LORI MARINO

The Kimmela Center for Animal Advocacy and President, Whale Sanctuary Project, Kanab, Utah, USA

The problem of cetacean mental health in captivity is widespread as there are over 3,000 odontocetes confined to concrete tanks or small pens for entertainment or research globally (Ceta-Base, 2018). (There are no mysticetes in captivity.) The most common species in captivity are orcas (Orcinus orca), who are actually large dolphins, bottlenose dolphins (Tursiops truncatus), and beluga whales (Delphinapterus leucas), although other species, e.g., pilot whales, white-sided dolphins, harbor porpoises, are also kept. This review will, therefore, focus on orcas, bottlenose dolphins, and belugas as more is known about how these species cope with captivity than any other. However, it appears that the impact of captivity on other dolphin and porpoise species is comparable.

22.2 Who are Cetaceans and What Do They Need to Thrive?

22.2.1 Evolutionary history and phylogeny

Cetaceans evolved from ungulate-like terrestrial ancestors ~50 million years ago (mya) (Fordyce, 2009). Their closest living relatives are hippopotamuses (Geisler and Theodor, 2009). And while there were many morphological adaptations to a fully aquatic existence over the first 10–15 million years of their evolution in the oceans the most significant changes relevant to the issue of mental health occurred ~35 mya when early versions of modern cetaceans evolved much larger and more complex brains than their predecessors (Marino et al., 2004a; Montgomery et al., 2013). Moreover, odontocetes were beginning to evolve echolocation at this time as well (Geisler et al., 2011). These changes led to a radically enhanced level of cognitive abilities and social complexity so that, today, many modern cetacean cultures are among the most complex among nonhumans and certainly older than those of humans (Whitehead and Rendell, 2014). These evolutionary changes in brain size and complexity and behavior have direct relevance to their ability to adapt to captivity.

22.2.2 Brain size and complexity

Cerebral development

Cetacean brains are highly developed and complex and odontocetes are the most highly encephalized nonhuman taxonomic group known, with encephalization quotients ranging from 1.8 to 5.0, i.e., brain sizes from 1.8 to 5 times above expected size (Marino et al., 2004b). In orcas, for instance, the cerebrum constitutes an average of 81.5% of the total brain volume, compared with an average of 76.2% for humans (Wright et al., 2016). Neocortical surface area, measured by degree of gyrification, is also higher in many cetaceans relative to humans (Ridgway and Brownson, 1984). Cytoarchitectonic patterns in cetacean neocortex are far more varied and complex than previously thought and, although very different, rival the complexity found in humans and other primates (Hof et al., 2005).

In addition to the neocortex, the anterior cingulate and insular cortices, the temporal operculum, and paralimbic regions (all situated deep within the forebrain) are well developed in cetaceans (Hof and Van Der Gucht, 2007). The expansion of these areas in humans and other mammals is associated with high-level cognitive and social functions such as attention, prediction, social awareness, and empathy (Hof et al., 2005; Allman et al., 2011). Moreover, recent studies show that the anterior cingulate and insular cortices in larger cetaceans, such as orcas, contain a type of projection neuron, known as a spindle cell or Von Economo neuron (Hof and Van Der Gucht, 2007), which may be involved in social cognition (Allman et al., 2011).

The limbic system and emotional regulation

Recent work has shown that limbic functions in cetaceans are well integrated with other cortical functions (Pessoa and Hof, 2015). In cetaceans, the limbic system has been elaborated into neighboring regions to form a paralimbic lobe, which forms dense connections between core limbic structures, i.e., region of the brain specializing in emotion, memory, and motivation, and higher-order cerebral information processing, problem solving, and communication areas (Marino et al., 2004b).

Sensory systems

All odontocetes have well-developed auditory capacities using a broader range of frequencies than humans (Madsen and Surlykke, 2013). Acoustics, including echolocation, are their primary perceptual modality and, as such, an integral part of their experience of the world (Madsen and Surlykke, 2013). Vision is also well developed in cetaceans with acuity preserved above and below water in almost all species except freshwater dolphins (Madsen and Herman, 1980). Somatosensory perception (sense of touch, pain, body position, temperature) is also important for cetaceans in a number of contexts, including affiliative. Finally, odontocetes lack olfactory bulbs and taste buds and, therefore, do not possess smell or taste (Kishida et al., 2015).

