This article was originally published in a journal published by
Elsevier, and the attached copy is provided by Elsevier for the
author’s beneﬁt and for the beneﬁt of the author’s institution, for
non-commercial research and educational use including without
limitation use in instruction at your institution, sending it to speciﬁc
colleagues that you know, and providing a copy to your institution’s
All other uses, reproduction and distribution, including without
limitation commercial reprints, selling or licensing copies or access,
or posting on open internet sites, your personal or institution’s
website or repository, are prohibited. For exceptions, permission
may be sought for such use through Elsevier’s permissions site at:
Author's personal copy
Sources of stress in captivity
Kathleen N. Morgan
*, Chris T. Tromborg
Southwick’s Zoo, 2 Southwick Street, Mendon, MA 01756, USA
Department of Psychology, Sacramento City College, 3835 Freeport Boulevard, Sacramento, CA 95822, USA
Available online 25 July 2006
Animals housed in artiﬁcial habitats are confronted by a wide range of potentially provocative
environmental challenges. In this article, we review many of the potential stressors that may adversely
affect animals living in captivity. These include abiotic, environmental sources of stress such as artiﬁcial
lighting, exposure to loud or aversive sound, arousing odors, and uncomfortable temperatures or substrates.
In addition, conﬁnement-speciﬁc stressors such as restricted movement, reduced retreat space, forced
proximity to humans, reduced feeding opportunities, maintenance in abnormal social groups, and other
restrictions of behavioral opportunity are considered. Research in support of the claims for these
environmental elements as stressors for captive animals reveals no unique suite of behavioral or physiological
responses that will clearly indicate the cause of those responses; rather, it is up to us as managers and
caretakers of animals in captivity to evaluate enclosures and husbandry practices to ensure the optimal
well-being of animals in our care.
#2006 Elsevier B.V. All rights reserved.
Keywords: Stress; Captivity; Captive environments
The myriad species with which humans cohabitate are equipped with physiological and
psychological mechanisms for adapting to various levels of challenge from their surroundings.
Among these adaptive mechanisms is a suite of behavioral and physiological responses to stress.
The word ‘‘stress’’ has become used in so many different contexts that it has been argued by some
to be an essentially useless term (McEwen, 2000). Nonetheless, the general understanding of the
Applied Animal Behaviour Science 102 (2007) 262–302
This paper is part of the special issue entitled ‘‘Conservation, Enrichment and Animal Behaviour’’, Guest Edited by
Dr. Ronald R. Swaisgood.
* Corresponding author. Tel.: +1 508 286 3934; fax: +1 508 286 8278.
E-mail address: email@example.com (K.N. Morgan).
0168-1591/$ – see front matter #2006 Elsevier B.V. All rights reserved.
Author's personal copy
term in common parlance necessitates its continued use, and we will employ the term ‘‘stress’’
and related terms throughout this paper as follows.
For the purposes of this document, stress will be deﬁned as the experience of having intrinsic
or extrinsic demands that exceed an individual’s resources for responding to those demands
(Dantzer, 1991). Living systems have evolved to reduce these demands and maintain the status
quo through a series of physiological and sometimes behavioral responses. The tendency of
systems to maintain a steady state is referred to as homeostasis, and for some authors a ‘‘stressor’’
is anything that challenges homeostasis (e.g., Michelson et al., 1995; Selye, 1976). For the most
part, this is the deﬁnition of ‘‘stressor’’ that we will use throughout this paper. A ‘‘stressor’’ in this
case may be an actual physical challenge to homeostasis (such as exposure to a sudden change in
temperature, physical restraint or combat), or the threat of such a challenge (such as a direct stare
from a more dominant individual, or the approach of a human with handling gloves). In either
case, stressors result in a cascade of physiological events designed to prepare the body for
homeostatic challenge—the so-called ‘‘ﬁght or ﬂight’’ response.
In general, the ‘‘ﬁght or ﬂight’’ response involves increased autonomic activity and shifts in
the metabolic proﬁle of an organism as it adjusts to some perceived threat from its surroundings.
Acute, short-term stressors are typically associated with behavioral responses of orientation,
alarm, and increased vigilance. Physiological components of this response proﬁle include
tachycardia, increased respiration rate, increased glucose metabolism, and an increase in various
isomers of glucocorticoids (GCCs), which shift metabolism toward energy mobilization and away
from energy conservation. In comparison, chronic, long-term stress results in prolonged elevation
of GCC levels that in effect become self-sustaining, as prolonged high levels of circulating GCCs
damage areas of the brain responsible for terminating the stress response (for a review of this
mechanism, see Sapolsky and Plotsky, 1990). Physiologically, chronic stress may be indicated by
suppressed reproductive cycling (Chrousos, 1997), blunted activation of the HPA (hypothalamic-
pituitary-adrenal axis) response to acute stress (Goliszek et al., 1996), suppressed immune
responses (Barnett et al., 1992; Ferrante et al., 1998), reduced growth hormone levels and
subsequently inhibited growth rate (Chrousos, 1997; Tsigos and Chrousos, 1995), and reduced
body weight (Bartolomucci et al., 2004; Konkle et al., 2003). Behaviorally, chronic stress may be
indicated by reduced reproductive behavior (Gronli et al., 2005; Hemsworth et al., 1986a),
increased abnormal behavior (Carlstead and Brown, 2005; Schouten and Wiegant, 1997), reduced
exploratory behavior and increased behavioral inhibition (Carlstead and Brown, 2005; Carlstead
et al., 1993b; Vyas and Chattaji, 2004), increased vigilance behavior and increased hiding
(Carlstead et al., 1993b), reduced behavioral complexity (Rutherford et al., 2004), increased
aggression (Bartolomucci et al., 2004; Mineur et al., 2003), increased fearfulness and frequency of
startle (Boissy et al., 2001), and increased freezing behaviorand decreased latency to freeze (Korte,
2001). All of these physiological and behavioral measures have been used to operationally deﬁne
chronic stress in captive animals, as can be seen in the literature review below. For the purposes of
this article, we will consider a given behavior to be an indication of chronic stress if the authors of a
given publication consider it to be so, and substantiate their position with appropriate literature.
While acute stress responses can be considered adaptive, enabling animals to escape from
danger, chronic stress responses are fraught with danger to the long-term health of captive
animals (Broom and Johnson, 1993; Sapolsky, 1996; Sapolsky et al., 1990). Occasional exposure
of captive animals to environmental provocation might be considered as legitimate components
of long-term husbandry regimes (Chamove and Moodie, 1990; Moodie and Chamove, 1990),
particularly for those species targeted for eventual repatriation (McLean et al., 2000; Rabin,
2003). But relentless exposure to persistent stressors can have many deleterious consequences
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 263
Author's personal copy
that are particularly undesirable for animals maintained in captivity, including increased
abnormal behavior (Capitanio, 1986), increased self-injurious behavior (Bellanca and Crockett,
2002; Reinhardt and Rossell, 2001), impaired reproduction (Moore and Jessop, 2003; Tilbrook
et al., 2002) and immunosuppression (Kanitz et al., 2004). Even if we were not compelled for
humane reasons to reduce stress in our captive populations, the economic impact of adverse
environments on captive animals should be sufﬁcient to demand our attention.
One of the putative sources of stress in captivity is interference with or prevention of animals’
engagement in species-typical behaviors for which they appear to have a ‘‘behavioral need.’’ The
concept of behavioral needs is controversial (Cooper, 2004; Hughes and Duncan, 1988; Jensen and
Toates, 1993); however, at least some animal welfare legislation assumes such needs exist
(Brambell, 1965;Sumpter et al., 1999) and animal care standards have been mandated accordingly.
Behavioral needs can be broadly deﬁned as behaviorsthat appear to be largely internally motivated,
since they may occur even in the absence of appropriate trigger stimuli. Such behaviors appear
to be those that an animal must perform, regardless of environmental conditions (Mench, 1998),
and preventing animals from performing such behaviors is thought to be detrimental to their well
being (Friend, 1989). It is not in the purview of this article to discuss the concept of behavioral
needs (for a review, see Dawkins, 1990); however, some researchers investigating sources of stress
in captivity describe behavioral deprivations in terms of behavioral needs. When a given author
uses this term in his or her work to describe results, we will also use the term in such a way.
Perhaps the greatest stressor in populations of captive animals are those over which the animal
has no control and from which they cannot escape. In this article, we review many uncontrollable
stressors that might confront animals in captivity. Our purpose is to identify and describe these
stressors, and to review the literature suggesting that they indeed have adverse effects on captive
populations. It is our hope that in so doing, we will provide a functional checklist for evaluation of
artiﬁcial environments as to their stress potential, so that improvements or alterations may be
made as necessary for the beneﬁt of animal well-being.
2. Abiotic environmental stressors: the presence or absence of critical sensory stimuli
Prior to the introduction of the concept of environmental enrichment (Markowitz, 1975), most
artiﬁcial environments were structurally simple and unresponsive to behavior. Typically, these
environments did not provide animals with opportunities to interact with their surroundings in
ways which promoted the development of sensory and cognitive abilities, or that allowed display
of species-typical behaviors.
Contemporary views of animal welfare have substantially changed the nature of captive
environments. Over the past several decades, scientists have developed strategies for improving
the conditions of captivity that include means by which to increase animals’ behavioral
opportunities. Researchers have investigated the effects of modifying the structure, complexity,
and interactivity of traditional and artiﬁcial environments on the behavior and health of captive
animals (e.g., Baumans, 2005; Markowitz, 1982; Markowitz and Spinelli, 1986; Shepherdson
et al., 1998).
Contemporary methods for improving artiﬁcial environments include, but are not limited to,
enhancing several abiotic parameters, such as increasing natural sound and improving substrate
complexity (Carlstead et al., 1993a; Lutz and Novak, 1995; Sneddon and Beattie, 1995).
Elements from natural habitats have been introduced into zoo exhibits, imbuing them with
an apparent naturalism for visitors and enhancing their ecological relevance to captive
animals (Hutchins et al., 1984). More complex, enriched environments offer animals greater
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302264
Author's personal copy
opportunities for exploration and withdrawal from observation. Increased behavioral options
allow animals to respond to adverse environmental conditions by managing conﬁnement-related
stress (Carlstead et al., 1993a).
Finally, in some instances, interactive or automated technologies have been employed to
increase opportunities for animals to engage in complex problem solving while contending with
variation in the physical properties of their environments (Markowitz, 1982). In essence,
intelligently managed zoological gardens attempt to preserve species-typical behavior (Markowitz,
1997; Rabin, 2003).
While many of these environmental enrichment strategies have undoubtedly improved the
conditions of captivity (Bloomsmith and Else, 2005; Kuehn, 2002;Sorensen et al., 2004;
Swaisgood et al., 2001), they have tended to underemphasize the inﬂuence of artiﬁcial
environments on the sensory behavior of captive animals. In some cases this apparent neglect
may be due to constraints imposed by the ﬁnances or structure of the facilities in which animals
are housed; in others, the dearth of information on species ‘‘umwelt’’ is to blame. While
enrichment techniques in many cases have the aim of improving animals’ abilities to cope with
the artiﬁcial conditions of captivity, the unfortunate truth is that we are often unaware of sensory
elements of the captive environment that animals may ﬁnd stressful. The sensory stimuli of which
we humans are aware are limited, and what is ‘‘out of sight’’ for us may inadvertently stay ‘‘out of
mind’’ when considering our animal charges.
In contrast to how humans perceive them, the artiﬁcial environments typical of captivity are
full of sensory stimuli that might be at best alien to an animal, if not overtly stressful. Unnaturally
intense, punctate, or constant sound, the odor or sight of historic ecological adversaries, the
elimination of scent-marks with daily cage cleaning, the rough and unyielding surfaces of gunite,
tile, wire, or concrete, and exposure to aberrant lighting conditions might all be sources of
environmental stress for animals in captivity. Below, we review evidence that suggests these
factors as sources of stress.
