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Abstract

Animal welfare science is a burgeoning field, but research on cetaceans (whales, dolphins and porpoises) is lacking. Bottlenose dolphins (Tursiops truncatus) are the most well-known and studied cetaceans, particularly in captivity, and thus are used in this review as a model for other cetacean species. Despite the public interest and need for such research, studies specifically investigating dolphin welfare are lacking. This review uses the three broad categories of behaviour, health, and cognition, to discuss how dolphin welfare has been assessed thus far, and could be assessed in future. We present welfare indicators validated in other species that could be applied to dolphins, including innovative measures, such as cognitive appraisal of emotions. We provide a summary of practical recommendations for validating the indicators of bottlenose dolphin welfare. This paper aims to stimulate further research into dolphin welfare which could improve the lives of the animals themselves and ultimately support regulatory decisions. We recommend uniting expertise in cetology and welfare science in order to develop a holistic approach to dolphin welfare assessment.
165
© 2017 Universities Federation for Animal Welfare
The Old School, Brewhouse Hill, Wheathampstead,
Hertfordshire AL4 8AN, UK
www.ufaw.org.uk
Animal Welfare 2017, 26: 165-176
ISSN 0962-7286
doi: 10.7120/09627286.26.2.165
Applying welfare science to bottlenose dolphins (Tursiops truncatus)
ILK Clegg*, CE Van Elk§and F Delfour
Laboratoire d’Ethologie Expérimentale et Comparée EA4443, Université Paris 13, Villetaneuse, France
Equipe Delphinarium, Parc Astérix, BP8, 60128 Plailly, France
§Dolfinarium Harderwijk, Strandboulevard 1, 3841 AB Harderwijk, The Netherlands
* Contact for correspondence and requests for reprints: isabella.clegg@leec.univ-paris13.fr
Abstract
Animal welfare science is a burgeoning field, but research on cetaceans (whales, dolphins and porpoises) is lacking. Bottlenose dolphins
(Tursiops truncatus) are the most well-known and studied cetaceans, particularly in captivity, and thus are used in this review as a
model for other cetacean species. Despite the public interest and need for such research, studies specifically investigating dolphin
welfare are lacking. This review uses the three broad categories of behaviour, health, and cognition, to discuss how dolphin welfare
has been assessed thus far, and could be assessed in future. We present welfare indicators validated in other species that could be
applied to dolphins, including innovative measures, such as cognitive appraisal of emotions. We provide a summary of practical recom-
mendations for validating the indicators of bottlenose dolphin welfare. This paper aims to stimulate further research into dolphin
welfare which could improve the lives of the animals themselves and ultimately support regulatory decisions. We recommend uniting
expertise in cetology and welfare science in order to develop a holistic approach to dolphin welfare assessment.
Keywords:affective states, animal-based measures, animal welfare, bottlenose dolphins, cetaceans, welfare assessment
Introduction
Research into welfare assessments for zoo and aquarium
(hereafter referred to as ‘zoo’) animals is increasing as farm
animal welfare assessment is proven to be feasible and valid
(Barber 2009; Whitham & Wielebnowski 2013). There is
much support for the adaptation of farm animal measures to
zoo animals (Swaisgood 2007; Hill & Broom 2009; Mason
& Veasey 2010), and zoological institutions are well set-up
for conducting measures due to the individualised care and
multiple daily interactions (Barber 2009).
In this review, we conceptualise welfare using Spruijt et als
(2001) description of a “…balance between positive
(reward, satisfaction) and negative (stress) experiences or
affective states. The balance may range from positive (good
welfare) to negative (poor welfare)”. This ‘feelings-based’
definition aligns with positions taken recently by many
others (eg Yeates & Main 2008; Mason & Veasey 2010;
Watters 2014; Dawkins 2015), and specifies measurement
of both positive and negative welfare. Our review also
prioritises animal-based over resource-based measures,
since they are more likely to accurately reflect welfare
(Webster 2005; Roe et al 2011; Whitham & Wielebnowski
2013). We also give equal consideration to indicators of
positive and negative welfare (Désiré et al 2002; Paul et al
2005; Boissy et al 2007; Yeates & Main 2008).
There is very little existing research on the welfare of
cetaceans (Ugaz et al 2013; Clegg et al 2015), in captivity
or the wild. Given that public interest often stimulates
research in the associated areas (eg with farm animal
welfare; Rushen et al 2011), cetacean welfare studies are
likely to increase markedly in the near future since the
public’s interest is at a high level and intensity (Grimm
2011; Ventre & Jett 2015). Although many questions posed
are, in fact, ethical dilemmas (eg ‘Should we keep dolphins
in captivity?’), objective data on the animals’ welfare state
would aid in these personal decisions (Jiang et al 2007;
Clegg et al 2015). Published farm welfare assessments have
shown how this type of data can be gathered, for instance
the Welfare Quality® project for farm animals (2009a,b,c)
and its subsequent cross-species adaptations (eg Mononen
et al 2012; Clegg et al 2015; Barnard et al 2016).
While cetology, the study of cetaceans, has burgeoned
(Hill & Lackups 2010), there are very few studies on
cetacean welfare and methods of assessment (Galhardo
et al 1996; Clark 2013; Ugaz et al 2013; Clegg et al 2015).
Bottlenose dolphins (Tursiops truncatus) are the most
studied cetacean species (Hill & Lackups 2010), and the
most common in captivity (Pryor & Norris 1998; Wells &
Scott 1999), thus we choose them as the focus species for
this review of how welfare science could be applied to
cetaceans. We arrange the relevant cetology knowledge
Universities Federation for Animal Welfare Science in the Service of Animal Welfare
166 Clegg et al
into behaviour, health-related and cognition research, all
well-established specialities (Wells 2009). These three
categories are derived from Webster’s (2005)
‘Triangulation’ principle for the measurement of welfare,
where accumulating information from each specialty
increases overall validity. Importantly, while our review
includes wild research and welfare applications (wild
animal welfare should be measured: Jordan 2005; Ohl &
van der Staay 2012), our discussions orientate towards
captive dolphins since their environment is closely
controlled by humans. The necessity for dolphin welfare
research is clear: there are 250 bottlenose dolphins in the
European Association of Zoos and Aquaria facilities
(EAZA 2015), 444 animals listed in US and Canadian
dolphinaria (in 2011; Ceta-base), and many others
worldwide not registered on an official record, all main-
tained in a huge range of facility types that differentially
impact welfare (Joseph & Antrim 2010).
