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Assessing the Effectiveness of Environmental Enrichment in Bottlenose Dolphins (Tursiops truncatus)

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Abstract

Environmental enrichment is often used to improve well-being and reduce stereotyped behaviors in animals under human care. However, the use of objects to enrich animal environments should not be considered to be effective until its success has been scientifically demonstrated. This study was conducted at Asterix Park in France in April 2009. The study investigated the use of 21 familiar objects with a group of six bottlenose dolphins (Tursiops truncatus). The dolphin trainers introduced four different objects into the dolphin pool every day on a rotating basis. Using a focal-object sampling method, we collected and analyzed data from twenty-one 15 min sessions. The results revealed a positive correlation between interest behaviors and interactive behaviors. Some dolphins had "favorite toys". However, only 50% of objects elicited manipulative behaviors. These findings demonstrate that dolphins do not treat all objects provided to them as "toys". Behavioral changes in the animals subsequent to the introduction of objects do not necessarily indicate an enrichment effect of the objects; rather, the motivation for the dolphins' behaviors toward the objects must be investigated. The animals' behavior must be considered in light of the social context and of the animals' individual behavioral profiles. The relevance of a constructivist approach to evaluating the effectiveness of enrichment programs is discussed.

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... Consistent with previous work assessing the effectiveness of environmental enrichment [31,32], principal component analysis (PCA) was conducted to identify potential underlying patterns among the ethogram measures. The submissive social context, although in the original ethogram, was not included in PCA because no submissive contexts were observed during coding. ...
... Lastly, Kruskal-Wallis tests were used to investigate individual differences in enrichment use [31,32]. Because Dwass-Steel-Critchlow-Fligner (DSCF) post hoc tests control for family-wise error [33], DSCF post hoc tests were used for significant Kruskal-Wallis tests without adjustment of alpha [34] to determine which individuals differed from each other in their use of specific objects, enrichment manipulation behaviors, and social contexts of enrichment use. ...
... Visual inspections of scatterplots of the remaining 760 occurrences of enrichment use revealed non-curvilinear relationships among all variables. Consistent with other investigations of enrichment use [31,32], PCA was conducted to identify potential underlying components among the 23 coded variables, including the duration of use of specific categories of enrichment devices (i.e., forage, toys, structural, nesting, technology, art, and other), the frequency of manipulation behaviors (i.e., carry, examine, oral, play-on, vocalize, active tactile, tool, wear, and other), the duration of manipulation behaviors (i.e., nest, rest, and out of view), and the duration of enrichment use in social contexts (i.e., solitary, affiliative, proximate, and aggressive). ...
Article
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Environmental enrichment provides mental stimulation and minimizes abnormal behaviors in captive animals. In captive chimpanzees, individual animals may vary in the ways in which they benefit from enrichment or use enrichment devices, so investigating nuances in enrichment use may improve the welfare of captive chimpanzees. In the current study, three ethograms measuring distinct features of enrichment use (i.e., enrichment object, manipulation behavior, and social context) were evaluated by coding videos of captive chimpanzees (Pan troglodytes) at Chimpanzee Sanctuary Northwest in Cle Elum, WA. A total of 732 min and 58 s of video footage was coded from a larger video archive (i.e., 2054 videos) of enrichment use that spanned a decade. A principal component analysis (PCA) revealed that different categories of enrichment objects were more often associated with specific manipulation behaviors and social contexts, suggesting that enrichment objects might fulfill different behavioral and social needs in captivity. Specifically, toy objects were associated with active tactile behaviors in affiliative contexts while oral behaviors were used with foraging objects in solitary contexts. Additionally, individual chimpanzees showed unique preferences for enrichment objects, indicating that caregivers of captive chimpanzees should consider individual needs instead of a “one size fits all” approach to enrichment provisions.
... For BDs, the presence of humans together with toys was associated with a lower rate of agonistic behaviors between animals, which is an interesting result to further investigate. It has already been shown that BDs are likely to interact with caretakers outside of training sessions and interact with toys more frequently when caretakers are involved [79,80]; combining these two kinds of enrichment might therefore increase their enriching properties. EAFPs engaged in socio-sexual interactions more often when toys were provided. ...
... When aiming to give more opportunities of control to captive animals, the needs of a given species and even of each individual must be considered when utilizing different types of enrichment, social groupings, or habitat configurations [91][92][93]. Differences of reaction to each type of enrichment among the three groups we studied might therefore reflect preferences for certain type of enrichment [79,80], and also the way they interact with each type of enrichment (alone, together, with or without distance between individuals). The differences we found between groups could be linked with species-specific traits, such as shyness for YFPs, and individual differences might play a role in the reaction to enrichment [79]. ...
... Differences of reaction to each type of enrichment among the three groups we studied might therefore reflect preferences for certain type of enrichment [79,80], and also the way they interact with each type of enrichment (alone, together, with or without distance between individuals). The differences we found between groups could be linked with species-specific traits, such as shyness for YFPs, and individual differences might play a role in the reaction to enrichment [79]. In addition, the animals' management and especially the training routine and the relationship with caretakers might have been a factor that influenced the preference for a certain type of enrichment and even explain the preference for interacting with caretakers rather than socializing with conspecifics. ...
Article
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Research on the welfare of captive odontocetes has increased in recent years, but has been mostly focused on bottlenose dolphins (Tursiops truncatus). Few studies investigated potential welfare indicators using quantitative data linked to a range of conditions or stimuli that are thought to impact the animals’ emotional state. Since odontocetes are social animals that engage in various social interactions, these interactions might inform us on their welfare state. We investigated pectoral contact laterality and the effect of the context on several social behaviors in three groups of captive odontocetes (Yangtze finless porpoises, YFPs: Neophocaena asiaeorientalis asiaeorientalis; East-Asian finless porpoises, EAFPs: N. a. sunameri, and bottlenose dolphins, BDs). Animals exhibited patterns depending on the time of the day for most of the social behaviors we analyzed; social separation was associated with lower rates of social behaviors for the two analyzed groups (YFPs and BDs), the accessibility to several pools was associated with higher rates of social behaviors for BDs. The effect of enrichment, disturbances and public presence was less clear and strongly depended on the group, the type of enrichment and disturbance. Our results confirm that captive odontocetes’ social behaviors are influenced by the context, and that, depending on the group, some of them, such as pectoral contacts, other body contacts, agonistic interactions or social play exhibit consistent patterns across contexts. Monitoring these behaviors might be useful to adapt the captive management to each species and group. The different responses among the three studied groups confirm that species and groups react differently to a stimulus and therefore, management decisions should be species/group specific. We recommend that more studies should be conducted to validate our findings in other groups of odontocetes under human care.
... However, van Praag et al. (2000) suggested that older animals still experience neurological benefits of enrichment, even when their interactions with enrichment may not be as frequent as younger individuals. Age differences in dolphin object play have been described in observational studies (e.g., von Streit & Ganslosser, 2013), and the effectiveness of familiar objects applied as enrichment items was also explored with dolphins, revealing some individual preferences and varying levels of interaction (Delfour & Beyer, 2012). ...
... Many of these objects are subjectively classified as "toys" and tend to become part of the daily environmental landscape in managed care. Research suggests that habituation to items makes them less effective as enrichment devices (Delfour & Beyer, 2012;Kuczaj et al., 2002;Line & Morgan, 1991;Maki & Bloodsmith, 1989;Markowitz & Aday, 1998;Schapiro, Bloomsmith, Suarez, & Porter, 1996). Thus, the dynamic and variable nature of ingestible enrichment and human involvement, when compared to static objects, may explain why the most complex enrichment class, Human Interaction/Ingestible/Object, produced the highest mean proportion of participation. ...
... The systematic, variable schedule for enrichment sessions used in this study was an effective model for eliciting high levels of participation. The application of enrichment should be strategically implemented and unpredictable in its presentation, while being mindful of variability and reinforcement value (e.g., Clegg et al., in press;Delfour & Beyer, 2012;Kuczaj & Walker, 2012), in order to optimize the effectiveness of subsequent enrichment efforts and activities (Hill & Broom, 2009;Hoy et al., 2010). Enrichment must also be applied strategically in efforts to reinforce desirable behaviors (e.g., pro-social, affiliative, calm) and avoid accidentally reinforcing undesirable behaviors (e.g., aggressive) (e.g., Kuczaj et al., 1998). ...
Article
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Application of environmental enrichment, as a means to successfully decrease undesired behaviors (e.g., stereotypic) and improve animal welfare, has been documented in a variety of zoological species. However, a dearth of empirical evidence exists concerning age, sex, and individual differences in response to various types of enrichment tools and activities in Atlantic bottlenose dolphins (Tursiops truncatus). This study involved a comparative assessment of enrichment participation of three resident, bottlenose dolphin populations, over the course of 17 months, with respect to sex and age class (calf, sub-adult, adult). Enrichment sessions were randomly assigned, conducted, and categorically assessed based on participation during seven, broad based enrichment classes (Object, Ingestible, Human, or a combination of the three). Overall, the proportion of participation in enrichment sessions was high (≥ 0.74), with individual differences in participation noted among the three populations. Sessions involving Humans and/or Ingestible items resulted in a significantly higher mean proportion of participation. Sub-adult and adult males were significantly more likely to participate in enrichment sessions, as well as engage in Human Interaction/Object sessions. Calves participated significantly more than adults or sub-adults across all enrichment classes with no noted differences between males and females. These data can serve as a tool to better understand the intricacies of bottlenose dolphin responses to enrichment in an effort to develop strategic enrichment plans with the goal of improving animal well-being and welfare.
... This reinforcement is either primary (i.e., fish or social contact) or secondary (i.e., toys or environmental change) (Ramirez, 1994). Man-made objects (called "toys") are also used by the caretakers as enrichment items (Delfour & Beyer, 2011;Kuczaj, Lacinak, & Fad, 2002). Toys are often used to improve the animals' welfare by increasing the complexity of the dolphins' environment and to give them the opportunity to engage in play behavior with the provided objects (Kuczaj et al., 2002). ...
... More complex, enriched environments offer animals improved opportunities for exploration, for withdrawal from human observation and represent an enrichment, which allows a reduction of stereotypical behaviors (Carlstead, Brown, & Seidensticker, 1993). "Toys" are generally used as enrichment for cetacean species (Kuczaj et al., 2002) but providing objects to dolphins does not always engender play activity (Delfour & Beyer, 2011). Here, the presence of toys in the pool elicited social play. ...
... A previous study showed that Parc Astérix dolphins were interested in objects and sometimes interacted with some of them and their presence increased social play, a sign of good mental health in these social animals (Delfour & Beyer, 2011 Slater, 1973). For instance, seaweed play was negatively correlated with agonistic behaviors of bottlenose dolphins (Slooten, 1994). ...
Article
Social play varies among species and individuals and changes in frequency and duration during ontogeny. This type of play is modulated by environmental changes (e.g., resource availability). In captivity, cetaceans and their environment are managed by humans, and training sessions and/or public presentations punctuate the day as well as other frequent or occasional events. There is a lack of research on the effects of environmental events that occur in captivity and might affect dolphins' behavior. We studied the context in which nine bottlenose dolphins (Tursiops truncatus) played socially and the events that could potentially impact this social interaction. The dolphins' social play behavior was significantly more frequent and lasted longer in the morning than in the afternoon and was present before and after interactions with their trainers with a non-significant tendency to be more frequent before and after a training session than a public presentation. In an experimental paradigm using familiar environmental enrichment, our results demonstrated that environmental enrichment tended to increase social play duration whereas temporary noisy construction work around the pool and display of agonistic behaviors by members of the group significantly decreased it. These results contribute to better understand the social play distribution in captive bottlenose dolphins and the impact of different events within their daily lives. Since play decreases or disappears when animals are facing unfavorable conditions, the evaluation of social play may relate to the animals' current well-being. We suggest that social play has potential to become an indicator of bottlenose dolphins' current welfare state.
... Also, delphinids display object manipulation either directly or through use of the environment (i.e., water flow, Yamamoto, Furuta, Taki, & Morisaka, 2014). 'kovich et al., 1970;Delfour & Beyer, 2011;Greene et al., 2011;Kuczaj et al., , 2008Norris & Dohl, 1980 Atlantic spotted dolphins Stenella frontalis ropes, scarves mouth, rostrum, pectoral fins, tail fluke Herzing et al., 2012. Note. ...
... Types of enrichment include: visual, auditory, olfactory, feeding, tactile, structural and social objects or events (Hoy, Murray, & Tribe, 2009), and human-animal interactions that challenge animals' cognitive abilities (e.g., husbandry training and positively reinforced interactions between the animals and their keepers/trainers/visitors, Laule & Desmond, 1998;Swaisgood & Shepherdson, 2005). Several examples of documented environmental enrichment can be found for terrestrial mammals (e.g., Skibiel, Trevino, & Naugher, 2007 Renner & Kelly, 2006;and bottlenose dolphins, Clark, 2013;Delfour & Beyer, 2011;Greene et al., 2011;Paulos et al., 2010). ...
... In dolphinaria, few studies have described and analysed dolphins' manipulative behaviors or assessed the effectiveness of environmental enrichment. Delfour and Beyer (2011) showed that some dolphins interact with objects while others do not. Therefore, Delfour and Beyer insisted that enrichment could not be proven effective until animals' playful interactions with provided objects and/or events had been scientifically demonstrated. ...
Article
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Cetaceans are well-known to display various play activities: numerous scientific papers have documented this phenomenon in wild populations and for delphinids under human care. The present study describes analyses of bottlenose dolphin (Tursiops truncatus) interactions with man-made objects introduced to their habitat as part of an environmental enrichment program. At Parc Asterix Delphinarium (France), 9 bottlenose dolphins were presented with 21 different objects. During 17 hours and using object-focal follows, we studied the dolphins' behaviors directed toward the objects, according to the objects physical properties (i.e. complexity and buoyancy). We also documented the body parts the animals used to manipulate the objects. The results show that young dolphins displayed more playful actions towards the introduced objects than their older conspecifics. In general, subjects preferred the objects classified as simple and floating, they displayed a larger variety of behaviours, they spent more time and were more creative with them than with other types of objects. Finally, there was significantly more contact and " manipulation " with the dolphin head area than with the fins, fluke or other body parts. By analyzing the dolphins' behaviors and actions they directed towards the introduced objects, the present study discusses meanings dolphins might give to their surroundings and the relevance of play behavior to their welfare.
... Program plans often include staff adding stimuli in the form of objects and problem-solving devices [18][19][20][21][22][23]. However, not all environmental enrichment is equally effective at eliciting the desired behavior [24,25]. One method for developing a successful environmental enrichment program is a SPIDER model, which lays out a framework that includes six steps for designing successful programs: Setting Goals, Planning, Implementing, Documenting, Evaluating, and Readjusting [26]. ...