Basedontheamountofresearchfocusingonaudio-vocal behavior in nonhuman animals,
one might rightly conclude that the auditory sensory modality is a critical feature of many of
their natural histories (Byrne, 1982; Ehret, 1980). Yet much remains unknown about the
auditory ranges of most species. This ignorance prevents adequate assessment of auditory risks
to animal welfare, since in modern facilities that house animals, relatively high levels of
unnatural noises in variable frequencies are routinely produced. Unfortunately, many of the
surfaces within these facilities are extremely acoustically reﬂective (Gamble, 1982; Tromborg,
1993). Recordings of the sound pressure levels (spl) at two Northern California zoological
parks (San Francisco and Sacramento) ranged from a low of 62 dB (spl) to a high of 72 dB
(spl), with an average of 70 dB (spl), and was inﬂuenced by the number of visitors, the
intensity of their conversations, the presence of maintenance machinery or exhibit water
features, and the amplitude of sounds of surrounding urban transportation systems (Tromborg
and Coss, 1995). Ambient sound in laboratories is no better. During cage cleaning, for
example, sound pressure levels at a primate research center exceeded 80 dB (spl) (Morgan,
personal observation; Peterson, 1980). Sound levels exceeding 90 dB (spl) have been recorded
in some laboratories housing rats (Pfaff and Stecker, 1976), and over 110 dB when ventilation
equipment was running in others (Sales et al., 1999). In these and similar studies, sound
pressure levels correlated with caretaking activity.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 265
Author's personal copy
These sound levels contrast sharply with sound levels in natural environments. In the wild,
ambient noise levels are highest in rain forest habitats, moderate in riverine habitats, and lowest
in savannah habitats—but in no case do sound pressure levels in nature approach the levels
recorded at zoos or in laboratories. In rain forest habitats, ambient noise levels range from 27 dB
at 06:00 to 40 dB at 15:00, largely a consequence of wind and rustling of leaves (Waser and
Brown, 1986). In riverine habitats, sound intensities range from 27 dB at 06:00 to 37 dB at 07:00,
while in savannah habitats the levels range from 20 dB at 06:00 to 36 dB at mid-day. In riverine
habitats, ambient noise arises largely from bird vocalizations, insect stridulations, and rustling
vegetation. In savannah habitats, virtually all noise arises from wind.
Many laboratory animals begin to exhibit symptoms correlated with elevated stress when
ambient sound pressure levels approach 85 dB (spl) for extended periods of time (Anthony et al.,
1959). The typical sound pressure levels measured in zoos and in laboratories are lower than this
but still substantially higher than the 20 dB (spl) to 40 dB (spl) characteristic of various natural
habitats. Clearly sound pressure levels in captivity exceed those found in the natural environment
Elevated sound pressure levels have been shown to exert deleterious inﬂuences on many
species of laboratory animals (Gamble, 1982), affecting their behavior in ways that could
introduce confounds into behavioral studies. This is especially true when there is an irregular
periodicity of sounds of moderate to high intensity. Consider the periodic loud sounds of metal
striking metal that may occur in an animal facility during cage cleaning—such sounds are
typically full of harmonics in a wide range of frequencies, and can often be extremely loud (in
excess of 80 dB (spl); Tromborg and Coss, 1995). Commercial trucks when backing up emit high
frequency, punctate sounds in excess of 90 dB (spl) (Tromborg and Coss, 1995). Firework
displays – a not uncommon event in city greenspaces that also accommodate zoos – can exceed
120 dB (spl) in short, punctate bursts. Continuous loud sounds may be produced by
environmental control systems such as air pumps, air conditioners, and heaters, and by activities
such as ﬂoor washing and lawn mowing (for a review of sound pressure levels associated with
these and other animal maintenance activities, see Sales et al., 1999).
Both constant and periodic sounds can subtly inﬂuence the physiology of some particularly
sensitive species. Compared with chronic background or repetitive noise, high amplitude
punctate, aperiodic, or unpredictable noise is especially effective at provoking distress responses
(Cottereau, 1978; Gamble, 1982; Stoskopf, 1983). This type of reactivity is especially evident in
easily aroused species, particularly those that are targets of predators in nature (Meyer-Holzapfel,
1968; Stoskopf, 1983).
Animals continuously subjected to intense noise manifest stress responses by exhibiting
elevated levels of arousal (Gamble, 1982), both behaviorally and physiologically. Loud sound is
well known to have adverse effects on blood pressure and heart rate in humans (Hagerman et al.,
2005; Smith, 1991) and other animals (Geverink et al., 1998; Salvetti et al., 2000).
Physiologically, prolonged exposure to intense noise is associated with increased activity in the
sympathetic division of the autonomic nervous system. Its prolonged activation is correlated with
increased activity in the hypothalamic-pituitary-adrenal (HPA) system, elevated metabolic rates,
increased blood pressure, and tachycardia (Ames, 1978; Anthony et al., 1959; Henkin and
Knigge, 1963). This arousal can have deleterious long-term effects on animals that experience it
directly (for a review, see Sapolsky et al., 1987), but also on offspring in utero. Exposure of
pregnant animals to noise-induced physiological arousal results in immunosupression (Sobrian
et al., 1997), exaggerated distress responses to aversive events (Morgan and Thayer, 1997),
changes in auditory threshold (Canlon et al., 2003), increased disturbance behaviors (Schneider
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302266
Author's personal copy
et al., 2002), impaired learning (Nishio et al., 2001; Morgan et al., 1999), abnormal social
behavior (Clarke and Schneider, 1993; Morgan et al., 1997), and suppressed exploratory behavior
(Poltyrev et al., 1996) in offspring. Such long-term effects of exposure to loud sound are
important considerations for conservation-minded managers of animals housed in the typically
noisy surroundings of captivity.
Behavior of adult animals in captivity is also affected by noise. In zoos and aquaria, noise from
visitors increases as visitor numbers increase, and this correlates with increased vigilance
behaviors in harbor seals (Suarez and Morgan, unpublished data), cotton top tamarins
(Tromborg, 1993), and orangutans (Birke, 2002). Caretaker sounds result in more frequent
clinging to adults by infant gorillas (Ogden et al., 1994), and noise made by humans shouting and
metal clanging increases heart rate and activity in cattle (Waynert et al., 1999). Laboratory rabbits
alter their behavior in signiﬁcant ways when exposed to normal laboratory sounds in nonsound
isolated housing (Jildge, 1991), including shifting their normal activity patterns from night to
day. And noise in rabbitries is associated with abnormal behavior and startle that can result in
serious injury (Marai and Rashwan, 2004). Loud sound has been shown to increase vigilance and
activity in rats (Krebs et al., 1997) and agitation behaviors in pandas (Owen et al., 2004). In the
wild, caribou respond to the sound produced by aircraft ﬂyovers with increased activity, although
the degree of reaction varies with time of year (Maier et al., 1998). Similar effects of aircraft noise
have been found in captive desert mules and mountain sheep (Bleich et al., 1990; Weisenberger
et al., 1996). These data indicate that anthropogenic noise generated in the course of routine
human activity may have adverse effects on our nonhuman animal charges.
Sounds other than those produced by humans might also be stressful for captive animals. For
prey species, the sound, smell, and sometimes sight of their historical predators may be constant
when in captivity. Such sounds may be a continual source of stress. Crows, for example, respond
with defensive behaviors to the sound of raptors (Hauser and Caffrey, 1994) as do mice (Hendrie
and Neill, 1991), suggesting that the sounds of historical predators are perceived as threating and
therefore a potential source of stress. The sound of conspeciﬁcs may also be stressful under
certain conditions. For example, the sound of chimpanzee screams has been shown to evoke
cardiac orienting responses in young chimps (brachycardia associated with increased vigilance
and attention), regardless of their early experiences with other chimps (Berntson et al., 1989). At
the same time, sound (including music, the sound of prey, and the sound of conspeciﬁcs) has been
used as an enrichment strategy for some species (e.g., Cloutier et al., 2000; Markowitz et al.,
1995; Shepherdson et al., 1989). Thus the impact of different sounds on animals in captivity is by
no means unequivocal.
Adding to our difﬁculty in understanding the potential impact of sound on captive animals is
the fact that our own detection of sound is quite limited. In some cases, anthropogenic sound that
is stressful to nonhuman animals in captivity may not be detectable by humans. Many devices
common in captive environments such as computer monitors, closed circuit security cameras and
televisions, and ﬂuorescent lights produce high-frequency sounds (higher than 20 kHz) that
despite our inability to hear them are potentially quite loud to animals that detect sound in this
range. In one study, 24 out of 39 sources of sound in captiveenvironments included frequencies in
excess of 60 kHz (Sales et al., 1988). And in many cases, these sounds may be extremely loud,
despite our not being able to hear them. For example, sound pressure levels exceeding 75 dB have
been reported at frequencies in excess of 60 kHz in some laboratory animal housing (Milligan
et al., 1993).
Ultrasonic sound is produced and detected by a number of species from a variety of taxa,
including hummingbirds (Pytte et al., 2004), swiftlets (Fullard et al., 1993), rats (Sanchez, 2003),
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 267
Author's personal copy
mice (D’Amato and Moles, 2001), prairie dogs (Heffner et al., 1994), bats (Grifﬁn et al., 1960),
ground squirrels (Wilson and Hare, 2004), some species of ﬁsh (Mann et al., 2001), dolphins
(Lammers et al., 2003), orca (Szymanski et al., 1999), hamsters (Johnston, 1992), dogs (Lipman
and Grassi, 1942), and voles (Blake, 2002). Since it is clear that the ability to detect ultrasound
has evolved in a number of different taxa and also that our understanding of comparative
perception is limited, it is likely that many other species detect ultrasound. Thus, the potential for
stress induced by exposure to anthropogenic ultrasonic sound in captive environments should not
A number of animals also detect infrasound, including giraffe (von Muggenthaler et al., 1999),
elephants (McComb et al., 2003), cassowaries (Mack and Jones, 2003), hippopotamus (Barklow,
1997), pigeons (Quine, 1979), tigers (von Muggenthaler, 2000), chameleons (Barnett et al.,
1999), rhinoceros (von Muggenthaler, 1992), alligator (Vliet, 1989), moles (Mason and Narins,
2002), prairie dogs (Heffner et al., 1994), and okapi (Lindsey et al., 1993). Others such as mole
rats that spend most of their lives underground are sensitive to seismic vibration at frequencies
well below human thresholds (Kimchi and Terkel, 2002). Again, the diversity of species known
to respond to sounds below the human threshold for hearing suggest that many other species also
detect infrasound, although the auditory ranges of few have been studied. Clearly more needs to
be done to describe the auditory proﬁles of captive species. Because many devices (such as
trucks, pumps, ﬁlters, and other engines) used in captive environments generate seismic vibration
and other infrasonic sound, there is potential for animals sensitive to these sounds to be distressed
by them. Additional research is needed to describe the acoustic nature of captive environments
(including ambient sounds above and below the range of normal human hearing) and how these
sounds might adversely affect captive animals, so that we can develop effective strategies for
ameliorating such effects.
2.2. Light conditions
Lighting conditions in captive environments are designed for human convenience, and this
presents a host of potential problems for nonhuman animals living in such environments. In some
captive settings, light level may be constant or nearly constant. In others, lighting may be varied
periodically according to a ﬁxed schedule. In either instance, artiﬁcially maintained
photoperiodicity generally suits human needs and does not reﬂect natural light conditions.
Photoperiod not withstanding, another feature of lighting in captivity that may adversely affect
animal welfare is the intensity and spectral composition of the light. Fluorescent lighting that is
favored because of its reduced maintenance costs may also restrict access to particular
wavelengths of light needed for optimal animal well-being. Strong contrasts between light and
dark areas of an animal’s environment may arouse fear (Grandin and Johnson, 2005), as may
ﬂicker in ﬂuorescent light bulbs. If animal welfare is to be maximized in captivity, then attention
to lighting must be given (Belhorn, 1980; Hediger, 1964).
Traditionally, animals housed in artiﬁcial surroundings have been subjected to arbitrary light
cycles, commonly 12 h of light alternating with 12 h of dark. On the other hand, constant lighting
is a common practice in many agricultural settings (Hester, 1994). Neither of these lighting
regimes consider the effect of light cycles on behavior. Constant exposure to extended
photoperiods can alter the melatonin to serotonin ratio, affecting the rate of catabolic and
anabolic activity of important enzymes in the central nervous system (van Rooijen, 1984).
Continuous exposure to light also suppresses circadian activity (Ikeda et al., 2000), and as anyone
who has ever experienced jet lag can tell you, disruption of normal circadian rhythms is stressful.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302268
Author's personal copy
In at least one study, varying light conditions produced differences in sleep behavior in rats
(Vanbetteray et al., 1991). Disruptions of sleep and circadian cycles have been used to induce
stress in some experiments; thus, if lighting conditions can adversely affect sleep, they have
obvious impacts on stress. In mice, the stressful effect of disruptions in light conditions is quite
apparent, resulting in increased levels of plasma corticosterone and reduced latencies for
aggression (van der Meer et al., 2004). In chickens too, continuous lighting is associated with
CBC levels indicative of stress, and longer periods of tonic immobility (Zulkiﬂi et al., 1998). The
timing of light cycles thus is a factor that may be a source of stress for animals maintained in
Light intensity also varies in different captive housing situations. Keeping animals in constant
low light is a common practice aimed at reducing aggression, but it may in and of itself be
detrimental to welfare (Martrenchar, 1999). On the other hand, bright light may also be stressful.
Red deer kept under bright light conditions show more fearful behavior than did deer housed
under dim light (Pollard and Littlejohn, 1994), and injuries due to ﬁghting increase under bright
light for turkeys (Moinard et al., 2001). These data suggest that light of high intensity may arouse
some species in a way that is detrimental to their optimal maintenance in captivity.
