The Harmful Effects of Captivity and Chronic Stress on the Well-being of Orcas
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Journal of Veterinary Behavior
https://doi.org/10.1016/j.jveb.2019.05.005
Accepted/uncorrected ms. online
The Harmful Effects of Captivity and Chronic Stress on the Well-being of Orcas
(Orcinus orca)
a b c d e
Lori Marino , Naomi A. Rose, Ingrid N. Visser Heather Rally, Hope Ferdowsian ,
f
Veronica Slootsky
a
Whale Sanctuary Project, 4100 Kanab Canyon Rd, Kanab, Utah 84741
b
Animal Welfare Institute, 900 Pennsylvania Ave SE, Washington, DC 20003
c
Ingrid Visser, Orca Research Trust, P.O. Box 402043, Tutukaka, New Zealand, 0153
d
Foundation to Support Animal Protection, 501 Front St. Norfolk, VA 23501
e
University of New Mexico School of Medicine, Department of Internal Medicine, MSC10
550, 1 University of New Mexico, Albuquerque, NM 87131
f
Mid Atlantic Permanente Medical Group, 5999 Burke Commons Road, Burke, VA 22015
Corresponding author: Lori Marino, marinolori@outlook.com
Abstract
Orcas are large, deep-diving cetaceans who are known for their global distribution, wide-
ranging behavior, intelligence, and social complexity. They possess one of the largest and
most complex brains in the mammalian kingdom. However, they are the third most
common species of cetaceans kept in aquariums and marine theme parks. Most spend
many years, and sometimes decades, in captivity. At the time of writing, 63 individuals are
held in concrete tanks globally.
The scientific data on how both wild-caught and captive-born orcas fare in captivity is
increasingly robust in demonstrating that they cannot thrive under artificial circumstances
in concrete tanks. In captivity, orcas exhibit a wide range of abnormal behaviors and often
die at an early age from infections and other health conditions that are uncommon in a
wild setting. Though numerous papers and reports describe these adverse effects, they
do not offer a clear and systematic explanation for why captive orcas suffer chronic stress
and how it affects their well-being.
We describe likely mechanisms for the high levels of morbidity and mortality in captive
orcas, including the impact of chronic stress on physiology and illness. We conclude that
orcas are poor candidates for maintenance in captivity and suggest that a radical shift is
required in their treatment, in order to meet their complex needs.
Keywords: orca, killer whale, captive, stress, disease, mortality, aquarium, marine park
1
Harmful Effects of Captivity and Chronic Stress on the Well-being of Orcas Journal of Veterinary Behavior
Introduction could explain the relationship between
conditions of captivity, stress, and the
Orcas (Orcinus orca, also known as killer high rates of morbidity and mortality
whales) are part of the worldwide observed in captive orcas.
commercial trade in cetaceans and are
the third most commonly confined The Basis for Capacities and
cetacean species after bottlenose Needs of Orcas
dolphins (Tursiops truncatus) and beluga
whales (Delphinapterus leucas). As of Orca Evolution and Phylogeny
January 2019, 63 orcas were held in The evolutionary history of any
concrete tanks globally species, including orcas, determines the
(www.orcahome.de/orcastat, last kinds of adaptations that animal
accessed 15 Jun 2019). A slight majority possesses. Orcas are members of the
(53.2%) were born in captivity, and a order Cetacea, which contains two
further 29 were captured at a very young modern suborders: Mysticeti (baleen
age; 21 of these captured animals were whales) and Odontoceti (toothed whales,
recently taken from Russian waters. Most dolphins and porpoises). There are six
of these individuals have spent years, odontocete families, comprising
and sometimes decades, in captivity approximately 80-85 species (Miller,
(www.orcahome.de/orcastat). 2016). The orca is the largest member of
Despite decades of advances in the odontocete superfamily Delphinoidea
veterinary care and husbandry (Gulland and the only member of the genus
et al., 2018), cetaceans in captive Orcinus (Dahlheim and Heyning, 1999).
facilities (e.g., marine theme parks, Globally, orcas are distinguished by
aquariums, zoos) consistently display different ecotypes (a reproductively-
behavioral and physiological signs of isolated population of orcas distinguished
stress and frequently succumb to by cultural traditions such as prey
premature death by infection or other preference, foraging techniques, vocal
health conditions. The breadth of dialect, and group size; Ford, 2009).
available scientific data demonstrates Modern cetaceans evolved from
that, by every appropriate metric, captive terrestrial ancestors into the semi-aquatic
orcas do not fare as well as their free- Archaeoceti (“ancient whales”) in the
ranging counterparts (Small and Tethys Sea approximately 50-55 million
DeMaster, 1995; Woodley et al., 1997; years ago (Gingerich and Uhen, 1998;
Jett and Ventre, 2015; Robeck et al., Fordyce, 2008). The first radiation was
2015). then replaced by the Neoceti (“new
In this paper we summarize how whales”) at the Eocene-Oligocene
orcas are especially vulnerable to the boundary (~35-23 mya) (Uhen, 2010;
negative effects of the constricted Geisler et al., 2011), who evinced the
artificial environments they experience in earliest detectable changes in cetacean
marine theme parks, aquariums and brain size and structure (Marino et al.,
zoos. First, we describe the complex 2004a).
needs of orcas based on their Orca Neuroanatomy
evolutionary history, brain anatomy,
physiology and cognitive-behavioral As a group, modern cetaceans,
characteristics. Then we describe the and therefore orcas, possess the
morbidity and mortality patterns seen in neurobiological foundations of complex
captivity, as well as how these patterns psychology, emotion, and behavior: 1)
are associated with a failure to meet the large relative brain size, 2) an expanded
complex needs of this species. We neocortex, 3) well-differentiated cortical
conclude by describing mechanisms that cytoarchitecture, and 4) an elaborated
limbic system. These neurobiological and
2
Harmful Effects of Captivity and Chronic Stress on the Well-being of Orcas Journal of Veterinary Behaviorsensory characteristics act as a In mammals, expansion of the
guidepost to the kind of environment neocortex, which is critical for higher-
orcas need in order to thrive. In addition order functions, occurs through folding of
to these general characteristics, the the surface and is, thus, indexed by
brains of orcas (and other cetaceans) surface area. The modern cetacean
exhibit more specific characteristics neocortex is among the most highly
relevant to intelligence, awareness and convoluted of all mammals. Orcas are the
emotionality that are expected to affect most gyrencephalic of all mammalian
their ability to adjust to living in concrete species, including modern humans
tanks. (Manger et al., 2012). Average cortical
2
surface area in orcas, at 14,207 cm , is
Encephalization
the highest of the cetaceans (Ridgway et
While absolute brain size is related to al., 2016) and significantly greater than in
2
intelligence, relative brain size is humans (i.e., 1,500-2,000 cm ) (Prothero
considered a better predictor of cognitive and Sundsten, 1984). The “gyrification
capacity across species (Marino et al., index” (GI), which compares neocortical
2004b). Relative brain size is typically surface area to total brain weight, ranges
expressed as an encephalization from 2.4-2.7 for odontocetes, exceeding
quotient (EQ) (Jerison, 1973), which the value of 1.75 for modern humans
represents the average brain size of a (Ridgway and Brownson, 1984).
given species in comparison with other
In addition to neocortical surface
species of the same average body
area, there are several other dimensions
weight.
of the orca brain that serve as strong
Odontocetes, and in particular predictors of complex cognitive abilities.
