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Can We Assess Marine Mammal Welfare in Captivity and in the Wild? Considering the Example of Bottlenose Dolphins



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.
Aquatic Mammals 2018, 44(2), 181-200, DOI 10.1578/AM.44.2.2018.181
Can We Assess Marine Mammal Welfare
in Captivity and in the Wild?
Considering the Example of Bottlenose Dolphins
Isabella L. K. Clegg1, 2 and Fabienne Delfour1, 2
1Laboratoire d’Ethologie Expérimentale et Comparée EA.4443, Université Paris 13, Villetaneuse, France
2Parc Astérix Delphinarium, Plailly, France
Abstract Key Words: animal-based measures, animal
welfare, bottlenose dolphins, Tursiops truncatus,
The welfare of a range of terrestrial animals can marine mammals, welfare assessment
now be objectively estimated thanks to the well-
established, but still expanding, field of welfare What Is Animal Welfare Science?
science. Despite continuing difficulties regarding
definitions, it is generally agreed that welfare is Defining Animal Welfare
assessed most accurately using multiple “ani-
The concept of animal welfare appeared rapidly on
mal-based measures”—that is, those evaluating
the public agenda in the 1960s after reports started
aspects of the animal itself such as its behaviour.
to emerge detailing the conditions within inten-
In addition, scientists combining behavioural,
sive farming systems (Veissier et al., 2008). The
physiological, and cognitive animal-based indica-
study of animal welfare has since been established
tors of welfare have found this approach is supe-
and expanded to laboratory, companion, and now
rior to using one-dimensional measures. But can
zoo-housed animals (Webster, 2005; Whitham &
the same approaches be used for marine mam-
Wielebnowski, 2013). Numerous definitions of
mals, and would assessments of their welfare have
animal welfare were proposed during this time that
the same relevance in captivity as in wild environ-
generally fell into either “health-based,” “natural-liv-
ments? There is no reason why not, and we review
ing,” or “feelings-based” definitions, depending on
the past decades of marine mammal research
which of these three factors researchers thought to be
relevant to welfare, as well as the more recent
most influential to the overall state of welfare (Fraser
advances in the field where this topic is starting to
et al., 1997). Although a single definition has still not
be addressed directly. We then use the example of
been agreed upon, there seems to be a general con-
bottlenose dolphins (Tursiops truncatus) to exam-
sensus that welfare is predominantly concerned with
ine what the measures within an all-encompassing
how the animal is feeling (Broom & Fraser, 2015;
(i.e., “comprehensive”) welfare assessment might
Dawkins, 2015). Health can of course greatly influ-
look like. Looking to the future, we suggest direc-
ence welfare through altering how an animal feels,
tions for developing assessments for captive ani-
and a “natural” way of life is relevant in certain situ-
mals and explore how protocols might differ in
ations and, thus, is still included in some welfare
wild settings. In conclusion, we find that the first
paradigms. However, “feelings-based” definitions of
steps are being made towards objectively assess-
welfare are most often adopted in studies indepen-
ing marine mammal welfare in captivity—through
dent of the species concerned (Bracke et al., 1999;
application of terrestrial animal approaches as
Spruijt et al., 2001; Boissy et al., 2007; Yeates &
well as through novel paradigms. Regarding bot-
Main, 2008; Mason & Veasey, 2010; Watters, 2014).
tlenose dolphins, several welfare measures have In this review, we also advocate that an ani-
been proposed and should now be further vali-mal’s welfare concerns how it is feeling, and we
dated and applied. It is hoped that this review will follow the specific definition proposed by Spruijt
encourage continued research in marine mammal et al. (2001), which states that welfare is “a bal-
welfare assessment given the demonstrated initial ance between positive (reward, satisfaction) and
achievements of bottlenose dolphin welfare stud-negative (stress) experiences or affective states.
ies and the potential for application to many dif-The balance may range from positive (good wel-
ferent captive and wild contexts. fare) to negative (poor welfare)” (p. 159). When
182 Clegg and Delfour
welfare state is considered as a product of an ani-
this topic, and perhaps also due to the relatively
mal’s feelings, the study of emotion and affective
recent acceptance that animals are indeed likely
states becomes key in developing welfare mea-
to experience a range of emotions and affective
sures and assessments (Désiré et al., 2002; Boissy
states, it is now agreed upon that positive emotions
et al., 2007; Yeates & Main, 2008). Affective
and welfare should be measured and promoted as
states are defined as free-floating mood states,
part of good practice protocols (Boissy et al., 2007;
resulting from shorter-term emotions and feel-
Yeates & Main, 2008; Mellor & Beausoleil, 2015).
ings stimulated by the individual’s environment,
Thus, more recent welfare definitions, such as that
and research on these phenomena in humans and
of Spruijt et al. (2001) followed in this review, dis-
other species has guided the principles used when
cuss a continuum of poor to good welfare for which
assessing animal welfare (Russell, 2003; Paul
the balance of positive and negative experiences
et al., 2005; Mendl et al., 2010).
dictates the welfare state at a given point in time
(Boissy et al., 2007; Yeates & Main, 2008; Watters,
Principles of Assessing Welfare
Welfare science has many applications for improv-Another aspect of welfare assessments is that
ing the lives of animals kept by humans. To pro-two different types of welfare measures are gen-
mote good welfare and avoid poor welfare for an erally used: (1) animal-based measures (data are
animal, we must be able to measure welfare objec-taken directly on the animal’s behaviour and health,
tively. It is worth noting here that a fundamental for instance) and (2) resource-based measures (data
aspect of assessing welfare is its inherent subjectiv-taken from resources provided to animal, e.g.,
ity. In fact, we will never be able to completely and enclosure space). Resource-based measures were
accurately measure this subjective and transitional used more frequently in earlier assessments and
state. However, this should not deter researchers research because they are more practical and easier
since the use of many multidimensional indicators to standardise (Whay et al., 2003; Veissier et al.,
over a sufficient time frame can certainly lead us to 2008). Although resource-based welfare measures
informed estimations of an animal’s level of wel-still constitute welfare laws and regulations in most
fare (Dawkins, 2006; Blokhuis, 2008). Thus, the cases (e.g., for zoo animals: Animal Welfare Act,
second key principle of measuring welfare is that 1966; EC Council Directive, 1999), data yielded
it is a holistic, all-encompassing phenomenon that from animal-based measures are now considered to
should thus be assessed using multidimensional be more accurate indicators of an animal’s welfare
measures (Whay et al., 2003; Boissy et al., 2007; (Dawkins, 2006; Whitham & Wielebnowski, 2009;
Yeates & Main, 2008). The main categories of these Roe et al., 2011).
different measures are behaviour, physiology, and
General welfare paradigms, such as the Five
cognition since they are also the three components
Freedoms (Farm Animal Welfare Council [FAWC],
of emotional responses (Désiré et al., 2002; Paul
1992) or the Five Domains (Mellor & Reid, 1994),
et al., 2005). Webster (2005) explained the func-
which detail the different aspects of any animal’s life
tion of multiple measures using the Triangulation
in general terms, are often used to select and organise
principle, wherein the three components of wel-
the measures included within species-specific
fare measures are points on a triangle, and the true
welfare assessments (Welfare Quality®, 2009a;
centre is the animal’s actual welfare: the predicted
Mononen et al., 2012; Clegg et al., 2015). After the
welfare state starts on one of the points when we
initial proposal for an assessment, the validity of the
have information from a one-dimensional measure,
selected measures should be confirmed—that is, are
and adding second and third bearings (measures
they measuring what they intend to measure (Rushen,
from other components or “dimensions”) brings
2003). Validation is usually conducted in separate
the predicted welfare ever closer to the centre. So,
studies from which a few potential measures from
when developing a welfare assessment (a group of
different disciplines (e.g., behavioural and physi-
welfare measures), researchers include measures
ological) may be applied concurrently to animals
from different dimensions to capture as much
in contexts of highly likely poor and/or good wel-
information about the animal’s internal state as pos-
fare (Désiré et al., 2002; Castellote & Fossa, 2006),
sible and, thus, make a more accurate evaluation of
or through using large-scale epidemiological data
welfare (Whay et al., 2003; Pritchard et al., 2005;
(Rushen, 2003). In a significant advance for animal
Clegg et al., 2015).
welfare science, a novel technique from human
In the past, welfare research and assessments experimental psychology through which the cogni-
have been heavily focussed on identifying signs tive bias of an animal is tested has also been shown
of poor welfare in animals, where good welfare to be able to validate welfare measures (Harding
was thought to result from an absence of suffering et al., 2004; Mendl et al., 2010). Cognitive biases,
(Dawkins, 1980; Broom & Johnson, 1993). As data which are present in humans and animals, describe
and practical knowledge have increased regarding the effect an individual’s emotional state has on
183Assessing Marine Mammal Welfare
cognitive processing (e.g., making a judgment). For
measures are often used (e.g., Draper & Harris,
example, it has been shown in a wide range of spe-
2012). However, there is a noteworthy amount of
cies that when placed in poorer welfare situations,
zoo research that has been conducted on single
more pessimistic judgments are made and vice versa
measures of welfare that could be developed to
(latest reviews by Baciadonna & McElligott, 2015;
be included in overall assessments, including
Roelofs et al., 2016). Therefore, correlating animals’
cortisol measurement (Menargues et al., 2008),
cognitive biases to potential indicators of welfare is
stereotypic behaviour (Shepherdson et al., 2013),
starting to be used as a method of validation (e.g.,
and qualitative keeper assessments of behaviour
Wichman et al., 2012; Clegg et al., 2017a).
(Whitham & Wielebnowski, 2009). In general,
studies in this setting are making significant prog-
Examples of Welfare Assessments ress towards rendering potential welfare indica-
The key principles above are integrated in several tors “measurable,” such as the recent work on the
established welfare assessment protocols, mostly play behaviour of African elephants (Loxodonta
within the farming sector. The 2004 Welfare africana) (Vicino & Marcacci, 2015), and others
Quality® project developed extensive welfare are starting to validate chosen measures by cor-
assessments of 30 to 50 measures for farmed pigs relating them with other welfare data (e.g., using
(Sus scrofa domesticus), cattle (Bos taurus), and behavioural and physiological indicators; Pifarré
laying hens (Gallus gallus domesticus) (Welfare et al., 2012; Baird et al., 2016). Encouraging dis-
Quality®, 2009a, 2009b, 2009c), which are slowly cussions have also started on establishing uni-
being incorporated into codes of best practice versal zoo welfare frameworks that include more
and European strategies (Blokhuis et al., 2010). animal-based measures (Kagan et al., 2015).