... The vast majority of facilities utilized environmental enrichment that was included in the survey categories. Environmental enrichment for marine mammals can incorporate the addition of stimuli to meet species-appropriate needs including objects (e.g., balls and buoys; [24]), visual stimuli (e.g., television [47]), problems [18,48], novel scents for appropriate species [49][50][51], and training sessions [52]. The effectiveness of the enrichment depends on a number of factors including presentation ...
... Environmental enrichment, training, and habitat characteristics of bottlenose dolphins schedule and novelty [24,25]. Prolonged exposure to enrichment can result in habituation and loss of effectiveness requiring constant evaluation and resetting of the enrichment [52,53]. ...
Article
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In recent decades, animal welfare science has evolved to utilize a multidisciplinary approach to assess the welfare of animals in accredited zoos and aquariums. Science-based animal welfare assessments have become an essential component of management programs and widespread application is expected by animal care professionals. Management practices for bottlenose dolphins in accredited facilities incorporate several programs that potentially impact animal welfare including environmental enrichment and animal training. Additionally, habitat characteristics, such as the dimensions of the habitat, have been proposed to affect welfare. While accredited facilities are required to meet high standards of care, habitat characteristics and management practices are not standardized across locations. Knowledge and subsequent application of these practices and habitat characteristics can enhance our understanding of factors associated with positive welfare. As part of a larger study of dolphin welfare titled “Towards understanding the welfare of cetaceans in zoos and aquariums” (colloquially called the Cetacean Welfare Study), survey data were collected from 86 bottlenose dolphins in 40 habitats at 38 facilities in seven countries. The major aims of this paper are to provide general descriptive information regarding dolphin management in accredited zoos and aquariums and to provide supplemental context to the other research published from the Cetacean Welfare Study data set. This paper provides a review of current habitat characteristics and management practices at those 38 accredited zoos and aquariums. These data enabled the identification and quantification of how cetacean management practices differed between participating facilities accredited by the Alliance for Marine Mammal Parks and Aquariums and the Association of Zoos & Aquariums. Variables were selected based on their potential association with welfare including the physical habitat, environmental enrichment, and training programs. The variables were also used for subsequent research in this collection of related papers to investigate important connections between potential indicators of welfare and habitat characteristics, environmental enrichment, and training programs.
... These include balls or barrels (e.g. dolphins: Delfour and Beyer, 2012;orcas: Kuczaj et al., 1998orcas: Kuczaj et al., , 2002sea lions: Smith and Litchfield, 2010), rafts (e.g. dolphins: Delfour and Beyer, 2012;seals: Grindrod and Cleaver, 2001), and buoys (e.g. ...
... dolphins: Delfour and Beyer, 2012;orcas: Kuczaj et al., 1998orcas: Kuczaj et al., , 2002sea lions: Smith and Litchfield, 2010), rafts (e.g. dolphins: Delfour and Beyer, 2012;seals: Grindrod and Cleaver, 2001), and buoys (e.g. dolphins: Neto et al., 2016;seals: Grindrod and Cleaver, 2001;polar bears: Canino and Powell, 2010). ...
... When these objects stimulate inspection behaviour this could be classified as a beneficial response and play is increasingly viewed as a positive indicator of welfare (Held and Ŝpinka, 2011;Mellor, 2015 but see Blois-Heulin et al., 2015 for counterargument). According to a study by Delfour and Beyer (2012), where 21 objects were offered to bottlenose dolphins in random sets of four objects over a two-week period, only 50% of objects were manipulated by dolphins and the others did not elicit a behavioural response, positive or negative. Consistent with other zoo animals (see Young, 2003 for a review), simple contiguous objects with no moving parts rouse immediate interest and interaction but are quickly habituated to by marine mammals. ...
Article
Marine mammals include cetaceans, pinnipeds, sirenians, sea otters and polar bears, many of which are charismatic and popular species commonly kept under human care in zoos and aquaria. However, in comparison with their fully terrestrial counterparts their welfare has been less intensively studied, and their partial or full reliance on the aquatic environment leads to unique welfare challenges. In this paper we attempt to collate and review the research undertaken thus far on marine mammal welfare, and identify the most important gaps in knowledge. We use 'best practice case studies' to highlight examples of research promoting optimal welfare, include suggestions for future directions of research efforts, and make recommendations to strive for optimal welfare, where it is currently lacking, above and beyond minimum legislation and guidelines. Our review of the current literature shows that recently there have been positive forward strides in marine mammal welfare assessment, but fundamental research is still required to validate positive and negative indicators of welfare in marine mammals. Across all marine mammals, more research is required on the dimensions and complexity of pools and land areas necessary for optimal welfare, and the impact of staff absence for most of the 24-hour day, as standard working hours are usually between 0900-1700.
... Various studies with larger species of dolphins, primarily bottlenose dolphins (Tursiops truncatus), have addressed some aspects of enrichment (Clark, 2013a;Delfour & Beyer, 2012;Eskelinen et al., 2015;Kuczaj et al., 2002). In a recent study, Eskelinen et al. (2015) evaluated enrichment preference in terms of sex, age, and individual preference for different enrichment classes for a group of bottlenose dolphins. ...
... Another study of enrichment for cetaceans was conducted by Delfour and Beyer (2012), where the enrichment efficacy and needs of a group of bottlenose dolphins were evaluated. Some dolphins had individual preferences for enrichment items, or "favorite toys," and were found to interact more with enrichment devices that elicited visual interaction. ...
... While some aspects of enrichment have been evaluated for cetaceans (Clark, 2013a;Delfour & Beyer, 2012;Eskelinen et al., 2015;Kuczaj et al., 2002), the effects of enrichment are not yet fully understood. Enrichment has proven to be incredibly nuanced, with aspects such as species' characteristics, individual preference, other demographics, enrichment type, and habitat constraints influencing its effectiveness. ...
Article
Full-text available
Environmental enrichment is a crucial element of promoting welfare for animals in captivity. However, enrichment programs are not always formally evaluated for their efficacy. Furthermore, there is little empirical evidence of enrichment evaluation for species of small cetaceans in zoological settings. A wide range of variables may potentially influence enrichment efficacy and how it in turn affects behavior. The purpose of this study was to determine the most preferred environmental enrichment, and method of presentation, for a species that has not been well studied in captivity, the pantropical spotted dolphin (Stenella attenuata). In order to determine which enrichment items and method of presentation were most effective at eliciting enrichment interaction, we systematically examined how several variables of enrichment influenced enrichment interaction. The results suggested that presenting enrichment after training sessions influenced interaction with the enrichment. The results also indicated preference for enrichment type and a specific enrichment device. Finally, factors that influenced interaction were also found to influence aberrant behavior. The results support the premise that enrichment be “redefined” for each species and each individual.
... Apart from food provision, there are other events occurring in the captive environment which are thought to be rewarding for dolphins, but for which there are only a few studies. Bottlenose dolphins have been shown to voluntarily interact and play with toys and other enrichment items and so seem to view them positively on the whole (Clark, 2013;Delfour and Beyer, 2012;Kuczaj et al., 2002). However, we have little to no knowledge on dolphins' actual motivation for non-food enrichment events (Clark, 2013;Delfour and Beyer, 2012). ...
... Bottlenose dolphins have been shown to voluntarily interact and play with toys and other enrichment items and so seem to view them positively on the whole (Clark, 2013;Delfour and Beyer, 2012;Kuczaj et al., 2002). However, we have little to no knowledge on dolphins' actual motivation for non-food enrichment events (Clark, 2013;Delfour and Beyer, 2012). Measuring anticipatory behaviour could help in answering this question, and the results would be of interest to researchers and managers of zoo collections alike (Krebs et al., 2017;Watters, 2014). ...
... These observations were conducted between December 2016 and February 2017. Table 3 Definitions of behaviours used for measurement of participation in the three events (adapted from Brando, 2010;Delfour and Beyer, 2012;Eskelinen et al., 2015). ...
Article
Anticipatory behaviour describes the actions taken to prepare for an upcoming event. Bottlenose dolphins (Tursiops truncatus) in captivity are known to display anticipatory behaviours before feeding sessions, but it is unknown whether they would anticipate non-alimentary events. Furthermore, there is no published information available for any species on whether the level of anticipatory behaviour is predictive of an animal's actual participation in the following event or reward: answering this question would bring us closer to understanding this behaviour and its related affective states. In this study, we used sound cues to condition dolphins to the arrival of toys in their pool or a positive Human-Animal Interaction (HAI) with a familiar trainer, and measured their anticipatory behaviour before each event. The protocol was validated since the dolphins performed significantly more anticipatory behaviour before the toys and HAI contexts than a control situation, by means of increased frequencies of surface looking and spy hopping. Furthermore, we found that dolphins showed more anticipatory behaviour before the HAI than the toys context (Linear Mixed Model with 1000 permutations, all P < 0.001). In the second part of the investigation, higher anticipatory behaviour before toy provision, HAIs, and feeding sessions was significantly correlated to higher levels of participation in the event itself (measured by time spent with humans/toys, and number of times dolphins left during feeding sessions; LMM with 1000 permutations, respectively: β = 0.216 ± 0.100 SE, P = 0.039; β = 0.274 ± 0.097 SE, P = 0.008; β = -0.169 ± 0.080 SE, P = 0.045). Our results suggest that toys and HAIs were perceived as rewarding events, and we propose that non-food human interactions play an important role in these animals' lives. We also provide some of the first empirical evidence that anticipatory behaviour is correlated to the level of participation in the following event, supporting anticipatory behaviour as a measure of motivation, and hope that this stimulates further work regarding the use of this behaviour to assess and improve animal welfare.
... Animals respond differently to environmental enrichment due to life history traits such as age, sex, and/or social status (Eskelinen, Winship, & Borger-Turner, 2015;Kastelein & Wiepkema, 1989). Socially isolated, subordinate, or independent individuals (Delfour & Beyer, 2012;Hunter et al., 2002) and physically impaired individuals (Eskelinen et al., 2015) may not respond favorably to enrichment. Some individuals demonstrate object preferences, as has been observed in dolphins (Delfour & Beyer, 2012). ...
... Socially isolated, subordinate, or independent individuals (Delfour & Beyer, 2012;Hunter et al., 2002) and physically impaired individuals (Eskelinen et al., 2015) may not respond favorably to enrichment. Some individuals demonstrate object preferences, as has been observed in dolphins (Delfour & Beyer, 2012). For example, Hunter, Bay, Martin, and Hatfield (2002) observed that a group of harbor seals (Phoca vitulina concolor) and gray seals (Halichoerus grypus) showed the most behavioral changes in the presence of a bubble net while one seal preferred a platform and another preferred a grass bed. ...
... Other changes may not be of interest to the animal. For example, bottlenose dolphins only interacted with half the objects to which they were exposed (Delfour & Beyer, 2012). Habituation to toys is a common problem in marine mammals (Goldblatt, 1993). ...
Article
Harbor seals in the wild live in a stimulating environment; therefore, nonhuman-animal caretakers have increasingly been using environmental enrichment to improve the well being of seals under human care. The purpose of this study was to evaluate an object-based environmental enrichment program during a four-month period on stimulating exploration and play and improving conspecific social interactions and human–animal relationships (HAR). Zoo staff conducted the environmental enrichment program as part of the animal care program. Seals were given objects haphazardly and were observed for 20 minutes, and seals’ responsiveness during training sessions before and after enrichment was assessed. Seals showed interest in objects throughout the study and interacted more times per session with objects during the later months. Seals showed preferences for objects that were suspended in the water column (e.g., rope). Seals did not show more affiliative behavior but did show some aggressive behavior during enrichment sessions in comparison with free-swimming sessions. One seal showed better responsiveness to trainers in training sessions that followed an enrichment session than in other trainings sessions. Overall, the enrichment program was successful in increasing intrinsically motivated behaviors and showed that object-based enrichment has the potential to improve HAR between seals and their trainers.
... Since anticipatory behaviour levels can be used to understand which objects and events might be rewarding for captive animals (van der Harst and , it could also be applied to bottlenose dolphins in order to discover what elements of their environment they find rewarding: so far, we know only that they will voluntarily interact with enrichment items (Delfour and Beyer, 2012;Kuczaj et al., 2002) but not whether and how they value such items . One study has shown that captive bottlenose dolphins voluntarily sought tactile contact from familiar humans (Perelberg and Schuster, 2009) but again more information on how the animals perceive Human-Animal Interactions (HAIs), perhaps through their levels of anticipation for such events, would be instrumental to welfare discussions. ...
... Evidence for wild and captive dolphin play is abundant (reviews by : Kuczaj and Eskelinen, 2014;Paulos et al., 2010), including copious examples of object play (recent papers: Delfour and Beyer, 2012;Greene et al., 2011;Kuczaj and Makecha, 2008;Paulos et al., 2010), and evidence of inventing games (Pace, 2000). McCowan et al. (2000) showed that captive dolphins monitored their bubble quality as well as "plan" for the behaviour: this suggests involvement of conscious thought and appraisal, strengthening the notion that play impacts affective state. ...
... Clark (2013) supports cognitive enrichment with dolphin species, hypothesising that floating, simplistic objects are not sufficient to hold the dolphins' interest in the long-term. However, behaviour should be monitored to investigate whether this is indeed the case (Hill and Broom 2009), and such data, which shows responses to definable, repeatable contexts, could also aid in finding welfare indicators (Delfour and Beyer, 2012). The Human-Animal Relationship (HAR) is only just beginning to be investigated in other species in relation to cognitive enrichment and welfare (Whitham and Wielebnowski, 2013) and, due to the multiple, daily, and often close-contact interactions, is very likely to contribute to the welfare state of captive dolphins (Brando, 2010;. ...
Thesis
Welfare science is now an established discipline which enables objective measurements of animal welfare to be made. Bottlenose dolphins (Tursiops truncatus) are a common cetacean species kept in captivity, and although questions are arising over their quality of life in this environment, very few studies have focussed on objectively measuring their welfare. This thesis aimed to address this lack of data by developing animal-based indicators of bottlenose dolphin welfare. An initial review identified potential dolphin welfare measures, before selected behavioural indicators were measured in relation to training sessions. A judgement bias test was then adapted to dolphins, where optimistic biases were significantly linked to higher frequencies of synchronous swimming in their ‘free-time’ and lower frequencies of anticipatory behaviour before training sessions, (concurring with there ward-sensitivity theory). A penultimate study showed that anticipatory behaviour predicted participation in the upcoming event, and positive Human-Animal Interactions were anticipated more than access to toys. A final, on-going experiment has developed and applied a standardised protocol for measuring dolphins’motivation during training sessions in relation to social and health-related welfare problems. Although overall welfare is still difficult to measure, this thesis has proposed some first measures of dolphin emotions and affective states. Synchronous swimming is a likely indicator of positive emotions and social support, although more research should investigate variability between contexts. Anticipatory behaviour seemed to indicate motivation for events, and we suggest it reflects reward sensitivity as in other animals : further work into frequency thresholds would render it a valuable welfare indicator. A major objective of the thesis is to stimulate more research on welfare measures for bottlenose dolphins and other cetacean species in captivity.