Species also differ in their thresholds for light detection (for example, both dogs (Miller and
Murphy, 1995) and cats (Gunter, 1995) are more sensitive to light stimuli than are humans),
which may inﬂuence how they respond to light of varying intensity. When given a choice, species
show differences in their preferences for lighting of different intensities, as indicated by the
amount of time spent in each condition. Turkey poults, for example, appear to prefer lighting that
is dimmer than what is preferred by ducklings (Barber et al., 2004). Rats also prefer lower light
intensities, and the strength of this preference is dependent on eye pigmentation (with albino
strains showing a stronger preference for dim light conditions (Blom et al., 1995; Schlingmann
et al., 1994). Such strain differences may not be surprising, since increased rates of light-induced
lesions to the eye are more common in albino rats, and also more common among rats housed in
cages that are higher on a rack (and thus have a greater exposure to light) (Rao, 2001; Greenman
et al., 1982).
Cage height is an infrequently addressed variable in many studies of captive animal behavior
(Reinhardt and Reinhardt, 2000), but one that nonetheless may have a signiﬁcant effect on animal
welfare—at least in part due to differences in the amount of light received by animals housed in
different tiers. While being housed at different heights subjects animals to many potential
stressors (including different degrees of proximity to direct gaze by human caretakers), it also
clearly subjects animals to differing amounts of ambient light (Shapiro et al., 2000). Such
variability in perceived illumination may adversely affect animal welfare. For instance, long-
tailed macaques housed in lower-tier cages (where less light is received) exhibit more abnormal
behavior and less overall activity than do macaques housed in upper-tier cages (Shapiro et al.,
2000). Similar effects of low light intensities have been found in rhesus macaques (Draper, 1965;
Issac and De Vito, 1958).
Cage height affects the development and form of stereotypies in wild-caught roof rats housed
in captivity (Callard et al., 2000), presumably because of the different light levels to which rats
are exposed at different cage heights. In mice, being housed in cages higher in a rack system is
associated with greater emotionality (a possible indicator of stress) and a greater likelihood of
developing diabetes (Ader et al., 1991), a disorder that is promoted by stress (Carter et al., 1987).
Similarly, laying hens housed in the top tier of a three-tier battery cage system show longer
periods of tonic immobility and greater overall fearfulness of a number of different stimuli
(Jones, 1985, 1987). Data such as these have resulted in recommendations for uniform
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 269
Author's personal copy
illumination in captive environments (International Primatological Society, 1989;National
Research Council, 1996;USDA, 1991). Clearly, many researchers believe that availability of
light can have a signiﬁcant impact on captive animal well-being.
Wavelength is another attribute of light that may affect animal well-being. Animals differ
from one another and from humans in their sensitivities to different light wavelengths, and this
may affect their stress levels in captivity. Many species of birds, invertebrates, and some reptiles
and mammals detect ultraviolet (UV) wavelengths of light, and may in fact require information
provided by such wavelengths to inform decisions about foraging or social interactions
(including mate choice). For these species, wavelengths of light in the short end of the
electromagnetic spectrum are part of their color space, and therefore necessary for optimal
perception of their surroundings (Cuthill et al., 2000).
In a few studies, deprivation of critical light wavelengths affects physiological measures in
ways typically indicative of stress. Lab-housed rhesus macaques showed more abnormal
behavior when maintained under an artiﬁcial lighting regime compared to natural full-spectrum
light (O’Neill, 1989). Domestic chicks reared under UV-deﬁcient light conditions show increased
plasma corticosterone, along with reduced exploratory behavior (Maddocks et al., 2001).
European starlings also show elevated levels of plasma corticosterone when housed in UV-
deﬁcient light conditions (Maddocks et al., 2002b). This species also shows a preference for UV
light conditions when viewing potential mates, as do blue tits (Maddocks et al., 2002a,b). In
budgerigars too, mate choice is affected by UV light (Pern et al., 2003). For some species, then,
successful reproduction and maintenance in captivity may depend greatly on the availability of
appropriate wavelengths of light.
While ﬂuorescent lights can be used to increase available spectra for animals, these lights are
accompanied by yet another potential problem for nonhuman animals. Although the illumination
provided by ﬂuorescent bulbs appears constant to humans, these bulbs emit light discontinuously.
Their ﬂickering is invisible to most humans under normal conditions, but might be detectable by
a variety of species (D’Eath, 1998). For humans, the lowest ﬂicker frequency at which images
fuse so that no ﬂicker is detected (referred to as the critical ﬂicker fusion frequency, or CFF)
occurs from about 45 to 60 Hz, depending on what part of the visual ﬁeld is focused on the
ﬂickering image (Brundrett, 1974). However, for many animals, CFF is higher (D’Eath, 1998).
Flicker fusion in dogs occurs at frequencies in excess of 80 Hz (Coile et al., 1989), and domestic
chickens may have a CFF of about 105 Hz (Nuboer et al., 1992). At least some animals show a
preference for higher-frequency ﬂuorescent lighting (Greenwood et al., 2003), while others
appear to prefer lower-frequency lighting (Widowski et al., 1992). Such discrimination suggests
that animals can indeed detect some kind of difference between these two types of lighting—
most likely, because of differences in their CFF. Yet we know very little about CFF in different
species. Adding to the difﬁculty is the fact that CFF changes with where in the eye the ﬂickering
image is resolved, with age (Eisner and Samples, 1991), and in some species, with temperature
¨fer et al., 1978). It is clear that much more needs to be learned about the visual worlds of
captive species, and how light intensity, wavelength, and quality affect their behavior and
physiology. Such information is essential to optimize well-being in captivity.
Virtually all mammals other than primates are considered macroosmatic—that is, they depend
largely on olfactory cues (Slotnick et al., 2005). Although many macroosmatic species have
evolved other sensory systems that are regularly used to direct their activities, their primary sense
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302270
Author's personal copy
nonetheless remains olfaction. In some cases, odors have been used as a form of environmental
enrichment, with the goal of reducing behavioral indicators of stress (e.g., Jones et al., 2002;
Pearson, 2002; Wells and Egli, 2004). However, for many animals living in captivity, the odors to
which they may be exposed can be chronic sources of distress.
Prey animals in captivity, for instance, may be constantly exposed to the smell of their
historical predators. There are abundant data to suggest that this is a source of stress. Studies of
laboratory rats have shown that exposure to cat odor is sufﬁcient to raise plasma levels of
corticosterone (File et al., 1995) and increased blood pressure (Dielenberg et al., 2001), as well as
to produce long-lasting changes in anxiety-like behavior (Adamec and Shallow, 1993; Perrot-Sinal
and Petersen, 1997) and increases in defensive behavior (Adamec et al., 1998; Dielenberg et al.,
2001). In fact, exposure to predator odor is so effective at eliciting arousal in rats that it is routinely
used to induce a stress response in this species. Similar changes in behavior and/or physiology
have been seen following exposure to predator odor in other species, such as voles (Perrot-Sinal
et al., 1999), spotted frogs (Lefcort et al., 1999), crayﬁsh (Hazlett and Schoolmaster, 1999),
beaver (Engelhart and Mullerschwarze, 1995), ﬁsh (Jachner, 1995), hedgehogs (Ward et al., 1996),
cotton-top tamarins (Buchanan-Smith et al., 1993), and wapati (Chabot et al., 1996).
The odor of conspeciﬁcs may also be stressful under some conditions. Frog species, for
instance, actively avoid substrates that have been scent-marked by unfamiliar conspeciﬁcs, while
showing a preference for substrates marked by themselves or by near neighbors (Waldman and
Bishop, 2004). Among callitrichids, the scent marks of stressed individuals are investigated by
conspeciﬁcs more frequently than those of nonstressed conspeciﬁcs (Epple, 1985), suggesting
that animals can become aroused by detecting arousal in others. Chemical cues from conspeciﬁcs
have been shown to affect the attractiveness of foods in rats (Galef, 2002), and odor cues from
frustrated or frightened conspeciﬁcs inhibit rat behavior (Schultz and Tapp, 1973). A similar
effect has been shown in pigs, which will avoid food hoppers sprayed with urine from a frustrated
conspeciﬁc (Vieuille-Thomas and Signoret, 1992). These data suggest that a variety of animals
may be able to detect distress in conspeciﬁcs based on odor cues alone, and that these odor cues
themselves may be stressful to individuals perceiving them.
For many species, chemical communication is essential for normal social interaction and
reproductive behavior. The inﬂuence of conspeciﬁc odor on development and maintenance of
rodent sexual behavior is well-documented (Slotnick et al., 2005), but similar activating or
inhibiting effects of conspeciﬁc odor on sexual behavior have been found for goats and sheep
(Gelez and Fabry-Nys, 2004), marmosets (Barrett et al., 1990), giant pandas (Swaisgood et al.,
2000), cattle (Cupp et al., 1993), and pigs (Dorries et al., 1995). To the extent that we wish
animals maintained in captivity to be reproductively successful, it appears that we must attend to
the effects of captivity on availability and potency of chemical cues.
One element of captivity that may interfere with these cues is routine cage cleaning. Many
animals use scent marks to delineate territory or to indicate reproductive status, and for these
species, the constant removal of these scent cues may be stressful. In response to cleaning, such
species usually attempt to re-anoint their surroundings (Hediger, 1964). Because some species
also increase rates of scent-marking when distressed (e.g., callitrichids; Epple, 1985), the effect
of cage cleaning on rates of scent marking may be misinterpreted as indicative of stress.
Nonetheless, it is clear that cage cleaning and subsequent removal of olfactory cues may indeed
be stressful. Removing scent marks has been shown to increase aggression among group-housed
mice, as does the transfer of bedding from a novel cage of conspeciﬁcs (van Loo et al., 2000).
Cage cleaning also results in increased tongue-ﬂicking and investigatory behavior in captive
rattlesnakes and stimulates efforts to remark cages in other snakes through a decreased latency to
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 271
Author's personal copy
defecate (Chiszar et al., 1980). Green iguanas in captivity similarly show a decreased latency to
defecate in a clean cage (Morgan, personal observation), as do rats (Saibaba et al., 1996). Some
species also show changes in behavior in responseto odors that typically accompany many cleaning
products. Pocket gophers, for instance, have been shown to actively avoid pine needle scent
(Epple et al., 1996), and pungent smells (such as citronella) increase vigilance behaviors in mice
(Kemble and Bolwahnn, 1997). In contrast, domestic cats show an attraction to bleach residue on
the hands of handlers (Tromborg, personal observation). Other pungent odors associated with
particular bedding types such as cedar or pine is associated with adverse impacts on the rodent liver
(Davey et al., 2003) and immune system (Sanford et al., 2002). Taken together, these data suggest
that an understanding of the impact that odor has on animals in captivity is essential for creation
of captive environments conducive to animal well-being and reproduction (Kleiman, 1994).
2.4. Thermal and tactile experience
In the wild, many animals have the ability to migrate when ambient temperatures deviate from
their preferred ranges. In captivity, however, the ability of animals to move when temperatures
are other than optimal is greatly curtailed or absent altogether. In captivity, animals are routinely
exposed to temperatures for which their species is not adapted. Species that evolved in warmer
climates (such as elephants, lions, and giraffe) are housed in temperate zone zoos that see
signiﬁcant cold at different times of year, while species from colder climates (such as polar bear
and penguins) are housed in zoos where snow rarely falls.
The consequences for animals under these conditions are very real, and often far from ideal.
One of the authors worked at a national primate research center in the United States during
graduate training, and remembers the number of frost-bitten tails each year that developed among
rhesus macaques raised in ﬁeld cages at that facility. Although the animals were provided with
shelters and heat lamps during cold weather, frostbite nevertheless occurred, especially among
subordinate individuals who were unable to command warmer and preferred resting perches.
Temperature also affects the behavior of animals in ways that may not only reﬂect distress, but
that may compromise the mission of the facility housing them. For instance, visibility to visitors
of zoo-housed gorillas on exhibit has been shown to correlate negatively with increases in
ambient temperature (Stoinski et al., 2002).
Extreme temperatures are well-known stressors, and indeed are often used as provocateurs in
studies of behavioral and physiological responses to stress. Thus it should not be surprising to
ﬁnd temperature as a frequent source of discomfort and distress among captive animals.
Domestic pigs, for example, show increases in salivary corticosterone when temperatures exceed
17 8C, while low temperatures increase huddling behavior (Hillman et al., 2004a) and high-
frequency vocalization (Hillmann et al., 2004b) in this species. Distress calls in chicks increase
with increases in temperature (Herbert and Sluckin, 1969), while infant rats separated from their
littermates and dams emit more ultrasonic vocalizations at lower temperatures (Shair et al.,
2003). Low temperatures (9 8C) result in a higher frequency of stereotypic behavior in Asian
elephants (Rees, 2004). And rabbits show abnormal maternal and sexual behavior when
temperatures get too high (Marai and Rashwan, 2004). Results from these studies and many
others suggest that ideal thermal ranges are unique for each species and developmental age,
making temperature control a particular challenge for captive animal management. To make
matters more complicated, the effect that temperatures have on stress responses in animals appears
to be dependent to some degree on individual differences, such as weight. Bigger pigs, for example,
can tolerate larger ranges of temperatures compared to smaller pigs (Hillman et al., 2004a).