While the individual measures were species-spe-
Regarding animals in the wild, it is only
cific, the overarching principles and criteria of the
just being acknowledged that assessing their
Welfare Quality® Assessments can be adapted to
welfare is even possible or worthwhile, despite
other animals (Botreau et al., 2012), and this first
some protagonists pointing out the significant
occurred for farmed foxes (Vulpes spp.) and mink
benefits that measuring welfare could have for
(Neovison vison) (Mononen et al., 2012), and
conservation projects, public outreach, and the
more recently shelter dogs (Canis lupus familia-
animals themselves (Kirkwood et al., 1994; Paquet
ris) (Barnard & Ferri, 2015) and bottlenose dol-
& Darimont, 2010; Papastavrou et al., 2017). There
phins (Clegg et al., 2015). The Welfare Quality®
are, however, a few examples of studies teaming
framework is seen by the field as a comprehen-
welfare science principles to wild marine ani-
sive, standardised, and practical way to measure
mals. For example, the issue of marine debris was
animal welfare, but one which needs more devel-
examined in terms of impacts on individual animal
opment on aspects such as assessing emotional
welfare (Butterworth et al., 2012). A recent review
states (Botreau et al., 2007; Mellor, 2016).
was conducted outlining specific measures that
The Welfare Quality® project has been the
might be applied to wild dolphin welfare assess-
most ubiquitous and well-validated effort towards
ments (Clegg et al., 2017b). Finally, with the aim
establishing welfare assessments (Blokhuis et al.,
of establishing effective conservation protocols for
2010; Veissier et al., 2013); nevertheless, there
cetaceans, the International Whaling Commission
are other approaches which have also garnered
(IWC) proposed a Five Domains Model adapted
support. One of these is the Five Domains Model,
to wild cetaceans (Butterworth, 2017b). Therefore,
which is fundamentally based on the Five Freedoms
although wild animal welfare measurement is only
but differs in that it facilitates measurement of the
just emerging in the scientific domain, the applica-
degree of the impaired freedom (poor welfare)
tions for marine mammals and their conflicts due
(Mellor, 2016). Developed in New Zealand, this
to anthropogenic causes seem to be high on the
model has been incorporated in the country’s
agenda (Papastavrou et al., 2017).
regulations for research, teaching, and testing Given the progress in the field and the
manipulations, and it is being worked on further approaches to welfare assessments discussed
to allow measurement of positive affective states above, we see no reason why such developing
as well (Mellor & Beausoleil, 2015). The Welfare welfare measures should not be achieved for
Quality® Assessments and the Five Domains marine mammals. In the next section, we examine
Model have been used almost exclusively in the whether any welfare measures exist already and
farming and laboratory animal industries; and compile those studies that have been conducted on
apart from the C-Well© Assessment for bottlenose topics that are closely related to marine mammal
dolphins (Clegg et al., 2015), there are very welfare. Since welfare research on bottlenose dol-
few examples of animal-based, comprehensive phins is the most advanced (Clegg et al., 2017b),
assessments for zoo-housed species. Instead, we use examples of measures for this species
resource-based questionnaires with unvalidated where appropriate.
184 Clegg and Delfour
What Research Has Been Conducted on
was a much stronger focus on behaviours that
Marine Mammal Welfare?
later have been shown to be linked to emotional
states (Kastelein & Wiepkema, 1988; Gygax,
Early Studies Linked to Marine Mammal Welfare
1993; Galhardo et al., 1996). A few years later, a
Despite the recent public and media attention sur-
study on bottlenose dolphins explicitly attempted
rounding marine mammal welfare in captivity
to identify indicators of poor welfare, finding that
(Jiang et al., 2007; Ventre & Jett, 2015), very few
social isolation, inappetence, changed relation-
studies have posed direct questions on how to mea-
ships with humans, and increased rake marks all
sure these animals’ quality of life (Ugaz et al., 2013;
resulted from severe social stress (Waples & Gales,
Clegg et al., 2017b). However, while not explicitly
2002). An investigation into the acoustic behav-
investigating animal welfare, there are many stud-
iour of two belugas (Delphinapterus leucas) found
ies on wild and captive marine mammals that focus
that vocalisation rate decreased temporarily after
on measures relevant to welfare and could one day
transportation to a new facility, leading it to be
be included in overall assessments. Reviews com-
suggested as a welfare indicator (Castellote & Fossa,
piling the literature relevant to potential welfare
2006). In the next decade or so, perhaps due to the
measures for cetaceans and pinnipeds can be found
rise of environmental enrichment programs in zoos
elsewhere (see, respectively, Clegg & Butterworth,
and aquaria (Hoy et al., 2010), a large proportion
2017a, 2017b). Herein, we examine the progres-
of marine mammal welfare research focussed on
sion of welfare-focussed research on marine mam-
enrichment provision (e.g., Grindrod & Cleaver,
mals to understand where the next advances in the
2001; Kuczaj et al., 2002).
field might occur.
While the study of marine mammals has been Marine Mammal Enrichment Studies and
well-established for decades, research effort is Their Relevance to Welfare
biased towards certain topics and certain species. When enrichment is defined precisely—as the
For example, cetaceans, bottlenose dolphins, and addition of stimuli or the provision of choices
killer whales (Orcinus orca) are the most investi-designed to stimulate any one or more of the
gated and are the marine mammals for whom the senses (Azevedo et al., 2007)—it does not nec-
topics of health, physiology, and distribution are essarily impact the welfare state of the animal.
predominantly focussed (Hill & Lackups, 2010; A more general definition often used is that
Hill et al., 2016). Therefore, welfare-related find-enrichment is any husbandry activity that aims
ings in past studies can be found but are not rep-to improve animals’ well-being, and this is often
resentative of all marine mammal species or all misconstrued, resulting in enrichment being con-
aspects of welfare measurement. Many early stud-sidered as something that always improves wel-
ies in the wild and captivity that looked at stress fare (Hoy et al., 2010). In addition to being inac-
hormone concentrations in different species (e.g., curate, this assumption has resulted in enrichment
in harbour seals [Phoca vitulina]: Riviere et al., programs and related research often not attempt-
1977; and bottlenose dolphins: Thomson & Geraci, ing to measure the welfare impacts (Newberry,
1986) have helped to build baselines for indicators 1995; Hoy et al., 2010). Marine mammals live in
such as cortisol levels, which have been used as an environment very different to our own where
a welfare measure for farm and domestic animals they enact subjective worlds (Delfour, 2010b);
(e.g., Carlstead et al., 1993; Gimsa et al., 2012). and as humans, we continue to make anthropocen-
Health and other physiological parameters were tric assumptions about which enrichment items
often investigated in early wild and captive studies; should increase welfare the most. Unfortunately,
and as a result, there are many reviews on disease we are often wrong—for example, bottlenose
symptoms and prevalence in marine mammals (see dolphins played more with simple versus complex
Dunn et al., 2001; Miller et al., 2001; Van Bressem enrichment objects (Delfour et al., 2017). The last
et al., 2008). Although social and other behaviours problem is that since validated welfare indicators
appeared less frequently in the literature, long-term are sparse for most species (Rushen, 2003), even
studies were starting to establish themselves and if enrichment studies want to measure the welfare
used their identification abilities and life-history impacts, the tools to do so are often lacking (Clegg
knowledge of populations to publish on welfare- et al., 2015).
relevant topics such as affiliative and aggressive
So, what have marine mammal enrichment
behaviour (Herzing, 1996; Herzing & Johnson,
studies shown so far, and can they be relevant to
1997) and reproductive behaviour (reviewed in
welfare measurement? In the 1990s and 2000s,
Wells, 2009).
several studies published data on providing
In the 1990s, the first marine mammal studies enrichment to captive marine mammals. “Toy”
to use the term welfare emerged, and although the objects (Kuczaj et al., 2002), acoustic stimulation
animals’ feelings were still not discussed, there (Berglind, 2005), pool design changes (Krajnaik,
185Assessing Marine Mammal Welfare
1996), and cognitive challenges (Reiss, 2006) within the zoo industry. The framework, termed
have been presented to dolphin species, and all of the C-Well© Assessment, was adapted to bottlenose
the above to pinniped species (e.g., Kastelein & dolphins from the well-established Welfare Quality®
Wiepkema, 1989; Wassel et al., 1996; Grindrod & Assessments (2009a, 2009b, 2009c). First, species-
Cleaver, 2001). In most of these studies, the time specific measures were proposed using the literature
spent with the items is measured and, according to and tested for face validity using expert opinion.
a subjective assessment, the authors conclude that They were then tested for feasibility on 20 bottlenose
the enrichment is “successful”; however, can we dolphins from three facilities and were partially
say that animal welfare has been improved? Later validated using contexts such as sick animals or
in the 2000s, we started to realise far more detailed social disturbances. The C-Well© Assessment is
assessments would have to take place to discover made up of 36 multidimensional measures, 58% of
whether enrichment was actually leading to good which are animal-based, and produces individual
welfare, and a number of papers provided some welfare scores which can be compared on many
direction for how to achieve this in marine mammals levels such as by age, sex, group, or facility.
(Delfour & Beyer, 2012; Clark, 2013; Clegg et al., However, the assessment needs more work to fully
2015). Subsequently, recent studies are more often validate the measures, which are also currently
conducting meticulous analyses of the animal-based unweighted. Nevertheless, the project developed
impacts of enrichment; and by using this work, we standardised methods and scoring thresholds for
can see that enrichment indeed has the potential to measuring dolphin welfare and represents a first step
promote positive welfare states in marine mammals. towards practical assessments in zoo settings.