... For YFPs, the distance swam in their preferred direction was also lower right before training than at other times, which might be explained by their display of anticipatory behaviours (e.g., spy-hops) and by their tendency to stay close to the trainers' office before training. Enrichment is often used for captive odontocetes (Kuczaj et al., 2002;Delfour and Beyer, 2012;Clark, 2013;Eskelinen et al., 2015;Perez et al., 2017;Serres and Delfour, 2017). As enrichment efficiency and consequences on animals' behaviour might depend on species and even groups (Mellen and Sevenich MacPhee, 2001;Kuczaj et al., 2002;Eskelinen et al., 2015), studying each captive group in order to optimize the use of enrichment is needed. ...
... Among types of enrichment, live fish, toy(s) and humans for YFPs, and toy(s) and humans for BDs affected these behaviours. The impact of the presence of humans interacting with animals on their behaviours is congruent with the fact BDs are attracted by the interaction with humans outside of training sessions and are more likely to play with toys when humans are involved (Delfour and Beyer, 2012;Eskelinen et al., 2015). Toys and live fish also seemed to be effective in affecting the animals' behaviour. ...
... Toys and live fish also seemed to be effective in affecting the animals' behaviour. Individual preferences for particular items have been shown in BDs (Delfour and Beyer, 2012;Eskelinen et al., 2015), a deeper analysis on the effect of each type of enrichment on each individual's behaviour might be useful. In most facilities, live fish is rarely provided to captive odontocetes as part of a routine management, or as enrichment (Brando et al., 2017), a deeper investigation on the effect of this kind of enrichment would also be useful to determine the best way to use it. ...
... Play has been extensively studied in captive odontocetes, including locomotor, object, and social play, but few studies investigated its link with welfare (Held & Špinka, 2011, Serres & Delfour, 2017. Many welfare-oriented studies on captive odontocetes focused on enrichment, which aims to increase desirable behaviors (including play) while decreasing undesirable behaviors (Delfour & Beyer, 2012;Eskelinen, Winship, & Borger-Turner, 2015). These studies analyzed the animals' interactions with the provided items or the impact of the presence of enrichment on the animals' behavior, including surfacing events (Maiorano, 2016) or circular swimming (Bahe, 2014). ...
... Solitary play is important because, in a human-controlled environment, it allows individuals to exert a control over their own activity (Greene, Melillo-Sweeting, & Dudzinski, 2011). Enrichment has been often studied to determine its effects on captive animals and to find ways to use it efficiently (Delfour & Beyer, 2012;Hoy, Murray, & Tribe, 2010;Kuczaj, Lacinak, & Turner, 1998;Maiorano, 2016;Mason, Clubb, Latham, & Vickery, 2007;Shepherdson, Mellen, & Hutchins, 1998;Shyne, 2006). This tool is widely used in captive odontocetes to increase environmental stimulation and improve animal welfare (Kuczaj et al., 1998;Makecha & Highfill, 2018). ...
... This tool is widely used in captive odontocetes to increase environmental stimulation and improve animal welfare (Kuczaj et al., 1998;Makecha & Highfill, 2018). To ensure of the efficiency of enrichment, it was suggested that it should be strategically used, monitored, and routinely evaluated (Delfour & Beyer, 2012;Mellen & Macphee, 2001). Here, we did not analyze the reaction of each individual to the presence of enrichment. ...
Article
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The number of welfare-oriented studies is increasing in captive animals, including odontocetes species that are widely kept in zoos and aquaria. However, validated welfare indicators are lacking for captive odontocetes. We studied the effect of several conditions (time of the day, delay to training, social grouping, public presence, housing pool) and stimuli (enrichment, unusual events) on the solitary behavior of Yangtze finless porpoises (Neophocaena asiaeorientalis asiaeorientalis), East Asian finless porpoises (N. a. sunameri), and bottlenose dolphins (Tursiops truncatus). Each group exhibited different behavioral variations depending on the context. However, some common patterns were found. The frequency of solitary play increased in the 3 groups in positive conditions and decreased in negative contexts. Jumping was mostly displayed in conditions that are thought to be stressful or exciting. Stereotypical behaviors for Yangtze finless porpoises and environment-hitting behaviors for bottlenose dolphins were more frequent during social separation and less frequent when enrichment was provided, suggesting that they could indicate mild stress, lack of stimulation, or frustration. Finally, environmental rubbing seemed to be mostly displayed in quiet contexts. The frequency variation of studied behaviors depending on the context provides preliminary information on their potential use as welfare indicators.
... Instead, nonsystematic methods and subjective measures are typical, if an assessment is conducted at all. This approach leaves some question as to the effectiveness of various enrichment programs (Broom, 1988;Canali & Keeling, 2009;Clegg & Delfour, 2018;Delfour & Beyer, 2012;Hoy et al., 2010;Makecha & Highfill, 2018;Newberry, 1995), which range from simply adding objects to an enclosure to social housing (Daoudi et al., 2017;Yeater et al., 2013), training (Ramirez, 1999;Westlund, 2014), introducing scent (Nelson Slater & Hauber, 2017;Samuelson et al., 2016), or supplying more naturalistic or challenging feeding opportunities (Fernandez & Timberlake, 2019;McPhee, 2002;Wagman et al., 2018) to name a few. There is evidence that some enrichment programs may even result in an increase in unwanted behaviors, such as increased aggression (Franks et al., 2009), manipulation of the enrichment to the point in which it becomes dangerous for the animals (Hahn et al., 2000;Hare et al., 2007), or other undesirable behaviors (Bloomsmith et al., 1991). ...
... There is evidence that some enrichment programs may even result in an increase in unwanted behaviors, such as increased aggression (Franks et al., 2009), manipulation of the enrichment to the point in which it becomes dangerous for the animals (Hahn et al., 2000;Hare et al., 2007), or other undesirable behaviors (Bloomsmith et al., 1991). Systematically monitoring the animals' responses to environmental enrichment can allow researchers to evaluate, in a nonbiased fashion, enrichment programs' welfare outcomes (Delfour & Beyer, 2012;Samuelson et al., 2016;Shyne, 2006). ...
... Unfortunately, few studies present research focused on the possible unintended consequences of environmental enrichment or on individual differences in animals' reactions to enrichment programs (Bayne, 2005;Carlstead, 1991;Hare et al., 2007;Hoy et al., 2010). In many dolphin facilities, enrichment programs are primarily focused on toy making (Brando et al., 2018;Clark, 2013;Delfour & Beyer, 2012;Kuczaj et al., 2002), with little scientific monitoring of behavioral interest or engagement with the toys. When there is behavioral monitoring, the effects of enrichment items are sometimes unclear and context-dependent (Delfour & Beyer, 2012;Neto et al., 2016). ...
Article
Bottlenose dolphins (Tursiops truncatus) are viewed as a highly intelligent species, capable of complex behaviors, requiring marine parks to maintain dynamic environmental enrichment procedures in order to ensure their optimal psychological and physiological well-being in human care. In this study, two experiments were conducted to determine the effects of different forms of enrichment on the behavior of bottlenose dolphins. In Experiment 1, the most successful enrichment included highly novel items, which resulted in avoidance, but also what is frequently considered positive behavioral changes including a reduction in circle swimming and an increase in social behavior. In Experiment 2, the use of choice resulted in negative unintended social consequences. These two experiments together demonstrate that the results of deploying enrichment may not be as clear-cut as previously presumed. In order to maintain positive benefits of enrichment, the results of this study suggest that unique forms of enrichment should be implemented on a variable schedule that is offered several times a year and consistently evaluated for effectiveness.
... Although the impacts of enrichment programs are generally positive, the magnitude of their effects may vary greatly between individuals of the same species, especially when the enrichment is based on the introduction of manipulative objects [see Delfour and Beyer, 2012]. In these situations some animals will interact with novel objects, even without food rewards and in the absence of the trainers, while others show no interest or even aversion to the objects. ...
... In these situations some animals will interact with novel objects, even without food rewards and in the absence of the trainers, while others show no interest or even aversion to the objects. In concordance with Delfour and Beyer [2012], our own experience with bottlenose dolphins at Zoomarine attests that while some animals, usually the youngest, display great interest in the enrichment objects provided, other individuals interact much less, if at all, with such objects. It would be important to understand this variation in response and motivation, but even more relevant to develop strategies to extend the benefits of environmental enrichment to those animals less motivated to object exploration and play. ...
Article
Enrichment programs may contribute to the quality of life and stress reduction in bottlenose dolphins (Tursiops truncatus) kept in zoos and aquaria. The results of these programs are generally positive in terms of welfare, but the magnitude of their effects may vary greatly between individuals of the same species, especially when the enrichment plans are based on the introduction of manipulative objects. Some animals will interact spontaneously with novel objects, even without food rewards and in the absence of the trainers, while others show no interest or even aversion toward the objects. To determine if formal training can improve these conditions, we measured the effects of an operant conditioning program in the manipulation of objects by dolphins that initially avoided them. This program took place between April and October 2013 at Zoomarine Portugal. Subjects were two female and two male bottlenose dolphins (adults with ages from 17 to 35 years) that after a preliminary analysis showed avoidance or low interest in the manipulation of various toys. The level of interaction with introduced enrichment objects was observed before and after formal training to explore the toys (sixteen 20-min observation sessions per animal "before" and "after training"). In all subjects, an index of interest in object manipulation, in the absence of trainers, increased significantly after the application of the training techniques. The results show that an initial reinforcement program focused on the manipulation of toys may overcome resistance, improving the effects of environmental enrichment plans, and it is a potentially useful strategy to increase the welfare of some captive animals. Zoo Biol. XX:XX-XX, 2016. © 2016 Wiley Periodicals, Inc.
... However, it is unclear whether these characteristics are true among all male dolphins, if males are merely more interested in manipulating objects in their environment, or if the sex differences in interest extend to all stimuli, regardless of form. Bottlenose dolphins also display preferences to "favorite toys" (Delfour & Beyer, 2012), thus individual variation may also require consideration when developing or adapting enrichment programs for these animals. ...
... Overall both species of dolphins spent relatively little session time engaged with the television, similarly to what has been reported in dogs (Graham et al., 2005) and cats (Ellis & Wells, 2008). However, a few individuals' attention approached that of socially housed primates (Bloomsmith et al., 1990), spending over 14% (Kuczaj et al., 2002), the mean duration of interactions with specific objects (Delfour & Beyer, 2012) or the presence of interactions rather than the total percentage of time spent interacting with the enrichment. Thus, exact comparisons between the time dolphins spend watching and interacting with video to other forms of enrichment are currently unavailable. ...
Article
This study assessed the interest toward novel video clips as enrichment stimuli in two species of captive dolphins (Tursiops: n = 11; Steno: n = 5). Videos were played at underwater viewing windows while the animals were housed with conspecifics, and responses were subsequently analyzed based on general content of each novel video. Interest levels (i.e., percentage of time watching and behavioral rate) were compared between species and within species across video categories. While the varied video contexts did not produce significant differences among the time spent watching or behaviors observed, species differences and sex differences were noted. Rough‐toothed dolphins displayed significantly more behaviors, particularly interest and bubble behaviors, than bottlenose dolphins, with no differences observed between the species for the percentage of time spent watching. Among bottlenose dolphins, males watched the television longer, and responded behaviorally significantly more, displaying a higher rate of bubble and aggressive behaviors than females. Male rough‐toothed dolphins displayed significantly more aggressive behaviors than females, with no other sex differences noted. Overall, these data suggest that television may serve as a useful enrichment device for certain individuals and species of cetaceans, as well as a cognitive experimental tool, as long as sex, species, and individual differences are taken into consideration when interpreting results.
... Environmental enrichment, associated with the well-being concept in animals, first consisted of improvements to the captive animal environment [8]. This relatively new concept was well studied in aquatic mammals, particularly dolphins [9]. Several studies suggest that environmental enrichment for animal welfare allows the animal to express behaviours and use abilities, such as cognition [7]. ...
... It is difficult to know if this preference for a hexagon and triangle is due to previous experiences with objects with a similar geometric form. Studies on dolphins [9] demonstrated that when new objects are introduced into the pool, dolphins are visually attracted by them, manipulate some of them and may have their favourite object. A similar process could be taking place in this study with new shapes, although the square is not attractive before training, maybe because it was not a new shape for Daniel. ...
Article
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Studies on the cognitive abilities of manatees are limited despite their importance for the environmental enrichment and welfare of individuals in captivity and the understanding of manatee behaviour in the wild. Our study analyses how the presence of new stimuli and their association with food may have changed the behaviour of an Antillean manatee called Daniel. First, Daniel was observed in the absence of stimuli and subsequently, in step two, presented with the presence of four different geometrical shapes. During step three, we trained Daniel to eat from the square, while in step four he was presented with the four shapes without food. The behaviour and interaction of the manatee with the square increased considerably. We observed that three and twelve months after training the manatee still chose the square and displayed behaviours toward this specific shape. This study allowed us to formally demonstrate the ability of manatees to associate visual cues with food and increase activity with environmental and occupational devices. Our results open up new perspectives for behavioural studies on manatees, in particular those associated with cognition, management and welfare in captivity.
... In fact, both in nature and in controlled environment, bottlenose dolphins frequently interact with objects (Greene, Melillo-Sweeting, & Dudzinski, 2011;Kuczaj & Eskelinen, 2014). Different objects arouse different degrees of interest (Delfour et al., 2017;Neto et al., 2016) and the study of preference toward objects relies on a wide bibliography and consolidated procedures (Delfour & Beyer, 2012;Neto et al., 2016). Therefore, in the present study, we hypothesize that dolphins' anticipatory behavior increases in relation to increased preference for the objects, and then, we test the possibility of using anticipatory behavior to distinguish the dolphins' preferences toward different objects and use it as a preference test. ...
... Then, we observed each animal using a continuous sampling throughout the 10 minutes sessions and calculated the percentage of time spent by each dolphin interacting with the two types of objects. Finally, we checked whether the time spent on object A was significantly longer than for objects B (Delfour & Beyer, 2012;Neto et al., 2016). ...
Article
The preference tests have made a great contribution to promoting animal welfare. However, they are not always easily applicable and have some criticalities. Recently the anticipatory behavior has been used to detect the animals’ preference. In this study, we attempted to investigate the relationship between preference and anticipatory behavior. To this end, we tested on a group of dolphins (Tursiops truncatus) whether, with anticipatory behavior, it is possible to distinguish the animals’ preference for different objects and then use it as a preference test. Anticipatory behavior is exhibited throughout the animal kingdom, it is easy to induce and measure, and does not have the criticalities of other preference tests. Therefore, its use as preference test could facilitate the study of animals' preferences and contribute to the promotion of their welfare. Our results support the hypothesis of use anticipatory behavior as a preference test. In fact, dolphins have anticipated the arrival of objects highly preferred with a frequency three times higher than shown toward objects less preferred, providing further evidence of the correlation between anticipatory behavior and the animals’ preference.