This review compiles what we believe to be literature on
wild and captive bottlenose dolphins most relevant to
welfare, suggesting some farm and zoo animal approaches
which could be adapted to cetaceans, with final recommen-
dations on initial studies and how the dolphin welfare disci-
pline might evolve. A strong focus is maintained on those
areas of cetology that merit further investigation to answer
questions on bottlenose dolphins’ quality of life.
Published work on dolphin welfare
There are very few studies of dolphin welfare, either in
captivity or the wild (Ugaz et al 2013; Clegg et al 2015). Thus,
there are no validated measures, ie ones that we know are
linked to positive or negative affective states, as yet. Given the
dearth of welfare research, in some cases findings from other
cetacean species are extrapolated to bottlenose dolphins.
Studies of wild dolphin welfare
Only a handful of studies have focused on welfare
concepts with regard to wild cetaceans, and even within
these direct mentioning of the word ‘welfare’ is rare. A
popular topic has been assessments of the impacts of
tourist boats on various cetacean species (eg Stockin
et al 2008; Christiansen & Lusseau 2015), although the
focus remains at population-level indicators. Long-term
data revealed that rate and repetitions of wild bottlenose
dolphin whistles were potential indicators of short-term
stress (Esch et al 2009). A more recent study suggested
that an upward shift in whistle frequency was linked to
increased emotional arousal (Heiler et al 2016).
Butterworth et al (2013) empirically evaluated dolphin
welfare in the Taiji drive hunts, an annual harvesting of
dolphins in Japan, but this research only concentrated on
welfare at the point of death. In the first and only
teaming of wild marine mammal research with animal
welfare science to our knowledge, Butterworth et al
(2012) used the Five Freedoms to discuss how entangle-
ment affects individual animal welfare in a number of
species, including dolphins.
Studies measuring captive dolphin welfare
Similarly, there are only a handful of captive dolphin studies
that have endeavoured to develop welfare measures. Ugaz
et al (2013) correlated salivary cortisol to behavioural param-
eters in 23 T. truncatus, concluding that welfare was better in
open (enclosed area of the sea) than closed (artificial water
and pool) facilities due to lower cortisol levels and less
floating and circular swimming. Castellote and Fossa (2006)
suggested acoustic activity as a welfare measure for belugas
(Delphinapterus leucas) and found it dropped to low levels
during stressful events, but they did not correlate it with other
parameters and only studied two animals. In a multi-discipli-
nary approach, Waples and Gales (2002) looked at inappe-
tence, social behaviour, lethargy, weight loss and blood
parameters in three T. truncatus with substantially deterio-
rating welfare likely due to social stress, revealing useful
associations although again limited by sample size.
The C-Well© Assessment
In the first development of a welfare assessment protocol for
dolphins, Clegg et al (2015) studied 20 T. truncatus in three
facilities and adapted a well-established farm animal assess-
ment (Welfare Quality® 2009a,b,c) to this species (the C-
Well© Assessment). The research used 36 multi-dimensional
measures, 58% of which were animal-based, to yield indi-
vidual welfare scores comparable on many different levels
(eg by measure, criteria, in total; among pools, sex, age class,
facilities). Although the measures were unweighted, they
were validated through expert opinion and application in
specific contexts, and have associated standardised methods
and thresholds. Some are reviewed in the relevant categories
in Research relevant to dolphin welfare.
Given the lack of existing studies on dolphin welfare indi-
cators, the next section is a review of cetology disciplines
relevant to welfare. We expanded Webster’s (2005) welfare
measurement categories to behaviour, health (from
Webster’s ‘physiology’) and cognition (from ‘neurobi-
ology’). Health, while still including physiology, encom-
passes longer-term welfare indicators, and cognition
includes experimental psychology methods potentially
valuable for assessing welfare.
Research relevant to dolphin welfare
Health
Health-welfare interface
Health and welfare interact directly and indirectly as part of
a complex relationship (Walker et al 2012). A reasonable
level of health is considered a prerequisite for good animal
welfare (Webster 2005; Hill & Broom 2009), while poor
health is a likely contributing factor to poor welfare (Fraser
et al 1997; Dawkins 2004; Boissy et al 2007; Mason &
Veasey 2010). But do all components of poor health affect
welfare? We refer back to our definition of welfare (Spruijt
et al 2001) to address this: the balance of affective states
and health and should only be impacted when poor health
© 2017 Universities Federation for Animal Welfare
Applying welfare science to bottlenose dolphins 167
either directly impacts affective state through, for example,
nausea, lethargy or pain, or indirectly through loss of
function. Poor health (eg an asymptomatic tumour) does not
always affect emotional state and hence welfare, as we
define it (Fraser et al 1997; Mason & Veasey 2010).
Health parameters in dolphins
An infection or disease can cause pain and/or ‘sickness
behaviour’, which includes inappetence, lethargy, depres-
sion, and anti-social behaviours, all of which have direct or
indirect effects on affective state (Broom 1991; Millman
2007; Sneddon et al 2014). Dolphins tend to mask
symptoms of pain and disease as a survival adaptation
(Waples & Gales 2002; Castellote & Fossa 2006), which
therefore may only become obvious when the health
problem is severe. Perhaps, as a consequence, little is
published about indicators of pain in dolphins, with excep-
tions for extreme situations, such as their behavioural
response to killing methods in the wild (Butterworth et al
2013). Weary et al (2006) and Sneddon et al (2014) provide
cross-species advice for identifying behavioural and physi-
ological pain markers, such as studying behavioural differ-
ences after analgesia administration. Inappetence and
lethargy in dolphins have been correlated with many
different diseases and together are generally reliable as poor
health indicators (Joseph et al 1986; Johnson et al 2009).
However, they can also be caused by social stress or even
reproductive events such as oestrus (Waples & Gales 2002),
where the associated affective states may vary from
negative to positive. Studies on the behavioural and haema-
tological characteristics of inappetence, where differentia-
tions are made depending on whether it was caused by poor
health or social stressors, are much needed.