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302272
Author's personal copy
Social housing may also affect ideal temperature range. Group-housed mice, for instance, show
temperature preferences that are a degree or so cooler in comparison with singly housed animals
(Gordon et al., 1998).
In captive environments, aberrant social behavior is a common problem, and temperature can
have a direct affect on such behavior—for good and for ill. Captive cichlids, for example, ﬁght
more at higher temperatures (Ratnasabapathi et al., 1992), while captive mice ﬁght more at
intermediate temperatures (Greenberg, 1972). Pigs play less at lower temperatures (Olsen et al.,
2002), and huddle more (Hillman et al., 2004a), as do geckos (Shah et al., 2003). Captive infant
baboons spend more time huddling with their mothers at lower temperatures, and spend more
time away from their mothers at higher temperatures (Brent et al., 2003). Warmer temperatures
increase ‘‘buller behavior’’ behavior in domestic cattle (in which steer repeatedly mount and ride
a penmate until that penmate is injured or killed) (Blackshaw et al., 1997). And gerbils groom at
different frequencies dependent on temperature (Thiessen et al., 1977). Some of these changes in
behavior as a function of temperature have clear and direct impacts on animal well-being in
captivity (e.g., ‘‘buller’’ behavior); others are a bit more subtle. To the degree, however, that we
wish to maintain species-typical social behaviors in captivity, temperature may be one of many
abiotic factors to consider.
Indeed, most animal welfare legislation explicitly dictates allowable temperature ranges for
different species (Besch, 1990). Regulations such as these would suggest that maintaining
optimal temperatures for animals is little more than a matter of adjusting thermostats in animal
enclosures. However, in many cases the thermostats that control the onset or offset of heating or
cooling units are not located in such a way as to accurately reﬂect the microclimate in the
immediate vicinity of the animals (van Wagenberg et al., 2005). The placement of monitoring
devices for temperature must be carefully considered, if we wish to ensure that temperature is not
an unintended stressor in captivity.
One way that animals can behaviorally thermoregulate in nature is by seeking microclimates
with low surface temperatures (i.e., low longwave radiation). Alternatively, they may avoid
sunlight or heat-releasing visible light (such as that produced by incandescent lighting)—so-
called shortwave radiation (Langman et al., 1996). Most captive environments limit an animal’s
ability to thermoregulate in this way. Even if shade or shelter is provided to reduce direct
exposure to heat or cold, the surfaces on which captive animals are maintained may prevent
effective thermoregulation. In fact, many of the behavioral changes observed in animals in
response to temperature (reviewed above) can be altered by changes in substrate.
Substrates that are common in captivity, such as concrete, gunite, tile, soil, grass, wood, rock,
plastic, rubber, and/or metal vary in their thermal inertia—the speed with which they gain and
lose heat. In addition to composition, the color of ﬂooring or cage surfaces can also affect their
thermal properties; darker colors tend to absorb heat, while lighter colors reﬂect it. To the degree
that a given exhibit or captive environment is surrounded by surfaces with high thermal inertia
and high heat reﬂectance properties, temperatures may exceed those preferred by an animal even
when it has sought shelter in a shaded area.
Few if any studies, however, have been conducted to assess the thermal properties of common
ﬂooring materials employed in captive animal housing. In one study of thermal inertia in
substrates commonly found in urban settings, concrete and wet soil were found to have the
greatest thermal inertia; the substrate with the lowest thermal inertia was turf (Swaid, 1991).
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 273
Author's personal copy
Another study examined the thermal properties of light and dark-colored gunite surfaces in a zoo
exhibit for pinnipeds. Light-colored gunite in this study reﬂected 41% of direct sunlight and
effectively eliminated the cooling effect of any shaded areas in the exhibit; temperatures in
shaded areas were as high at those in unshaded areas, resulting in a mean surface temperature of
33 8C(Langman et al., 1996). Painting the gunite a darker color, however, reduced its shortwave
reﬂectance by 33%.
For animals that reside near ground level, ambient temperature is not merely a function of
downward-directed infrared radiation from the sun and upper atmosphere, but also of the upward
infrared radiation emitted by ground surfaces. When the temperature of the substrate exceeds that
of the overlying air (as in the case of substrates with high thermal inertia such as concrete, stone,
or gunite), temperatures immediately above the substrate can be much higher than ambient air
temperatures would predict (Asaeda et al., 1996). Such observations suggest that the
microclimate inside gunite-coated or similar exhibits may be very different from what we
ourselves experience outside of the exhibit.
Variations in local microclimate or in the thermal properties of substrates do contribute to
differences in behavior and well-being. Mice with inadequate bedding for burrowing, for
instance, show an increased metabolic rate and reduced core body temperature (Gordon, 2004).
Cooling of the ﬂoor when temperatures exceed 25 8C reduces lying behavior in pigs, and
increases feeding and growth rate (Huynh et al., 2004). Animals also vary in their preferred
substrate temperature. Farrowing sows prefer warmer substrates than they do at other times in
their life cycle (Phillips et al., 2000), suggesting that pigs seek environments conducive to
maintaining neonatal piglet body temperature. As temperatures rise, juvenile pigs prefer to rest
on cool bare concrete, but at lower temperatures, warmer straw-bedding is preferred (Fraser,
1985). Cattle prefer straw bedding to rubber mats when temperatures are low (Manninen et al.,
2002). And unsheared sheep prefer cooler substrates for resting, while sheared sheep prefer
resting surfaces with lower thermal conductivity (Faerevik et al., 2005).
But temperature is not the only quality of substrate in captivity that may impact an animal’s
well-being. Different surface materialsalsovaryintheirhardnessandresistanceto
compression, and thus in the stress that they put on legs and joints (Bargai and Cohen, 1992).
Surface materials also vary in how much friction they offer, and thus how much resistance to
slipping they provide (van der Tol et al., 2005; Applegate et al., 1988). Such factors are critical
contributors to lameness, and as such, play a major role in captive animal well-being (Grandin
and Johnson, 2005). Additionally, smooth surfaces (although easier to clean) are also more
acoustically reﬂective (Forthman, 1998; Tromborg, 1993); given the impact that sound may
have on animals in captivity (reviewed above), this aspect of housing substrate is another
When animals are given a choice, they appear to select substrates that vary not only by their
thermal qualities, but by their softness and/or the footing purchase they provide. Cattle appear to
prefer substrates that afford better footing and therefore less chance of slipping (Hultgren, 2001).
Mice prefer running wheels made of material that offers a better purchase when running
(Banjanin and Mrosovsky, 2000), and bedding material that is soft enough to allow for burrowing
and nest construction (Ago et al., 2002). Sheared sheep prefer straw substrates to bare wood or
rubber mats, and spend less time recumbent when provided with straw immediately after
shearing (Faerevik et al., 2005). Young pigs prefer substrates that are most similar to soil, and
spend the least time on concrete when given a choice (Beattie et al., 1998). Hamsters prefer
solid ﬂooring with bedding over wire mesh ﬂooring, and spend their time differently when
housedonwiremeshcomparedtosolidﬂooring(Arnold and Estep, 1994). Rats prefer large
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302274
Author's personal copy
particle bedding (such as wood shavings or paper bedding) over wire mesh or small particle
bedding (e.g., sawdust) (van de Weerd et al., 1996),andsolidﬂooringovergridorwiremesh
ﬂooring, if given a choice (Manser et al., 1995).Thenatureofthesubstratealsoappearsto
affect commonly accepted physiological measures of stress. For instance, grid and plastic
ﬂoors appear to be stressful for rats, as measured by signiﬁcant changes in blood pressure,
heart rate, and body temperature compared to when the animals are housed in wood chip
bedding (Krohn et al., 2003). Rats housed on coarse sawdust show greater sensitivity
to pain than do rats housed on ﬁner sawdust (Robinson et al., 2004), and rats housed in
cages with wire mesh ﬂoors rapidly develop nerve injury and soreness in the hindlimbs
(Mizisin et al., 1998). Housing substrate can even inﬂuence cognitive ability—homing
pigeons housed in plastic containers (even when provided with adequate ventilation) show
impaired navigational abilities compared to pigeons housed in other kinds of containers
(Sandberg et al., 1999). The impact of housing substrate on cognition in this case appears to be
a consequence of stress induced by the nature of the container. Taken together, these
observations suggest that the nature of the substrate may have a substantial inﬂuence on animal
stress in captivity.
Many species of animal build nests, both for the raising of young as well as for resting and
shelter. In a smooth-ﬂoored or barren captive environment, nest building is not possible, and the
inability to do so may result in aberrant behavior that suggests distress. Animals will work for
access to nest-building material (Anna et al., 2002; Cooper and Appleby, 2003), suggesting that
nest-building is a behavioral need in some species.
In addition to allowing for species-typical nest building behavior (when appropriate),
complex substrate in the form of earth, straw, or other similar bedding also provides
manipulanda, which can reduce boredom and the frequency of associated abnormal behaviors,
and increase the frequency of species-typical behaviors (Baker, 1997; Chamove et al., 1982;
Fraser et al., 1991). In some cases, a more complex substrate can also improve social
interactions, perhaps by providing retreat opportunities for subordinate animals (Armstrong
et al., 1998), or by providing an alternative outlet for exploratory behavior. Pigs housed in
barren pens, for example, direct more chewing and rooting behaviors at penmates than do pigs
raised in pens with deep straw bedding (de Jong et al., 1998). Ultimately, providing captive
animals with a more complex substrate can enhance the range of behavioral opportunities and
conceivably, reduce stress.
The data we have reviewed thus far suggest that a variety of sensory elements in the
environments of captive animals – including the quantity, quality, and periodicity of light, the
presence or absence of particular odors, the pitch, frequency, and sound pressure level of sounds,
and the heat indices, slickness, softness, and manipulability of substrate – have potential as
sources of chronic stress. Unfortunately, many of the components of these sensory elements that
are most disturbing to captive nonhuman animals are not readily detectable by human caretakers.
Furthermore, our knowledge of the sensory worlds or umwelts of most species is extremely
limited, and thus our ability to predict what kinds of stimuli might be stressful to a given animal is
impaired. In order to optimize animal well-being in captivity, it is imperative that we have a better
understanding of species-typical sensory abilities and their role in natural histories. Much work
remains to be done in this arena.
Nonetheless, it is our charge as animal stewards interested in conserving natural behavior in
captivity to promote animal well-being by reducing sensory sources of stress whenever we are
able to do so. To do this with our limited human sensory capabilities requires technological
assistance. Table 1 lists the potential sensory stressors we have identiﬁed, and some of the
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 275
Author's personal copy
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302276
Potential environmental stressors and means by which to measure them
How to measure Suppliers Additional information
Species particularly at risk
D.A.S. Distributiion (www.dasdistribution.com) All
Radio Shack (www.radioshack.com)
Action Electronics (www.action-electronics.com)
Scantek Inc. (www.scantekinc.com)
Pulsecho Systems (www.pulsecho.com)
Bruel and Kjaer (www.bkhome.com)
IET Labs (www.ietlabs.com)
available bat detectors
Bat Conservation International
BatBox LTD (www.batbox.com),
Laar Techologies (www.laartech.biz)
Comparing bat detectors
Rodents; species that hunt rodents;
marine mammals; chiropterans
Geophones Geo Space, L.P. (www.geospacelp.com ) Large species (e.g., elephants, giraffe,
rhinoceros, large marine mammals, okapi,
crocodilians, hippopotamus); species that
live underground (e.g., mole rats)
Sound Devices (www.sounddevices.com)
Overall light levels Commercially available
DAS Distribution (www.dasdistribution.com)
Light spectra Commercially available
Spectrum Technologies (www.specmeters.com)
Typically measured indirectly
using commercially available
Species with high photoreceptor densities in
the eye or high densities of one-to-one wiring
between photoreceptors and ganglion cells in
the eye; insects
For sound pressure level of infrasonic and ultrasonic sounds, sounds must be recorded, slowed down, and played through a dB meter. Infrasound and ultrasound can also be
assessed using using sound spectra analysis hardware and software.
Author's personal copy
technologies available to measure them. It is our hope that this list will help animal caretakers to
better assess the sensory stress potential of captive environments.
3. Conﬁnement-speciﬁc stressors
Environmental stimuli such as those reviewed above are by deﬁnition everywhere; the primary
difference between such stimuli in nature and the same stimuli in captivity is in the animal’s
ability to control its exposure to these stimuli. In the wild, an animal can generally move away
from aversive light or sound; it can seek shelter from undesirable climactic conditions, dig into
the earth to cool itself, and time its daily activities to coincide with whatever environmental
variables are most suitable. The captive animal, however, has no such luxury. In general, animals
in captivity have little or no control over the timing, duration, and/or nature of the light, sound,
odors, or temperatures to which they are exposed. For the most part, this lack of control is a direct
result of conﬁnement.