Delphinoidea, are the most highly The anterior cingulate and insular
encephalized nonhuman taxonomic cortices, the temporal operculum, and
group known, with EQs ranging from 1.8 paralimbic regions (all situated deep
to 5.0 – significantly higher, as a group, within the forebrain) are well developed in
than any other species except modern orcas and other cetaceans (Jacobs et
humans. Orca EQ is approximately 2.2- al.,1979; Marino et al., 2004b; Hof and
2.3 (Marino, 1998; Marino, 2008; Van der Gucht, 2007). The expansion of
Ridgway et al., 2016), compared to these areas in cetaceans is arguably
human EQ which is 7.0 (Marino, 1998). associated with high-level cognitive and
The brains of adult orcas weigh on social functions such as attention,
average 6,621 g (Ridgway et al., 2016), prediction, social awareness and
compared with the approximately 1,300 g empathy (Allman et al., 2005; Hof et al.,
average human brain (Marino, 1998). 2005). It has been suggested that the
elaborated opercular region of the orca
Cerebral expansion brain serves a similar function to the
The orca telencephalon is characterized speech-related opercular region in
by three elaborated concentric tiers of humans (Marino et al., 2004b). Moreover,
limbic, paralimbic and supralimbic tissue. recent studies show that the anterior
One measure of the profound cingulate and insular cortices in larger
corticalization of orca brains is that the cetaceans contain a type of projection
cerebrum constitutes an average of neuron, known as a spindle cell or Von
81.5% of the total brain volume, Economo neuron (Hof and Van der
compared with an average of 76.2% for Gucht, 2007), which may be involved in
humans (Wright et al., 2016). As a result, social cognition (Allman et al., 2005) and
the orca brain has been described as adaptive intelligent behavior (Allman et
being more corticalized than the human al., 2005) in mammals. Although
brain (Wright et al., 2016). hippocampal volume in orcas is the
smallest among cetaceans relative to
3
Harmful Effects of Captivity and Chronic Stress on the Well-being of Orcas Journal of Veterinary Behaviorbrain size (0.4%), the reduction of this brain structures involved in emotions,
structure was apparently accompanied memory and motivation. The richly
by the transfer of a number of interconnected components of this
hippocampal functions (memory, system include the amygdala, cingulate,
learning, and navigation) to other parts of hippocampus, hypothalamus, and related
the brain, such as the highly developed structures such as the putamen, caudate,
entorhinal cortex or cerebellum (Wright et and, perhaps, the thalamus (Stephani,
al., 2016). 2014). Recent work on orcas has shown
that “limbic functions” are well integrated
Some authors have suggested with other cortical functions and
that odontocetes brain size is driven by emotional and cognitive processing are
developmental prolongation as a capacities that have co-evolved.
response to the increased learning Therefore, emotions and forms of
demands of living in complex social cognition in realms such as reasoning,
networks (Whitehead and Mann, 2000; learning and abstraction are not
Connor, 2007). Overall enlargement of independent of one another (Marino et
the orca brain is associated with al., 2004b; Morgane et al., 2005; Pessoa
protracted pre- and post-natal and Hof, 2015).
developmental periods, as it is in other
mammals (Whitehead and Mann, 2000; The limbic system of orcas has
Charvet and Finlay, 2012), characterized been elaborated into a neighboring
by long periods of maternal investment in region, e.g., paralimbic lobe, which forms
offspring care and learning, thus a transition to neocortical functions.
selecting for complex social and cognitive Though orca brains differ from other
abilities (Whitehead and Mann, 2000). mammalian brains by having a
The high EQs and well-developed brains proportionately small hippocampus – due
of orcas exemplify the positive correlation to a lack of olfactory structures – whilst
between relative brain size and other limbic structures, such as the
complexity, on the one hand, and social amygdala, caudate, internal capsule, and
complexity on the other, found in a wide thalamus, are well developed (Marino et
range of mammals (Marino, 2002; al., 2004b). It has been argued that the
Reader and Laland, 2002; Byrne and highly elaborated paralimbic lobe
Corp, 2004; Dunbar, 2009; Marino et al., replaced several hippocampal functions
2007). involved in emotion, as there are dense
connections between the paralimbic
Finally, improved methods of cortex and core limbic structures (Marino
cellular visualization and analysis reveal et al., 2004b).
that the cytoarchitectonic patterns in
cetaceans are far more varied and Sensory regulation
complex than previously thought (Hof et
al., 2005). These cytoarchitectonic All odontocetes have well-developed
patterns, in addition to encephalization auditory capacities that are used in a
and neuroanatomical complexity, are variety of ways, including for surveillance
also evidence of cetacean behavioral and of the environment, detection of prey and
social complexity (Hof et al., 2005). communication. Some cetaceans do lose
hearing as they age (Ketten, 2004);
presbycusis is common across the class
Mammalia. However, in almost all other
The limbic system and emotional ways, cetaceans differ significantly from
regulation other mammals in how they sense,
Evidence for orcas’ emotional complexity process and use sound. In orcas and
stems in part from neuroanatomical data. other echolocating cetaceans, sounds
The mammalian limbic system is a set of are received and conducted through the
4
Harmful Effects of Captivity and Chronic Stress on the Well-being of Orcas Journal of Veterinary Behaviorlower jaw to the middle ear, inner ear, and discrimination of some tastes (Nachtigall
then to primary auditory centers in the and Hall, 1984; Kishida et al., 2015).
brain. A fat filled channel in the lower jaw
serves to receive and conduct the sound Finally, somatosensory perception
waves (see Cozzi and Oelschlager, (sense of touch, pain, body position,
2016, for a detailed discussion). temperature) is important for cetaceans
Odontocetes can hear sounds across a in a number of contexts, including social
broader frequency range than most contact. Cetacean skin is well innervated
terrestrial mammals and their ability to and, thus, quite sensitive to touch (Tyack,
echolocate is an integral part of their 2000). Touch plays an important role in
experience of the world (Madsen and social bonding, sexual encounters,
Surlykke, 2013), generating a mental maternal care, and other affiliative—and
representation of objects and even aggressive—contexts (Connor et
surroundings that is processed cross- al., 2000; Dudzinski et al., 2010).