In lieu of reliable pain indicators, physical bodily damage
has been used as a health-related welfare measure in other
captive species (Broom 1991; Welfare Quality® 2009a,b,c;
Mononen et al 2012), and for wild animals as well (eg
Jordan 2005; Cattet et al 2008). Clegg et al (2015) proposed
the percentage of rake marks (superficial lesions and scars
caused by conspecifics in play, sexual and aggressive
behaviours; Scott et al 2005) on the body as a welfare
measure for bottlenose dolphins, since such marks can be
used as a proxy indicator of aggression levels and social
stress (Scott et al 2005; Orbach et al 2015). However, this
measure requires further investigation, for example to
differentiate rake-mark levels due to high levels of play and
aggression while controlling for age and sex differences.
Longer-term measures of dolphin health could also be useful
for assessing welfare. Body Condition Scoring (BCS), an
assessment of the extent of body fat present (Roche et al
2009), has been favoured as a general welfare measure (eg
wild: Mann & Kemps 2003; Pettis et al 2004; Cattet et al
2008; captive: Roche et al 2009; Welfare Quality®
2009a,b,c; Mononen et al 2012) and it has already been used
in wild health assessments of T. truncatus (Fair et al 2014;
Schwacke et al 2014). Joblon et al (2014) produced a stan-
dardised protocol using stranded short-beaked common
dolphins (Delphinus delphis), and Clegg et al (2015)
developed a standardised BCS graphic for T. truncatus but
did not test its reliability. The next step for these BCS tools
is to correlate the results to other measures of affective state:
Roche et al (2009) conducted this with cows, concluding
that BCS may serve as a proxy indicator for hunger, satiety
or feeling ill (leading to inappetence). Other health-related
conditions such as diarrhoea, skin inflammation, eye
condition, and coughing, have been used as farm animal
welfare measures (Welfare Quality® 2009a,b,c; Mononen
et al 2012), some of which were proposed for T. truncatus
welfare (skin and eye condition, coughing; Clegg et al
2015), but have not been studied in relation to affective
states. Haematological indices can be measures of disease
states, especially when the pathology is advanced, but so far
have had limited use in welfare assessments due to potential
high inter- and intra-individual variation. Although wild
dolphin health assessments have published their data and
established baselines (Thomson & Geraci 1986; Dierauf &
Gulland 2001; Wells 2009), and captive dolphin voluntary
blood sampling is readily achievable using positive rein-
forcement training (Brando 2010), studies have not yet
linked ranges of blood values to health-related welfare.
Population measures of longer-term health and welfare such
as longevity and reproductive rate should also be considered
(Dawkins 1998; Barber 2009). However, as with farm
animals, parameters, such as high reproductive success, do
not necessarily indicate that welfare is good (Dawkins
1980). For captive dolphin populations, baselines are being
established by projects (notably in the US) allowing access
to their valuable multi-species databases (Small &
DeMaster 1995; Innes et al 2005; Venn-Watson et al 2011).
Welfare conclusions from fitness measures should be
supported by other data (Swaisgood 2007), such as in
Christiansen and Lusseau’s study (2015) linking distur-
bance behaviour from whale-watching boats, body
condition and foetal growth rate in minke whales
(Balaenoptera acutorostrata). Data on the incidence and
severity of diseases can also be used as population-level
health parameters: such wild studies are available (eg Reif
et al 2008; Schwacke et al 2014), but data are not published
for captive dolphins. However, extensive records are kept
for most captive dolphins (C van Elk, personal communica-
tion 2016) and, thus, peer-reviewed publications on the
nature of their diseases would be beneficial for establishing
standardised health assessments.
Physiological parameters
Measures of physiological responses can contribute to
assessments of emotions and affective states (Désiré et al
2002; Webster 2005; Boissy et al 2007). Endocrine
responses to stressors are most commonly used (eg Moberg
& Mench 2000), but as interest increases in positive
welfare, other markers are being considered: for example,
the balance of sympathetic and parasympathetic systems
(for a review, see Boissy et al 2007), and indicators of
eustress (positive stressors, eg mate acquisition, experi-
enced by the animal; Selye 1975). Within dolphin physi-
ology research, numerous studies of physiological measures
Animal Welfare 2017, 26: 165-176
doi: 10.7120/09627286.26.2.165
168 Clegg et al
of stress for wild T. truncatus (eg Ortiz & Worthy 2000; Fair
et al 2014; Schwacke et al 2014) have provided useful
baselines, which will start to elucidate individual variation
and repeatability questions (Atkinson et al 2015). Sample
collection in the wild is challenging since taking blood is
not possible without restraint and faecal samples are
difficult to obtain (Atkinson et al 2015). This area, specifi-
cally, is where training for voluntary samples in captivity
has exceptional advantages; for example, voluntary saliva
collection is feasible and can provide accurate cortisol
measurements in T. truncatus (Pedernera-Romano et al
2006; Ugaz et al 2013). Other sampling protocols are also
possible with training, such as blood, faecal, blow (expira-
tion of air) and biopsy collection. As for terrestrial animals,
marine mammals experience diurnal and seasonal variation
in cortisol levels (for a review, see Atkinson et al 2015),
which would need to be taken into account in any welfare
assessment and suggests that a conservative range would
need to be used in any conclusions made, as opposed to a
single threshold. Additionally, a recent review advised
caution when applying terrestrial animal stress models to
marine mammals. While corticosteroid pathways seem to be
similar, evidence indicates other neuroendocrine hormones
(eg catecholamines) may be regulated very differently
(Atkinson et al 2015). Further, long-term studies on
cetaceans in captivity could start to answer such questions
on hormone regulatory systems. Innovative new collection
techniques enabling accurate animal identification (example
with cetaceans: whale blow), and insightful behavioural
correlations, must also guide future progress (Möstl &
Palme 2002): advice very applicable to dolphin studies.
Behaviour
Social behaviour
Behavioural measures are an important component in
welfare frameworks (Dawkins 2004; Maple 2007), with
some believing that they are more informative about
welfare than health since behaviours are likely more indica-
tive of emotional state (Gonyou 1994; Joseph & Antrim
2010). There have been a number of long-term studies of
wild dolphin behaviour (Wells 1991; Mann et al 2000;
Parsons et al 2006), including social relationships within
their fission-fusion societies (Mann et al 2000; Wells 2009).