For example, Australian sea lions (Neophoca cine-Concurrently, separate studies from different
rea) showed less stereotypic swimming after toy research groups have been conducted on measures
objects were introduced (Smith & Litchfield, 2010), which are included in the C-Well© framework
and Australian fur seals (Arctocephalus pusillus or closely related. For example, advances have
doriferus) showed higher behavioural diversity after taken place in our understanding of dolphin play
foraging-based enrichment was applied (Hocking and affiliative behaviours, which are commonly
et al., 2015). The diversity of belugas’ play behav-used indicators of positive welfare in other species
iours increased when enrichment items were pres-(Boissy et al., 2007; Held & Špinka, 2011) in terms
ent (Hill & Ramirez, 2014), and bottlenose dolphins of influencing factors (Dudzinski & Ribic, 2017;
interacting with a cognitive enrichment device then Harvey et al., 2017; Serres & Delfour, 2017) and
became more interested in the underwater aspect of the links with emotion (Paulos et al., 2010; Kuczaj
their home environment (Clark et al., 2013). These et al., 2013). Research reporting the first cognitive
studies measured potential animal-based measures bias tests conducted with marine mammals show
of welfare during enrichment to suggest that it has that optimistic decisions in bottlenose dolphins
positive effects. After further validation of such were correlated to higher levels of synchronous
measures, these correlations could aid future welfare swimming in their free time, suggesting that fol-
studies for which the proven “positive impact” of lowing further investigation, this affiliative behav-
enrichment devices could be used to simulate posi-iour could be used as an objective welfare indicator
tive affective states (Clegg & Butterworth, 2017a). within assessments (Clegg et al., 2017a). Holistic
assessments of pinniped and other marine mammal
Recent Advances: Comprehensive Assessment of
species’ welfare are notably less common than for
Marine Mammal Welfare
cetaceans. A unique report on sea lion species’ wel-
In the last few years, the advances made in ter-fare in circuses started the discussion for pinnipeds;
restrial animal welfare science seem to have led and although consensus was reached among experts
to a notable increase in the amount and quality of regarding the important resource-based measures,
investigations with marine mammals. In particular, there was much variation on the animal-based eval-
we are seeing the first studies attempting to mea-uations, and it was concluded that more research
sure marine mammal welfare using multidimen-was urgently needed (Hopster & de Jong, 2014).
sional, animal-based measures of both positive and In one of the first references to emotions and pin-
negative welfare leading to more comprehensive, nipeds, a study recently found some indications that
holistic evaluations. A multi-facility study found motor lateralisation was caused by changes in emo-
bottlenose dolphins had higher levels of cortisol tional state in captive California sea lions (Zalophus
when kept in a closed versus open system, which californianus), but again, more research is needed
itself was correlated to higher levels of floating and before conclusions are able to be made for welfare
circular swimming (Ugaz et al., 2013). A welfare or its measurement (Le Ray et al., 2017).
assessment protocol for dolphins was developed
There has also been some movement in wild
by Clegg et al. (2015), representing the first appli-
marine mammal research towards develop-
cation of an operational farm animal assessment
ing welfare assessments. Recently, it has been
186 Clegg and Delfour
promulgated in multiple reviews that such assess-to only consider health problems of animals in
ments would greatly aid conservation and eco-terms of their impact on emotional and affective
logical objectives (Paquet & Darimont, 2010; states (Fraser et al., 1997; Mason & Veasey, 2010;
Papastavrou et al., 2017; Seuront & Cribb, Clegg et al., 2017b). In other words, an asymp-
2017). Perhaps in response to these recommen-tomatic tumour with no resulting pain would not
dations, the IWC has taken a large step forward be considered to cause poor welfare in an animal,
and is in the early stages of developing a com-but an infection that results in inappetence, pain,
prehensive assessment for wild cetaceans using and sickness could indeed be used as an indirect
the Five Domains Model to develop measures measure of poor welfare. Nevertheless, the rela-
for as many aspects of the animals’ lives as pos-tionship between health and affective states is
sible (Butterworth, 2017b). Given the advances complex and not fully understood in humans or
in marine mammal welfare research described animals: negative affective states have a poten-
above, there have also been multiple reviews tial impact on morbidity, mortality and longev-
recently published on what types of specific ity (Walker et al., 2012). Therefore, we consider
measures might be included in cetacean (Clegg a few key health measures that might be linked
& Butterworth, 2017a; Clegg et al., 2017b) and to bottlenose dolphin welfare (for a larger review,
pinniped (Clegg & Butterworth, 2017b) welfare see Clegg et al., 2017b).
assessments in both wild and captive settings. The main impacts of an infection or disease on
Therefore, in answer to the question of whether an animal’s affective state are pain and/or “sickness
marine mammal welfare is already being stud-behaviour,” which describes a suite of effects in-
ied, we can see that (1) decades of research on cluding inappetence, lethargy, depression, and anti-
unidimensional but relevant measures are slowly social behaviours (Broom, 1991; Millman, 2007;
starting to be gathered together and integrated, Sneddon et al., 2014). Therefore, developing mea-
(2) farm animal welfare techniques are being tri-sures for these indicators of poor health would
alled and adapted successfully in captive settings, certainly be useful as part of welfare assessments
and (3) the first few examples of comprehen-and would be feasible for sickness behaviours. Pain
sive assessments are emerging but by no means is more difficult to measure in dolphins since they
well-established. We will now further investigate are known to mask their symptoms for adaptive
what the exact measures within a welfare assess-reasons (Waples & Gales, 2002; Castellote & Fossa,
ment might be and how they would be conducted. 2006), and, thus, proxy measures of pain may have
For this, we will use the bottlenose dolphin as a to be used such as the severity of injuries or a
specific example since the species has the most developmental stage of the disease (as proposed in
research available in this area. Clegg et al., 2015). Body Condition Scoring (BCS)
is used in many farm animal welfare assessments
What Are Some Potential Welfare Measures (Welfare Quality®, 2009a, 2009b, 2009c; Mononen
of Bottlenose Dolphin Welfare? et al., 2012) since it is a good overall reflection of
health status. BCS has been used in wild cetacean
While the potential measures are reviewed sepa-health assessments (Hart et al., 2013; Joblon et al.,
rately in this section, the objective would always 2014) and was also suggested as a bottlenose dol-
be that they are conducted as part of a comprehen-phin welfare measure (Clegg et al., 2015). In set-
sive assessment as this is the most accurate way tings where individual welfare measures are not
to measure welfare (Bracke et al., 1999; Webster, possible (i.e., for some wild populations), epide-
2005; Botreau et al., 2007). The measures are miological measures such as morbidity and repro-
organised into three main categories according ductive success can still give us some idea of health
to the Triangulation principle discussed earlier and possibly welfare (Dawkins, 1998; Barber,
(Webster, 2005): (1) physiology, (2) behaviour, 2009). Since such measures are not always accurate
and (3) cognition. Although health parameters are welfare indicators (e.g., fecundity in farm animals),
not thought to be directly involved in emotional the most effective use of epidemiological data are
responses, we start by examining their utility in in conjunction with other animal-based measures
welfare frameworks for bottlenose dolphins. (Dawkins, 1980). For example, a recent study on
minke whales (Balaenoptera acutorostrata) found
Health Parameters in Relation to Welfare correlations between disturbance behaviour from
Since welfare science was born out of veterinary whale-watching boats, body condition, and foetal
medicine, welfare evaluations were traditionally growth (Christiansen & Lusseau, 2015), thus ren-
linked closely with the health status of an animal dering foetal growth a meaningful welfare measure
(Dawkins, 2006). More recently, and especially for when the other sources of data are not avail-
for those adopting the “feelings-based” defini-able. More studies are needed, and more data needs
tions of welfare as we have here, it is common to be published, on baselines for epidemiological
187Assessing Marine Mammal Welfare
parameters in captivity and in the wild to supple-
et al., 2014; Biancani et al., 2017). Cortisol mea-
ment those available (for T. truncatus: Small &
surement was proposed as a measure in the C-Well©
Demaster, 1995; Innes et al., 2005; Reif et al.,
Assessment of Clegg et al. (2015), and a few studies
2008; Schwacke et al., 2014) before such measures
are available showing potential correlations to
would be deemed valid enough to use as welfare
welfare (e.g., Ugaz et al., 2013). The most significant
of these was able to demonstrate that an increase in
salivary cortisol could be detected on days in which
Physiological Welfare Measures
construction work was being conducted near to the
In terms of welfare assessment, physiological mea-
dolphin pool (Monreal-Pawlowsky et al., 2017).
sures (e.g., cortisol levels and breathing rate) are
In addition, there is still the ubiquitous problem
differentiated from health parameters in that they
that cortisol concentrations vary diurnally, and we
function to measure the physiological component
have not established reference baselines (Atkinson
of emotional responses (Désiré et al., 2002; Boissy
et al., 2015). Nevertheless, studies are continuing
et al., 2007). Physiological measures are advanta-
to work towards understanding the different sources
geous as they can indicate emotional responses
of variation, and it would be prudent to “watch this
which are not obviously seen in the animal’s behav-
space” for progress on using cortisol levels as a
iour, and they enable us to differentiate between
welfare measure for this species.
behaviours performed to satisfy a “need” (e.g.,
Other potential physiological measures linked to
finding food to reduce hunger and increase blood
welfare could be those linked towards respiration
glucose levels) and those performed with no link
rate and depth. An increased breathing rate has
to short-term physiological needs (e.g., grooming)
been shown in response to boat traffic in wild
(Boissy et al., 2007). While physiological indica-
dolphin populations (e.g., Janik & Thompson, 1996;
tors are often used in individual studies on farm
Nowacek & Wells, 2001) and is thought to be a sign
animal emotions and welfare (Reefmann et al.,
of stress in captive dolphins (St. Aubin & Dierauf,
2009; Leliveld et al., 2016), not many are included
2001; Jensen et al., 2013). However, no link was
in comprehensive welfare assessments due to prob-
found between breathing rate and cortisol concen-
lems with feasibility and standardisation of equip-
tration in wild harbour porpoises (Phocoena pho-
ment (Velarde & Dalmau, 2012; Veissier et al.,
coena); and since in bottlenose dolphins, breathing
2013). However, this could be a distinguishing
rate also increases with energetic output (Williams
point between farm and zoo animal welfare assess-
et al., 1999), this parameter might only be useful
ments since the former are often conducted on large
in terms of welfare as a measure of arousal. Other
groups and with limited means of identifying indi-
aspects of respiration, such as inhalation duration
viduals; while for the latter, it is more feasible and
or frequency of coughing, could be useful health-
often desirable that welfare is measured per indi-
related measures as they can indicate respiratory
vidual (Barber, 2009; Clegg et al., 2015). In addi-
disease (Dunn et al., 2001; Clegg et al., 2015). To
tion, the “trainability” of captive marine mammals
fully understand the impact of respiratory disease
(Brando, 2010) would allow many physiological
on the animal’s affective state, however, further
measures to be conducted non-invasively (when
work is necessary. Physiological measures such as
farm animals would need restraint or sedation), and,
heart rate and hear rate variability have been used to
thus, physiological measures might have a promi-
assess farm animal emotions (Rietmann et al., 2004;
nent role in bottlenose dolphin welfare assessment.