modally, i.e., across hearing and vision Orca Psychology: Cognitive,
(Pack and Herman, 1995). As sound is Emotional and Social Behavior
transmitted efficiently in water, the large
proportions of the auditory nerve coincide Since psychological, behavioral
with the need for rapid sound uptake and and ecological characteristics determine
processing (Ridgway, 1990). how well members of any species
(individual differences notwithstanding)
In odontocetes, there are two adapt to artificial settings (Mellen and
primary auditory cortices. One is located MacPhee, 2001; Clubb and Mason,
in the suprasylvian gyrus along the vertex 2003) it is important to consider the
of the hemispheres, lateral and adjacent psychological qualities of orcas, including
to the primary visual cortex (Popov et al., self-awareness, emotions, social
1986). The other, recently discovered, complexity and culture.
exists in the temporal lobe (Berns et al.,
2015). These two primary auditory Self-awareness
regions provide evidence for a high Self-awareness, the ability to
reliance on complex acoustic processing conceive of and think about oneself, i.e.,
in odontocetes. an autobiographical “me”, is part of
Vision is also well-developed in subjective experience, also referred to as
orcas and acuity is preserved above and phenomenology. Orcas have
below water (Madsen and Herman, demonstrated several abilities indicative
1980). Dolphins appear to perceive of self-awareness. These abilities include
similar patterns in two-dimensional forms imitation, which requires an
as humans do (Tomonaga et al., 2014), understanding of the relation between
and they may possess some form of color one’s own body and another’s. Orcas
vision (Davies et al., 2012). Delphinoids have demonstrated the ability to imitate
use sight for a range of purposes, from the novel actions of conspecifics
prey capture to social interactions (Blois- (Abramson et al., 2012). Another is mirror
Heulin et al., 2012). self-recognition, i.e., the ability to use a
mirror to investigate one’s own body. In a
It is unclear to what extent orcas study of their responses to mirrors, orcas
and other odontocetes possess smell show contingency checking behavior—a
and taste. They lack a vomeronasal correlate of self-directed responses
organ and olfactory bulbs, yet olfactory exhibited by most individuals who
reception genes, while reduced, are not demonstrate mirror self-recognition
absent (Kishida et al., 2007). While no (Delfour and Marten, 2001).
taste buds have been found, there is
some behavioral evidence for the
5
Harmful Effects of Captivity and Chronic Stress on the Well-being of Orcas Journal of Veterinary BehaviorEmotions propeller strikes and was bleeding
profusely. The adults supported the
Observations of orcas reveal that injured juvenile by ‘cradling’ this
they experience deep emotions and individual between them. Fifteen days
strong social attachments. These later, in the vicinity of the boat strike, two
observations include reports of long- orcas were observed supporting a third,
range contact calling when separated presumed to be the same juvenile,
from others, grieving behaviors, and although it is unclear if the juvenile
helping (epimeletic) behaviors. In survived the trauma (Ford et al., 1994a).
addition to assisting individuals in
distress, epimeletic behavior often Epimeletic behavior in orcas is not
involves adult individuals attending to a limited to dead or injured individuals. For
dead individual by keeping them afloat, example, there are multiple accounts of
lifting or pushing the individual, physical support by others during
performing attempts that look like entanglements, including one example in
“resuscitation”, and carrying them around September 2014 off the coast of New
by the mouth or on the body (Bearzi et al., Zealand when a female was supported
2018). These types of behaviors have by her two most recent offspring, with a
been characterized by scientists as third (her eldest, an adult male) nearby
expressions of bereavement or concern (Visser, unpublished data, Figure 2,
about the breaking of strong social bonds Supplemental Material). ‘Standing by’
(Bearzi et al., 2018). has also been documented in a number
of instances during strandings of orcas
Almost all reports of cetaceans around the New Zealand coastline where
responding to dead or injured individuals orcas who were not stranded have
have come as opportunistic observations remained near those on the beach, at
in the wild, as there would be no way to times risking stranding themselves
ethically study this behavior (Visser, unpublished data).
experimentally. The longest and best
documented example of this type of Social Complexity, Culture, and
bereavement behavior in a free-ranging Behavioral Ecology
orca was during July through August
2018 in the Salish Sea off the coast of Orcas are a cosmopolitan species
Washington State, USA. A 20-year-old and the ocean’s apex predator. They
orca known as J35 or Tahlequah gave feed on a large variety of aquatic species
birth to a female calf who died within thirty (Baird, 2002), although distinct
minutes. The calf was carried on J35’s populations tend to specialize on specific
back, rostrum and in her mouth for 17 prey types (Rendell and Whitehead,
days. When the body slipped off, she 2001; Song, 2018). Orcas, when not
retrieved it. Other members of the pod, foraging or hunting, often travel by
particularly her eight-year-old son, were swimming in a consistent direction at a
also observed carrying the dead calf. steady pace and frequently engage in
Members of her pod may have shared synchronized dives (Ford, 2009),
food with her during the ordeal, as she suggesting an important social or
was not observed feeding on her own ecological purpose for traveling
(Mapes, 2018; NOAA Fisheries, 2018, independent of locating food. One
Figure 1, Supplemental Material). population of orcas has been measured
traveling at a rate of over 20 km/hr (Ford,
Also in the Salish Sea, an adult 1989). Depending upon the population
male, adult female and two younger and hunting practices, orcas routinely
orcas were observed after one of the swim tens of kilometers a day in a straight
juveniles was hit by a ferry. The juvenile line (Visser, 1999b; Dahlheim et al.,
had visible lacerations attributed to 2008; Durban and Pitman, 2011;
6
Harmful Effects of Captivity and Chronic Stress on the Well-being of Orcas Journal of Veterinary BehaviorMatthews et al., 2011; Fearnbach et al., prey (Barrett-Lennard et al., 1996). In the
2014). Maximum daily distance has been Antarctic, one population of orcas locates
measured at 252 km (Matthews et al., seals hauled out on ice floes and
2011) with maximum sustained distances dislodges them by grouping together and
of 160-225 km/day for up to forty days rushing the floe, creating a wave that
(Durban and Pitman, 2011; Matthews et washes the seal into the water (Smith et
al., 2011). Additionally, relatively high al., 1981; Visser et al., 2008; Pitman and
sustained speeds (3.7 ± 0.2 m s–1) for up Durban, 2012). Orcas at Punta Norte,
to 30 minutes (Guinet et al., 2007) have Argentina, hunt sea lion and elephant
been recorded for the species. seal pups by beaching themselves and
capturing the pups, typically in the surf
Although there is substantial zone (Lopez and Lopez, 1985). A similar
variation in the depths to which different behaviour is observed in the Crozet
orca populations, ecotypes and Islands, where orcas hunt elephant seal
individuals dive, there is ample evidence pups (Guinet and Bouvier, 1995). In both
for routine deep diving in the species locations adults appear to actively teach
globally. In some populations, individuals this technique (which is dangerous as it
dive in excess of 750m several times a can lead to stranding) to juveniles (Lopez
day (Towers et al., 2018), others 200 m and Lopez, 1985; Guinet and Bouvier,
several times a day (Reisinger et al., 1995).