22.2.3 Psychology and behavioral adaptations

Orcas, beluga whales, and bottlenose dolphins are among the most cognitively sophisticated and intelligent animals on the planet. Their large complex brain, far from being a protective feature, is a risk factor for poor coping in captivity because it is essentially impossible to meet their complex needs. Orcas, belugas, and bottlenose dolphins are long-lived in the wild and experience an extended juvenile period of several years (Whitehead and Rendell, 2014). They are sophisticated problem solvers with high-level capacities for intraspecies and interspecies cooperation, and possess complex communicative functions as well as capacities for comprehending and mimicking human language. They live in complex social networks with individual social roles and learned cultural traditions spanning many generations (Connor, 2007; Lusseau, 2007; Whitehead and Rendell, 2014). In all three species, mothers and their offspring stay together during a protracted weaning and post-weaning stage that lasts several years until reproductive maturity (Fedak et al., 2009). In some populations of orcas, mothers and male offspring stay in the same group for life (Foster et al., 2012). Belugas and orcas experience post-reproductive senescence which aligns with the strong matriarchal nature of their groups (Brent et al., 2015; Ellis et al., 2018).

Cetaceans are generally long-distance and deep-diving animals who fully exploit the three-dimensionality of the water space. For instance, belugas migrate over thousands of kilometers (Lydersen et al., 2001) and orcas can travel over 100–200 km/day (Pitman and Durban, 2012). They dive to depths of several to hundreds of meters, depending on the species and population (Lydersen et al., 2001; Ford, 2009; Stewart, 2009; O’Corry-Crowe, 2018). While the opportunity to engage in traveling and diving is clearly related to physical health and conditioning, the need to move and travel is equally a psychological one. The free movement in the three-dimensional world of the ocean provides opportunities for hunting and foraging, as well as exploration, socializing, experiencing challenges, and the expression of choice – all of which are critical to mental health in cetaceans, and all of which are either absent or greatly diminished in marine parks.

Finally, cetaceans, including all three of the species above, not only have deep emotional attachments to each other, but they show clear and strong capacities for empathy both within and across species. Observations of many cetacean species include reports of long-range contact calling when separated from others, grieving behaviors, and epimeletic behaviors (Reggente et al., 2016; Bearzi and Reggente, 2017).

To conclude, the psychology of cetaceans, and particularly the three species most commonly kept in captivity, is one characterized by a keen intelligence and need for stimulation and new challenges through travel, a high reliance upon learning and group care for juveniles, strong emotional ties, and rich cultural traditions. Therefore, the question of mental health in captivity can be addressed by asking whether these are the kinds of beings whose needs could be met in concrete tanks in entertainment parks.

22.2.4 How well are these needs met in captivity?

Cetaceans in marine parks are typically housed in shallow concrete tanks a miniscule fraction of the size of their natural home ranges (Couquiaud, 2005; Rose et al., 2017). For example, the minimum US space standards for orca enclosures of 15 meters for horizontal distance and 4 meters for depth are grossly inadequate for natural movements and postures for adult orcas, who average 6.0–7.6 meters long (Rose et al., 2017). Marine parks and aquariums have claimed that captive cetaceans do not need to travel or dive extensively because their food is provided for them at the surface, ¹ but these statements ignore the physiological adaptations to traveling and diving that need to be met for health and welfare (Clubb and Mason, 2003, 2007; McPhee and Carlstead, 2010). In addition, the barrenness and uniformity of captive display tanks are a striking contrast to the natural environment and do not provide enough challenges or variety in activities to keep an individual stimulated, motivated, and thriving (Couquiaud, 2005).

Captive dolphins and whales are kept in artificially produced groups or ‘collections’ which do not resemble a natural social group. Commonly, individuals of different species and genetic backgrounds are forced together, bred artificially, and separated by transfers to other facilities without regard for social bonds, including those of mothers and their offspring (Waples and Gales, 2002; Rose et al., 2009). Jett and Ventre (2015) showed that captive orcas are at the highest risk of dying between ages 2 and 6 years (when juveniles may be weaned but still socially dependent upon their mother) and suggest that mortality would be reduced by avoiding separation of mothers and calves.

