavioural differences between individuals and populations of stickleback, Gasterosteus aculeatus. Anim. Behav. 68, 1339–1348.

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