... Previous research suggests that environmental enrichment can be effective in increasing the habitat use and social play of bottlenose dolphins [45,46]. However, behavioral responses to different enrichment types and objects vary [47]. In the present study, dolphins receiving sinking enrichment more often had lower activity levels. ...
... This suggested that, in general, providing each specific enrichment type between a quarter and half the month may be positively related to interactions with the enrichment, which may be associated with higher activity levels. Importantly, some dolphins have preferred enrichment objects that are resistant to habituation [47], and this should be considered when developing an enrichment schedule. Notably, this finding is not suggesting that enrichment should only be provided 26% to 50% of the month, but that providing more types of enrichment on this moderate schedule is related to higher activity levels. ...
Article
Full-text available
Environmental enrichment can be used to improve the welfare of dolphins in zoos and aquariums. Bottlenose dolphins under professional care are typically provided with a range of enrichment that has a variety of features and levels of complexity at various frequencies. In the present study, a subset of data from a larger study entitled “Towards understanding the welfare of cetaceans in zoos and aquariums” (colloquially called the Cetacean Welfare Study) was used to examine the relationship between activity level and enrichment buoyancy as well as enrichment provisioning schedules. Survey data were collected from accredited zoos and aquariums related to the types of enrichment provided to the dolphins and the frequency and duration they were supplied. Non-invasive bio-logging devices were used to record the dolphin kinematics one day per week over the course of two five-week data collection periods. Activity level related positively with the total duration of time non-stationary enrichment was provided. In addition, providing a larger number of enrichment types each between 26% and 50% of the days in a month (i.e., rotating many different types of enrichment across days on a moderate schedule) was positively related to activity level. Activity level was negatively related to the number of times sinking enrichment was provided. Understanding how the temporal schedule and features of various types of enrichment are related to activity levels will aid in developing progressively more effective enrichment programs.
... These include introduction of objects to induce echolocation behavior (e.g. Delfour & Beyer, 2012) and playbacks of dolphin phonations (e.g. Kristiansen, 2008). ...
Thesis
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Sound is the primary sensory modality for dolphins, yet policies mitigating anthropogenic sound exposure are limited in wild populations and even fewer noise policies or guidelines have been developed for governing dolphin welfare under human care. Concerns have been raised that dolphins under human care live in facilities that are too noisy, or are too acoustically sterile. However, these claims have not been evaluated to characterize facility soundscapes, and further, how they compare to wild soundscapes. The soundscape of a wild dolphin habitat off the coast of Quintana, Roo, Mexico was characterized based on Passive Acoustic Monitoring (PAM) recordings over one year. Snapping shrimp were persistent and broadband, following a diel pattern. Fish sound production was pulsed and prominent in low frequencies (100 - 1000 Hz), and abiotic surface wave action contributed to noise in higher frequencies (15 - 28 kHz). Boat motors were the main anthropogenic sound source. While sporadic, boat motors were responsible for large spikes in the noise, sometimes exceeding the ambient noise (in the absence of a boat) by 20 dB root-mean-squared sound pressure level, and potentially higher at closer distances. Boat motor sounds can potentially mask cues and communication sounds of dolphins. The soundscapes of four acoustically distinct outdoor dolphin facilities in Quintana Roo, Mexico were also characterized based on PAM, and findings compared with one another and with the measurements from the wild dolphin habitat. Recordings were made for at least 24 hours to encompass the range of daily activities. The four facilities differed in non-dolphin species present (biological sounds), bathymetry complexity, and method of water circulation. It was hypothesized that the greater the biological and physical differences of a pool from the ocean habitat, the greater the acoustic differences would be from the natural environment. Spectral analysis and audio playback revealed that the site most biologically and physically distinct from the ocean habitat also differed greatly from the other sites acoustically, with the most common and high amplitude sound being pump noise versus biological sounds at the other sites. Overall the dolphin facilities were neither clearly noisier nor more sterile than the wild site, but rather differed in particular characteristics. The findings are encouraging for dolphin welfare for several reasons. Sound levels measured were unlikely to cause threshold shifts in hearing. At three of four facilities, prominent biological sounds in the wild site - snapping shrimp and fish sounds - were present, meaning that the dolphins at these facilities are experiencing biotic features of the soundscape they would experience in the wild. Additionally, the main anthropogenic sounds experienced at the facilities (construction and cleaning sounds) did not reach the levels of the anthropogenic sounds experienced at the wild site (boat motor sounds), and the highest noise levels for anthropogenic sounds fall outside the dolphins' most sensitive range of hearing. However, there are anthropogenic contributors to the soundscape that are of particular interest and possible concern that should be investigated further, particularly pump noise and periodic or intermittent construction noise. These factors need to be considered on a facility-by-facility basis and appropriate mitigation procedures incorporated in animal handling to mitigate potential responses to planned or anticipated sound producing events, e.g. animal relocation or buffering sound producing activities. The central role of bioacoustics for dolphins means that PAM is a basic life support requirement along with water and food testing. Periodic noise is of highest concern, and PAM is needed to inform mitigation of noise from periodic sources. Priority actions are more widespread and long-term standardized monitoring, further research on habituation, preference, coupling and pool acoustics, implementation of acoustics training, standardization of measurements, and improved information access.
... Although cetaceans are not like many terrestrial species who climb or fly onto different structures in the 3D space of their habitats, and indeed offshore species might rarely come into contact with the bottom substrate at all, these animals still need environmental variation to compensate for the time and cognitive efforts that would be spent hunting and foraging in the wild. Enrichment describes the addition of items and environmental changes to promote behavioural diversity and enhance animal welfare (Hoy et al., 2010;Delfour & Beyer, 2012). Simple, floating objects seem to be the norm for cetacean enrichment programs (Clark, 2013;Lauderdale et al., 2021), and while these objects can be engaging for cetaceans (the same way a cardboard box provides endless play possibilities for children, Delfour et al., 2017), variable and novel enrichment is a critical tool for stimulating exploration, natural behaviours and cognitive challenge. ...
Article
In order to continue its business sustainably, any industry that uses animals must largely align their ethical position with that of the general public: ‘the mainstream social ethic’. Although zoos are transitioning from entertainment venues to conservation actors, many cetacean (whale and dolphin) facilities present the animals in unnatural-looking enclosures and entertainment-driven contexts. But what is the ‘mainstream social ethic’ regarding cetacean facilities, and what might it mean for the industry’s future? The evidence is first reviewed on cetacean welfare and the purported purposes for displaying cetaceans in the past and present. The mainstream social ethic is then defined, suggesting we may be at a crossroads for this industry. Welfare has improved in the last decades but could be further enhanced through providing more choice and control in cetaceans’ environments, particularly in enrichment, training and social groupings. Sanctuary settings provide a potential environment with more choice and control, but are still in the very initial stages of development. Fundamental, structural changes to the mission, presentation of the cetaceans and business model seem to be needed to realign the public display of cetaceans with the mainstream social ethic of the times.
... For example, a dolphin that does not play may be sick, disinterested, annoyed, anxious, bored, frustrated, or scared. However, if t behavioral profile indicates that it is introverted, non-curious, and dislikes novelty, then sign of diminished well-being (Delfour & Beyer, 2011). While certain objects caused interest and manipulation in some dolphins other objects did not elicit a response in others. ...
... For example, a dolphin that does not play may be sick, disinterested, annoyed, anxious, bored, frustrated, or scared. However, if t behavioral profile indicates that it is introverted, non-curious, and dislikes novelty, then sign of diminished well-being (Delfour & Beyer, 2011). While certain objects caused interest and manipulation in some dolphins other objects did not elicit a response in others. ...
... A few facilities have dedicated lists outlining daytime and nighttime enrichment activities and safety criteria. Delfour & Beyer (2012) investigated the use of objects by bottlenose dolphins and found that only 50% of all presented objects elicited manipulative behaviors. Thus, not every toy is a successful enrichment device, and not every behavioral change subsequent to the introduction of a new object necessarily indicates an enrichment effect. ...
Article
In 2012, two marine mammal welfare and well-being workshops were held: one from 19-21 March 2012 at the Harderwijk Dolfinarium in the Netherlands, and the other from 9-11 November 2012 at Hubbs-SeaWorld Research Institute in San Diego, California. Well over 150 international participants attended, from Europe as well as North America. Herein, we present a summary of the presentations. The aim of the workshops was to discuss topics relevant to marine mammal welfare and well-being from a holistic perspective, including training, enrichment, nutrition, habitat choice, social behavior, anatomy and physiology, acoustics, and cognition. Presenters were asked to apply knowledge and information gained from research on wild and captive animals in order to strengthen, improve, and build on existing marine mammal care programs. Many of these topics require more research for us to make evidence-based decisions on animal needs and preferences-what promotes the reduction of negative welfare and/or what in-creases positive welfare and well-being.
... Leger et al., 2009;physiology: Worthy, Worthy, Yochem, & Dold, 2013;reproduction, Asper, Young, & Walsh, 1988;Robeck et al., 2009). Even research on aspects of cognition and sociality of bottlenose dolphins has been conducted in both wild and captive settings and resulted in information that facilitated more species-appropriate forms of enrichment and social groupings for captive animals (Fabienne & Helen, 2012;Waples & Gales, 2002). Research with killer whales may benefit from similar studies. ...
Article
Full-text available
The welfare of killer whales (Orcinus orca) has received worldwide attention recently. The purpose of this study was to sample the peer-reviewed scientific research on killer whales with a complementary comparison to Atlantic bottlenose dolphins (Tursiops truncatus) to ascertain the primary topics of research conducted with these two cetaceans. A second objective of the study was to assess the relationship between the research topic and the setting in which the research was conducted. From a database-driven search of peer-reviewed academic journal articles, 759 unique articles involving killer whales, 2,022 unique articles involving Atlantic bottlenose dolphins, and 38 additional articles that included both species were retained for analysis. Coders categorized each article by topic (Anthropogenic Response, Cognition, Distribution, Echolocation, Foraging/Predation, Health/Physiology, Interactions with Humans, Sociality, and Vocalization) and research setting (Natural Habitat, Captivity, or Both). Most studies of killer whales involved animals in their natural habitat (90%) and the majority of killer whale studies, regardless of setting, concentrated on health and physiology, such as contaminants and genetic variability (31%), foraging and predation behaviors (26%), and geographic distribution (20%). The majority of the studies (68%) involving bottlenose dolphins were also conducted in their natural habitat, but there was significantly more research comparatively with captive animals and with greater diversity. The results suggested that research with killer whales has been dominated by a limited range of topics with relatively little research conducted on topics that directly address issues of welfare. Similar to killer whales, research with Atlantic bottlenose dolphins has been dominated by health and physiology (48.5%) and distribution (17.6%). In contrast to killer whales, topics such as sociality (9.5%) and cognition (5%) were more prominent in research incorporating Atlantic bottlenose dolphins. Both species are still in need of additional research on questions related to behavioral patterns.
... Up to now, most enrichment items in marine mammals are floating hard plastic objects that animals can push around, given during daytime and often under supervision. Delfour and Beyer (2012) researched the use of objects by bottlenose dolphins and found that only 50 % of the object elicited manipulative behaviors. Not every toy seems to be a successful enrichment device and not each behavioral change subsequent to the introduction of objects necessarily indicates an enrichment effect. ...
Chapter
Wild animals in entertainment have long been popular. A wide variety of wild animals are held in captivity worldwide. Some are housed in modern zoos, sanctuaries, research facilities and wildlife centers, while others live their lives as actors in (traveling) circuses, in entertainment parks or on movie sets. Good animal welfare and quality of life matters first and foremost to the individual animal, but is also fundamental to meaningful and successful conservation , research and education programs. It is important to consider the animal’s perspective and the species-specific requirements that are not always compatible with our entertainment goals. This chapter will focus specifically on the topic of entertainment and performing captive wild animals in zoos, marine parks and circuses worldwide and which conditions need to be fulfilled to warrant good animal welfare, i.e. thriving captive wild animals.
... The analyses of reinforcement in the CA indicated that behaviors associated with primary reinforcement alone versus primary and secondary reinforcement were emitted under a non-specific context most frequently, suggesting that some of the secondary reinforcers were not conditioned effectively. Reinforcing value varies among individuals, and some environmental enrichment devices, which may be used as secondary or learned reinforcers, may not actually be reinforcing to animals (Delfour & Beyer, 2012;Eskelinen, Winship, & Borger-Turner, 2015). Although an arduous task, identifying what was reinforcing to each study subject, specifically in terms of secondary reinforcement, may have influenced the findings of this study. ...
Article
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When analyzing animal behavior, it is important to consider the influence of learning principles. The create response of bottlenose dolphins, elicited by a discriminative stimulus, or an SD (visual cue presented to an animal by a trainer), has been described as an elective, often novel response based on arbitrary preferences of individual animals. The goal of this study was to identify the potential influence of reinforcement theory, response class, and primacy and recency on the create responses of bottlenose dolphins. Three, male subjects with an established mastery of the create paradigm, identified in this study as a non-specific, non-repeat contingency, were assessed over eScholarship provides open access, scholarly publishing services to the University of California and delivers a dynamic research platform to scholars worldwide. the course of two months while under stimulus control (pre-assessment), followed by evaluations of the create response (create assessment) using a double-blind sampling model. During the preand create assessments, each response was quantified regarding response class, frequency of request, and reinforcement type, frequency, and magnitude. When presented with the create SD, the dolphins elected to produce behaviors predominantly associated with the more recent training context (create assessment) versus behaviors associated with training that occurred months prior (pre-assessment), which may demonstrate the effects of primacy versus recency. Additionally, the create trials were associated with reinforcement on a high frequency and magnitude, fixed, low ratio schedule, and the subjects most often performed the behaviors associated with the greatest magnitude of primary reinforcement, which highlights the influence of reinforcement and the law of effects. Lastly, two subjects never responded with high energy behaviors in the create contingency, and one subject performed significantly more low and medium energy responses when compared to high energy behaviors, capturing the effects of a response class characterized by intensity under a fixed ratio reinforcement schedule. Thus, the create response was not represented by arbitrary elective preferences but rather, partially driven by the learning theories examined.
... Research specifically with bottlenose dolphins found that the timing of the enrichment is just as important as the type of enrichment [6]. Another study examining object enrichment with common bottlenose dolphins (Tursiops truncatus) found that only 50% of the objects provided elicited the desired behavioral goal [7]. This demonstrates the importance of setting goals as well as documenting, evaluating, and readjusting an enrichment program to ensure the behavioral needs of animals are met [8,9]. ...