Coulon et al., 2015) but have not yet been applied in
Unfortunately, there are very few physiological
dolphin welfare investigations.
measures of emotion which have been sufficiently
studied in dolphins to merit their inclusion in a wel-Behavioural Welfare Measures
fare assessment; and, thus, for the moment, we can
Studying certain behaviours from an animal’s reper-
only outline a few that may be useful pending fur-
toire is increasingly believed to be the most informa-
ther research.
tive approach to measuring welfare (Gonyou, 1994;
Measuring cortisol levels (or those of its
Maple, 2007), and this is likely also true for marine
derivatives) is one of the most common physiological
mammals (Joseph & Antrim, 2010; Clegg et al.,
indicators of stress used with captive terrestrial
2017b). In general, there are still many unknowns
animals (e.g., Bachmann et al., 2003; Hekman et al.,
regarding marine mammal behaviour and its ontog-
2012; Palme, 2012) and those in the wild (e.g.,
eny (Hill & Lackups, 2010), so further ethological
Tarlow & Blumstein, 2007; Bechshoft et al., 2012).
studies on a range of species in the wild and captiv-
For bottlenose dolphins, cortisol concentrations
ity would certainly aid the development of welfare
can be measured from serum or plasma after blood
measures. Regarding bottlenose dolphins in par-
sampling (Thomson & Geraci, 1986; Ortiz &
ticular, those welfare indicators labelled as having
Worthy, 2000), and more recently from urine, faeces,
potential are almost all behavioural measures, and
and saliva (Pedernera-Romano et al., 2006; Fair
we discuss the most significant of these below.
188 Clegg and Delfour
Social Behaviours—Bottlenose dolphins, like
rubbing and contact is thought to reflect social bonds
many other delphinid species, live within com-
(Kuczaj et al., 2013; Dudzinski & Ribic, 2017) and
plex social networks (Shane et al., 1986; Wells,
has been shown to decrease the likelihood of aggres-
1991) and are dependent on close social bonds for
sive behaviour (Tamaki et al., 2006), and so could be
survival (Pack & Herman, 2006; Stanton & Mann,
investigated as a measure of positive welfare.
2012). Whether in the wild or captivity, this means
Social play is a prosocial beh
aviour generally
they are more likely to suffer from social stress taken to reflect positive welfare since it is thought
than animals that rely less on social bonds and to occur only when an animal’s primary needs have
group living situations (Waples & Gales, 2002). been satisfied (Held & Špinka, 2011; Bateson,
At the same time, they also may have greater 2014), although some caution has been advised
opportunities for achieving positive welfare states regarding its measurement and the fact that play can
as a result of strong bonds with others and stress evolve into bouts of fighting (Boissy et al., 2007).
buffering (Clegg et al., 2017b). Studies have confirmed that this is also the case with
The significant role of social stress in causing
dolphin play (see review by Kuczaj & Eskelinen,
poor welfare states has been documented in a variety
2014), and recent progress was made towards using
of species and contexts (e.g., Shively et al., 1997;
it as a welfare measure when researchers found
Sapolsky, 2005; Papciak et al., 2013). One study
captive bottlenose dolphins conducted less social
found social stress to be the likely cause of mortality
play when noisy construction work was occurring
and morbidity in three bottlenose dolphins, caused
next to the pool or agonistic interactions had taken
by social instability and the consequent aggressive
place (Serres & Delfour, 2017). The most meaning-
interactions (Waples & Gales, 2002). As suggested
ful way to measure dolphin play remains unclear
by the authors, indicators such as social isolation,
(Serres & Delfour, 2017), and attempts could be
inappetence, high aggression levels, and extensive
made to develop and validate an index such as that
rake mark coverage could be used as measures of
used for African elephants by Vicino et al. (2015).
social stress, and likely for poor welfare as well.
Synchronous swimming, when two or more
Rake marks have been proposed in a number of
dolphins swim in parallel, mirroring each others’
other cases as a proxy measure for aggression
movements, is perhaps the affiliative behaviour
since many aggressive encounters go unseen when
with the most convincing research supporting
studying wild and captive dolphins (Scott et al.,
it as a welfare measure thus far. This behaviour
2005; Marley et al., 2013), and the percentage
reflects social bonding in wild and captive dolphins
of new rake marks could be an objective way to
(Connor et al., 2006b; Holobinko & Waring, 2010;
measure this aspect of welfare (Clegg et al., 2015).
Sakai et al., 2010), and was found to be correlated to
Using actual levels of aggressive behaviour could
optimistic judgements made by captive dolphins in
also be a possible measure since this is used in
a study testing cognitive bias (Clegg et al., 2017a).
the Welfare Quality® frameworks (2009a, 2009b,
Optimistic judgement biases are known to be linked
2009c), but more investigation would be needed
to positive affective states, and the experimental
into whether both acting and receiving aggression
paradigm is one of the only well-validated tests
are linked to negative affective states or whether the
of welfare (Mendl et al., 2009, 2010). Further
relationship between dominance, subservience, and
investigations are still needed into this measure,
stress is more complicated as in some primate spe-
however, since synchronous swimming can also
cies (e.g., Abbott et al., 2003; Sapolsky, 2005).
be shown in stressful contexts during which it
In terms of how social behaviour can lead to
acts as a form of social support (Connor et al.,
positive welfare in animals, it is thought activities
2006a). Differentiating this behaviour by speed
such as close bonds, cooperative behaviour, and
and distance to partner could lead to certain types
prosocial tactile interactions (e.g., grooming and
of synchronous swimming being used as welfare
play) lead to positive affective states; however,
indicators (Clegg, 2017).
it is relatively difficult to prove this (Boissy et al.,
Lastly, interspecific social behaviour towards
2007; Yeates & Main, 2008; Mellor & Beausoleil,
humans can reveal much about an animal’s welfare
2015). Regarding dolphin species, our knowledge
(Whitham & Wielebnowski, 2009; Hosey & Melfi,
of affiliative social behaviour is relatively well-
2014) as well as representing an opportunity to
established thanks to studies in the wild (long-term
induce positive affective states itself (Hemsworth,
studies particularly, e.g., Herzing, 2000; Connor
2007; Whitham & Wielebnowski, 2013; Coulon
et al., 2006b), captivity (Tamaki et al., 2006; Harvey
et al., 2015). Despite captive marine mammals
et al., 2017), and those that have compared both
often having close working relationships with
(Dudzinski, 2010; Dudzinski et al., 2012). There
their caretakers and sometimes unfamiliar guests,
are a few behaviours that have been proposed to
which can involve much time spent in close con-
have links to positive emotions but have not yet
tact with each other, the human–animal relation-
been validated in this way—for example, pectoral
ship (HAR) is studied very little in this setting
189Assessing Marine Mammal Welfare
(Clegg & Butterworth, 2017a). Past results have from farm animal frequencies (Clegg et al., 2015).
been mixed regarding dolphin behaviour towards More research is also needed on negative affec-
unfamiliar guests swimming with them (Frohoff & tive states such as boredom and frustration which
Packard, 1995; Kyngdon et al., 2003; Trone et al., are also likely to be key correlates of understimu-
2005). Concerning their familiar trainers, a study lating environments and could be used to supple-
showed that bottlenose dolphins voluntarily sought ment measures of stereotypies (Mason et al., 2007;
tactile contact out of feeding sessions (Perelberg & Burn, 2017). A study on zoo elephants found the
Schuster, 2009), while another recent investigation odds of performing stereotypies increased by 26%
confirmed that they positively anticipated non-food for every 10% increase in time housed separately
tactile interactions with trainers and more than the (Greco et al., 2017). Frustration and boredom in
provision of enrichment (Clegg et al., 2018). This captive dolphins is barely discussed in the literature
partially validates the comparable HAR measure (Clark, 2013), and future work will have to use the
included in the C-Well© Assessment (Clegg et al., few speculative indicators proposed (e.g., excessive
2015), based on a simple approach-avoidance test anticipatory behaviour and tail slaps/side breaches;
used for farm animals (De Passillé & Rushen, 2005). Clegg, 2017) and create experimental paradigms to
More work is needed on this aspect of captive dol-test these.
phins’ lives since training sessions and public pre-
Anticipatory Behaviour—The behaviour an
sentations make up a large part of their daily routine
animal performs in preparation for a predictable,
(Clegg et al., 2017c), and results may be able to aid
upcoming event has been termed anticipatory behav-
in developing similar welfare measures regarding
iour (Spruijt et al., 2001). Animals from a range of
human–animal interactions in the wild.
taxa and cognitive abilities are able to anticipate pre-
olitary Behaviours—A dolphin’s responses to
dictable events due to the clear adaptive value, and
its surrounding environment and its solitary activ-
researchers have found that, in general, anticipatory
ity might also reflect its welfare state. Following
behaviour for a positive or negative event is differ-
the above discussion on social play, it is likely that
entiable (Moe et al., 2006; McGrath et al., 2016).
solitary play also reflects positive emotions (Held
Interestingly, anticipatory behaviour towards rewards
& Špinka, 2011). However, although not often
specifically is thought to have a link with welfare.