Surprisingly, ethological studies of captive populations
have not, until recently, been commonplace (Dudzinski
2010). Social behaviour measures will foreseeably be one of
the most important tools in assessing dolphin welfare: as
highly social mammals (Pryor & Norris 1998; Mann et al
2000), they are susceptible to social stress. Sudden changes
in conspecific associations, aggression levels and social
isolation have been correlated with declines in welfare
(Waples & Gales 2002). Excessive or abnormal aggression
levels are used as farm animal welfare measures (Webster
2005; Welfare Quality® 2009b; Mononen et al 2012), and
using existing ethograms of aggressive behaviours to
analyse frequencies over time could reveal dolphins’
‘excessive’ and ‘normal’ thresholds (Samuels & Gifford
1997; Scott et al 2005). Increased quantity and severity of
rake marks could serve as a proxy indicator for levels of
aggression and social stress (Waples & Gales 2002; Scott
et al 2005). Clegg et als (2015) rake-mark assessment,
currently using very conservative thresholds, might be
validated to allow monitoring of aggression levels. Rake-
mark quantification is an example of a method where
collaboration between wild and captive researchers might
be fruitful, since aggression is harder to observe in the wild
and rake-mark levels could be used as proxy measures
(Clegg et al 2015; Scott et al 2005).
While social stress is a negative consequence of being a
social mammal, the highly social life of dolphins also has
positive effects. Positive social (ie affiliative) behaviour has
been proposed as an indicator of good welfare in other
species (Boissy et al 2007; Buchanan-Smith et al 2013).
Affiliative behaviour has been well-documented in wild
Tursiops spp (Herman & Tavolga 1980 (early review);
Connor et al 2000, 2006; Sakai et al 2006), and a little less
so in captivity (Tamaki et al 2006; Dudzinski 2010). Gentle
rubbing behaviours between dolphins are thought to be
analogous to allogrooming in terrestrial mammals (Tamaki
et al 2006; Kuczaj et al 2013) and may have potential as a
measure of good welfare (Boissy et al 2007), along with
synchronous swimming (thought to reflect social bonds;
Connor et al 2006). Dudzinski (2010) and Kuczaj et al
(2013) reviewed both wild and captive social affiliative
behaviour, agreeing that in both settings tactile behaviours
seem to be used to express emotions.
Play
Play behaviour is one of the strongest potential welfare indi-
cators for animals, mainly because it is more likely to occur
in the absence of threats and utilitarian needs (Bel’kovich
et al 1991) and is linked to positive emotions (Held &
Špinka [2011] reviewed link with welfare). Play is also
likely to improve long-term fitness and health, as well as
being socially contagious and therefore capable of
spreading good welfare in groups (Held & Špinka 2011);
these less-acknowledged benefits are especially relevant to
the welfare of group-living dolphins. Despite this, play is
not commonly used as a measure in welfare assessments
(Welfare Quality® 2009a,b,c), most likely because of its
inherent variability (Held & Špinka 2011) and difficulty of
measurement There is also evidence for some species that
play may not always be linked to a positive emotional state
(Blois-Heulin et al 2015).
Evidence for wild and captive dolphin play is abundant (for
reviews, see Paulos et al 2010; Kuczaj & Eskelinen 2014),
including copious examples of object play (recent papers:
Kuczaj & Makecha 2008; Paulos et al 2010; Greene et al
2011; Delfour & Beyer 2012), and evidence of inventing
games (Pace 2000). McCowan et al (2000) showed that
captive dolphins monitored their bubble quality as well as
‘planned’ for the behaviour; suggesting involvement of
conscious thought and appraisal and strengthening the
notion that play impacts affective state. Hill and Ramirez
(2014) studied play in 14 belugas (Delphinapterus leucas)
over three years, revealing differences between adult and
© 2017 Universities Federation for Animal Welfare
Applying welfare science to bottlenose dolphins 169
young preferences and showing that bouts were longer and
more diverse when enrichment devices were involved.
Where play is studied in captivity, the influence of any prior
conditioning should be noted: Neto et al (2016) showed that
when trainers positively reinforced dolphins’ interactions
with toys, their interest in the objects increased outside of
the sessions. This technique could be used to increase the
benefits of the toys to the dolphins but, until we have other
measures of positive affective states available in this
situation, the motivation to play may be influenced. In any
case, as with all species, standardised measurements are
needed. A study of African elephants (Loxodonta africana)
addressed this using a play index (Vicino & Marcacci
2015), and a similar approach might be possible with
dolphins. Such a behavioural measure could easily be appli-
cable to wild dolphin welfare assessments, for example to
investigate whether exposure to more environmental or
social stressors results in reduced play frequencies.
Abnormal behaviour
Abnormal behaviours are most often studied in the context
of stereotypic behaviour, which has been most recently
defined as “…repetitive behaviour induced by frustration,
repeated attempts to cope, and/or CNS dysfunction”
(Mason & Rushen 2008). Abnormal behaviours are seldom
observed in wild animals, although Miller et al (2011a)
suggest they observed stereotypic swimming in lemon
sharks (Negaprion brevirostris). In one of the only studies
describing abnormal behaviour in wild dolphins, the causes
and effects of solitary living for T. truncatus were investi-
gated, and certain aspects were concluded as abnormal (eg
behaviour oriented excessively towards humans; Müller &
Bossley 2002). Stereotypic behaviour is commonly investi-
gated as a welfare measure for captive animals (for a
review, see Mason & Rushen 2008). There are scarcely any
published studies with captive dolphins, and the small
handful existing are outdated (Gygax 1993 and Clark 2013
describe this literature), making it hard to identify any
common explanatory variables. Stereotypic swimming has
been discussed in the literature as a concern for captive
dolphins. There are disparities among definitions of this
behaviour (Gygax 1993; Miller et al 2011b), but terrestrial
animal studies also suffered similar problems with pacing
behaviours and found that the variability and possible
functions must be meticulously analysed for it to be defined
as a stereotypy (Mason & Rushen 2008). Sobel et al (1994)
observed preferences in the directionality of circular
swimming, but did not measure whether the route around
the pool was fixed and whether the animal was vigilant at
the time. There is little evidence correlating stereotypic
swimming with other potential factors of welfare. For
example, although Ugaz et al (2013) found that in closed
facilities there were higher rates of circular swimming as
well as higher cortisol levels, they did not statistically test
for a correlation between these two factors. Clegg et al
(2015) included a stereotypy measure but based thresholds
on terrestrial animal frequencies, since there was no data
from dolphin species. Since there are ongoing questions
about whether higher stereotypy frequency infers poorer
welfare, even in terrestrial animals (Mason & Latham 2004;
Dawkins 2006; Mason & Rushen 2008), future studies on
this phenomenon in dolphins should aim to correlate
suspected stereotypic behaviour with other indicators of
welfare to validate it as an indicator. Basic work regarding
the appearance of stereotypies is also needed, for example,
the two main types of stereotypy defined in terrestrial
mammals are ‘oral’ and ‘movement’ (Webster 2005; Mason
& Rushen 2008), so a fundamental investigation would be
to ascertain whether the same is true for dolphins.