Moreover, unlike in the free-ranging situation, captive cetaceans cannot manage conflict by dispersal and are forced to live in a confined space with individuals they may not get along with (Waples and Gales, 2002; Couquiaud, 2005). The result of such unnatural confinement, artificial group composition, and breeding is heightened social tension and aggression (Sweeney, 1990; Waples and Gales, 2002).

Arguably one of the less obvious but more impactful aspects of the captive environment on cetaceans is the lack of control (i.e., loss of autonomy) inherent in a situation in which movement, feeding, social relationships, and every other facet of everyday life is determined by humans. Feeding and show times are highly scheduled daily events and compliance during performances and husbandry practices is linked to outcome (access to social interaction, amount of food, and access to environmental enrichment, etc.). In addition, captive cetaceans are unable to control the noise of audiences, filtration devices, and other physical and sensory aspects of their artificial environment. Dolphins in ‘petting pools’ and ‘swim-with’ programs are forced to make physical contact with humans who enter what little space they have to themselves (Couquiaud, 2005; Stewart and Marino, 2009). This ongoing lack of autonomy is not as precisely measurable as tank size but is one of the most insidious sources of stress and poor well-being for captive cetaceans.

In conclusion, there is essentially no correspondence between the artificial environment of entertainment parks and the natural history and adaptative characteristics of cetaceans. The impact is the same for both wild-caught and captive-born individuals, attesting to the deep fundamental discordance between life in concrete tanks and what all cetaceans need to thrive.

22.3 The Effects of Chronic Stress on Mental (and Physical) Health

The mental health of captive cetaceans must be understood in terms of how the maladaptiveness to the conditions of captivity causes chronic stress and, ultimately, a cycle of abnormal behavior and increased morbidity and mortality. Most definitions of stress are rooted in the foundational concept of homeostasis and the ability of an organism to adapt to various circumstances (Selye, 1976). All animals have evolved to be adapted to their natural environments and, likewise, the stresses found in nature (Tooby and Cosmides, 1990; Panksepp, 2010). The stress responses to these natural situations may be beneficial to the organism, permitting an appropriate response to the stressor (e.g., flight from a predator) and a return to homeostasis once the stressor is no longer present. Other stressors are severe, repetitive, chronic, or outside of the adaptive capabilities of an organism. These types of stressors contribute to a constantly high allostatic load and, therefore, have serious consequences for health and well-being (McEwen, 2017).

A normal stress response involves activation of the hypothalamic–pituitary–adrenal (HPA) axis and a subsequent return to baseline levels and homeostasis. But when the stress is prolonged and severe the physiological effects on the brain and the rest of the body are damaging to organs, the immune system, and the brain (Atkinson et al., 2015). Brain dysfunction, in turn, perpetuates abnormal responses to stress in a cycle of impairment. The HPA axis and its effects are highly conserved across mammals (Morgan and Tromborg, 2007; Lupien et al., 2009). Orcas and other cetaceans share brain mechanisms involved in mounting a stress response with other mammals and adhere to the classic HPA model (Thomson and Geraci, 1986; Romano et al., 2002; Fair et al., 2014; Levin, 2018; for reviews, see Atkinson et al., 2015; Atkinson and Dierauf, 2018). Living in concrete tanks is a situation that produces a constant high level of stress, taking a toll on mental and physical health in captive cetaceans.

The long list of emotional, psychophysiological, and behavioral changes associated with these neurological alterations, in humans and other mammals, includes increased anxiety, posttraumatic stress, cognitive impairment, depression, and mood dysregulation (Buwalda et al., 2005; McEwen, 2006, 2017; Lupien et al., 2009).

Moreover, both acute and chronic stressors that occur early in life have an important impact on an individual’s ability to cope with stressors later in life (McEwen, 2017). And therefore, as described below, multigenerational captivity perpetuates cycles of psychopathology in cetaceans.

22.3.1 Behavioral abnormalities

Captive cetaceans exhibit a range of abnormal behaviors that are common sequelae of mental illness in most complex animals. These include but are not limited to stereotypies, self-harming, hyperaggression, depressive behaviors, and failures in nursing and parent–offspring attachment. These behavioral problems are a consequence of chronic stress and lead to increased morbidity and mortality.