In addition to reducing or eliminating control over exposure to a number of environmental
variables, conﬁnement in captivity brings with it a host of other potential stressors, largely in the
form of restricted choice. Whether in zoos, laboratories, or agricultural settings, animals in
captivity are limited in their freedom of movement, their ability to retreat from conspeciﬁcs and
from human caretakers, and the timing and nature of their food and mate choices. Below, we
review data suggesting that each of these factors may be potential stressors for captive animals.
3.1. Restricted movement
It seems a matter of common sense that one of the greatest potential stressors in captivity
would be restriction of movement due to small cage or pen size. Yet this is an area in which
intuitively obvious answers may lead one astray in any efforts to improve conditions for captive
animals. Current cage size standards in the United States and elsewhere are based primarily on
arbitrary professional judgment, and not empirical analyses. And the empirical studies that do
exist have produced mixed results.
Hediger (1955, 1964) considered restricted movement due to space limitations to be one of the
primary contributors to captivity-induced stress, and some of the earliest studies of abnormal
behavior in captive animals supported this contention (e.g., Levy, 1944). More recent work has
also suggested an adverse effect of conﬁnement in small spaces. In one study of the impact of
captivity on 35 different species of carnivore, infant mortality in captivity and stereotypic
locomotion in the form of pacing was found to correlate positively with species home range size
in the wild (Clubb and Mason, 2003, 2007), suggesting that the impact of enclosure size on
captive animals is a matter of natural history to some degree. In other studies of group-housed
pigs, housing the animals in smaller pens increased rates of agonistic behavior (Lammers and
Schouten, 1985; Wiegand et al., 1994). A similar increase in aggression with decreased enclosure
size has been observed in buffalo calves (Napolitano et al., 2004), male turkeys (Buchwalder and
Huber-Eicher, 2004), and captive dama gazelle (Cassinello and Pieters, 2000).
Overall activity and conversion of feed to body weight are two other variables that appear to be
compromised for some species when housed in smaller enclosures. Pigs in smaller pens, for
example, spend more time sitting or standing motionless, and show reduced growth rates
compared to pigs housed in larger enclosures (Pearce and Patterson, 1993). The same effect of
pen size on growth rate has been shown in sheep (Horton et al., 1991). These effects of pen size on
growth rate have been interpreted by authors as indicators of chronic stress (recall that suppressed
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 277
Author's personal copy
growth is a common physiological consequence of chronic stress). Impaired growth rate due to
stress is clearly undesirable in animals such as pigs that are raised for agricultural purposes.
However, such impairment is also undesirable for those interested in conservation of endangered
species in captivity; captive populations will fail to thrive if restricted space and subsequent stress
increase rates of aggression and/or delay development through slowed growth rates.
Adverse impacts of enclosure size have also been found on rodent behavior, particularly with
respect to sex and reproduction. Rats housed in smaller cages, for instance, show less frequent
mounting, reduced intromission, reduced ejaculation frequency, and longer post-ejaculatory
intervals compared to rats housed in larger pens (Saito et al., 1996). To the extent that crowding
and spatial restriction suppresses reproduction in other species, it is a serious problem for those
interested in sustaining captive populations.
Other studies of the effects of cage size on well-being have been less equivocal. Increasing
enclosure size for great apes species, for instance, has been found to have little or no effect on
behavior in one study (Wilson, 1982), while in another speciﬁcally of zoo-housed orangutans,
enclosure volume and usable surface area predicted behavior activity levels (Perkins, 1992).
Some authors have found a decrease in rates of abnormal behavior concomitant with an increase
in cage size (e.g., Draper and Bernstein, 1963; Paulk et al., 1977). But in other studies, more
ambiguous results have been found. Transferring a young gorilla to a larger, more naturalistic
exhibit, for instance, decreased play behavior, and increased some stereotypies while reducing
others (Goerke et al., 1987). Similarly, moving an adult chimpanzee from a small cage to a larger,
more open naturalistic exhibit reduced abnormal behavior, but also activity in general (Morgan
et al., 2002). Housing singly caged rhesus monkeys in larger cages did not reduce abnormal
behavior (Line et al., 1990), even when the new cage was six times larger than their standard cage
(Kaufman et al., 2004). The same lack of effect of a larger cage on abnormal behavior has been
observed in captive cynomolgus monkeys (Crockett et al., 1995). And in one study, the frequency
of abnormal behavior actually increased with an increase in cage size (Bayne and McCully,
Increasing cage size may actually be stressful for prey animals that are hunted in open spaces,
such as small rodents (Hughes, 1969). And even for species that in the wild live in what appears to
our human eyes to be substantial open space do not always prefer the largest available living
spaces. Dolphins given a choice between three pool sizes choose to spend most of their time in
moderate-sized areas, rather than the largest area available (Shyan et al., 2002). Findings such as
these have led some authors to suggest that species natural history is a better predictor of animals’
responses to conﬁnement and enclosure size than is any other variable (Clubb and Mason, 2003;
Shyan et al., 2002). Unfortunately for many species in captivity – particularly domestic species –
data on natural habitat use are limited or nonexistent. Nonetheless, it may well be that it is not the
quantity of space available to the animal which is important, but its quality—what it affords
animals in the way of behavioral opportunity.
3.2. Absence of retreat space
One of the behavioral opportunities that is limited for animals in captivity is their ability to
move away from one another or from human passers-by. The lack of sufﬁcient retreat space is a
signiﬁcant potential stressor for captive animals. Whether on exhibit at zoos and aquaria, housed
in compartment-style caging in labs, or in intensive management systems in agricultural settings,
animals in captivity are often maintained under conditions that afford little or no concealment
opportunity. For many species, this is clearly stressful.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302278
Author's personal copy
Bank voles raised in barren and open caging, for instance, show more stereotypies than do voles
raised in caging with sufﬁcient bedding to serve as a burrow (Cooper et al., 1996). Gerbils in barren
caging develop more stereotypic digging than those reared in cages with artiﬁcial burrows
(Waiblinger and Ko
¨nig, 2004; Wiedenmayer, 1997). Mice show more stereotypic wire-gnawing
when housed in barren cages compared to when provisioned with cardboard tubes in which to hide
(Wurbel et al., 1998). Rabbits raised in conventional barren caging show more restlessness, bar-
gnawing, timidity, and self-grooming than do rabbits raised in caging enriched with a shelter and
nesting material (Hansen and Berthelsen, 2000). Rats in barren cages without burrows show
greater fearfulness and less exploratory behavior than do rats housed in cages furnished with
hiding places (Townsend, 1997). Free-range broiler chickens range less when tree cover is reduced
or absent (Dawkins et al., 2003), and domestic hens rest and preen less with less cover (Newberry
and Shackleton, 1997). Pygmy goats and Romanov sheep in a petting zoo showed higher rates of
undesirable behavior (threats or aggression directed at visitors) when they were unable to retreat
(Anderson et al., 2002). Captive anoles show longer and more persistent bouts of tonic immobility
when housed in cages that provide no hiding areas (Henning and Dunlap, 1978). And mice in
barren cages self-administer anxiolytic drugs more often than do mice in cages enriched with
hiding places (Sherwin and Olsson, 2004). These data suggest that a wide variety of species from
varying taxa require some opportunity for concealment for their optimal well-being.
Adding retreat spaces improves many indicators of animal welfare. Mixing unfamiliar
animals is a sometimes unavoidable part of captive husbandry, yet in many species, such mixing
triggers aggressive behavior. Provision with retreat space, however, can reduce aggression in
some circumstances in which unfamiliar or incompatible animals must be housed together Young
pigs in newly formed groups, for instance, ﬁght less when hiding places are available (McGlone
and Curtis, 1985). Provision of a nest box increased ﬁghting and plasma corticosterone in mice,
but also improved immune system function and increased the frequency of positive social
behaviors (Marashi et al., 2003). And provision of a camouﬂage barrier reduced aggression and
stereotypic behavior in zoo-housed gorillas (Blaney and Walls, 2004). These data suggest that
when animals are housed in social situations that are potentially stressful, the presence or absence
of adequate retreat space inﬂuences how those situations affect their well-being.
In many cases, data suggest that the reduction of distress provided by the addition of retreat
space is directly related to the need to cope with potential threat. Animals show a preference, for
example, for retreat space that is easily defended. Thick-tailed geckos prefer hiding places that
are narrow and difﬁcult to enter (Shah et al., 2004). And mice prefer nest boxes with only one
opening, resting in them with their heads oriented towards the opening (van de Weerd et al.,
1998). Animals also appear to prefer retreats that prevent detection by predators; when given a
choice, rats prefer opaque enclosed shelters, as opposed to transparent shelters (Manser et al.,
1998; Patterson-Kane, 2003). These data support the contention that a reduction or absence of
retreat opportunities and hiding places can be a source of distress for animals in captivity. Once
again, it may not be quantity of space but what complexity of space affords an animal that
determines enclosure impacts on well-being.
3.3. Forced proximity to humans
In many instances, the perceived threat from which animals seek to escape through the use of a
retreat space are ourselves—the human caretakers of these animals. Particularly for animals
housed in zoos, proximity to humans may be greater than is comfortable for some species. Many
zoos struggle with the conﬂict that often exists between what might be best for an animal’s well-
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 279
Author's personal copy
being, and the need to provide paying visitors with what they paid for—the opportunity to see
exotic animals. Some zoos known to the authors meet visitor pressure for viewing the animals by
employing forced lockout, in which animals are barred from re-entering their off-exhibit holding
areas during the times that the zoo is open to the public. In others, visitors are allowed close
contact in a variety of ways (i.e., through petting zoos, live animal presentations, bringing
animals out into the zoo grounds while visitors are present, or allowing some species to range
freely throughout large enclosed exhibits or throughout the zoo) (personal observation; Hosey,
2005). To be fair to zoos, the underlying intention for increased visitor-animal interaction is to
promote the empathy and sense of connectedness needed to improve attitudes and behavior with
respect to conservation. Regardless of intention, however, forced proximity to or contact with
humans can be deleterious to animal well-being.
Species vary in their ﬂight distances from humans (reviewed in Tarlow and Blumstein, 2007),
but the ability of zoo exhibit designers to take this information into account when a new exhibit is
constructed may be limited. In some cases, the total space available for a new exhibit may limit
the amount or quality of retreat space that can be allocated to a species. In other cases, the data
available on species ﬂight distances are sparse or variable. In the case of zoos in which age of the
facility, ﬁnances, or imperfect knowledge of species needs result in exhibits with limited retreat
space for their residents, visitor impact on many zoo animals may be enormous. On a day-to-day
basis, visitors to a zoo may be one of the few unpredictable variables that animals experience;
feeding times, cage cleaning, and animal caretakers may be relatively consistent, but the number
of visitors and visitor behavior varies from moment to moment. To the degree that this variability
breaks up an otherwise monotonous existence, it may be have a positive effect on well-being
(Morris, 1964). However, visitors also vary in the degree to which they attempt to interact with
captive animals, and in the nature of those attempted interactions. For many species, it is clear
that these visitor behaviors affect their behavior and levels of arousal.
The visitor effect has been best documented in nonhuman primates (Hosey, 2005). Zoo-housed
primates direct more behavior at active audiences, for example, and show greater overall activity
when audiences are active (Chamove et al., 1988; Hosey and Druck, 1987; Mitchell et al., 1992b)—
which of course attracts more visitors! For some species (e.g., golden-bellied mangabeys), visitor
presence increases within-group aggression, and animals selectively direct aggression to different
visitor targets (Mitchell et al., 1991, 1992a). Even in laboratory settings, human activity levels
correlate positively with intraspeciﬁc aggression in primates (Lambeth et al., 1997).
In addition to promoting aggression, human presence appears to reduce the frequency of
species-typical behaviors, and in some cases, overall activity. The presence of visitors, for
example, decreases play and other positive social behavior in cotton-top tamarins (Glatston et al.,
1984). In one study of zoo-housed chimpanzees, large crowds of visitors were associated with a
decrease in observed foraging, grooming, and play (Wood, 1998). In another study of zoo-housed
leopards, overall activity was suppressed when visitors were present, and large increases in
visitor numbers resulted in increased pacing (Mallapur and Chellam, 2002), a behavioral
indicator of agitation or stress. Similar effects of visitor numbers have been observed with visitor
presence in captive grey-cheeked mangabeys (Hall et al., 2005) and Soemmerring’s gazelle
(Mansour et al., 2000). In one zoo, wild-caught capybara showed increased escape behavior
whenever keepers entered the exhibit, despite having been in captivity for over 2 years
(Nogueira et al., 2004). Similar retreat behavior has been shown in captive dolphins used in a
‘‘swim-with-a-dolphin’’ program (Kyngdon et al., 2003). And a study of the effects of human
presence on 12 species of zoo-housed ungulate found that vigilance increased when keepers were
outside of the exhibits, while feeding behavior decreased when keepers were inside the exhibits.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302280
Author's personal copy
Vigilance behavior also differed by sex, with females tending to show greater vigilance
(Thompson, 1989). (Recall that increased vigilance and overall arousal are putative behavioral
indicators of stress in many species—including our own.)