Article
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Accredited zoos and aquariums continually strive to ensure high levels of animal welfare for the animals under their professional care. Best management practices include conducting research to better understand factors that lead to optimal welfare and then turning findings into practice. The current study is part of the larger Cetacean Welfare Study or more formally, “Towards understanding the welfare of cetaceans in zoos and aquariums.” Facilities participating in the study were accredited by the Alliance of Marine Mammal Parks and Aquariums and/or the Association of Zoos and Aquariums. Animal management factors and habitat characteristics were examined in relation to two potential indicators of welfare for common ( Tursiops truncatus ) and Indo-Pacific ( Tursiops aduncus ) bottlenose dolphins. Specifically, we examined environmental enrichment, animal training, and habitat characteristics that were significantly related to behavioral diversity and route tracing, a form of stereotypic behavior. Behavior was recorded from 47 animals at 25 facilities around the world. Overall, the rate of route tracing behavior observed during the study was very low and few animal management factors or habitat characteristics were found to be related to this behavior. One factor, enrichment diversity, had a significant positive relationship with route tracing and an inverse relationship with behavioral diversity. This finding may be a product of a response mounted by animal care specialists to the behavior as opposed to a cause. Animals that engaged in this behavior were likely provided more diverse enrichment in attempts to ameliorate the stereotypic behavior. However, multiple factors were found to significantly relate to behavioral diversity, a potential positive indicator of welfare for bottlenose dolphins. Dolphins that were trained on a predictable schedule had higher behavioral diversity than those on a semi-predictable schedule. There was a positive significant relationship between behavioral diversity and the number of habitats to which an animal had access, and a significant inverse relationship with the maximum depth of the habitat. Finally, animals that were split into groups and reunited or rotated between subgroups had higher behavioral diversity than animals managed in the same group. Information gained from the current study suggested that animal management techniques may be more important in ensuring good welfare for bottlenose dolphins than focusing on habitat size.
... Joseph & Antrim, 2010) dolphin health, we also included frequency of testing and recommended ranges for salinity, total and faecal coliform, pH, and chlorine (ranges used: AWA, 1966;EAAM, 2013;Gage, 2009). The last measure concerned enrichment, since it is likely only strategically applied, variable, and individually relevant enrichment will promote good welfare (Delfour & Beyer, 2012;Eskelinen, Winship, & Borger-Turner, 2015). The wound percent cover range and relevant welfare score for the dolphin in each image. ...
Article
The field of welfare science and public concern for animal welfare is growing, with the focus broadening from animals on farms to those in zoos and aquariums. Bottlenose dolphins (Tursiops truncatus) are the most common captive cetaceans, and relevant regulatory standards are principally resource-based and regarded as minimum requirements. In this study, the farm animal Welfare Quality® assessment was adapted to measure the welfare of bottlenose dolphins, with a similar proportion of animal-based measures (58.3%). The “C-Well” assessment included 11 criterion and 36 species-specific measures developed in situ at three marine mammal zoological facilities, tested for feasibility and accuracy, and substantiated by published literature on wild and captive dolphins and veterinary and professional expertise. The C-Well scores can be calculated for each measure or combined to achieve an overall score, which allows for the comparison of welfare among individuals, demographics, and facilities. This work represents a first step in quantifying and systematically measuring welfare among captive cetaceans and can be used as a model for future development in zoos and aquariums, as well as a means to support benchmarking, industry best practices, and certification.
... In support of our results, lower FGCM concentrations during enrichment compared to absence of enrichment have been reported in the giant panda (Ailuropoda melanoleuca, [72]). Moreover, enrichment devices, including toys, have been shown to diversify captive odontocete behavior and reduce undesired behaviors [73]. Enrichment with toys has been shown to increase both object and social play in BDs, which is theoretically believed to be a reflection of good welfare and, subsequently, lower stress states [74]. ...
Article
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Although the use of fecal glucocorticoid metabolite (FGCM) measurements as non-invasive biomarkers for the stress response in mammals has increased, few studies have been conducted in odontocetes. We investigated if animal sex, age, pregnancy or contextual variations (season, sampling time, enrichment, social separation and presence of visitors) influenced the FGCM concentrations in presumably healthy, captive and endangered Yangtze finless porpoises (YFPs, N = 4) and bottlenose dolphins (BDs, N = 3). For YFPs, the FGCM concentrations were influenced by season (p = 0.01), diurnal variation (p = 0.01) and pregnancy (p = 0.005). Contextual variables that were associated with increases in FGCM concentrations included social separations (p = 0.003) and numbers of visitors (p = 0.0002). Concentrations of FGCMs were lower (p = 0.001) after exposure to environmental enrichment. For BDs, enrichment was associated with reduced concentrations of FGCMs (p < 0.0001). The presence of visitors also influenced this species' FGCM concentrations (p = 0.006). These results demonstrate that changes in the FGCM concentrations in YFPs and BDs may occur in response to contextual and social changes. In combination with other behavioral and physiological assessments, measurements of FGCMs may be a useful tool for monitoring cetacean welfare. Such monitoring may help researchers identify and better understand situations that may be stressful for animals and, therefore, improve management and husbandry. Furthermore, results from our study and inferences of the FGCM concentrations in cetaceans, and their potential relationship to stress, may be extrapolated to studies of free-ranging animals, which may help detect possible environmental or anthropogenic stressors that could be affecting these populations.
... Adding to the importance of social relationships for bottlenose dolphins, previous research has shown that when dolphins are given the choice between enrichment objects and social interactions, the latter was frequently selected [32]. This is not to imply that environmental enrichment is not important for dolphins, but to highlight the importance of social behavior for these species. ...
Article
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Bottlenose dolphins are a behaviorally complex, social species that display a variety of social behaviors. Because of this, it is important for zoological facilities to strive to ensure animals display species-appropriate levels of social behavior. The current study is part of the multi-institutional study entitled “Towards understanding the welfare of cetaceans in zoos and aquariums” commonly referred to as the Cetacean Welfare Study. All participating facilities were accredited by the Alliance of Marine Mammal Parks and Aquariums and/or the Association of Zoos and Aquariums. Behavioral data were collected on 47 bottlenose dolphins representing two subspecies, Tursiops truncatus and Tursiops aduncus , at 25 facilities. The social behaviors of group related activity ( group active ) as well as interacting with conspecifics ( interact with conspecific ) were examined for their relationships to both animal management factors and habitat characteristics. The behavioral state of group active and the rate of interact with conspecific were both positively related to the frequency of receiving new forms of environmental enrichment. Both were inversely related to the random scheduling of environmental enrichment. Additional results suggested interact with conspecific was inversely related with daytime spatial experience and that males displayed group active more than females. Overall, the results suggested that animal management techniques such as the type and timing of enrichment may be more important to enhance social behavior than habitat characteristics or the size of the habitat. Information gained from this study can help facilities with bottlenose dolphins manage their enrichment programs in relation to social behaviors.
... Most behavioral studies were conducted with wild populations, whose behavior is mainly influenced by foraging, prey availability, or predator avoidance [23]. In zoos and aquaria, however, behavior is mostly influenced by other factors, such as daily husbandry routines [24,25], social parameters [26], external disturbances [27], enrichment [28][29][30], human-animal interactions [31], the presence of visitors [32], and the animals' personalities [33][34][35][36]. ...
Article
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Zoos and aquaria must provide optimal husbandry conditions and the highest welfare standards for their animals. How the welfare state of an animal or a group of animals can be precisely assessed is currently under debate, and new approaches are necessary to reliably evaluate changes in welfare. One particular measure that is easily applicable is behavioral observations. However, for dolphins and other cetaceans under human care, reliable behavior-based measures are rare. Using long-term observations of a group of bottlenose dolphins, we investigate how their activity budgets and different behaviors changed over time and are impacted by construction noise. Additionally, we investigate whether behavioral differences are also reflected in changes in the dolphins’ performance during daily training sessions. Our results show that construction noise significantly alters the dolphins’ behavior. Play behavior decreases during construction periods; most importantly, the frequency of fast swimming activities significantly increased, and at the same time, a decrease in training performance is found. Additionally, inter- and intraindividual behavioral differences are attributed to factors, such as age or weaning. Significant changes in a dolphin’s activity budget can also pose potential welfare concerns. Thus, this study highlights the importance of regularly assessing and analyzing the behavior of dolphins under human care. Behavioral observations are essential welfare indicators and can—when complemented with other measures, such as assessment of training performance—provide zoo staff with important information about each individual’s state of welfare.
... Exploratory behavior has been rarely studied in marine mammals. Under human care, environmental enrichment was found to promote exploratory behavior in harbor seals (Phoca vitulina concolor) (Vaicekauskaite, Schneide & Delfour, 2018), gray seals (Halichoerus grypus) (Hunter, Bay, Martin & Hatfield, 2002), and bottlenose dolphins (Tursiops truncatus), with some interindividual variation seen in relation to their different personalities (Birgersson, Birot de la Pommeraye, & Delfour, 2014;Kuczaj, Makecha, Trone, Paulos, & Ramos, 2006), the type of introduced objects (Delfour & Beyer, 2012) and the sex and/or age of the individuals (Eskelinen, Winship, & Borger-Turner, 2015). In wild delphinids, this behavior has been reported in rough-toothed dolphins (Steno bredanensis) (Kuczaj & Yeater, 2007). ...
Article
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Exploratory behaviorincludes all the actions that an animal performs to obtain information about a new object, environment,or individual through using its different senses of perception. Here, we studied the development of the exploratory behavior of a bottlenose dolphin (Tursiops truncatus) calf aged from 39 to 169 days by investigating its acoustic productions in relation to an immersed object handled by a familiar human without without the calf being isolated from the original social group. The study was conducted between July 2015 and January 2016 at Parc Asterix dolphinarium (Plailly, France). Simultaneous audio and video recordings were collected using a waterproof 360° audio-video system named BaBeL,which allows localization of the dolphin that is producing sounds. During 32 recording sessions, for a total duration of 6 hr55 minof audio-video recordings, 46 click trains were attached to individual dolphins: 18 times to the calf, 11 times to its mother,and 17 times to another dolphin in the pool. When comparing the calf’s acoustical production to its mother’s, no significant differences were found in their click rate,mean click duration, or mean interclick interval (ICI). However, linear regression showed that calfs’ click ratesincreased with age and mean ICI decreased with age, probably due to an increase in its arousal. This nonintrusive methodology allows the description and analysis of acoustic signal parameters and acoustic exploratory behaviorof a dolphin calf within its social group.
... As Domino showed more interest toward the device, the effect caused by its presence was stronger on his activity than on Molly's. Individual preferences towards enrichment items were previously observed (Delfour & Beyer, 2012;Eskelinen et al., 2015) and differences in personality in dolphins have been documented (Highfill & Kuczaj, 2007). It is difficult to say if the camera and the enrichment device were simply not the type of objects which Molly was interested in. ...
Article
Cognitive enrichment aims to provide animals with opportunities to use their cogni- tive skills and to promote behaviors associated with positive wellbeing. Cooperation in mammals has been recorded during various behavioral contexts such as hunting, mating, playing, and parental care. Coordinated activity, often with some level of problem‐solving action included, is required during cooperation. To investigate dol- phins’ ability for collaborative problem‐solving, an enrichment device was introduced to two adult male Indo‐Pacific bottlenose dolphins (Tursiops aduncus). The device contained fish and ice and was designed to be opened by simultaneously pulling on both ends. After repeated presentation, it became apparent that only one dolphin had active interest in the device. To facilitate opportunities for problem‐solving by this individual, an alternative collaborator, a human partner, was provided. Still, both dolphins had access to the device throughout the entire experiment. After the first opening, the same dolphin was highly successful in collaborating with the human in both joined (93%) and delayed (100%) partner conditions. The device provided a novel opportunity for the dolphin to use his cognitive skills. Even though only one dolphin participated actively, both dolphins showed varying degrees of interest to the device throughout the study. Both dolphins spent an average of 48% and 16% of their time, respectively, with the device, which resulted in a significant decrease in their other two most frequently observed behaviors: swimming and poolside observation. As a novel cognitive challenge, the device may be considered as a type of cognitive enrichment.
... Exploratory behavior has been rarely studied in marine mammals. Under human care, environmental enrichment was found to promote exploratory behavior in harbor seals (Phoca vitulina concolor) (Vaicekauskaite, Schneide & Delfour, 2018), gray seals (Halichoerus grypus) (Hunter, Bay, Martin & Hatfield, 2002), and bottlenose dolphins (Tursiops truncatus), with some interindividual variation seen in relation to their different personalities (Birgersson, Birot de la Pommeraye, & Delfour, 2014;Kuczaj, Makecha, Trone, Paulos, & Ramos, 2006), the type of introduced objects (Delfour & Beyer, 2012) and the sex and/or age of the individuals (Eskelinen, Winship, & Borger-Turner, 2015). In wild delphinids, this behavior has been reported in rough-toothed dolphins (Steno bredanensis) (Kuczaj & Yeater, 2007). ...
Article
Full-text available
Exploratory behaviour includes all the actions that an animal performs to obtain information about a new object, environment or individual through using its different senses of perception. Here, we studied the development of the exploratory behaviour of a bottlenose dolphin (Tursiops truncatus) calf aged from 39 to 169 days, by investigating its acoustic productions in relation to an immerged object handled by a familiar human without isolation from its original social group. The study was conducted between July 2015 and January 2016 at Parc Asterix dolphinarium (Plailly, France). Simultaneous audio and video recordings were collected using a waterproof 360° audio-video system named BaBeL which allows localization of the dolphin that is producing sounds. During 32 recordings sessions, for a total duration of 6 hours 55 minutes of audio-video recordings, 46 click trains were attached to individual dolphins: 18 times to the calf, 11 times to its mother and 17 times to another dolphin in the pool. When comparing the calf’s acoustical production to its mother’s, no significant differences were found in their click rate, mean click duration, or mean interclick interval (ICI). However, linear regression showed that calf’s click rate increased with age and mean ICI decreased with age, probably due to an increase in its arousal. This non-intrusive methodology allows the description and analysis of acoustic signal parameters and acoustic exploratory behaviour of a dolphin calf within its social group.
... Finally, similarly to previous studies with primates (Bloomsmith et al., 1990;Bloomsmith & Lambeth, 2000), future research should examine the effectiveness of this form of enrichment in various social grouping of killer whales as well as with other individuals. Not all enrichment is equally enriching for individual animals (Delfour & Beyer, 2012;Eskelinen et al., 2015), and the effectiveness of this form of enrichment should be replicated with other individual killer whales as well as other cetaceans. Perhaps visual media could be used to promote social interactions between animals, to model new behaviors that the killer whales might attempt to replicate, or simply provide an option to investigate within their environment. ...