Stereotypies

One of the more prevalent behavioral abnormalities found in captive animals is stereotypic behavior (Mason and Latham, 2004; Mason and Rushen, 2008). There is a recognized correlation between a confined animal’s propensity to engage in stereotypical behavior and the size of their natural home range (Clubb and Mason, 2003, 2007).

Although the link between stereotypies and welfare is complex it is generally acknowledged that stereotypies are aberrant repetitive behaviors induced by the frustration of natural impulses, attempts to cope with a stressful environment, and/or brain dysfunction (Mason and Rushen, 2008) and are rarely observed in animals living in a natural habitat (Clegg et al., 2017). Environments that induce or increase stereotypies are typically worse, from a mental health and welfare perspective, than those which do not (Mason and Latham, 2004). Stereotypies, with their inappropriate level of repetition, are not infrequently associated with perseverative behaviors as well (Mason and Latham, 2004).

In captive cetaceans, oral stereotypies are common (Jett et al., 2017). These may include biting, chewing, and jaw-popping on hard tank surfaces and the steel gates used to separate them (Jett and Ventre, 2012; Visser, 2012; Visser and Lisker, 2016; Jett et al., 2017) in a behavior similar to ‘crib-biting’ in horses (Mason and Latham, 2004). The constant grating of the teeth causes severe wear that results in serious dental problems and subsequent systemic infections and mortality (Jett et al., 2017; see below).

Another common stereotypy in captive cetaceans is circling and repetitive swimming patterns (Jett and Ventre, 2011). These are not simply swimming preferences but repetitive uniform swimming behaviors that follow fixed trajectories and turning at predictable locations. While not studied nearly as well or extensively as they could be, there are reports of swimming stereotypies in captive cetaceans (Gygax, 1993; Ugaz Ruiz et al., 2013). Ugaz Ruiz et al. (2013) found that in closed facilities there were higher rates of circular swimming as well as higher cortisol levels than in open sea pen facilities, where the dolphins tended to swim in straight lines. When interpreting these findings, however, enclosure shape and size should be taken into account to determine how much it influences the formation and morphology of behaviors that look like stereotypies.

Self-harm

Self-harming (whether deliberate or as a result of other abnormal behaviors) is undescribed in free-ranging animals yet is one of the most common signs of distress and poor well-being in captive wild animals (Mason, 2010). As mentioned above, common oral stereotypies in orcas and other captive cetaceans result in damaged dentition (Jett et al., 2017). Jett et al. (2017) found that over 60% of captive orcas in the US and Spain had fractured mandibular teeth and 24% exhibited ‘major’ to ‘extreme’ mandibular coronal tooth wear down to the gingiva due to oral stereotypies (see Fig. 22.1). Dental pathology in captive orcas requires routine treatment with pulpotomies, drainage, antiseptics, and antibiotics and, even then, stereotypy-induced dental pathology is a major source of systemic infection and mortality in captive orcas (Jett et al., 2017).

In addition to the harmful results of repetitive actions like gate-biting and jaw-popping, captive cetaceans also engage in other forms of self-injurious behavior that inflict severe physical harm and trauma on the individual (Sweeney, 1988). One very young false killer whale (Pseudorca crassidens), named Chester, at Vancouver Aquarium exhibited extensive rubbing of his chin against tank walls and other hard objects causing a longstanding abrasion (Lipman, 2016). Another young captive, an orca named Morgan taken from the wild and confined in an entertainment park in Spain, continues to exhibit ‘unnatural and self-harming behaviors, including hitting her nose against the concrete tank, chewing the concrete and sliding out of the water – an action known as beaching’ (Walters, 2016). One of the more extreme cases of self-injury in a captive cetacean is Hugo, an orca who was captured from the wild in 1968 and held at Miami Seaquarium up until his death. Hugo and his tankmate Lolita performed in shows but Hugo (who was also highly aggressive toward trainers) exhibited very severe self-harm by regularly banging his head against the concrete walls of the tank, which, at one point, resulted in an injury to his rostrum which required surgery and eventually led to his death by brain aneurysm in 1980 (Jett and Ventre, 2011).

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