2015), while yet others dive deeper than
150 m at least once every five hours Another component of orca
(Baird et al., 2005). The current culture are vocal dialects (Ford, 1991;
maximum depth recorded is 1087m, for a Yurk et al., 2002; Ford, 2009), which are
female (Reisinger et al., 2015). learned variations in the structure of
vocalizations among animals who live
Free-ranging orcas live in highly sympatrically and come into acoustic
complex societies with long juvenile contact. Dialects form the basis of vocal
periods and differentiated relationships, clans, developed through social learning.
embedded in complex social networks For instance, dialect similarity is related
that rely upon learning and memory to group closeness; it decreases as one
(Baird, 2000; Williams and Lusseau, compares matrilineal groups within pods
2006). Orca social life within ecotypes is (extended families of closely related
strongly characterized by cultural mothers who are daughters, sisters, or
traditions, i.e., distinctive learned cousins, and their children), pods within
behaviors passed down from one clans (pods that share common calls),
generation to the next, which differ clans within communities, and
across groups and are underwritten by communities (Deecke et al., 2000; Ford
sophisticated social learning capacities et al., 2000; Yurk et al., 2002).
(Whitehead, 2008). Such culture
provides a way for individual whales to Vocal learning in cetaceans
express their identity and benefit from the reflects the same process by which
support of others in their group human languages develop and evolve
throughout their lives. Some orca cultural (Janik, 2014). It is based upon mimicry
traditions are exemplified by different and requires excellent long and short-
learned foraging strategies and other term memory and the ability to learn from
forms of cooperative behaviors (Rendell social feedback. Young orcas acquire
and Whitehead, 2001). Orca foraging is their repertoire of sounds from their
often accomplished through specialized, mother and other close family members,
learned tactics. For example, mammal- and they learn to selectively identify the
eating orcas typically hunt in small calls of outside groups (Deecke et al.,
groups and often remain silent in order to 2010; Crance et al., 2014). Vocal learning
better detect and, possibly, surprise their requires a substantial degree of social
7
Harmful Effects of Captivity and Chronic Stress on the Well-being of Orcas Journal of Veterinary Behaviorawareness and forms an important pathogens that are usually harmless but
component of orcas’ multiple cultural can cause disease under certain
traditions, as well as their identity and unnatural, unhealthy, or compromised
sense of security and cooperation in a conditions. These include a weakened
social group, as it does in many other immune system (see below for the effects
highly social mammals (Cohen, 2012). In of stress on the immune system), chronic
general, their acoustic capacity is central exposure to chemical irritants or trauma
to their lives; they navigate, find prey and to the skin, excessive or improper use of
mates, maintain social bonds, and antimicrobials, and an imbalance in the
generally process the details of their microbiota of the body or environment
surroundings using sound as much as, or (which may exist in tanks) (Reidarson et
instead of, light (Couquiaud, 2005; al., 2018).
Parsons, 2013, for reviews on
odontocete hearing and use of sound). Jett and Ventre (2011) found that
another common cause of death of
Morbidity and Mortality of Orcas captive orcas was gastrointestinal
Living in Captivity ulceration. Gastric ulceration is often
caused by prolonged stress, as well as
Causes of Illness and Death being associated with the bacterium
A 1979 review of the causes of Helicobacter pylori (Nomura et al., 1994).
death of 17 captive orcas in North Gastric disorders such as ulcers have
America who had died since 1965 also been associated with behavioral
revealed that infectious diseases were stereotypies in other captive animals
the primary cause of death (Nicol et al., 2005; Moeller et al., 2008)
(Ridgway,1979). This situation remains Although unreported (and unlikely, due to
largely unchanged today. Published their kinetic nature and time spent below
statements and records from the media, the surface) in free-ranging orca
the US National Marine Mammal populations, mosquito-transmitted
Inventory, and USDA Inspection Reports diseases have killed at least two captive
obtained under public records law orcas in marine theme parks. A 25-year
demonstrate that, between 1971 and old male orca died suddenly in 1990 at
2017, there have been 35 documented SeaWorld Orlando of St. Louis
orca deaths at SeaWorld facilities alone encephalitis (Buck et al., 1993). And a 14-
(Kielty, 2011; Robeck et al., 2015; Aiello year-old male orca died without prior
and Moses, 2016; Rose and Parsons, signs of illness in 2007 at SeaWorld San
2019). When causes of death were Antonio. Necropsy results confirmed the
available, the most commonly implicated presence of West Nile Virus in the brain
conditions were viral, bacterial and fungal tissue (St. Leger et al., 2011). Jett and
infections, gastrointestinal disease, and Ventre (2012) advanced the hypothesis
trauma (Jett and Ventre, 2012). Despite that the frequent “logging,” i.e., hanging
veterinary care and therapeutic motionless on the surface of the water in
intervention, at least 15 of the 22 orcas tanks, commonly seen in captive orcas,
who have died in US marine theme parks left them more vulnerable to mosquito
between 1990 and 2010 succumbed to bites and increased their risk of
infectious and inflammatory diseases, contracting mosquito-carried viral
including eight who reportedly died of diseases (Jett and Ventre, 2012).
pneumonia; three of encephalitis; three of
bacteremia; and one of leptomeningitis Pulmonary mycotic infection (fungal
(Kielty, 2011). pneumonia) is one of the most common
causes of death in captive and free-
Many of the infections captive ranging orcas and other marine
orcas succumb to are opportunistic mammals (Reidarson et al., 1999;
infections, that is, infections by
8
Harmful Effects of Captivity and Chronic Stress on the Well-being of Orcas Journal of Veterinary BehaviorRobeck and Dalton, 2002; Reidarson et more (Ford et al., 1994b; Newsome et al.,
al., 2018). Candida sp. is one of the most 2009).
common organisms to cause infection in
cetaceans and is on the rise (Ridgway, Prior to 1992, survivorship rates
1979; Reidarson et al., 1999, 2018), revealed that, despite provisioning and
potentially as a result of long-term and care, captive orcas clearly did not live as
aggressive antibiotic treatment (Dold, long as free-ranging orcas (Small and
2015), overtreatment of water for purity, DeMaster, 1995; Woodley et al., 1997).