Physiological indicators also suggest that at least in some cases, human proximity is stressful
for captive animals. Urinary cortisol is positively correlated with visitor numbers in zoo-housed
spider monkeys (Davis et al., 2005), and the presence of human caretakers engaged in routine
husbandry tasks increases heart rate in lab-housed rhesus macaques (Line et al., 1991). Heart rate
in lab-housed rhesus macaques continues to increase in the presence of a human observer, even
after 2 years of study during which time all behavioral responses to observation seemed to have
ceased (Line, Morgan, and Markowitz, unpublished data). The presence of a human also results
in stress-induced hyperthermia in farmed silver foxes (Bakkan et al., 1999). And in one review of
black rhinoceros breeding success in U.S. zoos, animal mortality was positively correlated with
the degree of public access to the animals (Carlstead et al., 1999).
In addition to forcing proximity to humans, however, the maintenance of animals in captivity
typically demands their direct handling. Evaluating the effects of handling by humans on
nonhuman animals can be challenging, since the word ‘‘handling’’ is used to refer to a wide
variety of procedures, from lifting an animal out of its home cage, holding or restraining it,
performing cage maintenance with the animal present, or moving the animal from one place to
another. Nonetheless it is clear that direct handling is stressful to animals—indeed, it has been
used as an operational deﬁnition of stress in many studies.
Animals living in captivity almost by deﬁnition are subject to at least occasional handling by
humans, and in many cases, this has been shown to be stressful. In one study, for example,
handling by humans adversely affected immune responses of laying hens (presumably because of
stress), despite the fact that the intention of the handling was to reduce fear of humans (Barnett
et al., 1994). And removal of wool by shearing (which involves intensive handling) increases
heart rate and plasma cortisol in domestic sheep more so than does social isolation or loud sound
(Hargreaves and Hutson, 1990).
At the same time, handling and/or close contact with humans has been advocated as a form of
environmental enrichment, particularly for social species housed in isolation (such as primates
(APHIS, 1999) or dogs (Wolﬂe, 1989)). In one study, increased positive human interaction with
chimpanzees was associated with decreases in abnormal behavior, increased social grooming,
and reduced aggression (Baker, 2004). But the effect of human contact – even on so-called
‘‘social’’ animals – varies wildly depending on the nature of that contact, and the individual
animal’s past experiences with humans (Hemsworth, 2003). Not surprisingly, aversive
experiences with humans result in animals that are more fearful of humans and more distressed
by human presence, and this is reﬂected both behaviorally and physiologically. For example, pig
farms at which sows showed a greater fear of humans had a greater percentage of stillborn piglets
(Hemsworth et al., 1999). Pigs that had been rebuffed by humans or inconsistently treated
showed a longer latency to approach humans than did pigs that had more pleasant interactions
with humans (Hemsworth et al., 1987). Dairy heifers that have unpleasant experiences with
humans show a greater latency to approach humans and higher plasma corticosterone than do
heifers that have pleasant interactions with humans (Breuer et al., 2003). And milk yield is lower
on dairy farms where handler attitudes towards the animals are negative and behaviors of
handlers directed towards the cattle are more aggressive (Waiblinger et al., 2002).
In comparison, positive interactions with humans can result in improved well-being. Stump-
tailed macaques that have ‘‘friendly’’ relationships with their caretakers are less disturbed by
routine husbandry and approach caretakers more often (Waitt et al., 2002). Gently handled
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 281
Author's personal copy
broiler chickens show less fear of humans and less plasma corticosterone than do nonhandled
birds (Hemsworth et al., 1994). Similarly, beef calves allow touch by a human more rapidly if
they have had extensive previous positive contact with humans (Boivin et al., 1997). And female
pigs that received pleasant handling also had higher rates of pregnancy compared to pigs that
received unpleasant handling (Hemsworth et al., 1986a). Part of what pleasant handling appears
to involve is meeting the animal on its own terms. For instance, pigs approach a human more
readily when the human does not approach them. They are also more willing to approach a human
if the human squats down rather than stands, does not wear gloves, and does not initiate
interaction or approach (Hemsworth et al., 1986c).
Animals also readily discriminate between individual humans. For instance, laboratory rats
show active avoidance of unfamiliar handlers, and approach familiar humans (Davis et al., 1997).
Beef cattle also avoid familiar humans less than unfamiliar humans (Boivin et al., 1997). In the
authors’ experiences at one national primate research center, different classes of personnel (such
as maintenance crew, animal caretakers, and research scientists) each wore different-colored
uniforms or lab coats, and animals clearly discriminated between humans with these different
‘‘coat colors’’ through their behavior, showing maximal agitation when confronted by humans in
white lab coats (the ‘‘uniform’’ of generally invasive vets or research scientists). Data such as
these suggest that human contact can be both a ‘‘blessing’’ and a ‘‘curse’’ to animals living in
captivity, depending on the type of human interaction.
3.4. Routine husbandry
Perhaps part of the reason for captive animals’ distress in the presence of humans is due to the
association of aversive routine husbandry events with their human caretakers. Certainly there are
speciﬁc types of routine events that are reliably signaled by the presence of speciﬁc humans or
human tools. For instance, walking into a laboratory housing rhesus macaques while carrying
leather gauntlet gloves used for handling animals for aversive procedures is so arousing to the
animals that we have used it speciﬁcally to induce a stress response in our subjects!
Data documenting the effects of routine husbandry procedures on the well-being of captive
animals are sparse, but those that do exist suggest that what we humans may think of as routine is
anything but to our animal charges (Balcombe et al., 2004). Even repeated events such as cage-
cleaning continue to evoke physiological and behavioral responses that are commonly associated
with stress. For instance, heart rate in captive primates increases during daily feeding and cage
cleaning (Malinow et al., 1974) and monthly cage changing (Line et al., 1989). Similar effects are
seen in rats (Duke et al., 2001; Saibaba et al., 1996; Sharp et al., 2003a). Interestingly, heart rate
also increases signiﬁcantly in rats that are mere ‘‘bystanders’’ or witnesses to routine events such
as cage-changing, vaginal lavage, or decapitation (Sharp et al., 2003b). It is likely that routine
events such as cage cleaning, cage changing, veterinary examination, or implementation of
typical experimental procedure adversely affect most animals in captivity.
3.5. Restricted feeding and foraging opportunities
Many animals in their natural habitats spend a large portion of their daily activity budget in the
search for and consumption of food (Herbers, 1981). In captivity, however, food is generally
provided. Often this food is substantially different from what the animals would consume
in nature; it may be more condensed, higher in protein, different in texture, and lower in
ﬁber than a typical ‘‘wild’’ diet, and generally takes much less time to eat. A typical ration at
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302282
Author's personal copy
one U.S. national primate research center for a single feeding of singly caged female rhesus
macaques was ﬁve large monkey biscuits (Morgan, personal observation); surely a much more
compact meal than macaques would normally consume in the wild. The hardness of the monkey
biscuits, however, slowed consumption; often, the animals held the biscuits in their cheek
pouches for half an hour or so to soften them before attempting to eat them.
Other than their hardness, such foods provided little in the way of a challenge for the
macaques such as they might be faced with if they were foraging on their own. Monkey biscuits
do not have to be found, harvested, or (other than softening) processed before consuming them.
For animals living in captivity, feeding oneself generally requires minimal effort.
Many studies have shown that animals will perform work to obtain food (Coulton et al., 1997;
Inglis and Ferguson, 1986; Inglis and Shepherd, 1994; Menzel, 1991; Reinhardt, 1994), even
when the same food is freely available to them. This phenomenon has been called
‘‘contrafreeloading,’’ and some data suggest that animals in barren environments are particularly
likely to display it. For example, in one study of laboratory rats, animals reared in enriched
environments showed little or no tendency to contrafreeload, while rats reared in impoverished
environments showed a strong preference to work for food over obtaining the same food when
it was freely available (Colburn and Tarte, 1976). Such data support the argument that foraging
is an inherently rewarding appetitive act, and one for which animals may have a behavioral
need. Appetitive behaviors are searching behaviors presumably motivated by an ‘‘appetite’’
for a particular stimulus (Wallace, 1979); in this case, the stimulus would be a potential food
item. Some authors have speculated that the frustration of appetitive behavior results in
locomotor stereotypies (Mason, 1993), as animals attempt to ‘‘search’’ for food in a restricted
environment. Some data support this hypothesis. For example, in one comparative study of
rates of stereotypies in eight species of captive primate, omnivorous species showed
signiﬁcantly more stereotypies than did frugivores or folivores; the authors interpret this
difference as due to the greater food search and handling time for omnivores that is limited in
captivity (Marriner and Drickamer, 1994). In another study, restricting the feeding of captive
giraffe in zoos resulted in increased locomotor activity (perhaps due to food-seeking),
compared to free-ranging giraffe (Veasey et al., 1996); over time, such increased activity could
result in pacing. Restricted feeding also correlates positively with stereotypic licking in giraffe
and okapi (Bashaw et al., 2001), and stereotyped chain-chewing in gilts (Appleby and
Lawrence, 1987). Conversely, requiring animals to work for their food appears to improve
behavioral indicators of well-being. For instance, providing part of the routine diet in an
enrichment device (the ‘‘Equiball’’) that requires some work to extract the food results in
reduced stereotypic behavior in stabled horses (Henderson and Waran, 2001). Similarly, a
foraging device that requires group-housed rats to search for food results in reduced aggression
(Johnson et al., 2004). Provisioning captive chimpanzees with straw bedding and scattered
food increases the animals’ foraging time, since part of their diet is now hidden in the cage
substrate. Such enrichment also decreases the frequency of regurgitation and reingestion, and
increases play and overall activity (Baker, 1997). Presenting lion-tailed macaques with intact
vegetables that require more processing time increases their overall feeding time, food intake,
and range of foods eaten compared to provisioning them with the same foods chopped into
smaller pieces (Smith et al., 1989). Puzzle feeders reduce some (but not all) stereotypic
behavior in captive rhesus macaques (Novak et al., 1998). Providing a walrus with a trough of
rocks in which to forage reduces stereotyped swimming and increases species-typical foraging
behavior (Kastelein and Wiepkema, 1989). And hiding food throughout the exhibit increases
exploratory behavior and decreases inactive behavior in leopard cats (Shepherdson et al., 1993).
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 283
Author's personal copy
Data such as these support the argument that reduced opportunities for foraging in captivity may be
Another aspect of feeding in captivity that is not found in nature is its predictability. Often, the
exact nature of the diet is invariable; animals are offered the same foods day after day. Some data
suggest that such invariability is undesirable to animals. For example, trainers of racehorses
correlate abnormal behavior in their equine charges with restricted variety of diet (McGreevy
et al., 1995). When horses were offered four versions of a concentrated diet that varied only in
ﬂavor and not in nutritional value, they nonetheless sampled from each of the ﬂavors (Goodwin
et al., 2005), suggesting a motivation for variety that the authors assert reﬂects the natural patch
foraging behavior that horses show in the wild.
Invariability of the diet is not the only predictable aspect of feeding in captivity; most animals
are also fed at speciﬁc and invariant times of day. The predictable availability of food in some
cases appears to generate abnormal behavior. For instance, stereotyped pacing and other
repetitive locomotor activity increases as feeding times approach and animals anticipate the
arrival of food (Friend, 1999; Vickery and Mason, 2004; Vinke et al., 2002; Waitt and Buchanan-
Smith, 2001). In one study of captive chimps, making feeding time unpredictable reduced
abnormal behavior and overall inactivity (Bloomsmith and Lambeth, 1995). In contrast, reducing
the reliability of signals announcing food arrival increased aggression in group-housed pigs
(Carlstead, 1986). And in laboratory cats, unpredictable feeding times were correlated with
higher levels of urinary cortisol (Carlstead et al., 1993b). In this latter study, however, a number
of variables were manipulated to produce a ‘‘stressful’’ environment of which unpredictable
feeding time was only one.
Finally, provisioning with commercially prepared, easy-to-eat diets allows little opportunity
for captive animals to engage in species-typical food handling or processing. Particularly for
carnivores, thwarted hunting prospects appear to be stressful. In comparison, providing some
opportunity for species-typical hunting behavior has been beneﬁcial for ﬁshing cats
(Shepherdson et al., 1993), polar bears (Markowitz, 1982), and cheetahs (Lindburg, 1998).