Article
Environmental enrichment is critical for maintaining cognitive welfare for animals in human care but is subject to individual preferences. The interest in a video-based enrichment was assessed for a single killer whale (Orcinus orca) in human care. The adult female was presented 20 video recordings featuring cetaceans, elephants, or humans with each video presented in two conditions: (1) with sound and (2) without sound. Four additional presentations in which the television displayed a blank screen served as controls. All sessions were videotaped and coded for time spent viewing the recordings, behavioral responses, and visual laterality. The killer whale spent significantly more time at the television when programs were on screen compared to when the television was present but blank. She was more likely to watch videos accompanied by sound than those presented without sound. Videos were more likely to be viewed monocularly rather than binocularly, with a right eye preference when viewing the videos the first time they were presented. The highest rates of behavioral responses occurred during videos of cetaceans. These results demonstrate that one killer whale responded to video recordings of different stimuli, suggesting that video recordings may be used as a form of enrichment for cetaceans and that not all video content and formats are equally interesting.
... The analyses of reinforcement in the CA indicated that behaviors associated with primary reinforcement alone versus primary and secondary reinforcement were emitted under a non-specific context most frequently, suggesting that some of the secondary reinforcers were not conditioned effectively. Reinforcing value varies among individuals, and some environmental enrichment devices, which may be used as secondary or learned reinforcers, may not actually be reinforcing to animals (Delfour & Beyer, 2012;Eskelinen, Winship, & Borger-Turner, 2015). Although an arduous task, identifying what was reinforcing to each study subject, specifically in terms of secondary reinforcement, may have influenced the findings of this study. ...
Article
When analyzing animal behavior, it is important to consider the influence of learning principles. The create response of bottlenose dolphins, elicited by a discriminative stimulus, or an SD (visual cue presented to an animal by a trainer), has been described as an elective, often novel response based on arbitrary preferences of individual animals. The goal of this study was to identify the potential influence of reinforcement theory, response class, and primacy and recency on the create responses of bottlenose dolphins. Three, male subjects with an established mastery of the create paradigm, identified in this study as a non-specific, non-repeat contingency, were assessed over the course of two months while under stimulus control (pre-assessment), followed by evaluations of the create response (create assessment) using a double-blind sampling model. During the pre- and create assessments, each response was quantified regarding response class, frequency of request, and reinforcement type, frequency, and magnitude. When presented with the create SD, the dolphins elected to produce behaviors predominantly associated with the more recent training context (create assessment) versus behaviors associated with training that occurred months prior (pre-assessment), which may demonstrate the effects of primacy versus recency. Additionally, the create trials were associated with reinforcement on a high frequency and magnitude, fixed, low ratio schedule, and the subjects most often performed the behaviors associated with the greatest magnitude of primary reinforcement, which highlights the influence of reinforcement and the law of effects. Lastly, two subjects never responded with high energy behaviors in the create contingency, and one subject performed significantly more low and medium energy responses when compared to high energy behaviors, capturing the effects of a response class characterized by intensity under a fixed ratio reinforcement schedule. Thus, the create response was not represented by arbitrary elective preferences but rather, partially driven by the learning theories examined.
... Bottlenose dolphins (Tursiops truncatus) have been the primary subjects with results indicating that human ratings of dolphins can be consistent across raters and over time. To date, individual differences have been reported for specific behaviors, including pectoral fin contact (Dudzinski et al., 2012) and responses to familiar and unfamiliar stimuli or preferences for specific environmental enrichment devices by dolphins (Delfour and Beyer, 2012;Eskelinen et al., 2015;Yeater et al., 2014). Only one study evaluated the consistency of dolphin traits, using adjective-based, trainer ratings over an almost two-year period that also included a major environmental catastrophe and a relocation (Highfill and Kuczaj, 2007). ...
Article
The topic of individual differences in animal behavior has garnered a great deal of recent attention across many species, but questions remain concerning the degree to which behavioral differences vary over time or by age and sex. The present study focused on white whales (Delphinapterus leucas), a species in which a high degree of behavioral variability may be expected due to the fact that belugas are large-brained, long-lived, and highly social in nature. A suite of 23 behavioral measures related to boldness, playfulness, sociability, and other traits were assessed in 41 seaquarium-based belugas that were housed in mixed age/sex grouping. The goals were to assess consistency within individuals over time as well as variations by age and sex. Nineteen of the 23 measures showed significant within-subject consistency over time, suggesting that stable behavioral differences appear to exist in this species. However, very few measures showed significant correlations with each other, indicating that they could not be grouped into identifiable factors that comprised recognizable clusters. It is suggested, therefore , that individual differences are best viewed as a complex array of characteristics that depend on an in-dividual's age and contextual variables that influence the degree to which specific sets of behaviors are expressed and co-vary.
... Performing animals spend most of their time off-stage, and these hours would be more enriching if behavior research was a priority of the performance paradigm. In a review of behavioral enrichment strategies for marine mammals, Clark (2013) identified a menu of cognitive tasks that challenge the skills of dolphins and sea lions, an improvement over more passive forms of enrichment that lead to rapid habituation (Delfour and Beyer 2012). Clark further suggested that complex behavioral challenges could compensate for the fundamental limitations of housing marine mammals in restricted aquatic environments. ...
Article
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Zoos, aquariums, and other captive animal facilities offer promising opportunities to advance the science and practice of behavior analysis. Zoos and aquariums are necessarily concerned with the health and well-being of their charges and are held to a high standard by their supporters (visitors, members, and donors), organized critics, and the media. Zoos and aquariums offer unique venues for teaching and research and a locus for expanding the footprint of behavior analysis. In North America, Europe, and the UK, formal agreements between zoos, aquariums, and university graduate departments have been operating successfully for decades. To expand on this model, it will be necessary to help zoo and aquarium managers throughout the world to recognize the value of behavior analysis in the delivery of essential animal health and welfare services. Academic institutions, administrators, and invested faculty should consider the utility of training students to meet the growing needs of applied behavior analysis in zoos and aquariums and other animal facilities such as primate research centers, sanctuaries, and rescue centers.
... For example, for a species that is generally human-shy in captivity and where the group is managed extensively, a pertinent question might be whether they show increased negative biases during days/periods when keepers or maintenance staff enter the enclosure. Individual differences such as personality and social hierarchy should be taken into account when imposing experimental manipulations to alter welfare state: if the effect of enrichment was being tested, experimenters should be aware that individuals with different personalities might perceive the resource in different ways, and that access to the enrichment itself might be dictated by position in the social hierarchy [15,112,113]. ...
Article
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Cognitive bias testing measures how emotional states can affect cognitive processes, often described using the “glass half-full/half-empty” paradigm. Classical or operant conditioning is used to measure responses to ambiguous cues, and it has been reported across many species and contexts that an animal’s cognitive bias can be directly linked to welfare state, e.g., those in better welfare make more optimistic judgements. Cognitive bias testing has only recently been applied to animals and represents a key milestone in welfare science: it is currently one of the only accurate methods available to measure welfare. The tests have been conducted on many farm, laboratory, and companion animal species, but have only been carried out in zoo settings a handful of times. The aims of this review are to evaluate the feasibility of cognitive bias testing in zoos and its potential as a tool for studying zoo animal welfare. The few existing zoo cognitive bias studies are reviewed, as well as those conducted on similar, non-domesticated species. This work is then used to discuss how tests could be successfully designed and executed in zoo settings, which types of tests are most appropriate in different contexts, and how the data could be used to improve animal welfare. The review closely examines the many variables are present in the zoo which cannot be controlled as in other settings, termed here the Zoo Environment (ZE) Variables. It is recommended that tests are developed after consideration of each of the ZE Variables, and through strong collaboration between zookeepers, managers, and academic institutions. There is much unexplored potential of cognitive bias testing in the zoo setting, not least its use in investigating animal welfare in zoos. It is hoped that this review will stimulate increased interest in this topic from zoo managers, scientists, and industry regulators alike.
... This differentiation allows us to test for the preference of these calves for natural or manmade objects (Greene et al., 2011). This last classification could be particularly useful in environmental enrichment studies, especially in studies related to object manipulation and its welfare implications in an effort to increase behavioral opportunities to benefit the inhabitants of captive centers (e.g., Cappiello et al., 2018;Delfour & Beyer, 2011;Delfour et al., 2017;Neto, Silveira, & Dos Santos, 2016). ...
Article
This research focused on different aspects of play behavior including ethogram, ontogeny, and individual differences, in one male and one female captive bottlenose dolphin calves (Tursiops truncatus) from November 2003 to June 2004. We presented the first peer-reviewed hierarchical description of a play ethogram in bottlenose dolphin calves which behaviors were grouped into three hierarchical levels: two categories -solitary and social play (intraspecific and interspecific play)-, four subcategories -locomotor, object, bubble play, and in the presence of humans-, and 35 play entries. This research was conducted in two phases: descriptive and quantitative. During the descriptive phase –from three to five months old-, we described 29 play entries. During the quantitative phase -from six to 10 months old – we described six new play entries. All social and solitary locomotor behaviors appeared when animals were three months old. Conversely, more complex behaviors concerning with play with objects, bubbles, and in the presence of humans were observed for six months old. There were not statistically significant intra-individual and inter-individual differences in the play behavioral diversity, in the time invested in play and in the Shannon’s evenness index. However, we observed statistically significant inter-individual but not intra-individual differences for the Shannon’s diversity index. The resulting ethogram offers a practical tool as a field guide or reference for quantitative research, for teaching of bottlenose dolphin behavior, and for facilitating the progress toward development of a complete ethogram in wild or captive bottlenose dolphin and other cetaceans, due to play might be applied as a welfare indicator and a tool to improve welfare.
... Certain types of structural enrichment may While not everyone agrees whether marine mamhave some limitations. One study examined the mals, especially cetaceans, should be kept under introduction of 21 familiar objects to a group of managed care, everyone does agree that these anibottlenose dolphins at a marine park (Delfour mals need to live enriched lives, with care taken to & Beyer, 2012). Their results revealed that the ensure an enriched social and physical environment dolphins only interacted with about half of the (as for all species living under the care of humans). ...
Article
Central to the growing concern for animal welfare is the need to enrich the lives of animals living in enclosed settings, including marine mammals whose lives in human care (i.e., captivity) have come under heavy scrutiny in recent years. This article is a brief review addressing environmental enrichment, its link to animal welfare, and its application to marine mammals. We define environmental enrichment and address the factors that call for it. Additionally, we highlight the role that research and zoos play in implementing enrichment. Finally, we address factors to take into consideration regarding environmental enrichment for marine mammals, including a review of different types of environmental enrichment.
Article
Environmental enrichment is a crucial element for the promotion of welfare of animals kept under human care. While a large variety of environmental enrichments has been proposed and studied for terrestrial animals, including a growing area represented by acoustical enrichment such as music, the same is not true for marine mammals. The purpose of this study was to evaluate the ability of classical music to act as an enrichment for bottlenose dolphins under human care (Tursiops truncatus); its effect on the dolphins’ behaviour were compared with that of a less complex auditory stimulus (rain sound), another novel, but visual enrichment (slideshow of photographs), and an already known form of enrichment (floating objects). The study was conducted on 8 dolphins housed in a dolphinarium in Riccione, Italy. Enrichments were provided for 20 minutes/day, on 7 days for each enrichment type. Their effect was evaluated by observing changes in behaviours expressed during or shortly after the provision of the enrichment. Some effects were unspecific, being shared by most, or all types of enrichment, including an increase of activity levels and synchronous swimming. However, only classical music was able to increase several social affiliative behaviours both during its presentation and after its removal. The results indicate that classical music has positive effects on behaviour, that qualify it as an effective environmental enrichment for dolphins in this context. Some aspects remain to be elucidated, including the mechanisms by which music exerts its effects, and how specific to classical music the latter are. Nonetheless, the specificity of effects on social behaviour suggest that classical music could be particularly useful when an improvement in social behaviours is needed.
Poster
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Poster presenting the results of a study of the impact of environmental changes and anthropogenic factors on the social play of bottlenose dolphins under human care.
Thesis
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Bottlenose dolphins are highly social cetaceans that strongly rely on acoustic communication and signaling. The diversity of sounds emitted by the species has been structurally classified in whistles, clicks and burst-pulsed sounds, with some whistles called « signature whistles » that are used as cohesion calls. During this thesis, we developed an easily deployable system that identifies the animal producing sound and allows simultaneous underwater behavioral observations. We tested this methodology with bottlenose dolphins infreedom and in captivity. The present doctoral thesis aims to better understand the communication of bottlenose dolphins within their social group. First, I developed two studies to describe how the signature and non-signature whistle rate of captive dolphins varies in relation to behavior and interaction with humans. Secondly, I present the design and implementation of an innovative methodology (BaBeL system) that allows the localization of vocalizing dolphins in a three-dimensional environment, and which can be used in captivity and with free-range dolphins. Finally, I present two applications of this location methodology to address research questions regarding the exploratory behavior of a young dolphin and the use of vocalizations for coordinated movements in bottlenose dolphins.
Article
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Cetaceans are long-lived, social species that are valued as ambassadors inspiring the public to engage in conservation action. Under professional care, they are critical partners with the scientific community to understanding the biology, behavior, physiology, health, and welfare requirements of this taxonomic group. The Cetacean Welfare Study was a highly collaborative research effort among zoos and aquariums accredited by the Alliance for Marine Mammal Parks and Aquariums and/or the Association of Zoos & Aquariums that provided important empirical and comparative information on the care and management of cetaceans. The goal was to identify factors that were related to the welfare of bottlenose dolphins and to develop reference intervals and values for common and novel indicators of health and welfare for common bottlenose dolphins ( Tursiops truncatus ), Indo-Pacific bottlenose dolphins ( Tursiops aduncus ), beluga whales ( Delphinapterus leucas ), and Pacific white-sided dolphins ( Lagenorhynchus obliquidens ). Data were collected from cetaceans at 43 accredited zoos and aquariums in seven countries in 2018 and 2019. This overview presents a summary of findings from the initial research articles that resulted from the study titled “Towards understanding the welfare of cetaceans in zoos and aquariums.” With multiple related objectives, animal-based metrics were used to advance frameworks of clinical care and target key conditions that were associated with good welfare of cetaceans in zoo and aquarium environments. As a result of this collaboration, species-specific reference intervals and values for blood variables and fecal hormone metabolites were developed and are freely available in an iOS application called ZooPhysioTrak. The results suggested that environmental enrichment programs and social management factors were more strongly related to behaviors likely indicative of positive welfare than habitat characteristics for common and Indo-Pacific bottlenose dolphins. These findings can be widely applied to optimize care and future science-based welfare practice.
Chapter
Most of the species from the order Cetacea appear to possess advanced cognitive abilities and close social networks and are also likely to experience different affective states comprising of more than just basic emotions. Welfare describes a balance of positive and negative affective states experienced by an individual, and this balance is a good indicator of how it perceives the surrounding environment. In this chapter, we discuss how the first steps in cetacean welfare science are being taken to establish this as a discipline. We discuss the pertinent areas of cetology that merit investigation to form the basis of possible cetacean welfare measures. In this arena of welfare assessment, much of the existing work comes from farm animal science, and this previous experience offers potential tools and techniques which could be adapted for cetaceans. We review these sources of information, make suggestions for relevant investigations and discuss how assessment of cetacean welfare might be accomplished.