or both (Medway, 1980). Cases of Between 1992 and 2014, husbandry
zygomycetes infection and fatalities have methods continued to evolve and a
also been recorded in captive orcas and growing proportion of the captive
other marine mammals (Robeck and population was captive-born. In 2015,
Dalton, 2002; Abdo et al., 2012; two papers revisited survivorship and
Reidarson et al., 2018). The rise in fungal lifespan in captive orcas.
infections in captive marine mammals Jett and Ventre (2015) evaluated
may be due to the development of a database comprised of captive orcas
resistance from increased use of anti- held in facilities in the USA and those in
fungal medications, among other factors foreign countries that send or receive
(Reidarson et al., 2018). animals to/from the USA (N = 201). Their
Survivorship and Longevity primary goal was to assess changes in
the captive population, rather than to
One set of metrics for comparing compare captive and free-ranging
captive versus free-ranging animal well- populations. They found that orcas who
being is life history parameters, such as entered USA facilities after 1985
survivorship and lifespan. Most of the (primarily through captive birth) survived
information about the life history of orcas better than those who entered captivity
derives from long-term studies of resident before 1985, which they attributed
ecotype populations in Washington state, generally to improved husbandry and the
British Columbia, and Alaska (Olesiuk et growing proportion of captive-born
al., 1990; Ford et al., 1994b; Olesiuk et animals in the sample. However, while
al., 2005; Ford, 2009; Matkin et al., 2014). survivorship in USA facilities has
Life history parameters for other improved over time, they noted that
ecotypes and populations around the survival to sexual maturity and
globe may vary. reproductive senescence remained poor
compared to free-ranging orcas.
In natural settings, both sexes of
orcas reach sexual maturity at 12-15 A separate analysis by Robeck et al.
years of age. Females give birth (2015) focused exclusively on a subset of
approximately every five years and the captive population; whales held by
experience reproductive senescence at SeaWorld Inc. The authors also found
approximately age 40 (Ford, 2009; Foster that annual survivorship rates had
et al., 2012a; Matkin et al., 2014; Brent et improved when compared to previous
al., 2015). Females live an estimated years. However, they also calculated an
maximum of 80 to 90 years and males an average life expectancy for captive-born
estimated maximum of 60 to 70 years. orcas that was invalid. The equation they
The mean life expectancy for free- used to calculate the value, —1 /
ranging orcas is 46 years for females and Ln(Annual Survival Rate), would only be
31 years for males (Olesiuk et al., 1990, valid if survival is constant from year to
2005). Calves are weaned at one to two year and over all age classes (DeMaster
years of age, but nurse opportunistically and Drevenak, 1988). Yet they
for two to three years longer, or possibly determined that Annual Survival Rate
(ASR) improved over time, violating the
9
Harmful Effects of Captivity and Chronic Stress on the Well-being of Orcas Journal of Veterinary Behaviorfirst assumption. In addition, survivorship (Anonymous, 1989; Reza, 1989;
rate in orcas declines with age (DeMaster Mooney, 1998). Conversely, there are no
and Drevenak, 1988; Matkin et al., 2014) reliable reports of free-ranging orcas
and is generally lower in calves (Olesiuk killing a human being, despite centuries
et al., 1990; Ford, 2009; Robeck et al., of encounters in the wild, including
2015), violating the second assumption. decades of in-water research (Visser,
DeMaster and Drevenak (1988) 1999a, 2000, 2005b) and in-water
specifically cautioned against using ASR tourism (Pagel et al., 2017). However, in
to calculate life expectancy for these and the 55 years since captive display of
other reasons. Robeck and colleagues orcas commenced, captive orcas have
also lowered the maximum estimated killed four human beings (three trainers
lifespan in free-ranging orcas by and one member of the public) and
excluding all whales in the Pacific seriously injured many more (Parsons,
Northwest populations whose exact age 2012; Wise, 2016).
was unknown (i.e., those who were older
than one year of age when the study In the wild there is room for
began in 1973) (Robeck et al., 2015). dispersal and avoidance behavior (Baird
and Dill, 1995). Therefore, conflicts rarely
Abnormal Behavior as a Contributor escalate into serious or injurious attacks.
to Morbidity and Mortality In the confined space of concrete tanks,
the whales are also held in artificially
Captive orcas exhibit a range of created “social groups,” both of which
abnormal behaviors, inter alia stymie the natural strategies orcas use in
hyperaggression, stereotypies, self- the wild to avoid escalation of
harming, rejection of offspring and failure aggression.
to nurse, which may contribute to
morbidity and mortality. Self-harming in free-ranging orcas
is undescribed in the scientific literature,
Hyperaggression but there are numerous examples of
Captive orcas exhibit a range of captive orcas engaging in self-injurious
hyperaggressive abnormal behaviors behaviors, such as banging their heads
(toward conspecifics and humans). Such against the sides of their tanks or against
aggression by captive orcas may be one the separation gates (Visser and Lisker,
of their most consequential social 2016; Pollard, 2019), actively exiting the
behaviours (Graham and Noonan, 2009). tank onto ledges for sustained periods to
It has been documented since the early avoid aggression (Visser and Lisker,
days of the captivity industry (Burgess, 2016) and refusing to eat (Hoyt, 1984;
1968; Martinez and Klinghammer, 1978) Romanov et al., 2015).
and has continued (Anonymous, 1989; Oral Stereotypies and Dental Disease
Anderson et al., 2016; Graham and and Injury
Noonan, 2010; Cornell, 2011; Visser,
2012; Sánchez Hernández and Molina One of the more common behavioral
Borja, 2013; Ventre and Jett, 2015; abnormalities found in captive animals
Visser, 2016; Visser and Lisker, 2016; across a wide range of species is
Jett et al., 2017). Although free-ranging stereotypies. Their occurrence is
orcas do have conspecific aggressive associated with psychological stress and
encounters, these appear to be rare generally with poor well-being (Mason
events and often involve behavior that and Latham, 2004). There have been
results in the displacement of others, but numerous reports of oral stereotypies in
limited (Visser, 1998) or no physical captive orcas, including biting and
injury (Bisther, 2002). The only recorded chewing on hard tank surfaces, hard
orca fatality from intraspecific aggression toys, and the steel gates used to separate
involved two females in captivity the whales (Graham and Dow, 1990; Jett
10
Harmful Effects of Captivity and Chronic Stress on the Well-being of Orcas Journal of Veterinary Behaviorand Ventre, 2012; Visser, 2012; Ventre In captivity, orcas are fed
and Jett, 2015; Almunia, 2017). These exclusively a diet of dead fish and squid,
behaviors lead to extensive and chronic as well as gelatin (to minimize
dental pathologies (Almunia, 2017; Jett et dehydration), often dropped directly into
al., 2017). In Jett et al. (2017), all of the the back of the oral cavity and swallowed,
subjects exhibited dental injury (N = 29), requiring little to no contact with, or
with up to 75% of their teeth showing manipulation by, the teeth. Nevertheless,
signs of damage. Visser and Lisker over 60% of captive orcas in the USA and
(2016) reported up to 10 broken Spain had fractured mandibular teeth and
mandibular teeth on one individual (see 24% exhibited “major” to “extreme”
Supplemental Material, Table 1 for mandibular coronal tooth wear down to
details). the gingiva (Jett et al., 2017).