studied as such, it could be that the two types of
Although some level of anticipation for a positive
play have different functions (Greene et al., 2011)
event reflects positive emotions such as excitement,
and, therefore, may be better considered as separate
an excessive level of anticipation may reflect nega-
welfare measures in the future. Bottlenose dolphins
tive welfare states such as boredom and frustration
are known to play on their own with objects and by
due to the surrounding environment being under-
producing bubbles (McCowan et al., 2000; Delfour
stimulating (Spruijt et al., 2001; van der Harst &
et al., 2017), so further work on the contexts where
Spruijt, 2007; Watters, 2014). Studies on laboratory
the different play behaviours are seen would be
rats (Rattus norvegicus) have found initial support
valuable (Greene et al., 2011; Kuczaj & Eskelinen,
for the reward-sensitivity theory since individuals
2014). In terms of links with welfare, stereotypic
in more deprived, barren environments will perform
behaviour involves solitary activity (in most cases)
more anticipatory behaviour before a food or social
which has been found in many species to reflect an
reward arrives (e.g., van den Berg et al., 1999;
understimulating environment (Mason & Rushen,
van der Harst et al., 2003; Makowska & Weary,
2006). Unfortunately, the link to welfare is not as
2016). The first studies on anticipatory behaviour in
simple as just measuring the degree of stereotypic
bottlenose dolphins have shown that behaviours such
behaviour: animals may show more stereotypies as
as spy-hopping and surface-looking were performed
a method of coping, or they may have acquired a
before training or shows during which the animals
stereotypy in a previous environment and are con-
were fed (Jensen et al., 2013; Clegg et al., 2017c).
tinuing to perform it (Mason & Latham, 2004).
Furthermore, a recent publication demonstrated
There are very few studies available on the preva-
that higher levels of anticipatory behaviour
lence of stereotypic behaviours in captive dolphins
before training sessions in bottlenose dolphins
(for a review, see Clark, 2013); the predominant ste-
were correlated to pessimistic judgement biases,
reotypy reported is circular swimming, which has
indicating negative affective states and, therefore,
posed further problems since it is not clear whether
agreeing with the reward-sensitivity theory (Clegg &
the activity is indeed repetitive, invariant, and
Delfour, 2018). More research is clearly needed on
without function (Gygax, 1993; Sobel et al., 1994;
this topic before anticipatory behaviour can be used
Ugaz et al., 2013). More research into this topic is
as a welfare measure for dolphins or other species.
greatly needed. A measure of stereotypic behav-
However, it is also worth bearing in mind that just
iour was proposed in the C-Well© Assessment,
the anticipation of something positive, regardless of
but the thresholds for the acceptable, suboptimal,
the consummation of the reward, can induce positive
and poor welfare designations had to be adapted
emotions (Gimsa et al., 2012; Opiol et al., 2015);
190 Clegg and Delfour
therefore, it is likely worth investigating anticipatory
or negatively connoted emotions, respectively
behaviour as a multifunctional welfare tool.
(Rogers, 2002; Leliveld et al., 2013). The task now
is to discover reliable ways to measure literalities,
Cognitive Welfare Measures
which can manifest in many different forms and can
Returning to the Triangulation concept and what is
vary inter-individually (Rogers, 2010). For example,
thought to be the most accurate approach to mea-
the cetacean studies most relevant to the concept
suring emotions, it is advantageous to apply cog-
of emotional lateralisation have demonstrated that
nitive measures when evaluating affective states
during nonthreatening situations, wild belugas and
or welfare (Harding et al., 2004; Webster, 2005).
killer whales placed their calves on their right sides
Understandably, cognitive measures are rarely
(i.e., information processed by the left hemisphere),
included in practical welfare assessments since
with killer whales then moving the young to their
they are often either invasive in nature (e.g., mea-
left sides when the context became increasingly
suring brain wave activity) and/or require a signifi-
threatening (Karenina et al., 2010, 2013). Findings in
cant amount of time to train the animals (Paul et al.,
other species also look promising: a link was recently
2005). Fortunately, new techniques are being inves-
shown between hand preference and cognitive bias
tigated that render it easier to assess the cognitive
in common marmosets (Callithrix jacchus; Gordon
component of emotional responses; and while cogni-
& Rogers, 2015); and during an experimental test,
tive measures might not form part of assessments,
one male and one female California sea lion differ-
they can still be used to validate other behavioural
entially used their flippers in a task with either nega-
and physiological measures (Paul et al., 2005; Mendl
tive versus positive conditions (Le Ray et al., 2017).
et al., 2009).
However, more work is needed before measures
The major development in this area over the last
of laterality can reliably indicate an individual’s
10 years is certainly cognitive bias testing: human
psychology paradigms have helped us to measure
how cognitive processes are influenced by emotion
What Are the Next Steps Towards
in animals (Harding et al., 2004; Mendl et al., 2009).
Assessing Marine Mammal Welfare?
While there are several types of cognitive bias, the
most common to be measured are judgement biases
Now that the existing research as well as some
(decision making under ambiguity) through which
potential measures of marine mammal welfare
numerous studies in a wide range of taxa have
have been outlined, we explore what the next
shown that animals in poorer welfare conditions
directions for this field might be. While research
judge more pessimistically, and those in better wel-
is likely to initially progress on the most well-
fare conditions make more optimistic judgements
studied species (i.e., bottlenose dolphins) or in the
(latest reviews by Baciadonna & McElligott, 2015;
more feasible experimental settings (i.e., in cap-
Roelofs et al., 2016). A judgement bias test was
tive facilities), we argue that the time has come
applied to marine mammals in a study on bottlenose
for multidimensional expertise regarding different
dolphins in which it was found that dolphins who
marine mammal species to collaborate and start
conducted more synchronous swimming outside
welfare discussions across many species. The
of training sessions made more optimistic judge-
recent, evident movement advocating for marine
ments in the test (Clegg et al., 2017a). The study
mammal welfare to be measured in captive set-
was not able to conclude a causal relationship, but
tings (Ugaz et al., 2013; Brando et al., 2016;
the results suggest that synchronous swimming, as a
Clegg et al., 2017b), in the wild (Butterworth,
bond-affirming, affiliative behaviour (Connor et al.,
2017b; Papastavrou et al., 2017; Seuront & Cribb,
2006b; Holobinko & Waring, 2010), may induce
2017), and during rehabilitation (Petrauskas et al.,
positive emotions or affective states in dolphins
2006; Moore et al., 2007; Nicholson et al., 2007)
(Clegg et al., 2017a). This work is an example of
should be addressed by scientists, industry stake-
how cognitive measurement of welfare, studied
holders, and governments.
through taking the time to train the animals in a task, Those aiming to develop welfare assessments
can be used to validate other (behavioural) welfare for marine mammals in any of the situations above
measures. While cognitive bias testing may seem should establish the methods in situ (Dawkins,
like a technique only suited to captive research, it 2006)—that is, using animal-based data—as it
may in fact be possible in wild settings where the is very important to make sure the measures are
animals’ natural preferences and aversions can be valid and feasible for the animals in that particular
used (Brilot et al., 2009). environment. For captive studies, there is often the
Another proposed cognitive measure of welfare is
problem of small sample sizes, which may greatly
the lateralisation of brain function since it is thought
limit statistical power and, thus, the ability to
that human and at least some animal brains may
validate measures, so, where possible, interfacility
favour the left or right hemisphere to treat positively
collaborations should be established (e.g., as in
191Assessing Marine Mammal Welfare
Miller et al., 2011; Dudzinski et al., 2012; Clegg
that are feasible above water and can be conducted
et al., 2017c). Long-term collaborations should
in a relatively short time in case access to animals
also be sought between the captive facilities and
is restricted; a good example would be behavioural
academics in the field, whether it be to establish
measures such as the frequency of synchronous
graduate projects at the facility and/or to hire full-
swimming. This behaviour could be investigated in
time ethologists or welfare scientists to conduct the
correlation with other measures to find out whether
research (Maple, 2007; Barber, 2009).
it might also be a sign of positive welfare or social
The remarkable propensity of captive marine
support in wild bottlenose dolphins or in other
mammals to learn tasks through positive rein-
delphinid species. Acoustic research and any welfare
forcement conditioning (Brando, 2010) should be
measures developed in relation to this (Castellote &
exploited in research projects: further cognitive
Fossa, 2006) will also be very important in such set-
bias tasks, preference testing, and voluntary physi-
tings for which noise pollution is becoming a seri-
ological sampling are all possible using such train-
ous threat to marine mammal welfare (Butterworth,
ing. In the past, some facilities have shied away
2017a). Research groups that have been conduct-
from conducting experimental studies on cogni-
ing long-term studies on certain populations will
tion as it was thought that isolation of the animals
be incredibly valuable for these first wild welfare
was necessary (I. Clegg, pers. obs., September
studies since they often have the advantage of life
2015), but the recent cognitive bias tests were per-
history data, genetic information, and reliable iden-
formed while the dolphins stayed in their group
tification of individuals (Wells, 2009). Support from
(Clegg et al., 2017a). In fact, this approach is being
regulatory bodies will also help greatly in expanding
encouraged in research on other species (e.g.,
the focus to include behavioural and welfare aspects
Malassis & Delfour, 2015) as a way to limit iso-
of conservation research, and it is very promising
lation stress from being separated (Roelofs et al.,
to see international bodies like the IWC looking to
2016), and it may also help us to develop new
develop welfare assessments (Butterworth, 2017b).
paradigms based on situated actions which could
Finally, the epistemology of science indicates that
reveal different aspects of the animals’ cognitive
questions asked by scientists were, are, and always
abilities (Delfour, 2015). Given that there are only
will be linked to or inspired by the society they
a few validated welfare measures in existence for
live in. The rarefaction of basic resources such as
marine mammals, the first studies will find it the
land, energy, and water has already raised conflicts
hardest. Similar to early animal welfare research,
between humans and terrestrial animals, and the
situations should be used when welfare is highly
extent of our impact is now starting to be revealed for
likely to be good or poor, and this applies to captive
marine species (Butterworth, 2017a; Papastavrou
and wild welfare investigations. A study on welfare
et al., 2017). Measuring the welfare of marine and
measures for belugas used this approach by taking
other animals still has a long way to progress and
data before and immediately after the animals were
will be helped by other branches of science bringing
transported (Castellote & Fossa, 2006), and the
with it new paradigms, theories, and concepts. Of
fact that dolphins have been shown to perform less
course as ethologists, we believe that the behaviour
social play (Serres & Delfour, 2017) and had higher
of the animal will remain one of the keystones in
cortisol levels when noisy construction work was
assessing their welfare, but we acknowledge that
taking place in proximity (Monreal-Pawlowsky
we need to understand the animals’ umwelt—their
et al., 2017) also shows how supposed negative
subjective perception of their environment—to
events can be used in welfare research (without
effectively study, understand, and thus protect them
being experimentally imposed).