Providing live ﬁsh in a pool reduced stereotypic behavior in captive tigers, and provisioning with
horse leg bones did the same, both for lions and tigers (Bashaw et al., 2003). Note that in addition
to providing animals with greater opportunities to engage in species-typical feeding behaviors,
the techniques employed in these studies also increased the variety of available diet. It is
therefore somewhat impossible to determine with any certainly which manipulation (increasing
behavioral feeding opportunity or increasing dietary variability) was responsible for any
Easy-to-eat diets have also been found to have deleterious effects on carnivore dentition
(Haberstroh et al., 1984; Vosburgh et al., 1982; Wenker et al., 1999); feeding whole-prey items in
contrast improves dental condition (Lindburg, 1998). In addition, one study of large cats in zoos
showed that whole-carcass feeding reduced stereotypic behavior in off-exhibit areas, but
increased hiding behavior on exhibit (McPhee, 2002). The net beneﬁt from intact carcass feeding
to carnivores in captivity has yet to be determined.
3.6. Abnormal social groups
Most of the animals employed in laboratories or in agriculture are social species, as sociality is
one of the characteristics of a species that facilitates the process of domestication (Price, 1984).
Yet despite this we often maintain these animals in total or near total isolation from conspeciﬁcs.
For many animals in captivity, such isolation is clearly stressful. In fact, social isolation has been
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302284
Author's personal copy
used to induce stress in many research investigations. The data resulting from these and similar
investigations show an adverse effect of such isolation.
Singly housed laboratory dogs, for instance, display more abnormal behaviors than do group-
housed dogs (Hetts et al., 1992; Hubrecht et al., 1992). Isolated piglets displays more escape
attempts and less play behavior than do group-housed piglets (Herskin and Jensen, 2000). Dairy
calves raised in isolation are more fearful than are group-reared calves (Boe and Farevik, 2003).
Separating ewes from conspeciﬁcs increases respiration rate, serum cortisol, vocalization, and
locomotion—all of which can be reduced by the addition of a single conspeciﬁc pen partner
(Carbajal and Orihuela, 2001). Similar effects of social isolation on physiological and behavioral
parameters associated with stress are found in rats (Genaro et al., 2004; Weiss et al., 2004) and
cattle (Boissy and Le Neindre, 1997). And the adverse impact of social isolation on primates is so
profound that it has generated an entire body of literature in and of itself (perhaps best known
through the work of Mason (e.g., Mason and Fitz-Gerald, 1962; Mason, 1991b) and Harlow (e.g.,
Harlow and Harlow, 1971). Adding to ﬁndings such as these is the fact that many animals will do
work to gain access to conspeciﬁcs. Given a choice between working for food or access to a social
companion, for instance, tufted capuchins will work for social contact over food—even after
several hours of food deprivation (Dettmer and Fragaszy, 2000). Singly housed dairy calves
(Holm et al., 2002) and rats (Patterson-Kane et al., 2002) will also work for access to a social
companion. For some species, social isolation is without doubt a stressful experience.
In other captive situations, animals are maintained in social groupings that would not
generally occur in nature (e.g., Stoinski et al., 2001). Japanese macaques, for example, live in
multi-male, multi-female groups in the wild. Yet one of the authors works on occasion at a zoo in
which an exhibit of this species consists entirely of juvenile males. These animals show a great
deal of social tension and very little natural activity, engaging instead in intensive monitoring of
the others in their group. In Boston, Massachusetts, the recent exploits of a young gorilla named
‘‘Joe’’ made national news as he repeatedly escaped from his outdoor exhibit and on one
occasion, even left the zoo grounds before he was recaptured. Joe was the only sub-adult male in a
small family group of gorillas that included an adult silverback. In the wild, a gorilla of Joe’s age
would have emigrated from his natal group under pressure from the dominant silverback male; in
this case, one might interpret Joe’s escape attempts as efforts to ‘‘emigrate’’ from what was no
longer an appropriate social group for his species. Anecdotal observations such as these suggest
that housing animals in social groups that are not species-typical may also be stressful—though
whether or not it is as stressful as keeping a social animal in isolation remains to be determined.
In addition to maintaining animals in social isolation or abnormal social groups, humans
sometimes crowd too many animals into an enclosure, or remix groups repeatedly as a
consequence of routine husbandry practices (such as veterinary checks or transport). Such
practices also have documented ill effects on animal well-being. Crowding rhesus macaques
results in signiﬁcant increases in injuries due to increased ﬁghting (Boyce et al., 1998). A similar
effect of crowding on aggression is seen in farmed red deer (Blanc and The
´riez, 1998). And
crowding in gilts is associated with impaired sexual behavior and increased levels of plasma
corticosterone (Hemsworth et al., 1986a,b,c). Stress resulting from social instability is
hypothesized to explain mortality in several cases of captive dolphins (Waples and Gales, 2002).
The mixing of unfamiliar pigs of similar ages and weights evokes severe aggression (Francis
et al., 1996). And social instability deriving from repeated mixing reduces weight gain in group-
housed female rats, and increases plasma corticosterone (Haller et al., 1999). Again, the effects of
both crowding and social instability on common physiological and behavioral measures of stress
are so well documented that both are often used as research paradigms to induce stress. Yet many
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 285
Author's personal copy
husbandry procedures in captivity involve crowding and the mixing of social groups, even if only
temporarily. In nature, animals can retreat from agonistic encounters or avoid dominant
conspeciﬁcs in potential conﬂict situations. In captivity, such conﬂict avoidance strategies may
be impossible to employ. As suggested previously, the nature of social groups and the
opportunities for conﬂict avoidance may be critical factors in the well-being of social species
maintained in captivity.
4. Discussion: predictability, control, and boredom
What many if not all of the potential stressors reviewed above have in common is the inability
of the captive animal to control them. Indeed, perhaps the greatest stressor in the lives of captive
animals is their perceived or actual inability to control most aspects of their surroundings
(Sambrook and Buchanan-Smith, 1997). Animals in captivity generally do not have control over
what individuals serve as their social partners or their mates. They have little or no control
over how much space they are able to put between themselves and other conspeciﬁcs, or
between themselves and humans. They have little or no control over what kinds of food they
are offered, nor when that food is made available. Nor are they generally able to control
relevant environmental stimuli such as quantity, quality, and timing of lights, sounds, odors, or
The importance of controllability in animal welfare is a complex subject, and one that is
problematic for study (Sambrook and Buchanan-Smith, 1997). Nonetheless many investigators
have argued that control is essential for animal well-being (e.g., Friend, 1991; O’Neill, 1989),
and some data suggest a direct relationship between lack of control and behavioral and
physiological operational deﬁnitions of well-being (for a review, see Mineka and Kelly, 1989).
For example, hens that could control delivery of extra food and extra light showed less self-
directed behavior than did hens without this control (Taylor et al., 2001). Rhesus macaques that
could control the occurrence of loud, unpleasant sound showed lower cortisol levels than did
macaques exposed to the same sounds without any ability to control them (Hanson et al., 1976).
Similarly, dogs (Seligman et al., 1968) and rats (Seligman and Beagley, 1975) that had received
inescapable shock and had subsequently ‘‘given up’’ all efforts to escape regained more adaptive
behaviors for coping with the shock when they were trained to control it. Maier and Seligman
(1976) call this giving up behavior ‘‘learned helplessness,’’ and it is a phenomenon accompanied
by a number of symptoms of chronic stress, including anorexia and subsequent weight loss
(Rickards et al., 1997), inhibition of exploratory behavior (Wommack et al., 2004), and aberrant
immune responses (Overmeier, 2002). If captivity affords animals little or no control over most
aspects of their daily lives – particularly those that they may ﬁnd stressful – then captive
environments may also promote helplessness and the loss of adaptive coping strategies. If we
have conservation of bio- and behavioral diversity among our husbandry goals, such passivity is
an undesirable consequence of captivity. To the degree that captive environments afford animals
little or no control over most aspects of their daily lives, they may be inherently stressful and also
deleterious to long-term conservation efforts.
Another aspect of captivity that may be stressful to animals is its predictability (see review in
Bassett and Buchanan-Smith, 2007). However, some studies have shown that animals given
a choice will choose predictability over unpredictability, particularly over aversive events
(Gliner, 1972). The impact of predictability or its lack appears to depend largely on the nature of
the event or stimulus to be predicted (van Rooijen, 1991). Being able to predict the occurrence of
events that are essential for survival (such as feeding or the opportunity to seek shelter) may be
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302286
Author's personal copy
essential for captive animal wellbeing, as some of the data reviewed above suggest. At the same
time, however, the very predictability of routine husbandry schedules has been shown to
stimulate undesirable behaviors (such as pacing), which can be eliminated or reduced by
randomizing the timing of husbandry activities. Such observations have led some researchers to
propose that the relentless predictability of routine husbandry and/or environmental stimuli
present in captive environments in and of itself is stressful (Pepperberg, 2004; van Rooijen,
1991), because of the boredom that results.
It may be essential to introduce animals to a certain amount of unpredictability, if one of the
goals of maintaining animals in captivity is conservation and eventual repatriation (Appleby,
1997). After all, novelty, unpredictability, and variability are all common features of the natural
environment. To the degree that captivity affords animals little or no opportunity to manage
important aspects of their lives (such as quality, quantity, and timing of food and water, choice of
mates or other social partners, etc.), then captivity is also unlikely to provide animals with the
kinds of experiences they will need to succeed outside of our care. To the extent, however that
captive animals rely on routine to reduce anxiety about essential environmental features that they
cannot control themselves (such as provision with food, water, and shelter), then failure to
provide such assurances will surely be a cause of distress. The challenge, then, is to determine the
optimal balance of variability and routine that is ideal for each species—and probably for each
individual (for potential solutions, see Bassett and Buchanan-Smith, 2007). To some degree, we
can rely on existing natural history data to guide us through this challenge; in many cases,
however, the data most needed do not yet exist. Additionally, we may rely on careful observation
and monitoring of species physiological and behavioral responses to elements of the captive
environment for clues as to which (if any) of these elements may be causing stress at a given place
Unfortunately as the literature reviewed above suggest, while there may be many behavioral
and physiological indicators of stress, there are none that are unique to a given stressor in
such way as to provide a clear diagnosis for the concerned caretaker. Many of the stressors
reviewed above produce the same or very similar effects on animals, and some produce
different effects in animals of different ages, sexes, or with different previous experience. This
ambiguity makes such behavioral and physiological responses unreliable symptoms for
troubleshooting a given captive situation; about all they may be able to tell us is that something
is amiss, but alas—not precisely what is amiss. And paradoxically, many animals respond to
stressors by exhibiting diametrically opposite suites of behaviors. That is, animals can respond
to noise with increased locomotor activity or with paralysis. They can exhibit increased
crypsis or increased investigatory behavior. They can become secretive or conspicuous.
They can become silent or exhibit increased vocal activity. In short, an examination of the
symptoms of stress will not generally help us to identify the source of the provocation.
Rather, we will have to rely on a better understanding of species natural history and a fuller
evaluation of all aspects of the captive setting when considering possible sources of stress in a
The authors would like to thank Kurt Fristrup for his assistance in identifying technologies for
monitoring infrasound in captive environments, and Ron Swaisgood and Matthew Miller for their
helpful comments on previous drafts of the manuscript. This article was also greatly improved by
feedback from two anonymous reviewers.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 287
Author's personal copy
Adamec, R., Kent, P., Anisman, H., Shallow, T., Merali, Z., 1998. Neural plasticity, neuropeptides and anxiety in
animals—implications for understanding and treating affective disorder following traumatic stress in humans.
Neurosci. Biobehav. Rev. 23, 301–318.
Adamec, R., Shallow, T., 1993. Lasting effects on rodent anxiety of a single exposure to a cat. Physiol. Behav. 54, 101–109.
Ader, D.N., Johnson, S.B., Huang, S.W., Riley, W.J., 1991. Group-size, cage shelf level, and emotionality in nonobese
diabetic mice: impact on onset and incidence of IDDM. Psychosom. Med. 53, 313–321.
Ago, A., Gonda, T., Takechi, M., Takeuchi, T., Kawakami, K., 2002. Preferences for paper bedding material of the
laboratory mice. Exp. Anim. 51, 157–161.
Ames, D.R., 1978. Physiological responses to auditory stimuli. In: Fletcher, J.L., Busnel, R.G. (Eds.), Effects of Noise on
Wildlife. Academic Press, New York, NY, pp. 23–46.
Anderson, U.S., Benne, M., Bloomsmith, M.A., Maple, T.L., 2002. Retreat space and human visitor density moderate
undesirable behavior in petting zoo animals. J. Appl. Anim. Welfare Sci. 5, 125–137.
Anna, I., Olsson, S., Dahlborn, K., 2002. Improving housing conditions for laboratory mice: a review of ‘‘environmental
enrichment’’. Lab. Anim. 36, 243–270.
Anthony, A., Ackerman, E., Lloyd, J.A., 1959. Noise stress in laboratory rodents: I. Behavioral andendocrine responses of
mice, rats, and guinea pigs. J. Acoust. Soc. Am. 31, 1437–1440.