Much of the risk for infectious disease in In order to treat abscesses and
captive orcas can be explained by its drain debris and pus from the tooth
association with poor dental health, cavity, the majority of captive orcas
which provides a pathway for pathogens undergo a modified pulpotomy procedure
to enter the bloodstream (Li et al., 2000). that subsequently requires daily flushing
An explanation for the link between (Ventre and Jett, 2015; Jett et al., 2017).
dental wear and pathology and infectious Additionally, teeth may have to be
systemic disease in orcas has been extracted (Jett et al., 2017). Dental
offered by Graham and Dow (1990), in pathology in captive orcas also requires
their description of one ill individual. They routine treatment with antiseptics and
reported that chewing on tank surfaces antibiotics. Chronic antibiotic use,
by the orca resulted in dental disease however, may result in drug-resistant
affecting the gingiva and pulp cavity, with pathogens (Davies and Davies, 2010;
necrotic, infected, or hyperplastic Dold, 2015) and altered immune system
exposed dental pulps. The authors function (Yang et al., 2017). Chronic
reported that the animal was also antibiotic use has also been associated
lethargic, leukocytic and suffered a risk of with disruption of intestinal flora
ensuing osteomyelitis, gingival cellulitis (Kilkkinen et al., 2002; Croswell et al.,
and systemic infection. 2009) and some forms of
photosensitivity/toxicity (Gould et al.,
While significant dental wear is 1995; Karagas et al., 2007; Karagas et
found in free-ranging orcas, it is typically al., 2007; Jett and Ventre, 2012,) and
isolated to those populations who have ototoxicity (Grill and Maganti, 2011).
very specific feeding habits, including
targeting certain prey with abrasive skin Following tooth extraction, or
(e.g., sharks) (Ford et al., 2011) or chronic infection, or disease of the soft
feeding using suction (Foote et al., 2009). tissues in or around the mandibles from
However, it should be noted that other infections of the teeth (that can extend
populations that feed extensively on into the surrounding structures),
elasmobranchs (e.g., Visser, 2005a) do remodelling of the bony architecture of
not have similar dental wear (Visser, the mandible may occur. One could
2005b). Regardless, extensive tooth speculate that gross changes to the
deterioration in free-ranging orcas is structural integrity of the mandible may
ecotype-specific. In populations that do have an impact on how the individual can
not have implicated feeding habits, dental process incoming echoes during
wear is mild to non-existent and dental echolocation.
fracture is rare (Foote et al., 2009; Ford
et al., 2011; Jett et al., 2017).
11
Harmful Effects of Captivity and Chronic Stress on the Well-being of Orcas Journal of Veterinary BehaviorThe Association Between Stress, the adaptive capabilities of an organism.
Disorder, and Death These types of stressors contribute to a
constantly high allostatic load and,
Importantly, the poor health and therefore, have serious consequences
short lifespans of captive orcas are most for health and well-being (Juster et al.,
clearly understood as connected 2010; McEwen, 2017).
elements in a cycle of maladaptiveness
to the conditions of captivity that involves The HPA Axis
behavioral abnormalities, physical harm
and vulnerability to disease. When the brain detects a threat, a
coordinated physiological response
Defining Stress involving autonomic, neuroendocrine,
metabolic, immune, and behavioral
Most definitions of stress are rooted in the factors is activated, largely dependent
foundational concept of homeostasis and upon the hypothalamus-pituitary-adrenal
the ability of an organism to adapt to (HPA) axis. (There are also other cellular
various circumstances (Selye, 1976). and neural responses that are not HPA-
Homeostasis refers to a dynamic state of dependent but play a role in stress.)
psychological and physiological Corticotrophin releasing hormone (CRH)
equilibrium in which vital somatic and is released from the hypothalamus,
psychological parameters are maintained causing the release of
in a range that is optimal for well-being adrenocorticotrophic hormone (ACTH)
(McEwen, 2000; Sapolsky, 2004). All from the pituitary gland and the release of
animals have evolved to be adapted to glucocorticoids from the adrenal gland.
their natural environments (or, more The main glucocorticoid involved in this
precisely, their ancestors’ environments) response is cortisol (Lupien et al., 2009).
(Tooby and Cosmides, 1990; Panksepp, Cortisol increases blood sugar through
2010). The entire suite of dynamic gluconeogenesis, suppresses the
homeostasis-maintaining mechanisms is immune system, influences the
termed allostasis (Sterling and Eyer, metabolism of fat, protein, and
1988; McEwen and Wingfield, 2003, carbohydrates and affects blood
2007) and the type, duration and pressure regulation. It also has central
magnitude of the stress response nervous system effects.
contributes to allostatic load, which has Mineralocorticoids are also released
consequences for health and well-being during the stress response and these
(McEwen and Wingfield, 2007; McEwen play an important role in the maintenance
and Rasgon, 2018). The brain is directly of electrolyte balance. Prolonged
involved in an organism’s ability to detect exposure to increased levels of
deviations from homeostasis and correct mineralocorticoids can lead to
them with a range of defenses, including detrimental changes in arterial pressure
cognitive and emotional responses and other aspects of fluid retention in
(McEwen, 2002; McMillan, 2005; marine mammals (Atkinson et al., 2015).