Anticipatory behaviour
Recently, anticipatory behaviour (a measure of ‘reward-
sensitivity’; Spruijt et al 2001) has been used as a welfare
measure in farm and zoo animals; low intensity anticipatory
behaviour is thought to reflect positive affective states and
high intensity anticipation indicates poorer welfare as the
animal is heavily dependent on the reward (Spruijt et al
2001; Watters 2014). While one preliminary study focused
on anticipatory behaviour in captive bottlenose dolphins
(Jensen et al 2013), further work is necessary given the
different training methods (ie conditioning to ‘rewards’) in
dolphin facilities, which might ultimately be closely linked
to welfare. Based on the reward-sensitivity paradigm it is
likely that dolphins showing moderate anticipatory
behaviour might experience positive affective states, while
those that perform it for excessive amounts of time might be
frustrated or have little other stimulation (Watters 2014). In
order to evaluate its utility for welfare assessment, future
studies with dolphins and other species should investigate
the association between anticipatory behaviour frequencies
and other welfare indicators, in order to understand what
might qualify as ‘excessive’ levels.
Cognition
Emotions
Emotions are defined as intense, short-lived affective
responses to an event, usually associated with specific phys-
iological changes (Dantzer 1988). Animals with higher
cognitive abilities may be capable of more complex
emotions (eg guilt) (Paul et al 2005), and while this might
result in increased chances of suffering, it could also lead to
higher potential for positive affective states. Research
beyond the ‘basic emotions’ (eg fear, rage, play; Mendl et al
2010) is essential to understand the valence and arousal
levels of affective states which make up overall welfare
(Leliveld et al 2013; Siegford 2013). Désiré et al (2002) and
Boissy et al (2007) provide reviews on measuring animal
emotion and the relevance to welfare.
Although dolphin emotion studies are scarce, there have been
more studies on negative than positive ones. Most studies
have looked at how sounds might reflect emotions, for
example, burst pulse sounds have been associated with
agonistic and aggressive behaviours (Overstrom 1983), and
long-term etho-acoustical projects have made headway in
pairing sounds to behaviour (eg Herzing 1996; Janik & Sayigh
Animal Welfare 2017, 26: 165-176
doi: 10.7120/09627286.26.2.165
170 Clegg et al
2013). Animal emotion research is now widening to measure
positive emotions as well (Boissy et al 2007), but there are no
strongly supported indicators as yet in dolphins (Kuczaj et al
2013). Tactile behaviour was suggested by Dudzinski (2010)
and Kuczaj et al (2013) to be linked to positive emotions in
dolphins, but has not yet been analysed in conjunction with
other indicators. Motivation and preference testing are appli-
cable to captive dolphins and could reveal indicators of
emotion (Gonyou 1994; Mendl et al 2010).
Environmental enrichment
This sub-section is applicable to dolphins under human care
only. Environmental enrichment is any technique designed
to improve biological functioning of captive animals
through environmental modification (Newberry 1995).
Bottlenose dolphins are good candidates for enhanced
welfare through enrichment due to their cognitive abilities
(Schusterman et al 2013) and propensity to, and creativity
within, play (Kuczaj & Eskelinen 2014). Enrichment has
been provided to captive dolphins for several decades, but
there are few published studies describing the animals’
responses (for a review, see Clark 2013). Furthermore,
enrichment is often assumed to automatically enhance
welfare even if it is unclear whether the animal’s affective
state will be improved (for reviews, see Swaisgood 2007;
Würbel & Garner 2007). Enrichment strategies should be
monitored to ensure that they are true enrichment by moni-
toring the animals’ responses and looking for signs of habit-
uation so that decisions can be made as to when, where and
how the enrichment is presented again (Kuczaj et al 2002;
Hoy et al 2010; Siegford 2013).
Recently, cognitive challenges have been presented as
enrichment, with positive results as long as the animals
possess the resources and skills to solve the problem
(Meehan & Mench 2007; Siegford 2013). Clark (2013)
supports cognitive enrichment with dolphin species,
hypothesising that floating, simplistic objects are not suffi-
cient to hold the dolphins’ interest in the long-term.
However, behaviour should be monitored to investigate
whether this is indeed the case (Hill & Broom 2009), and
such data, which shows responses to definable, repeatable
contexts, could also aid in finding welfare indicators
(Delfour & Beyer 2012). The Human-Animal Relationship
(HAR) is only just beginning to be investigated in other
species in relation to cognitive enrichment and welfare
(Whitham & Wielebnowski 2013) and, due to the multiple,
daily, and often close-contact interactions, is very likely to
contribute to the welfare state of captive dolphins (Brando
2010; Clegg et al 2015). Future investigations assessing
the HAR might aim to disentangle the effects of food rein-
forcement with the dolphins’ attitude towards the humans
themselves. An example of such an approach is shown by
Perelberg and Schuster (2009), who demonstrated that
outside of feeding sessions, a captive bottlenose dolphin
group approached humans to receive rubs and petting in
the absence of any other rewards. Given that many
cetacean species show much tactile behaviour during
intra-specific social affiliation (Dudzinski 2010; Kuczaj
et al 2013), investigating the frequency and dimensions of
voluntary human contact by the animals, during and
outside of training sessions, might be a meaningful
measure of their affective states.
