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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,
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-
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
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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