Wemelsfelder, 2007; Panksepp, 2010). Although the HPA axis is critical to
Many stressors are short-lived survival, its chronic activation and
and addressed through biological dysregulation can be detrimental to
adaptation. The stress responses to health and well-being (Sapolsky et al.,
these acute situations may be beneficial 2000).
to the organism, permitting an Chronic stress can occur if acute
appropriate response to the stressor stressors become frequent, repetitive, or
(e.g., flight from a predator) and a return prolonged in duration or intensity,
to homeostasis once the stressor is no causing either desensitization to the
longer present. Other stressors are stressor or, in many cases, sensitization
severe, repetitive, chronic or outside of
12
Harmful Effects of Captivity and Chronic Stress on the Well-being of Orcas Journal of Veterinary Behaviorso that organ systems eventually is involved in fear responses and
degrade. As a result, individuals become emotional regulation and is strongly
increasingly vulnerable to morbidity and affected by chronic stress, with the
mortality (Buwalda et al., 2005; McMillan, basolateral region responding with an
2005; McEwen, 2017). As Atkinson et al. increase in dendrites (Vyas et al., 2002),
(2015) state, “The type, magnitude and and the medial amygdala showing
duration of a stress response have a cost shrinkage and loss of dendrites (Bennur
to the animal… when stressors are et al., 2007; Lau et al., 2017).
chronic or severe, the accumulated costs
associated with the response(s) become The long list of emotional,
an allostatic overload, which can psychophysiological, and behavioral
contribute to physiological dysfunction changes associated with these
and increase the probability of disease neurological alterations, in humans and
and other pathologies” (p.464). other mammals, includes increased
anxiety, posttraumatic stress, cognitive
In addition to an overload and impairment, depression and mood
eventual dysregulation of the immune dysregulation (Buwalda et al., 2005;
system, chronic stress has profound McEwen, 2006; Lupien et al., 2009;
effects on brain structures, specifically McEwen, 2017). Within the prefrontal
the hippocampus, amygdala, and cortex, chronic stress causes
prefrontal cortex. In turn, these altered debranching of medial prefrontal neurons
brain structures impact the HPA axis and and shrinkage of dendrites, which may be
general stress response: related to cognitive rigidity and loss of
attentional control in humans and other
“The brain is the organ that animals (Liston et al., 2006). Additionally,
determines what is novel and orbitofrontal cortical neurons expand
possibly threatening and therefore dendrites that may be related to
‘‘stressful’’ and it orchestrates the increased vigilance and sensitivity to
behavioral and physiological fear-inducing stimuli (Radley et al.,
responses, whether health 2004). Moreover, both acute and chronic
promoting or health damaging. And stressors that occur early in life have an
the brain is a biological organ that important impact on an individual’s ability
changes in its architecture and its to cope with stressors later in life
molecular profile and its (McEwen, 2017).
neurochemistry under acute and
chronic stress and directs many The HPA axis and its effects are highly
systems of the body—metabolic, conserved across mammals (Morgan
cardiovascular and immune—that and Tromborg, 2007; Lupien et al.,
are involved in the short- and long- 2009,). Orcas and other cetaceans share
term consequences of being brain mechanisms involved in mounting a
‘‘stressed out’’ and the consequent stress response with other mammals and
health-damaging behaviors.” adhere to the classic HPA model (see
(McEwen, 2017, p. 2-3). Atkinson et al., 2015 and Atkinson and
Dierauf, 2018 for reviews, Thomson and
The hippocampus is involved in episodic Geraci, 1986; Romano et al., 2002,
and spatial memory and mood regulation. Houser et al., 2011; Fair et al., 2014;
It is also a gateway to the way the brain Levin, 2018). Maladaptive stressors—
responds to stressors. Substantial inter alia: confinement; sensory overload
evidence shows that sustained in the form of abnormal and excessive
glucocorticoid, e.g., cortisol, release sounds while, at the same time, sensory
leads to shrinkage of hippocampal deprivation due to static and barren
neurons and loss of dendritic spines environments; abnormal social
(McEwen, 2016). Similarly, the amygdala situations; loss of control and autonomy;
13
Harmful Effects of Captivity and Chronic Stress on the Well-being of Orcas Journal of Veterinary Behaviorboredom—can lead to dysregulation of calf development and learning (Ward et
the HPA axis and related health effects. al., 2009).
Numerous factors contribute to the
chronic stress experienced by orcas in Thus, orca calves rely upon their
concrete tanks. Some of the more salient mothers and closely-related female
contributors are described below. relatives within their natal pod for
protection, nourishment, and the
Social Stress development of essential life skills that
contribute to their long-term
Sociality and social intelligence psychological health, reproductive
evolved as a selective advantage that success and physical fitness. In the case
confers enhanced fitness to individuals of the resident ecotypes of orcas in the
(Silk, 2007). Indeed, animals living in Pacific Northwest, both male and female
complex social systems may benefit calves demonstrate life-long affiliations
from, inter alia, enhanced predator with their natal matriline; in most cases,
surveillance and avoidance, cooperative they never leave their maternal group
foraging and hunting, enhanced (Olesiuk et al., 2005). Male orcas
reproductive opportunities, or (including adults) experience a 3.1 to 8.3-
cooperative rearing of their young (Silk, fold increase in mortality risk in the year
2007). following their mother’s death (Foster et
Furthermore, the ability to engage al., 2012a). Therefore, in orcas it appears
in social learning through complex forms that a healthy mother-offspring bond is
of communication allows for the not only critical to calf survival, but also to
horizontal transmission of culture in that of her adult sons.
animal societies, which may promote By contrast, wild-caught orcas in
survival and adaptation to changing captive facilities have been removed from
environments (Whitehead et al., 2004). the ocean as young calves, sometimes
Thus, the evolution of sociality and as early as one year of age, resulting in
accompanying emotional complexity are an abrupt severing of the strong maternal
intimately tied to survival, which helps and family bonds upon which they
explain why social animals expend fundamentally depend for their health,
tremendous energy to establish and well-being and proper development.