Cognitive measures of dolphin welfare
Dolphins’ cognitive abilities are frequently compared to
those of great apes (Delfour 2010; Schusterman et al 2013),
and may be linked to their fusion-fission society (Connor
et al 2000; Maze-Foley & Würsig 2002). Dolphins display
co-operative hunting (Connor et al 2000), use tools (eg
Smolker et al 1997), and recognise their mirror image
(Reiss & Marino 2001; Delfour 2006). Studies of cognitive
bias, which investigate how emotional experiences affect
cognitive processes, may aid in our interpretation of
welfare, and constitute measures themselves (Paul et al
2005; Mendl et al 2009). Given the dolphins’ learning capa-
bilities (Brando 2010), many of the non-invasive cognitive
bias methods reviewed in Mendl et al (2009) used with
other species could be adapted. Paul et al (2005) also
reviewed evidence for memory and attention bias processes
in animals, concluding that if confirmed they could have
implications for measuring welfare.
In humans as well as non-humans, the brain hemispheres
process information differently, producing lateralised behav-
iours, ie a preference for either the left or right eye or body
part (Rogers 2002). It seems that animals may predomi-
nantly use the right hemisphere when stressed (see Rogers
2010), with Leliveld et al’s (2013) review going further to
conclude that negative emotions are managed by the right
hemisphere and positive emotions by the left (‘emotional
lateralisation’). Examples of lateralised behaviours in wild
and captive cetaceans are common, eg during foraging
(Clapham et al 1995; Silber & Fertl 1995), flipper-rubbing
(Sakai et al 2006), and visual discrimination tasks (Yaman
et al 2003; Delfour & Marten 2006). Most notably, Karenina
et al (2010, 2013) showed that belugas and killer whales
(Orcinus orca) placed calves on their right side in non-
threatening situations, with killer whales preferring the left
when the situation became increasingly threatening (in this
case proximity to boats). Sakai et al (2006) suggested a link
with positive affective state since the left pectoral fin and eye
were favoured during affiliative flipper-rubbing behaviour in
Indian Ocean bottlenose dolphins (Tursiops aduncus). These
last examples concerning lateralised behaviour and affective
states should form a basis for future research into welfare
implications of this phenomenon.
In the field of cognition, in particular, but also within health
and behaviour, researchers rarely study both wild and
captive dolphins, resulting in a skewed perspective of
particular topics in certain environments, and leading us to
an initial recommendation to increase collaborative efforts
and reviews (in accordance with Hill & Lackups 2010; Pack
2010). Finally, although we must understand the dolphins’
cognitive abilities, we should do so bearing in mind their
umwelt, ie their ‘subjective universe’, and the focus of etho-
phenomenological studies (Delfour 2006, 2010). For
example, an intermodal associative task was completed
© 2017 Universities Federation for Animal Welfare
Applying welfare science to bottlenose dolphins 171
very differently by bottlenose dolphin subjects due to the
dominance hierarchy at the time dictating participation and
mode of learning (Delfour & Marten 2006). Being
cognisant of the dolphins’ umwelt may help in determining
what is important to the dolphins, and thus how to provide
them with a good quality of life.
Considerations for developing dolphin welfare
measures
In this section we review recommendations on the design of
studies to investigate the measures discussed above. Welfare
measures should be developed in situ, thus ensuring applica-
bility to the dolphins and their environment (Dawkins 2006;
Maple 2007). The measures must also be species-specific
(Blokhuis 2008; Barber 2009; Hill & Broom 2009), and
examine welfare at an individual level where possible
(Siegford 2013). Zoological institutions have been advised
to employ scientists specifically dedicated to assessing
welfare (Maple 2007; Barber 2009), and facilities main-
taining dolphins should take this step also.
The first proposed measures for T. truncatus should be
validated through correlations with other parameters. Our
review addresses the potential measures for validation
which we identified with respect to cetacean health,
behaviour and cognition (Table 1). When establishing
welfare measures, studies of captive rather than wild
dolphins, are more likely to be successful due to greater
access to the subjects, their history, and their environment.
International, inter-facility collaborations are vital to
combat problems of low sample sizes and to control for
inevitable environmental variation. For wild dolphin
welfare indicators, long-term studies are the natural
starting point since most have individual behavioural,
physiological, as well as life history data (Wells 2009; Fair
et al 2014). While it would be inaccurate to apply all
measures for wild and captive animals without validation
(Jordan 2005), it is likely that many welfare indicators, at
least behaviourally, will be consistent between wild and
captive T. truncatus since their repertoires show similari-
ties (Mann et al 2000; Dudzinski 2010).
When validating measures, pre-existing conditions can be
used where it is likely the animal has very good or poor
welfare (Jordan 2005; Castellote & Fossa 2006; Whitham &
Wielebnowski 2013). For example, transportation offers
opportunities to assess welfare as it is assumed to induce a
substantial, but short-term, welfare change for captive
cetaceans (eg Castellote & Fossa 2006). Long-term states
associated with social contexts may be more salient for
welfare measurement: for example, the period after
transport when the animals are introduced to a new group.
Group changes are frequent enough in dolphinaria networks
to provide adequate sample sizes for analysis. The selected
behaviours and physiological parameters should then be
measured during these events (and cognitive data if
possible), with focal qualitative data (eg trainer ratings)
taken concurrently to support the presumed change in
welfare. Welfare measures should be conducted regularly,
and also separately from full assessments. For example,
behavioural measures of welfare could be applied on a
weekly basis to dolphin groups since behavioural moni-
toring has been advised as essential for ensuring good
welfare (Maple 2007), and especially with captive dolphins
(Waples & Gales 2002; Clegg et al 2015). Eventually,
comparing results from measures and assessments between
individuals can highlight associations with good or poor
welfare, thus indicating where changes in management
protocols should occur and stimulating improvements in
welfare of the animals themselves.
Conclusion
We have reviewed the literature on animal welfare science
and cetology in order to identify the most successful inter-
sections for developing bottlenose dolphin welfare
measures. A general theme is that collaborations, whether
wild-captive, across different cetology fields, or between
multiple captive facilities, are necessary if we want to
address this multi-dimensional concept.