Article
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The welfare of a range of terrestrial animals can now be objectively estimated thanks to the well-established, but still expanding, field of welfare science. Despite continuing difficulties regarding definitions, it is generally agreed that welfare is assessed most accurately using multiple "animal-based measures"-that is, those evaluating aspects of the animal itself such as its behaviour. In addition, scientists combining behavioural, physiological, and cognitive animal-based indicators of welfare have found this approach is superior to using one-dimensional measures. But can the same approaches be used for marine mammals, and would assessments of their welfare have the same relevance in captivity as in wild environments? There is no reason why not, and we review the past decades of marine mammal research relevant to welfare, as well as the more recent advances in the field where this topic is starting to be addressed directly. We then use the example of bottlenose dolphins (Tursiops truncatus) to examine what the measures within an all-encompassing (i.e., "comprehensive") welfare assessment might look like. Looking to the future, we suggest directions for developing assessments for captive animals and explore how protocols might differ in wild settings. In conclusion, we find that the first steps are being made towards objectively assessing marine mammal welfare in captivity-through application of terrestrial animal approaches as well as through novel paradigms. Regarding bot-tlenose dolphins, several welfare measures have been proposed and should now be further validated and applied. It is hoped that this review will encourage continued research in marine mammal welfare assessment given the demonstrated initial achievements of bottlenose dolphin welfare studies and the potential for application to many different captive and wild contexts.
Article
The field of welfare science and public concern for animal welfare is growing, with the focus broadening from animals on farms to those in zoos and aquaria. Bottlenose dolphins (Tursiops truncatus) are the most common captive cetaceans, and relevant regulatory standards are principally resource-based and regarded as minimum requirements. In this study, the farm animal Welfare Quality® assessment was adapted to measure the welfare of bottlenose dolphins, with a similar proportion of animal-based measures (58.3%). The 'C-Well®' assessment included eleven criterion and 36 species-specific measures developed in situ at three marine mammal zoological facilities, tested for feasibility and accuracy, and substantiated by published literature on wild and captive dolphins and veterinary and professional expertise. C-Well® scores can be calculated for each measure or combined to achieve an overall score, which allows for the comparison of welfare among individuals, demographics, and facilities. This work represents a first step in quantifying and systematically measuring welfare among captive cetaceans and can be used as a model for future development in zoos and aquaria, as well as a means to support benchmarking, industry best practices, and certification.
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Animal welfare is a high priority for pet owners and accredited zoos and aquariums. Current approaches to measuring welfare focus on identifying consensus among behavioral and physiological indicators of positive and negative emotions. Environmental enrichment is a common strategy used to improve the welfare of captive animals. In enrichment programs, knowledge of an animal’s ecology and individual history are applied to modify the animal’s current environment and management to increase environmental complexity, make the environment more functional or natural, and increase behavioral opportunities. While enrichment techniques for primates and large mammals are well-studied, reptile enrichment has received little attention to date despite a few promising studies. In this study, we monitored the responses of 16 leopard geckos to five types of enrichment (Thermal, Feeding, Olfactory, Object, and Visual) using a repeated-measures design. We measured both specific behaviors we expected to change in response to each enrichment type and four behavioral indicators of welfare: exploratory behavior, species-specific behaviors (behavioral thermoregulation and hunting), behavioral diversity, and abnormal repetitive behaviors. We found geckos interacted with all five types of enrichment at above-chance levels (i.e., no 95% CIs for engagement time overlapped with 0 sec). Geckos spent more time interacting with Thermal and Feeding enrichment than the other types (F(4,60) = 49.84, p < 0.001). Thermal, Feeding, Olfactory, and Object enrichments (but not Visual enrichment) changed specific relevant behaviors (e.g., Thermal enrichment altered thermoregulatory behaviors, Wilk’s lambda = 0.25, F(3,13) = 13.39, p < 0.001) and improved behavioral indicators of welfare (e.g., behavioral diversity, Wilks’ lambda = 0.30, F(12,178) = 12.31, p < 0.001). These results suggest that geckos respond to environmental enrichment, that their responses are predictable based on their ecology, and that environmental enrichment improves gecko welfare. As in mammals and birds, enrichments that address behavioral needs (here: thermoregulation and feeding) appear more effective than enrichments that simply provide novel stimuli to increase exploration. The extent to which our results can be generalized to other reptile species awaits further study, but we suggest that enrichment should be more widely used to improve reptile welfare.
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Group sizes, group composition, and association patterns of bottlenose dolphins (Tursiops truncatus) were investigated in the San Luis Pass area (Sep. 1995- Aug. 1996) of the Galveston Bay Estuary to examine differences in community structure of individuals inhabiting different portions of the estuary. Group sizes (n = 83) ranged from 1 to 29 (x̄ = 10.6) and were seasonally variable, with the largest groups occurring in spring (x̄ = 16.3) and the smallest groups during the fall (x̄ = 6.3). Seventy-one individuals were identified using photoidentification, and the sex of six dolphins (three males, three females) was determined. At least 31 (48.4%) groups were of mixed sex. Twenty-nine dolphins that were identified five or more times were used to calculate half-weight coefficients of association (COAs), which ranged from 0.00 to 0.83 (x̄ = 0.46). Coefficients of association for male pairs were higher than COAs for female and mixed-sex pairs. Permutation tests were performed to test for nonrandom associations and presence of preferred or avoided companions. The null hypothesis of random association was rejected, indicating that dolphins preferentially associated with some individuals and avoided others. In all replicates, three known-male pairs had significantly large COAs. These preliminary results suggested that, excluding mother-calf pairs that were not examined, male pairs formed the most stable social bonds.
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Cetaceans display considerable patterns of bubble formation and manipulation for different purposes. While position and acoustic functions of bubbles have been extensively discussed, few details are known about their use in playing behaviour. The aim of the present work was to conduct a systematic observational study on a novel pattern of fluke-made bubble rings (FBR) and associated play be-haviour in two captive calves of Tursiops truncatus. The birth of two, half-siblings bottlenose dolphins less than one month apart in the same aquarium presented a good opportunity to address the issue of individual differences and possible mimicry of such behaviour. Focal animal sampling (Altmann, 1974) sessions lasting 15 min were carried out for each calf according to a decreasing temporal schedule. The following parameters were scored and obtained for each calf: (a) mean frequency of FBR per session, (b) FBR by time of day, and (c) frequency of FBR associated play behaviour per session. FBR formation appeared to be, for both animals, a two-phase action producing a loud per-cussive sound. A trend in the mean frequency of FBR suggests a possible seasonal negative relation-ship with human activities. Moreover, the two calves usually were seen together and mimicked each other during FBR formation. Finally, 7 differ-ent behavioural categories were observed after FBR formation and their sequence appeared to be well defined. In conclusion, this paper describes a novel form of play in two bottlenose dolphin calves. Even though data are limited by a small sample size and are only suggestive, they do indicate that FBR formation and the calves' ability to manipulate bubble rings could reflect the learning flexibility of the young dolphins and implies a high behavioural versatility.
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GAP analyses are tools used to inform us about the short-comings of a scientific area or necessities in social–economic problems. In the last 20 years, environmental enrichment as an area of scientific investigation has come of age; this can be clearly seen by the number of publications produced in this area. For example, a search on the database The Web of Science©, using the keywords “environmental enrichment”, from 1985 to 2004 produced 744 articles. In this study we analysed these 744 articles and classified them by year into: type of environment (e.g., zoo, farm and laboratory); taxonomic classification (e.g., mammal, bird, etc.); type of enrichment (e.g., food, sensory, etc.); subject area (e.g., neurosciences and agriculture); country of publication; and gathered data on experimental design (e.g., sample sizes). Furthermore, we collected similar data on animal well-being and animal conservation for comparative purposes (keywords: “animal well-being” and “animal conservation”). The results from this study show that the number of environmental enrichment studies has been steadily increasing from a low level in the 1980s until 1999, when there was a noticeable acceleration in the number of articles published. Largely, this acceleration was a response to the growing interest in environmental enrichment by neuroscientists. The data also show a relative lack of, and recent decline in, publications in the area of agriculture. Thus, the data suggest a need for more research on enriching the lives of farm animals. Environmental enrichment publications over the 20 years of the study corresponded to 27% of all animal well-being publications in the period. One interesting comparison between enrichment and animal well-being revealed the virtual absence of research in animal well-being by neuroscientists. The detailed results of this study will help in identifying gaps in our knowledge about environmental enrichment, and how experimental designs might be improved.
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To study animal welfare empirically we need an objective basis for deciding when an animal is suffering. Suffering includes a wide range ofunpleasant emotional states such as fear, boredom, pain, and hunger. Suffering has evolved as a mechanism for avoiding sources ofdanger and threats to fitness. Captive animals often suffer in situations in which they are prevented from doing something that they are highly motivated to do. The “price” an animal is prepared to pay to attain or to escape a situation is an index ofhow the animal “feels” about that situation. Withholding conditions or commodities for which an animal shows “inelastic demand” (i.e., for which it continues to work despite increasing costs) is very likely to cause suffering. In designing environments for animals in zoos, farms, and laboratories, priority should be given to features for which animals show inelastic demand. The care ofanimals can thereby be based on an objective, animal-centered assessment of their needs.
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Environmental enrichment is a vague concept referring to improvements to captive animal environments. Some authors have applied the term to an environmental treatment itself, without any concrete evidence that the treatment represented an improvement for the animals. Others have used the term when the main beneficiaries may have been people rather than their captive animals. The criteria used to assess enrichment have also varied according to animal use (e.g. laboratory, farm or zoo animals). In this paper, environmental enrichment is defined as an improvement in the biological functioning of captive animals resulting from modifications to their environment. Evidence of improved biological functioning could include increased lifetime reproductive success, increased inclusive fitness or a correlate of these such as improved health. However, specifying an appropriate endpoint is problematic, especially for domestic animals. Potential methods of achieving enrichment that require further investigation include presenting food in ways that stimulate foraging behaviour and dividing enclosures into different functional areas. The quality of the external environment within the animals' sensory range also deserves greater attention. A common shortcoming of attempts at environmental enrichment is the provision of toys, music or other stimuli having little functional relevance to the animals. Failure to consider the effects of developmental factors and previous experience can also produce poor results. Environmental enrichment is constrained by financial costs and time demands on caretakers, and providing live prey to enrich the environment of predators raises ethical concerns. Future research on environmental enrichment would benefit from improved knowledge of the functions of behaviour performed in captivity and more rigorous experimental design.
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The zoo scientific community was among the first to focus attention on captivity-induced stereotypic behaviors, their causes, and methods of eradication. Environmental enrichment has emerged recently as the main husbandry tool for tackling this problem. An increasing number of research publications have attempted to evaluate the effectiveness of enrichment in reducing stereotypic behavior and to develop further concepts to explain how effective enrichment works. A review and meta-analysis of this literature indicates that enrichment is a successful technique for reducing stereotypic behavior in zoo animals. Enrichment was associated with significant reduction in stereotypy performance about 53% of the time. Published enrichment and stereotypy research is lacking for most zoo species, with most studies on large, charismatic, and often endangered species, but it is unclear whether stereotypies are more prevalent in these species. In addition, problems with scientific methods and data presentation, quantitatively detailed in this work, severely limit the conclusions drawn from zoo research. Further understanding of what kinds of enrichment works and what doesn't will require greater attention to experimental design, sample size, statistical analysis, and better descriptions of enrichment properties and the form of stereotypy. We recommend that future studies focus on increasing sample size (e.g., through multi-institutional studies), appropriate repeated measures design (e.g., with multiple baseline and experimental phases), providing full statistical information about the behavioral changes observed (including standard error), and ultimately the development of a predictive science for enrichment, stereotypies, and wellbeing. Zoo Biol 0:1–20, 2005. © 2005 Wiley-Liss, Inc.
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This case study examined the effect of environmental enrichment on the activity budgets of a male and female Australian Sea Lion (Neophoca cinerea) housed together at Adelaide Zoo. Using non-food-related (intrinsic) and food-related (extrinsic) enrichment objects, the study conducted an ABABA (withdrawal) experimental design over a 30-day period (180 hr). The study expected extrinsically reinforcing objects to be more effective than intrinsically reinforcing objects in reducing pattern swimming. The male sea lion spent more than 45% of scans engaged in pattern swimming during the initial baseline, which was reduced by at least 25% when enrichment items were present. However, there was no evidence of stereotypic behavior in the female sea lion, indicating that individual differences may exist. When enrichment was present, the study observed more active behaviors in both nonhuman animals. They spent more time interacting with the non-food-related objects overall. Therefore, introducing simple enrichment devices offers a cheap, practical, and effective method of adding complexity to the environment, which is likely to benefit the animals' welfare and enhance the zoo-visitor experience.
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In these papers we mainly consider how analyses of social play in nonhuman animals (hereafter animals) can inform inquiries about the evolution of cognitive mechanisms. Social play is a good behavioral phenotype on which to concentrate for when animals play they typically perform behavior patterns that are used in other contexts (e.g. predation, aggression, or reproduction). Thus, individuals need to be able to tell one another that they do not want to eat, fight with, or mate with the other individual(s), but rather, they want to play with them. In most species (primarily mammals) in which play has been observed, specific actions have evolved that are used to initiate or to maintain play. Furthermore, sequences of play usually differ from nonplay sequences (within species) and self-handicapping has also been observed, in which, for example, dominant individuals allow themselves to be dominated _only_ in the context of play. In our consideration of how play is initiated and maintained, we discuss issues including the evolution of play, the ecology of play, the sorts of information that are shared during play, what cognitive psychologists who study humans can learn from cognitive ethologists who study other animals, and what play can tell us about the emergence of mind in animals. These essays draw on literature from ethology, psychology, and philosophy.
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Enrichment can increase the complexity of the captive environment and possibly enhance captive animals' well-being by stimulating active behaviors and reducing stereotypical behaviors commonly seen in zoo felids. In this study, three different enrichment items were added to outdoor enclosures of felids at the Montgomery Zoo to test their effects on activity levels and stereotypic pacing. Bones, frozen fish, and spices (cinnamon, chili powder, and cumin) were presented over a 3-month period to six species of felids: cheetah, cougar, jaguar, lion, ocelot, and tiger. Proportion of time spent engaging in active behaviors and stereotypic pacing were compared before, during, and after treatments. All treatments resulted in a significant increase in activity level from baseline (bones: +15.59%; frozen fish: +35.7%; spices: +12.38%). Effects of enrichment items on activity levels were not sustained 7 days after removal. Proportion of time spent pacing significantly decreased during presentation of spices (-21.25%) and frozen fish (-26.58%), but not with the addition of bones. However, only the effect of frozen fish on stereotypic behavior was sustained 7 days after removal of the enrichment item. In conclusion, bones, spices, and frozen fish are inexpensive and easy-to-administer enrichment items that may be used to increase active behaviors of captive felids. Zoo Biol 26:371-381, 2007. (c) 2007 Wiley-Liss, Inc.