(Delfour, 2010a, 2010b).
As already emphasised, considering the welfare
of a wild animal is just as valid as considering that
of a captive animal, given that the concept describes
a balance of positive and negative affective states. Welfare science has evolved and now aims to assess
Furthermore, the increasing conflict between wild-how an animal is feeling by using objective, animal-
life and humans, and the pressures placed on them based measures of both positive and negative states.
to adapt to a changing environment, means that Overall assessments of welfare have been developed
welfare evaluations would be beneficial in relevant for a few terrestrial species and generally include
decision-making processes (Paquet & Darimont, behavioural and physiological measures, with new
2010; Papastavrou et al., 2017). Nevertheless, there approaches to conducting cognitive measures allow-
are obviously limitations when working in the wild, ing another dimension of indicators to be identified.
chiefly access to and identification of the animals, Past research on wild and captive marine mammals
which will mean that welfare assessments will be has largely been focussed on other topics than wel-
constructed differently to those for captive animals. fare, but there are many elements which can be used
To start, research could aim to develop measures to suggest potential measures, and dedicated welfare
192 Clegg and Delfour
research for these taxa is slowly increasing. Initial
studies have highlighted certain behavioural and
physiological welfare indicators, demonstrated that
cognitive tests are fruitful, and proposed a feasible
protocol for a comprehensive welfare assessment.
Research in captivity should build on these advances
by collaborating among facilities and disciplines to
design robust experiments with sufficient sample
sizes. Amid calls for welfare science applications to
wild marine mammals, a few projects have started
theoretical discussions, and hopefully progress in
this area will continue, perhaps capitalising on the
wealth of knowledge acquired by long-term research
programs. The objectives of this review were to first
show that welfare assessment of marine mammals is
indeed possible and that studies are already starting
to be conducted to that effect; and second, that the
holistic, multidimensional nature of welfare means
that there are copious opportunities for existing
marine mammal scientists to investigate aspects of
welfare concurrently or, better yet, in collaborations.
The authors would like to thank Niels van Elk and
Andy Butterworth for previous development of
the discussions found in this review.
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... Furthermore, in cases where manuscript submission requires authors to select themes, categories or keywords via dropdown lists, no options appeared for either welfare or conservation welfare on any of the conservation-based portals examined. Coupled with our workshop findings and literature analysis results, these insights support previous conclusions regarding the lack of synthesis between welfare science and conservation biology [11,24,30,53,[55][56][57][58]. To address this, the necessary next steps should be practical in nature and must expand the discussion beyond terrestrial examples. ...
... The applicability of captive animal physiological reference ranges to wild marine mammals remains an ongoing discussion [66]. Some assert that captive research can successfully be adapted to aid wild marine mammal conservation [57,89,[95][96][97], while others advocate that welfare in captivity is compromised to the point that wild-captive comparisons of behaviour, physiology or cognition are invalid [98]. For larger species such as baleen whales and other species not kept in captivity, there is very limited research from a few longer-term rehabilitation efforts that can be used to evaluate its applicability [99,100]. ...
... Furthermore, due to the complexities of finding free-ranging marine mammals and observing the same individuals over long time periods, welfare assessments may only provide a snapshot of individual welfare at that time [24], so measures of behavioural interactions and environmental variables that require a time series may not be applicable. The translation of welfare science principles into wild marine mammal conservation may also face some social and cultural limitations [59], given the ethical debate surrounding captive marine mammals [57]. Fostering open discussions to enable consensus-building and develop clear Terms of Reference documents might be a productive first step in the process of addressing the varying views, definitions and language currently used, and may help researchers to find common ground and pave the way for translating the applicable information. ...
Full-text available
Integrating welfare principles into conservation strategy is an emerging synthesis that encourages consideration of individual animals’ quality of life in research, policies and law. However, these principles have gained limited traction in marine compared to terrestrial animal conservation. This manuscript investigates several factors that may be contributing to this disparity. In order to gauge current understanding of animal welfare science principles by marine mammal researchers and other stakeholders, a “Welfare in the Wild” workshop was convened at the 32nd European Cetacean Society conference (La Spezia, Italy, April 2018). The workshop was attended by 30 participants who completed pre- and post-workshop surveys on animal welfare principles. The survey results highlight a range of different views about exactly what animal welfare science is and how it can be applied to marine mammals. Specifically, participants’ definitions appeared to vary depending on the type of employment or research they engaged in, indicating a need for an interdisciplinary common language. Secondly, we analysed the peer-reviewed literature in order to ascertain where marine mammal publications exploring welfare were being published. From 1950 to July 2020, a total of 299 articles featured both marine mammal taxa (one or more) and the word welfare in the title, abstract or keywords. This represents just 0.96% of the total peer-reviewed published papers on marine mammal taxa (n = 31,221) during the same period. When examining articles published within “Welfare and Ethics” (n = 6133) and “Aquatic-focused” (n = 139,352) journals, just 1.2% (n = 71) and 0.04% (n = 57) of articles, respectively, featured the word welfare when examining marine mammals. With the aim of exploring how explicitly including welfare evaluations in marine mammal research and management can benefit conservation outcomes, we framed our workshop and quantitative literature review findings to provide practical solutions to the language, translation and reception issues of this burgeoning cross-disciplinary collaboration.
... These studies suggest that it is possible to assess the animals' welfare and emotional states by evaluating their anticipatory behavior prior to an upcoming event, as well as determine whether the event is of interest and positive or negative. As a result, researchers consider the study of anticipatory behavior a promising welfare indicator (Anderson, von Keyserlingk, Lidfors, & Weary, 2020;Clegg & Delfour, 2018b;Krebs et al., 2017;Van der Harst & Spruijt, 2007;Ward, Sherwen, & Clark, 2018;Watters, 2014;Whitham & Wielebnowskil, 2013;Wolfensohn et al., 2018). ...
... Indeed, under human care, dolphins are involved in several activities (e.g., feeding, training, playing with objects, interaction with trainers, public demonstrations, and environmental enrichment), that are anticipated by signals that spontaneously induce anticipatory behavior (Clegg et al., 2018(Clegg et al., , 2017aJensen et al., 2013). Furthermore, anticipatory behavior has been proposed as a dolphins' welfare indicator (Clegg & Delfour, 2018b) and used to study their preference, interest, and emotional states toward different activities (Bigiani & Pilenga, 2021;Clegg & Delfour, 2018a;Clegg et al., 2018). ...
... Anticipatory behavior has been described in many taxa [e.g., in amphibians, fishes, reptiles, birds, and mammals (Abe & Sugimoto, 1987;Cooper, 1998;Folkedal et al., 2012;Galhardo, Vital, & Oliveira, 2011;Krebs et al., 2017;Reebs & Lague, 2000;Smith & Kabelik, 2017;Van Bergeijk, 1967;Zimmerman et al., 2011)]. Moreover, given its correlation with animal welfare (Clegg et al., 2018;Spruijt et al., 2001), it is considered a promising welfare indicator (Whitham & Wielebnowski, 2013;Clegg & Delfour, 2018b). However, anticipatory behavior is not currently used in welfare assessment methodologies. ...
Anticipatory behavior describes the actions taken to prepare for an upcoming event. It is considered a promising tool for welfare assessment, but it is not fully applied in zoos and other facilities. This is probably due to the need to train animals, which can take a long time and make its use impractical. In this work, we tested, on a group of six dolphins (Tursiops truncatus), the effectiveness of a new technique to induce and measure anticipatory behavior without training animals. Our results show how this new methodology, which we called The Fast Technique (TFT), has been able to induce and measure anticipatory behavior toward the event studied, i.e., the play sessions with objects (PSO). Furthermore, it has produced the same result obtained with The Classical Technique (TCT), which requires a training phase. Therefore, our finding demonstrates the efficacy of a new technique that could facilitate the use of anticipatory behavior for both research and animal welfare assessment protocols.
... Even more specifically, environmental enrichment programs are the principle technique used to improve animal welfare through the addition of stimuli to animal enclosures. The term enrichment can be defined in multiple ways, one notable difference being the requirement that the enrichment actually improves the welfare of the animal (Clegg & Delfour, 2018;de Azevedo et al., 2007). For the purposes of this paper, we define environmental enrichment as any alterations made to an animal's environment for the purposes of improving its biological or cognitive welfare (see Bloomsmith et al., 1991;Hoy et al., 2010;Swaisgood & Shepherdson, 2005, for similar usage of the term enrichment). ...
... 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). ...
... However, more and more frequently, the assumption of this link between presumed stereotypies and poor welfare has been questioned (Clegg et al., 2017;Franks et al., 2009;Greening, 2019;Poirier & Bateson, 2017). Enrichment programs and their welfare outcomes for bottlenose dolphins have received a lot of attention in recent years); however, formal assessments of said programs are still needed Clegg et al., 2017;Clegg & Delfour, 2018;Makecha & Highfill, 2018). In bottlenose dolphins under human care, the most prominent species-typical behaviors examined are affiliative social behaviors (Waples & Gales, 2002), exploratory and play behaviors (Kuczaj et al., 2002), swimming patterns (Gygax, 1993) and vocalizations known to be associated with these behavior states (Jones et al., 2020). ...
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.