We suggest that indicators, such as cortisol levels, inappe-
tence and bodily injuries, as well as body condition and
population fitness measures in the longer term, may help us
assess health-related welfare. Behavioural measures are
Animal Welfare 2017, 26: 165-176
doi: 10.7120/09627286.26.2.165
Table 1 Summary of the welfare-related topics in dolphin
health, behaviour and cognition which merit further
investigation in order to develop measures of welfare.
Evidence supporting each topic has been taken from
bottlenose dolphins (Tursiops truncatus) where possible,
but where these were lacking studies from other
cetacean species had to be used.
Category Aspects meriting further investigation
as dolphin welfare measures
Health Epidemiological measures (eg mortality,
reproductive success)
Disease prevalence
Body Condition Scoring
Cortisol (and other ‘stress’ hormone) levels
Rake mark percentage cover
Behaviour Excessive aggression
Affiliative behaviour
Play
Anticipatory behaviour
Abnormal and stereotypic behaviours
Cognition Emotions linked with sound production
Indicators of basic emotions
(eg fearful, playful, rage)
Indicators of more complex emotions
(eg contentedness, depression)
Cognitive bias testing
Visual and behavioural laterality
172 Clegg et al
likely to be the most informative for dolphin welfare, and
we have shown evidence that tactile affiliation, play, antici-
patory behaviour and stereotypic behaviours may be closely
linked to affective states. Cognitive measures reflect how
behavioural and physiological components are integrated to
form the affective states experienced by the animals, and
thus recent techniques, such as cognitive bias testing hold
much promise for welfare assessment.
Lastly, we identified practical recommendations for vali-
dating the first measures, concluding that although captive
studies should take the lead, long-term wild studies are also
rich sources of potential indicators. Any proposed measures
should be tested in situations likely to elicit changes in
welfare with adequate sample sizes to allow the major envi-
ronmental variations to be controlled for. Established
measures would allow facility managers to monitor and
improve the dolphins’ welfare, aid in regulatory decisions,
and could enrich wild dolphin research by revealing changing
affective states. This review’s findings are species-specific to
bottlenose dolphins, but the general principles and selected
measures could be adapted to other cetacean species. Our
overall aim was to present current cetology knowledge in
terms of measuring welfare, with the hope of stimulating
researchers globally to take up the challenge.
Acknowledgements
The authors are each indebted to a number of experts in
the various fields of cetology and welfare science for their
discussions and encouragement. This work forms part of
IC’s PhD, supported by CIFRE fund no 2014/0289, and
UFAW grant no 22-14/15.
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... Welfare science has moved on from considering good welfare as simply the absence of suffering and is now focussed on defining and measuring positive affective states, with behavioural measures being a key element in their evaluation ( Boissy et al., 2007;Yeates and Main, 2008). Support for "feelings-based" welfare definitions is strong, stipulating that health only impacts welfare if the animal's feelings are affected (e.g., feeling sick), and therefore encouraging research on identifying welfare indicators associated with health conditions (Mason and Veasey, 2010;Watters, 2014;Hemsworth et al., 2015;Clegg et al., 2017b;Veasey, 2017). This is not to say that health-related welfare measures are redundant: they are readily quantifiable, easy to standardise, and continue to be used in welfare assessment frameworks for a range of species (Welfare Quality R , 2009; Mononen et al., 2012;Clegg et al., 2015). ...
... Notably, when cetacean species are experiencing poor health, they often mask symptoms and 'sickness behaviour' until the pathology is well developed ( Waples and Gales, 2002;Castellote and Fossa, 2006). There is therefore a need to identify any behavioural indicators which reliably signal the early stages of health problems (Clegg et al., 2017b). These might be related to the animal's social behaviour, appetence or interaction with its environment. ...
... Qualitative measures such as those used in this study allows the harnessing of holistic knowledge from those caretakers who know the animals' behaviour and welfare the best (Whitham and Wielebnowski, 2009;Phillips et al., 2017), and up until now has not yet been exploited in dolphin research, despite the many hours of daily close physical contact spent between animal and caretaker. Such a tool, which is simple to execute accurately, generates meaningful data and facilitates daily monitoring of the animals, would be very valuable to captive dolphin management ( Clegg et al., 2015Clegg et al., , 2017b. A dolphin's "Willingness to Participate" in training sessions could indeed be influenced by many variables, and it is likely that for some of the days and data points during our study, we might not have been measuring welfare but instead an individual variation in satiety, or perhaps a time when other events in the pool where far more rewarding than training sessions. ...
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Welfare science has built its foundations on veterinary medicine and thus measures of health. Since bottlenose dolphins (Tursiops truncatus) tend to mask symptoms of poor health, management in captivity would benefit from advanced understanding on the links between health and behavioural parameters, and few studies exist on the topic. In this study, four representative behavioural and health measures were chosen: health status (as qualified by veterinarians), percentage of daily food eaten, occurrences of new rake marks (proxy measure of social activity), and willingness to participate (WtP) in Positive Reinforcement Training sessions as qualitatively measured by their caretakers. These data were collected multiple times a day, every day over the course of a year from a multi-facility, large sample size (n dolphins = 51), allowing powerful analyses of the relationships between measures. First, it was found that dolphins with a higher WtP score also had a significantly better health status, ate a higher percentage of their daily food, and a lower occurrence of new rake marks. In addition, the WtP score was significantly lower up to 3 days before the weekly veterinary diagnosis of a decrease in health state; the percentage of daily food eaten and new rake mark measures did not show any significant change before such a diagnosis. These results suggest that WtP in training sessions is a potential behavioural measure of dolphin welfare, and an indicator of early changes in the dolphins' health state. We therefore suggest measurement of WtP as a more practical and non-invasive tool to support veterinary care and general management. More work needs to be conducted to elucidate the influence of social behaviour on health, and to identify other potential welfare indicators, but this long-term study has shown that qualitative measures can be both practical and valid when assessing dolphin welfare.
... While repetitive swimming could be widespread across zoos, few data are published and Miller et al. (2011) found that dolphins in a multi-zoo study (N = 6 zoos and 18 dolphins) performed the behaviour in less than 5% of scans. Gygax (1993) was unable to conclude whether repetitive circular swimming in two dolphins was stereotypical, and suggested the behaviour requires more study whilst Clegg et al. (2017) concluded that adequate studies have not been carried out. Some repetitive circular swimming might not be a stereotypy because it is punctuated by the performance of other behaviours. ...