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In the wild, walrus calves are occupied with many behaviors necessary for survival. In captivity there is usually less to occupy them. Therefore it is necessary to develop other ways to occupy the animals to prevent negative behavior. In the present study, food in four different types of dispensers were tested on two walrus calves: fish in ice, fish in a nine-hole container, fish in a two-hole container, and fish in ice in a one-hole container. All four methods of offering fish had an effect on the animals' behavior. There were differences in the way the two animals responded to each of the four dispensers. The dispensers occupied one animal on average between 32-95% of the 90-min test periods, and the other animal for between 14-57% of the test periods. Due to the effect of learning and rapid development of the calves, which were shifting from a 100% formula diet to a 100% fish diet during the study period, the four methods cannot be compared. Besides the time feeding methods occupy animals, the practicality of a dispenser determines how often it will be used by the keepers. Of the four dispenser types tested in the present study, the nine-hole container was the most practical and was still used frequently by the keepers years after the study. Zoo Biol 0:1-12, 2007. (c) 2007 Wiley-Liss, Inc.
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The term "welfare" refers to the state of an individual in relation to its environment, and this can be measured. Both failure to cope with the environment and difficulty in coping are indicators of poor welfare. Suffering and poor welfare often occur together, but welfare can be poor without suffering and welfare should not be defined solely in terms of subjective experiences. The situations that result in poor welfare are reviewed in this study with special reference to those in which an individual lacks control over interactions with its environment. The indicators of poor welfare include the following: reduced life expectancy, impaired growth, impaired reproduction, body damage, disease, immunosuppression, adrenal activity, behavior anomalies, and self-narcotization. The uses of measures of responsiveness, stereotypies, and animal preferences in welfare assessment are discussed. The need to make direct measurement of poor welfare as well as to use sophisticated studies of animal preferences is emphasized.
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Research on the cognitive capacities of dolphins and other cetaceans (whales and porpoises) has importance for the study of comparative cognition, particularly with other large-brained social mammals, such as primates. One of the areas in which cetaceans can be compared with primates is that of object manipulation and physical causality, for which there is an abundant body of literature in primates. The authors supplemented qualitative observations with statistical methods to examine playful bouts of underwater bubble ring production and manipulation in 4 juvenile male captive bottlenose dolphins (Tursiops truncatus). The results are consistent with the hypothesis that dolphins monitor the quality of their bubble rings and anticipate their actions during bubble ring play.
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This study considers the use of nonsocial environmental enrichment by captive chimpanzees at the Primate Foundation of Arizona. The goal was to determine whether a relationship existed between controllability of enrichment items by captive chimpanzees and frequency of use. The study measured controllability, the ability of nonhuman animals to alter aspects of their environment by the potential destructibility of the enrichment item. This study examined additional factors that may affect enrichment use: individual age, sex, rearing history, social group composition, and availability of outdoor access. The chimpanzees in the study used destructible items--the enrichment category with the highest level of controllability--more than indestructible items across all age, sex, and rearing classes. Thus, controllability seems to be an important factor in chimpanzee enrichment. Younger individuals and groups with outdoor access used enrichment more than did older individuals and groups with indoor-only access. Individual sex, rearing history, and social group composition had minimal effects on enrichment use. These results support the importance of control to captive chimpanzees and further enable captive management to customize enrichment programs to the needs of particular animals.
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The polar bear (Ursus maritimus) in most zoos attracts high levels of public attention and can play an important role in conservation education. Polar bears in the wild are typically solitary; bears in captivity often house socially. This study reported behavioral evidence on how bears manage this situation and whether proximity leads to aggression. The study recorded location and behavior once per minute for 106 hr for 2 female polar bears at the Philadelphia Zoo; the samples represented all times of day bears spent in the enclosure (off-exhibit time spent in separate, indoor dens). When changing locations, 1 bear more frequently moved away from the other, effecting a net increase in interindividual distance. When either bear moved into an adjacent zone, 1 typically moved away. The bears occupied the same enclosure zone for a low proportion of time; proximity did not routinely lead to overt aggression. These data indicate polar bears make behavioral decisions, minimizing aggression, to manage social distance and that enclosure designers for solitary species--to facilitate social avoidance--should consider using topographical complexity and multiple pathways throughout.
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Social animals have to take into consideration the behaviour of conspecifics when making decisions to go by their daily lives. These decisions affect their fitness and there is therefore an evolutionary pressure to try making the right choices. In many instances individuals will make their own choices and the behaviour of the group will be a democratic integration of all decisions. However, in some instances it can be advantageous to follow the choice of a few individuals in the group if they have more information regarding the situation that has arisen. Here I provide early evidence that decisions about shifts in activity states in a population of bottlenose dolphin follow such a decision making process. This unshared consensus is mediated by a non-vocal signal which can be communicated globally within the dolphin school. These signals are emitted by individuals that tend to have more information about the behaviour of potential competitors because of their position in the social network. I hypothesise that this decision making process emerged from the social structure of the population and the need to maintain mixed-sex schools.
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Behavior enables an animal to interact with and survive in its environment. In cetaceans, as in all other animals, sensory systems exist to serve behavior. Perhaps more than most animals, cetaceans may be said to live in two worlds: their physical universe of air and water, and the social universe of the other dolphins around them. Their sensory systems serve them in both. In the physical universe, sensory systems are used in locomotion, foraging, maintaining physical and physiological equilibrium, and so on. In the social universe, sensory systems are used in communication In fact, it might be said that all social behavior constitutes communication.
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In these papers we mainly consider how analyses of social play in nonhuman animals (hereafter animals) can inform inquiries about the evolution of cognitive mechanisms. Social play is a good behavioral phenotype on which to concentrate for when animals play they typically perform behavior patterns that are used in other contexts (e.g. predation, aggression, or reproduction). Thus, individuals need to be able to tell one another that they do not want to eat, fight with, or mate with the other individual(s), but rather, they want to play with them. In most species (primarily mammals) in which play has been observed, specific actions have evolved that are used to initiate or to maintain play. Furthermore, sequences of play usually differ from nonplay sequences (within species) and self-handicapping has also been observed, in which, for example, dominant individuals allow themselves to be dominated _only_ in the context of play. In our consideration of how play is initiated and maintained, we discuss issues including the evolution of play, the ecology of play, the sorts of information that are shared during play, what cognitive psychologists who study humans can learn from cognitive ethologists who study other animals, and what play can tell us about the emergence of mind in animals. These essays draw on literature from ethology, psychology, and philosophy.
Chapter
Understanding and documenting the characteristics and features of the social sounds and associated behavior of free-ranging delphinids has historically been limited by lack of access to animals and poor underwater viewing conditions. Communication studies of delphinids have been undertaken in both captivity (see Herman and Tavolga 1980 for review) and in the wild (Connor et al. 1992; Norris et al. 1994). Even with a wealth of information about dolphin sound production and hearing capabilities from captivity, there are significant gaps in understanding how dolphins detect, decode, and decipher both their environmental and social signals in the wild. Although the abilities of dolphins to actively produce both echolocation signals and social sounds have been documented, little is understood about the sensory exposure and information available to, and utilized by, free-ranging delphinids. One way to address this issue is to review the use of conspecific social signals and behavior. Dolphins, like other animals, have been under evolutionary pressures for increased efficiency in their communication system. By observing critical environmental and social aspects of delphinid society we might gain insight into how these animals learn and selectively filter information in their environment.
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Dolphins have an advanced biosonar. In dolphin exhibits around the world an artificial setting (i.e. pool environment) is the most common mode of display. The bare and static environment in a pool does not provide many acoustic challenges for these animals. The acoustic aspect of a pool holding twelve bottlenose dolphins (Tursiops truncatus) was improved by introducing enrichment devices. The dolphins responded positively to tested acoustic enrichment additions, indicating that this kind of enrichment should be further exploited. The dolphin´s biosonar should be considered when designing facilities and enrichment devices.
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In the wild, animals are exposed to an ever-changing array of sensory stimuli. The captive environment, by contrast, is generally much more impoverished in terms of the sensory cues it offers the animals housed within. In a bid to remedy this, and promote better welfare, researchers have started to explore the merits of sensory stimulation (i.e. stimulation designed to trigger one or more of an animal's senses) as a potential method of environmental enrichment for captive animals. This paper reviews the research in this area, focusing specifically on auditory, olfactory and visual methods of sensory stimulation. Studies exploring the efficacy of each type of stimulation as an enrichment tool are described, where appropriate, making a distinction between those that occur in the animal's natural habitat, and those that do not. Overall, it is concluded that sensory stimulation harbours enrichment potential for some animals housed in institutional settings, although the specific merits gained from these enrichments are likely to depend upon a wide variety of factors including, for example, species, sex, age and housing conditions. Programmes of sensory enrichment that target the dominant sense for the species under scrutiny, using harmless, non-stressful stimuli, are likely to result in the greatest benefits for animal welfare. Stimuli specific to a species’ natural habitat should not always be considered meaningful, or advantageous, to an animal's welfare; in some cases stimuli that do not occur naturally in the wild (e.g. classical music) may offer more in the way of welfare advantages. Shortcomings in the research, and factors to consider when implementing enrichment of this nature, are discussed throughout.
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Environmental enrichment programs provide benefits to both captive animals and the facilities that house them, but cost time and resources to design, implement, and maintain. As yet, there have been few theoretically based guidelines to assist animal care staff in establishing cost-efficient enrichment methods that both elicit the desired behavioral changes and maintain their success over time. We describe several well-studied principles from the field of experimental analysis of behavior, including intrinsic reinforcement, extrinsic reinforcement, habituation, extinction, and schedules of reinforcement that could be very useful for evaluating the short- and long-term effectiveness of enrichment. We use this theoretical framework to generate testable hypotheses and provide examples of enrichment studies relevant to our predictions. In particular, we suggest that enrichment devices that offer extrinsic reinforcement (food, social access, etc. as a result of performing behaviors) should produce greater and more prolonged changes in behavior than devices that rely on the behavior itself being reinforcing to the animal. For techniques that provide no extrinsic reinforcement, using stimuli that are novel, are more different from the environment, have been withheld or altered in some way, or are presented less frequently may help reduce habituation. For techniques that provide extrinsic reinforcement, making reinforcement more difficult to obtain and providing more or higher quality reinforcers may increase the long-term success of the enrichment program. In addition, enrichment may be more effective if animal care staff avoid continuously reinforcing behaviors after they are established, enriching immediately after feeding, and exposing animals to enrichment when reinforcement is no longer available. While the current enrichment literature supports the application of behavior analytic theory, empirical evaluation of many of our predictions is still needed.
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This paper summarises recent findings on the causation of stereotypic behaviours and other abnormal repetitive behaviours (ARBs) in captive animals: primarily motivational frustration and/or brain dysfunction, with possible contributory roles also being played by habit-formation and ‘coping’ effects. We then review the extent to which ARBs occur in zoos and similar, estimating that at least 10000 captive wild animals are affected worldwide. We argue for ‘zero tolerance’ of such ARBs, because stress and poor welfare raise ethical issues, while abnormal behavioural phenotypes and possibilities of impaired brain development challenge both the indirect (e.g. educational) and the direct, intrinsic conservation value of affected animals. We then consider five potential means by which ARBs may be tackled: genetic selection; pharmacological treatment; the reinforcement of alternative behaviours; punishment; and environmental enrichment. All except punishment have potentially useful roles to play, but enrichment is the preferred approach: it is most likely to tackle the problems underlying stereotypic behaviours, and thence to improve both welfare and behaviour with few unwanted side-effects. Nevertheless, in zoos, environmental enrichment to date has only had partial success, with no study managing to abolish ARBs in all its subjects—suggesting either that the enrichments currently being used are never quite optimal, or that by the time they are tackled, ARBs have become resistant to change. We suggest some ways in which the effectiveness of enrichments may be enhanced; propose that certain properties of ARBs may usefully help evaluate their likely ‘treatability’; and emphasise that if improving welfare is more important than just reducing ARB, then additional measures are needed in order to first, reliably identify those individuals most at risk from poor welfare, and then, to fully evaluate the welfare impact of enrichments. This paper also emphasises, with examples, the enormous potential value of zoo-derived data for helping understand how taxon, ecological niche, rearing history, and current housing together affect animals’ responses to captivity.
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This paper presents a framework for analysing the social structure of populations in which interactions between some identified individuals can be observed. Statistics describing the nature, quality and temporal patterning of one or more interaction measures are used to define relationships between pairs of individuals or classes of individual. Multivariate techniques can then be used to display the social structure of the population. These displays indicate the social complexity of the population and can be used to classify relationships and examine patterns of relationship between classes of animal. They can also be used to define and delineate groups. This framework and these techniques should be particularly useful when analysing complex fission–fusion societies, as are found among the primates and cetaceans. 1997 The Association for the Study of Animal Behaviour
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In Odontocetes, bubbleblow is reported in several ethograms but its function is poorly understood. For the five captive beluga whales (Delphinapterus leucas) of the Vancouver Public Aquarium, we recorded the occurrence of this behaviour, its diurnal pattern and individual variability. We suggest that bubbleblow can be considered as a solitary play activity.
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Seven major types of sampling for observational studies of social behavior have been found in the literature. These methods differ considerably in their suitability for providing unbiased data of various kinds. Below is a summary of the major recommended uses of each technique: In this paper, I have tried to point out the major strengths and weaknesses of each sampling method. Some methods are intrinsically biased with respect to many variables, others to fewer. In choosing a sampling method the main question is whether the procedure results in a biased sample of the variables under study. A method can produce a biased sample directly, as a result of intrinsic bias with respect to a study variable, or secondarily due to some degree of dependence (correlation) between the study variable and a directly-biased variable. In order to choose a sampling technique, the observer needs to consider carefully the characteristics of behavior and social interactions that are relevant to the study population and the research questions at hand. In most studies one will not have adequate empirical knowledge of the dependencies between relevant variables. Under the circumstances, the observer should avoid intrinsic biases to whatever extent possible, in particular those that direcly affect the variables under study. Finally, it will often be possible to use more than one sampling method in a study. Such samples can be taken successively or, under favorable conditions, even concurrently. For example, we have found it possible to take Instantaneous Samples of the identities and distances of nearest neighbors of a focal individual at five or ten minute intervals during Focal-Animal (behavior) Samples on that individual. Often during Focal-Animal Sampling one can also record All Occurrences of Some Behaviors, for the whole social group, for categories of conspicuous behavior, such as predation, intergroup contact, drinking, and so on. The extent to which concurrent multiple sampling is feasible will depend very much on the behavior categories and rate of occurrence, the observational conditions, etc. Where feasible, such multiple sampling can greatly aid in the efficient use of research time.