maintain healthy social networks and why Captive-born orcas—who account for
they pay such an enormous cost when most of the orcas in captivity in the US
denied the ability to form species- today—have it no better, often
appropriate social bonds (Silk, 2007). experiencing insults to their social well-
As highly social animals, orcas being from the moment they are born into
depend upon healthy and robust social an unnatural, and frequently unhealthy,
relationships for proper neuroanatomical social environment. In the wild, female
and psychological development, as well orcas with calves would be surrounded
as the maintenance of mental health by a support network of related females
throughout life. As with most highly social (Foster et al (2012b), who would
species, the foundation to a healthy participate in protecting and rearing the
social life begins with a strong maternal newborn. Captive female orcas are
bond that develops between mother and typically deprived of a healthy social
infant. Disruption of this bond results in network upon which to depend for
severe, life-long consequences. Orcas physical or psychological support in
have a prolonged period of maternal infant rearing. Additionally, captive orcas
dependence after birth, with mothers have often endured early-life social
demonstrating a long inter-birth interval traumas themselves, which are
associated with investment in individual associated with long-term compromise of
social competence and maternal success
14
Harmful Effects of Captivity and Chronic Stress on the Well-being of Orcas Journal of Veterinary Behaviorlater in life, as has been described for This same mother rejected both
other species (Braun and Champagne, calves and repeatedly attacked them
2014; Hampson and Schwitzer, 2016). shortly after birth so they had to be
Thus, maternal neglect and separated from her. Furthermore, those
incompetence are all too common separations occurred within hours/days
phenomena in captive orca mothers of their birth and each was subsequently
(e.g., Visser and Lisker, 2016). The result isolated and hand-reared. Another calf
is that mother-calf separation, social separation was forced upon a wild-born
isolation, alienation, failure to nurse and female, held at the same facility, due to
subsequent hand-rearing, as well as the an alleged lack of milk, despite a strong
transfer of conspecifics or calves to other social bond exhibited by the mother. The
facilities, are all traumatic consequences mother repeatedly returned to the gate of
that often follow the birth of an orca calf the small (4.2x7.1 x 12.4 m) enclosure
in a marine theme park, aquarium or zoo. holding her calf, apparently in an attempt
to reunite with her (Free Morgan
To illustrate, Loro Parque is a Foundation, unpublished data). Social
relatively new facility (orcas were first isolation was also imposed on the other
housed there in 2006), located in the two calves born at Loro Parque, one for
Canary Islands, Spain. The four founding over 12 months and the other from birth
orcas (two males, two females, all captive until the day of her death (at 10 months,
born at various SeaWorld facilities in the 13 days old). As such, the separation
USA), were separated from their mothers issues have continued for the next
at very early ages (all less than 4 years, generation of orcas (Supplemental
see Supplemental Material, Table 1, for Material, Table 1).
details). With no mature females in the
founding stock, the social structure has Orcas in captive display facilities are
resulted in one of the most dysfunctional housed in artificial, man-made social
groupings of orcas ever held in captivity groups, which exacerbates social
(Visser and Lisker, 2016). The social stressors. Orcas in these groups, which
stressors these orcas were exposed to are frequently composed of individuals
were not limited to separation, but from genetically-distinct populations, are
included, inter alia, extremely unstable confined to concrete tanks a fraction the
social networks (one orca was size of their natural home range. The
transferred to five facilities, with different result of such unnatural confinement,
orca hierarchies at each park). artificial group composition, and captive
Inbreeding (uncle with niece) has breeding is that chronically disrupted
occurred in two of the three calves born social hierarchies, social tension, and
at Loro Parque. The mother of both heightened aggression are fundamental
inbred calves gave birth when she was to captive orca life. Similarly, free-ranging
under 8.5 years of age. In the wild, most orca social networks are weakened by
(77%) female orcas produce their first the loss of key individuals (Williams and
viable calf between 11 and 17 years of Lusseau, 2006), which is comparable to
age, but a few are primiparous as early the common practice of transferring
as 9 or as late as 21 years of age (Olesiuk captive individuals from one facility to
et al., 2005). The violations imposed on another.
this captive female were amplified when
she was impregnated only 123-135 days There is a large body of scientific
(4.1 to 4.5 months) after she gave birth. literature showing a strong relationship
Her second calf was born 661 days after among social isolation, chronic social
the first (i.e., 1.8 years). Typical (90%) stress, and depression in humans and
inter-calf interval in the wild is 3-7 years, many other mammals (Sandi and Haller,
although a few cases (3%) are as brief as 2015). In captive cetaceans, social
2 years (Olesiuk et al., 2005). alienation, instability, and subordination
15
Harmful Effects of Captivity and Chronic Stress on the Well-being of Orcas Journal of Veterinary Behaviorcan contribute to the development of stress to naturally wide-ranging species
illness and even death (Waples and by preventing species-typical behavior.
Gales, 2002). Wide-ranging carnivores held in confined
exhibits show typical physiological signs
The Stress of Confinement of chronic stress, such as adrenal
In humans, chimpanzees, and hypertrophy (Terio et al., 2004).
other animals, conditions of confinement Sensory Deprivation and Stress
have been associated with posttraumatic
stress disorder (PTSD), depression, and Much of the sensory information orcas
other mental disorders ( Başoğlu, 2009; evolved to expect and process is either
Ferdowsian et al., 2011; Aloni et al., substantially altered or absent in
2018), which are in part explained by the concrete tanks. Studies have shown that
influence of chronic stress on these factors affect animal behavior,
dysregulation of the HPA axis. Like other psychological well-being, and stress
wide-ranging mammals (Mason, 2010), levels, as well as sensory capacities
orcas are vulnerable to stress from (Couquiaud, 2005; Parsons, 2013; Clegg
confinement. The minimum USA and Butterworth, 2017, for reviews).
standards for orca enclosures of 15m for
horizontal distance and 4m for depth The natural environments of orcas
clearly do not meet the physical needs of contain multiple forms of auditory stimuli,
orcas (with a typical size of 5-8m across but cetaceans, as all marine mammals,
both sexes), including, inter alia, a range are adapted to the sounds they
of natural movements, postures, and encounter in the ocean (Couquiaud,
behaviors (Joseph and Antrim, 2010; 2005;Weilgart, 2007). Anthropogenic
Rose et al., 2017). sounds, in the ocean and in captive
enclosures, may pose unique challenges
Morgan and Tromborg (2007) to the auditory system and physiology of
noted that the negative impacts of cetaceans. A growing body of research
enclosure size are related to the natural has found that exposure to excessive or
history of a species, including the unnatural levels or types of acoustic input
roaming behavior of wild populations. For can cause a number of impacts to
example, in captivity, orcas are unable to cetaceans, including but not limited to
swim the distances or depths they would decline in reproductive success (due to
normally achieve. Abundant evidence physiological and behavioral changes),
shows that when a species is accelerated aging, suppression of the
physiologically adapted to large home immune response, as well as premature
ranges, the opportunity to travel is critical hearing loss (Romano et al., 2002;
to the health and well-being of its Weilgart, 2007, Wright et al., 2007).
members (Clubb and Mason, 2003; These impacts may be worsened in
Mason, 2010, McPhee and Carlstead, captivity, as cetaceans cannot evade or
2010). The confinement of naturally wide- escape aversive noises present in tanks
ranging mammals causes chronic stress and their surroundings (Couquiaud,
(Dawkins, 1998) and impairs the 2005). Nevertheless, the acoustic quality
development of brain structures involved of tanks and performance stadiums has
in sequencing behavior, thus decreasing often been neglected in the design of
behavioral flexibility (Robbins et al., captive cetacean enclosures
1996; Lewis et al., 2006). For example, (Couquiaud, 2005).
Clubb and Mason (2003, 2007) found
that natural home-range size predicted Processing of acoustic input by
captive infant mortality and stereotypic cetaceans in captive environments is
pacing behavior in carnivores, and that affected by many aspects of concrete
captive environments cause the most tanks and the surrounding stadium,
particularly the tendency of these
16
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