... The welfare of captive odontocete species is an increasing subject of research and discussion ( Brando et al., 2016 ;Butterworth, 2017 ;Clegg et al., 2015;Serres et al., 2019, Serres et al., 2020a, 2020b, 2020cvon Fersen et al., 2018 ). Health issues are often diagnosed late for odontocetes because these animals mask symptoms until the illness is serious ( Castellote and Fossa, 2006 ;Clegg and Delfour, 2018a ;Waples and Gales, 2002 ). Indicators which reliably signal health or welfare issues at early stages are therefore needed ( Clegg et al., 2017b ). ...
... Another analysis should be conducted at an individual level to ensure that the chosen parameter(s) are the most suitable for all the individuals within a social group. We suggest that caretakers should monitor animal welfare using the most informative session parameter(s) for each individual combined with physiological parameters (e.g., fecal glucocorticoids, breathing frequency), behavioral parameters (e.g., QBAs or direct observations), and cognitive measures when possible (e.g., cognitive bias, Clegg et al., 2018a ). Low participation scores, high leaving rates and/or low food intakes should be used as alerting factors potentially indicating a diminished welfare state, triggering closer investigation. ...
In captive facilities, odontocetes are subject to daily training/feeding sessions which often create close relationships between animals and their caretakers. Therefore, such sessions are thought to provide information that can be useful for welfare assessment. Recent studies on bottlenose dolphins (Tursiops truncatus) validated caretakers’ ratings of dolphins’ participation during training sessions as a welfare indicator. Even though their behaviour, adaptation to captive settings or relationship with humans may differ from bottlenose dolphins, many other odontocete species remain much less studied. In the present study, animals from three groups including Yangtze finless porpoises (Neophocaena asiaeorientalis asiaeorientalis), East-Asian finless porpoises (Neophocaena asiaeorientalis sunameri), and bottlenose dolphins were monitored during training sessions. Four variables were recorded: a participation score rated by caretakers, the leaving rate, the amount of food eaten, and the propensity to finish the attributed food. Bottlenose dolphins participated better in sessions: they were attributed higher participation scores, departed less and finished their food more often than finless porpoises. The context of the sessions, including time of the day, season, type of session, social grouping, occurrence of unusual events or presence of visitors affected the parameters recorded during sessions in the three groups. The inter-species differences and the context-related variations of the four measured parameters should be used to adapt the schedules and techniques of training sessions for each group. Such adaptation could improve training effectiveness and the human-animal relationship. In addition, the associations among the four measured parameters and between these parameters and the animals’ displayed activity revealed the most informative parameter for each group: participation score for Yangtze finless porpoises, food intake for East-Asian finless porpoises and leaving rate for bottlenose dolphins. These parameters best reflect the motivation of the animals during sessions, and may therefore be beneficial to integrate into welfare monitoring tools.
... In the present paper, we review the neural consequences of impoverished environments, the effects of short-term and chronic stress on mammalian brains (specifically, corticolimbic structures), and the neural foundations of stereotypy, with a focus on basal ganglia circuitry. We argue that neural inferences from other mammals to elephant and cetacean brains are strongly supported using the logic of triangulation (Thurmond 2001), which is employed in other animal welfare assessments (Clegg and Delfour 2018). Thus, we connect the known effects of impoverished environments on brains from experimental studies in other species as well as the shared clinical profiles in impoverished environments across species to infer the effects of captivity on the brains of elephants and cetaceans. ...
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The present review assesses the potential neural impact of impoverished, captive environments on large-brained mammals, with a focus on elephants and cetaceans. These species share several characteristics, including being large, wide-ranging, long-lived, cognitively sophisticated, highly social, and large-brained mammals. Although the impact of the captive environment on physical and behavioral health has been well-documented, relatively little attention has been paid to the brain itself. Here, we explore the potential neural consequences of living in captive environments, with a focus on three levels: (1) The effects of environmental impoverishment/enrichment on the brain, emphasizing the negative neural consequences of the captive/impoverished environment; (2) the neural consequences of stress on the brain, with an emphasis on corticolimbic structures; and (3) the neural underpinnings of stereotypies, often observed in captive animals, underscoring dysregulation of the basal ganglia and associated circuitry. To this end, we provide a substantive hypothesis about the negative impact of captivity on the brains of large mammals (e.g., cetaceans and elephants) and how these neural consequences are related to documented evidence for compromised physical and psychological well-being.
... This study was, however, carried out before the implementation of this period of quietness. Measuring animal welfare is a common phenomenon, especially in captivity, that is assessed using multidimensional resources and animal-based measures [68]. Consequently, further research on the daily movements, reproductive seasonality and habitat use of the island's spinner dolphin population [3,15,25,63,69], as well as individual physiological parameters (e.g., faecal glucocorticoid metabolites [70]), is necessary to inform the regulation amendments and effectively manage the welfare of Reunion Island's spinner dolphin population. ...
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Marine wildlife tourism has rapidly developed in Reunion Island, due to a large demand for interactions with a resident population of spinner dolphins (Stenella longirostris). The presence of dolphin-watching vessels close to dolphin groups can cause short-term impacts on their behaviour; cumulative incidences likely result in deleterious long-term impacts on the population. Using scan sampling, we collected behavioural data on spinner dolphins to evaluate the short-term effects of dolphin watching on their behaviour. The dolphins were less likely to begin socialising or diving while travelling and more likely to stay travelling and milling in the presence of vessels. Additionally, activity budgets for resting and socialising decreased simultaneously with increased travelling and milling. Avoidance responses significantly increased with an increase in the number of vessels and non-compliance with the local dolphin-watching guidelines. These behavioural responses are likely to have energetic costs for the dolphins, which may lead to decreased survival and reproductive success at individual and population levels. More restrictive regulations, increased surveillance and animal-based measures are key tools to adapt the conservation efforts in Reunion Island. Further studies on the island’s resident dolphin populations are necessary to ensure the continuity of dolphin-watching activities in a sustainable manner.
... Recent research developing objective standards for assessing cetacean welfare in captivity and in the wild (e.g. Clegg and Butterworth, 2017, Clegg and Delfour, 2018, Miller et al., 2018Brando et al., 2018) provides some reason for optimism about the possibility of establishing the kind of "adaptive management principles" that Ramp and BekoY require in cases where intervention is necessary. ...
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Recent decades have seen increasing opposition to cetacean captivity among the general public. However, these discussions often do not address captivity in the context of conservation. At the same time, approaches within conservation biology—compassionate conservation and multispecies justice—call for greater attention to the impact of conservation interventions on individual nonhuman animals. Many questions remain about the implications of these approaches for conservation practice. In this paper, we focus on two recent case studies in cetacean conservation. These case studies highlight how some forms of captivity can contribute to conservation and can help clarify what is at stake between advocates of these approaches and their critics. We argue that some forms of captivity can be ethically justified as part of an ex situ conservation effort, even in cases where they involve risk to individual cetaceans. available:
... However, and to our knowledge, only Clegg and colleagues' study (2015) used multiple variables to assess welfare in a cetacean, by applying 36 welfare measures to bottlenose dolphins, 58 % of them being animal-based measures Wielebnowski, 2013, 2009). Nevertheless, this assessment needs more work to fully validate the measures, which are also currently unweighted (Clegg and Delfour, 2018). Despite that, Clegg and colleagues' study represented an important first step in the development of comprehensive and practical welfare assessment tools for cetaceans. ...
Questionnaires are very useful tools when it comes to assessing zoo based animal measures and caretakers of these animals (such as keepers, trainers and veterinarians) are in the best position to provide accurate answers to these assessments. Our goal was (a) to empirically demonstrate the utility of a welfare questionnaire and (b) to examine the relationship between three constructs: personality, subjective well-being and welfare ratings, in a sample of killer whales (Orcinus orca) (n = 26). For this purpose, we applied the 4-factor personality structure previously applied to the species, a 4-item subjective well-being questionnaire, and we designed and applied a 39-item welfare questionnaire. The welfare questionnaire was composed by positive and negative welfare indicators related to social and environmental interactions, physical health condition, presence of species-typical and stereotypical behaviors, the capacity to accept situations, and relationships with conspecifics and humans, among others. Each killer whale was rated by an average of 12.5 raters. The mean interrater reliability for subjective well-being and welfare questionnaires was high, and the Principal Components Analysis and the Regularized Exploratory Factor Analysis, revealed one and six factors, respectively. We found some correlations among the three constructs, for instance, Extraversion (r = 0.62, 95% CI 0.02-0.06) and Dominance (r = 0.61, 95% CI 0.03-0.09) were associated to the subjective well-being factor, while subjective well-being was negatively associated with the Abnormal (r = -0.73, 95% CI −0.13 to −0.06) and Nervousness (r = -0.66, 95% CI 0.06-0.17) welfare factors, among others. The welfare questionnaire showed reliable and valid results. Thus, our research represents the first empirical evidence of the utility of assessing the welfare of cetaceans through the use of a multi-trait questionnaire. Therefore, facilities housing cetaceans could use welfare questionnaires to gradually monitor welfare and to intervene if needed. Finally, some of the correlations found closely resembled previous correlations found in primates, which could indicate a possible evolutionary convergence between Orders.
... While most animal care professionals are very good at determining when their animals are acting uncharacteristically, many are not trained in behavioral assessment techniques (Clegg & Delfour, 2018). Depending on the facility, animal care providers may or may not have a college degree, with a smaller percentage having master's degrees (Bureau of Labor Statistics, U.S. Department of Labor, Occupational Outlook Handbook, Animal Care and Service Workers; ...
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Comparative psychology has a long history of investigating topics that promote comparisons across disciplines, constructs, and species. One critical component of comparative analyses is to select the best data collection technique. Unfortunately, these observational skills are not always taught to individuals who need them the most, animal care professionals. To demonstrate the applicability of appropriate data collection techniques to this applied discipline, we conducted a multi-day workshop that provided attendees training and practice with several data collection techniques that could be used to evaluate animal behavior in both spontaneous and enrichment-provided settings. The program included (1) a presentation on different data collection techniques and the types of questions each technique can address, (2) two 20-minute sessions of observation practice at two different facilities, (3) a final summary presentation of the data collected, and (4) pre- and post-surveys conducted immediately before and at the end of the workshop. Out of 177 survey respondents, almost a third reported using behavioral data collection to manage animal behavior prior to the workshop. More than 90% of the respondents had heard of behavioral ethograms and 68% of the respondents had used one previously. Many of the respondents reported familiarity with different observation techniques. Eighty-two individuals completed the majority of the survey with 81% expressing satisfaction with the initial workshop presentation. Respondents completing both surveys showed significant improvement in their knowledge of behavioral data collection techniques. Ultimately, the workshop introduced and clarified behavioral observation techniques and their applications in a variety of contexts. Respondents indicated that they could and would utilize knowledge gained from the workshop at their own facilities.