... Spontaneous occurrences of play and attempts to stimulate play using enrichment (Section 5) have been reported for captive dolphin species (see reviews by Kuczaj and Eskelinen, 2014;Paulos et al., 2010) and beluga whales (Delfour and Aulagnier, 1997). Consistent with other vertebrate mammals (see Held and Špinka, 2011), the use of play as a welfare indicator in cetaceans appears to be based more on tradition than due to any validation against other welfare in- dicators ( Clegg et al., 2017;Serres and Delfour, 2017). Play will be considered further in Section 4.4 (social management). ...
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... The cognitive bias results of one animal or group should not be extrapolated to others without reassessment, and regular monitoring of an animal's bias should be encouraged where possible. Regarding the practical applications of cognitive bias testing for welfare assessments, we should also be aware that although it is one of the most valid approaches for measuring longer term emotional states currently available, it should still be used in conjunction with other measures [139], as this will help to ensure the construct validity of the tests. Only welfare evaluations that employ a suite of multidisciplinary indicators can hope to make a reasonable estimation of the animals' actual welfare state [9,140]. ...
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... The fact that anticipatory behaviour intensity significantly predicted participation in the upcoming event, shows the animals likely had a positive perception of the events in this case. This reinforces the importance of enrichment programs and HAIs in zoos as drivers of positive welfare (Brando et al., 2016;Clegg et al., 2017b). Nonetheless, more investigations are needed on anticipatory behaviour in all species in order to understand its intra-individual stability, context-dependent variability, and the thresholds reflecting different affective states. ...
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Animal welfare science is a burgeoning field, but research on cetaceans (whales, dolphins and porpoises) is lacking. Bottlenose dolphins (Tursiops truncatus) are the most well-known and studied cetaceans, particularly in captivity, and thus are used in this review as a model for other cetacean species. Despite the public interest and need for such research, studies specifically investigating dolphin welfare are lacking. This review uses the three broad categories of behaviour, health, and cognition, to discuss how dolphin welfare has been assessed thus far, and could be assessed in future. We present welfare indicators validated in other species that could be applied to dolphins, including innovative measures, such as cognitive appraisal of emotions. We provide a summary of practical recommendations for validating the indicators of bottlenose dolphin welfare. This paper aims to stimulate further research into dolphin welfare which could improve the lives of the animals themselves and ultimately support regulatory decisions. We recommend uniting expertise in cetology and welfare science in order to develop a holistic approach to dolphin welfare assessment.
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The field of welfare science and public concern for animal welfare is growing, with the focus broadening from animals on farms to those in zoos and aquaria. Bottlenose dolphins (Tursiops truncatus) are the most common captive cetaceans, and relevant regulatory standards are principally resource-based and regarded as minimum requirements. In this study, the farm animal Welfare Quality® assessment was adapted to measure the welfare of bottlenose dolphins, with a similar proportion of animal-based measures (58.3%). The 'C-Well®' assessment included eleven criterion and 36 species-specific measures developed in situ at three marine mammal zoological facilities, tested for feasibility and accuracy, and substantiated by published literature on wild and captive dolphins and veterinary and professional expertise. C-Well® scores can be calculated for each measure or combined to achieve an overall score, which allows for the comparison of welfare among individuals, demographics, and facilities. This work represents a first step in quantifying and systematically measuring welfare among captive cetaceans and can be used as a model for future development in zoos and aquaria, as well as a means to support benchmarking, industry best practices, and certification.
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Species have complex relationships with others in the wild, and some such as capuchin (Sapajus apella) and squirrel monkeys (Saimiri sciureus) naturally choose to associate with each other. There are a number of benefits of exhibiting such species in correspondingly mixed communities in captivity to enhance welfare through increased social complexity, which is potentially environmentally enriching in restricted captive enclosures. Monitoring the interactions between species is critical, however, particularly when members of one species are considerably larger and potentially more aggressive than the other. We report on the frequency and nature of interspecific interactions between S. apella and S. sciureus during four time periods over 3 years (2008-2010) following the formation of two mixed species groups at the 'Living Links to Human Evolution' Research Centre in Edinburgh Zoo, Scotland. Both the rate and the distribution of interspecific interactions among aggressive, affiliative and neutral categories of behaviour varied over time (P < 0.05). We predicted that S. apella would engage in more interspecific, particularly aggressive, interactions than S. sciureus than vice versa, as they are the larger, more social species and have a more pugnacious temperament. This was the case overall (P < 0.05), and particularly in 2009 and 2010. We predicted that affiliative interactions would increase over time as the number of youngsters increased and as the youngsters grew up together, establishing equable relationships and "territorial" boundaries. The data did not support this prediction. Both the most affiliative and least aggressive interspecific interactions were observed following internal enclosure refurbishment in 2008 and hence we argue that good enclosure design and husbandry is the most important factor in promoting positive interactions between individuals in mixed species groups. We conclude that long-term monitoring is important, and when combined with appropriate husbandry and enclosure upkeep, the welfare of individuals is enhanced in mixed species groups by the presence of other species. (c) 2013 Elsevier B.V. All rights reserved.
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The detection and assessment of pain in animals is crucial to improving their welfare in a variety of contexts in which humans are ethically or legally bound to do so. Thus clear standards to judge whether pain is likely to occur in any animal species is vital to inform whether to alleviate pain or to drive the refinement of procedures to reduce invasiveness, thereby minimizing pain. We define two key concepts that can be used to evaluate the potential for pain in both invertebrate and vertebrate taxa. First, responses to noxious, potentially painful events should affect neurobiology, physiology and behaviour in a different manner to innocuous stimuli and subsequent behaviour should be modified including avoidance learning and protective responses. Second, animals should show a change in motivational state after experiencing a painful event such that future behavioural decision making is altered and can be measured as a change in conditioned place preference, self-administration of analgesia, paying a cost to access analgesia or avoidance of painful stimuli and reduced performance in concurrent events. The extent to which vertebrate and selected invertebrate groups fulfil these criteria is discussed in light of the empirical evidence and where there are gaps in our knowledge we propose future studies are vital to improve our assessment of pain. This review highlights arguments regarding animal pain and defines criteria that demonstrate, beyond a reasonable doubt, whether animals of a given species experience pain.