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.
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Boredom is likely to have adaptive value in motivating exploration and learning, and many animals may possess the basic neurological mechanisms to support it. Chronic inescapable boredom can be extremely aversive, and understimulation can harm neural, cognitive and behavioural flexibility. Wild and domesticated animals are at particular risk in captivity, which is often spatially and temporally monotonous. Yet biological research into boredom has barely begun, despite having important implications for animal welfare, the evolution of motivation and cognition, and for human dysfunction at individual and societal levels. Here I aim to facilitate hypotheses about how monotony affects behaviour and physiology, so that boredom can be objectively studied by ethologists and other scientists. I cover valence (pleasantness) and arousal (wakefulness) qualities of boredom, because both can be measured, and I suggest boredom includes suboptimal arousal and aversion to monotony. Because the suboptimal arousal during boredom is aversive, individuals will resist low arousal. Thus, behavioural indicators of boredom will, seemingly paradoxically, include signs of increasing drowsiness, alongside bouts of restlessness, avoidance and sensation-seeking behaviour. Valence and arousal are not, however, sufficient to fully describe boredom. For example, human boredom is further characterized by a perception that time ‘drags’, and this effect of monotony on time perception can too be behaviourally assayed in animals. Sleep disruption and some abnormal behaviour may also be caused by boredom. Ethological research into this emotional phenomenon will deepen understanding of its causes, development, function and evolution, and will enable evidence-based interventions to mitigate human and animal boredom.
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Examining the role of play as related to individual and group social development is important to understanding a species. The purpose of our study was to examine whether there is a difference in the frequency of object play exhibited by dolphins from two groups – one captive and one wild. Data were collected with underwater video, with resulting videos event sampled for bouts of play involving various objects used by dolphins. From 159 hr of video data, roughly 102 min featured object play: 75 min of dolphins from RIMS and 26 min for dolphins near Bimini. A total of 304 bouts of object play were documented from or between dolphins at RIMS, while 73 bouts were observed by or between dolphins around Bimini. Juvenile dolphins engaged in solo and mutual play more than twice that of other aged dolphins from both study groups, although this result was not statistically significant. Similarly, male dolphins at RIMS exhibited object play slightly more than females, though this difference was not significant: at Bimini, male dolphins were not observed to play with objects during interactions with conspecfics (mutual) and engaged in object play about half as often as female spotted dolphins. Combining both study groups, dolphins played with about 23 different objects that were grouped into six categories: biological debris, human made objects, inanimate objects, other (e.g., wood, etc), people, and trash. The RIMS dolphins played most with all objects except people while Bimini dolphins interacted with sand more than any other object. Dolphins have been shown to exhibit higher cognitive functions, of which complex play is one example. The role of play in animals is considered important to development and maintenance of social relationships and to learning skills required ultimately for survival.
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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.
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DOLPHINS in a captive setting can be occasionally subjected to a variety of potentially stressful situations. The stress response comprises a variety of biological reactions to internal or external stimuli elicited when an individual perceives (real or not) a threat to its homoeostasis (Moberg and Mench 2000). The stress response is a complex interplay of behavioural and physiological strategies to cope with changes in the environment (Tsigos and Chrousos 2002, Sheriff and others 2011). Noise can act as a stressor to dolphins because cetaceans rely heavily on sound for many important life functions. This reliance on sound means it is quite likely that exposure to noise will have some detrimental effects on these life functions (Wright and others 2007). Observed effects of noise on marine mammals include: changes in vocalisations, respiration, swim speed, diving and foraging behaviour; displacement; avoidance; shifts in migration path; stress; hearing damage and strandings, but responses of marine mammals to noise can often be subtle and barely detectable (Weilgart 2007). If there is no obvious change in behaviour, stress is difficult to assess in dolphins, both individually and as a group. In order to detect the presence of stress responses in these situations, the endocrine response to stressors is assessed evaluating the hypothalamic–pituitary–adrenal (HPA) axis activity in dolphins and other cetaceans (Wright and others 2007, Amaral 2010). The HPA axis is a key element of the stress response and, when activated, the resultant hormonal cascade increases the levels of glucocorticoids (GCs) …
One of the main objectives of the Welfare Quality® project was to develop a standardised system for assessing the welfare of animals kept on farms or at slaughter and thus accommodate the main drivers underlying the vision (see Chapter 4). More specifically the need for such an assessment system arose because animal welfare is an important and growing concern for European citizens and of increasing relevance to supply chains and markets as well as policy making and regulatory bodies. It also addresses the fact that European consumers do not feel sufficiently informed about the welfare of farm animals and thereby struggle to take this issue into account when purchasing food or other animal-based products (European Commission, 2007a,b).
Motor lateralization is a behavioural asymmetry between the left and the right side of an individual due to hemispheric specialization. The right hemisphere controls the left side of the body and the left hemisphere the right side. The right hemisphere processes negative emotions such as fear and frustration, and on the contrary, the left hemisphere processes positive emotions such as happiness. This study, conducted at Parc Asterix Delphinarium (Plailly, France), tested the influence of supposedly positive, negative and neutral emotional situations on four California sea lions’ (Zalophus californianus) motor lateralization while performing a known exercise, here climbing on a stool. Latency between the caretakers’ command and the animals’ response was recorded. The results showed an interindividual variability in the effect of the supposed emotional situations on their motor lateralization and their response latency. The nature and the strength of this effect require deeper investigation by further studies, on a larger number of individuals and contexts.
Fecal glucocorticoid measurement is an important noninvasive tool to monitor animal health. A radioimmunoassay (RIA) method was developed to measure fecal cortisol in bottlenose dolphins under human care. The method was used to measure baseline hormone levels and evaluate the adrenal response to environmental challenges in a small number of individual dolphins. The method was validated by precision and accuracy tests and by comparison with liquid chromatography-mass spectrometry (LC-MS). The parallelism test suggested few matrix interferences. The assay showed a good degree of precision within assay (CV = 5.4%) and between assays (CV = 4.1%). The RIA significantly correlated with the LC-MS method (r = 0.838, P < 0.01). The recovery test and the comparison between RIA and LC-MS suggested that the RIA slightly underestimates fecal cortisol concentrations, although the degree of accuracy was good. This study established that bottlenose dolphins excrete appreciable amounts of fecal cortisol (healthy subjects: 0.2–9.5 ng/ g). Therefore, chronic HPA axis activation may be monitored in fecal samples by immunoassays after validating a suitable extraction protocol. The RIA could discriminate conditions of stimulation (pregnancy, parturition, isolation, transportation) and inhibition (diazepam administration) of the HPA axis and may, therefore, be useful for monitoring dolphin well-being.
Stereotypic behaviors (SB) are common in zoo-housed elephants, and these behaviors can be performed at high rates. Elephants perform different SB forms (e.g., weaving, pacing), but no published studies have evaluated the factors contributing to the development or performance of these different forms. Instead, as with most SB studies across species, elephant studies have relied on analyses that aggregate all SB forms, which limits the development and testing of form-specific hypotheses or abatement practices. Our objectives were to characterize the SB forms of North American zoo elephants and use multivariable epidemiological models to test form-specific hypotheses. We videotaped 77 elephants (African: N = 5 males, 31 females; Asian N = 8 males, 33 females) at 39 zoos who performed SBs and used a novel classification scheme and 5-minute instantaneous samples to characterize their SB forms. Locomotor and whole-body SBs were the most common, but most elephants who performed locomotor SBs also performed whole-body SBs. Thus, we characterized each elephant according to whether it included locomotion in its SB repertoire [Locomotor Presence (LP)] or only whole-body movements. We used binomial regression models fitted with generalized estimating equations to test hypotheses about which of 26 social, housing, management, life history, and demographic variables were most associated with LP. The odds of LP increased by 26% for every 10% increase in time housed separately (odds ratio = 1.026, p = 0.04), 96.2% for every additional social group with which an elephant had contact (odds ratio = 1.962, p = 0.01), and 46% for every 10% increase in time housed indoors (odds ratio = 1.046, p = 0.01). Age was non-significantly confounded with all three variables. We hypothesize that the social variables in our models increase LP risk because they are associated with uncontrollable social group changes, anticipation of potentially rewarding social experiences, or the frustration of social behaviors. The housing variable included in our model likely increases LP risk because indoor spaces are less complex, resulting in the channeling of walking or social avoidance behaviors into more simplistic movements. Overall, our results suggest that elephant managers may best be able to prevent locomotor SB by enhancing their elephants’ social environment and the spatial complexity of their enclosures. Future research should focus on determining whether addressing the risk factors for LP results in less frequent performance and identifying other temporally proximate eliciting factors.
Fractals have been applied to describe the complexity of behavioral displays in a range of organisms. Recent work suggests that they may represent a promising tool in the quantification of subtle behavioral responses in marine mammals under chronic exposure to disturbance. This paper aims at introducing the still seldom used fractals to the broader community of marine mammal scientists. We first briefly rehearse some of the fundamental principles behind fractal theory and review the previous uses of fractals in marine mammal science. We subsequently introduce two methods that may be used to assess the complexity of marine mammal diving patterns, and we apply them to the temporal dynamics of the diving patterns of killer whales in the presence and absence of sea kayaks, the sequential behavior of harbor and gray seals in environments with distinct levels of anthropogenic influence, and southern right whales with and without calves. We discuss the ecological relevance of identifying fractal properties in marine mammal behavior, and the potential strength of the fractal behavioral parameters in comparison to more standard behavioral metrics. We finally briefly address the relevance fractal methods may have for the design and implementation of management and conservation strategies.
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.