APHIS (Animal and Plant Health Inspection Service, United States Department of Agriculture), 1989. Animal welfare;
Draft Policy on Environment Enhancement for Nonhuman Primates, vol. 64, Number 135, Federal Register, July 15,
Appleby, M.C., 1997. Life in a variable world: behaviour, welfare, and environmental design. Appl. Anim.Behav. Sci. 54,
Appleby, M.C., Lawrence, A.B., 1987. Food restriction as a cause of stereotypic behavior in tethered gilts. Anim. Prod. 45,
Applegate, A.L., Curtis, S.E., Groppel, J.L., McFarlane, J.M., Widowski, T.M., 1988. Footing and gait of pigs on different
concrete surfaces. J. Anim. Sci. 66, 334–341.
Armstrong, K.R., Clark, T.R., Peterson, M.R., 1998. Use of corn-husk nesting material to reduce aggression in caged
mice. Comtemp. Topics Lab. Anim. Sci. 37, 64–66.
Arnold, C.E., Estep, D.Q., 1994. Laboratory caging preferences in golden hamsters (Mesocricetus auratus). Lab. Anim.
Asaeda, T., Ca, V.T., Wake, A., 1996. Heat storage of pavement and its effect on the lower atmosphere. Atmos. Environ.
Baker, K., 2004. Beneﬁts of positive human interaction for socially housed chimpanzees. Anim. Welfare 13, 239–245.
Baker, K.C., 1997. Straw and forage material ameliorate abnormal behaviors in adult chimpanzees. Zoo Biol. 16, 225–236.
Bakkan, M., Moe, R.O., Smith, A.J., Selle, G.-M.E., 1999. Effects of environmental stressors on deep body temperature
and activity levels in silver fox vixens (Vulpes vulpes). Appl. Anim. Behav. Sci. 64, 141–151.
Balcombe, J.P., Barnard, N.D., Sandusky, C., 2004. Laboratory routines cause animal stress. Contemp. Topics Lab. Anim.
Sci. 43, 42–51.
Banjanin, S., Mrosovsky, N., 2000. Preferences of mice, Mus musculus, for different types of running wheel. Lab. Anim.
Barber, C.L., Prescott, N.B., Wathes, C.M., Le Sueur, D., Perry, G., 2004. Preferences of growing ducklings and turkey
poults for illuminance. Anim. Welfare 13, 211–224.
Bargai, U., Cohen, R., 1992. Tarsal lameness of dairy bulls housed at two artiﬁcial insemination centers: 24 cases (1975–
1987). J. Am. Vet. Med. Assoc. 201, 1068–1069.
Barklow, W.E., 1997. Some underwater sounds of the hippopotamus (Hippopotamus amphibius). Marine Freshwater
Behav. Physiol. 29, 237–249.
Barnett, K.E., Cocroft, R.B., Fleishman, L.J., 1999. Possible communication by substrate vibration in a chameleon.
Barnett, J.L., Hemsworth, P.H., Cronin, G.M., Newman, E.A., McCallum, T.H., Chilton, D., 1992. Effect of pen size,
partial stalls, and method of feeding on welfare-related behavioral and physiological responses of group-housed pigs.
Appl. Anim. Behav. Sci. 34, 207–220.
Barnett, J.L., Hemsworth, P.H., Hennessey, D.P., McCallum, T.H., Newman, E.A., 1994. The effects of modifying the
amount of human contact on behavioral, physiological, and production responses of laying hens. Appl. Anim. Behav.
Sci. 41, 87–100.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302288
Author's personal copy
Barrett, J., Abbott, D.H., George, L.M., 1990. Extension of reproductive suppression by pheromonal cues in subordinate
female marmoset monkeys, Callithrix jacchus. J. Reprod. Fertil. 90, 411–418.
Bartolomucci, A., Pederzani, T., Sacerdote, P., Panerai, A.E., Parmigiani, S., Palanza, P., 2004. Behavioral and
physiological characterization of male mice under chronic psychosocial stress. Psychoneuroendocrinology 29,
Bashaw, M.J., Bloomsmith, M.A., Marr, M.J., Maple, T.L., 2003. To hunt, or not to hunt? A feeding enrichment
experiment with captive large felids. Zoo Biol. 22, 189–198.
Bashaw, M.J., Tarou, L.R., Maki, T.S., Maple, T.L., 2001. A survey assessment of variables related to stereotypy in captive
giraffe and okapi. Appl. Anim. Behav. Sci. 73, 235–247.
Bassett, L., Buchanan-Smith, H.M., 2007. Effects of predictability on the welfare of captive animals. Appl. Anim. Behav.
Sci. 102, 223–245.
Baumans, V., 2005. Environmental enrichment for laboratory rodents and rabbits: requirements of rodents, rabbits, and
research. ILAR J. 46, 162–170.
Bayne, K.A., McCully, C., 1989. The effect of cage size on the behaviour of individually housed rhesus monkeys. Lab.
Anim. 18, 25–28.
Beattie, V.E., Walker, N., Sneddon, I.A., 1998. Preference testing of substrates by growing pigs. Anim. Welfare 7, 27–34.
Belhorn, R.W., 1980. Lighting in the animal environment. Lab. Anim. Sci. 30, 440–450.
Bellanca, R.U., Crockett, C.M., 2002. Factors predicting increased incidence of abnormal behavior in male pigtailed
macaques. Am. J. Primatol. 58, 57–69.
Berntson, G.G., Boysen, S.T., Bauer, H.R., Torello, M.W., 1989. Conspeciﬁc screams and laughter: cardiac and behavioral
reactions of infant chimpanzees. Develop. Psychobiol. 22, 771–787.
Besch, E.L., 1990. Environmental variables and animal needs. In: Rollin, B.E., Kesel, M.L. (Eds.), The Experimental
Animal in Biomedical Research: A Survey of Scientiﬁc and Ethical Issues for Investigators, vol. 1. CRC Press, Boca
Raton, FL, pp. 113–131.
Birke, L., 2002. Effects of browse, human visitors, and noise on the behaviour of captive orangutans. Anim. Welfare 11,
Blackshaw, J.K., Blackshaw, A.W., McGlone, J.J., 1997. Buller steer syndrome: a review. Appl. Anim. Behav. Sci. 54, 97–
Blake, B.H., 2002. Ultrasonic calling in isolated infant prairie voles (Microtus ochrogaster) and montane voles (M.
montanus). J. Mammal. 83, 536–545.
Blanc, F., The
´riez, M., 1998. Effects of stocking density on the behaviour and growth of farmed red deer hinds. Appl.
Anim. Behav. Sci. 56, 297–307.
Blaney, E.C., Walls, D.L., 2004. The inﬂuence of a camouﬂage net barrier on the behaviour, welfare, and public
perceptions of zoo-housed gorillas. Anim. Welfare 13, 111–118.
Bleich, V.C., Bowyer, R.T., Pauli, A.M., Vernoy, R.L., Anthes, R.W., 1990. Responses of mountain sheep to helicopter
surveys. Calif. Fish Game 76, 197–204.
Blom, H.J.M., Vantintelen, G., Baumans, V., Vandenbroek, J., Beynen, A.C., 1995. Development and application of a
preference test system to evaluate housing conditions for laboratory rats. Appl. Anim. Behav. Sci. 43, 279–290.
Bloomsmith, M.A., Else, J.G., 2005. Behavioral management of chimpanzees in biomedical research facilities: the state
of the science. ILAR J. 46, 192–201.
Bloomsmith, M.A., Lambeth, S.P., 1995. Effects of predictable versus unpredictable feeding schedules on chimpanzee
behavior. Appl. Anim. Behav. Sci. 44, 65–74.
Boe, K.E., Farevik, G., 2003. Grouping and social preferences in calves, heifers, and cows. Appl. Anim. Behav. Sci. 80,
Boissy, A., Le Neindre, P., 1997. Behavioral, cardiac, and cortisol responses to brief peer separation and reunion in cattle.
Physiol. Behav. 61, 693–699.
Boissy, A., Veissier, I., Roussel, S., 2001. Behavioural reactivity affected by chronic stress: an experimental approach in
calves submitted to environmental instability. Anim. Welfare 10 (Suppl.), S175–S185.
Boivin, X., Garel, J.P., Mante, A., Le Neindre, P., 1997. Beef calves react differently to different handlers according to the
test situation and their previous interactions with their caretaker. Appl. Anim. Behav. Sci. 55, 245–257.
Boyce, W.T., O’Neill-Wagner, P., Price, C.S., Haines, M., Suomi, S., 1998. Crowding stress and violent injuries among
behaviorally inhibited rhesus macaques. Health Psychol. 17, 285–289.
Brambell, F.W.R., 1965. Report of the Technical Committee to Enquire into the Welfare of Animals Kept under Intensive
Livestock Husbandry Systems. London: HMSO Cmnd. 2836.
Brent, L., Koban, T., Evans, S., 2003. The inﬂuence of temperature on the behavior of captive mother–infant baboons.
Behaviour 140, 209–224.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 289
Author's personal copy
Breuer, K., Hemsworth, P.H., Coleman, G.J., 2003. The effect of positive or negative handling on the behavioural and
physiological responses of nonlactating heifers. Appl. Anim. Behav. Sci. 84, 3–22.
Broom, D.M., Johnson, K.G., 1993. Stress and Animal Welfare. Chapman & Hall, London, UK.
Brundrett, G.W., 1974. Human sensitivity to ﬂicker. Light. Res. Technol. 6, 127–139.
Buchanan-Smith, H.M., Anderson, D.A., Ryan, C.W., 1993. Responses of cotton-top tamarins (Saguinus oedipus)to
faecal scents of predators and non-predators. Anim. Welfare 2, 17–32.
Buchwalder, T., Huber-Eicher, B., 2004. Effect of increased ﬂoor space on aggressive behaviour in male turkeys
(Meleagris gallopovo). Appl. Anim. Behav. Sci. 89, 207–214.
Byrne, W., 1982. Primate vocalizations: a structural and functional approach to understanding. Behaviour 80,
Callard, M.D., Bursten, S.N., Price, E.O., 2000. Repetitive backﬂipping behaviour in captive roof rats (Rattus rattus) and
the effects of cage enrichment. Anim. Welfare 9, 139–152.
Canlon, B., Erichsen, S., Nemlander, E., Chen, M., Hossain, A., Celsi, G., Ceccatelli, S., 2003. Alterations in the
intrauterine environment by glucocorticoids modiﬁes the development programme of the auditory system. Eur. J.
Neurosci. 17, 2035–2041.
Capitanio, J.P., 1986. Behavioral pathology. In: Mitchell, G., Erwin, J. (Eds.), Comparative Primate Biology, Part A:
Behavior, Conservation, and Ecology, vol. 2. Alan R. Liss Inc., New York, NY, pp. 411–454.
Carbajal, S., Orihuela, A., 2001. Minimal number of conspeciﬁcs needed to minimize the stress response of isolated
mature ewes. J. Appl. Anim. Welfare Sci. 4, 249–255.
Carlstead, K., 1986. Predictability of feeding: its effect on agonistic behaviour and growth in grower pigs. Appl. Anim.
Behav. Sci. 16, 25–38.
Carlstead, K.E., Brown, J.L., 2005. Relationships between patterns of fecal corticoid excretion and behavior, reproduc-
tion, and environmental factors in captive black (Diceros bicornis) and white (Ceratotherium simum) rhinoceros. Zoo
Biol. 24, 215–232.
Carlstead, K.E., Brown, J.L., Seidensticker, J., 1993a. Behavioral and adrenocortical responses to environmental changes
in leopard cats (Felis bengalensis). Zoo Biol. 12, 321–331.
Carlstead, K., Brown, J.L., Strawn, W., 1993b. Behavioral and physiological correlates of stress in laboratory cats. Appl.
Anim. Behav. Sci. 38, 143–158.
Carlstead, K., Fraser, J., Bennett, C., Kleiman, D.G., 1999. Black rhinoceros (Diceros bicornis) in US zoos: II. Behavior,
breeding success, and mortality in relation to housing conditions. Zoo Biol. 18, 35–52.
Carter, W.R., Herrman, J., Stokes, K., Cox, D.J., 1987. Promotion of diabetes onset by stress in the BB rat. Diabetologia
Cassinello, J., Pieters, I., 2000. Multi-male captive groups of endangered dama gazelle: social rank, aggression, and
enclosure effects. Zoo Biol. 19, 121–129.
Chabot, D., Gagnon, P., Dixon, E.A., 1996. Effect of predator odors on heart rate and metabolic rate of wapati (Cervus
elaphus canadensis). J. Chem. Ecol. 22, 839–868.
Chamove, A.S., Anderson, J.R., Morgan-Jones, S.C., Jones, S.P., 1982. Deep woodchip litter: hygiene, feeding, and
behavioral enhancement in eight primate species. Int. J. Study Anim. Prob. 3, 308–318.
Chamove, A.S., Hosey, G., Schaetzel, P., 1988. Visitors excite primates in zoos. Zoo Biol. 7, 359–369.
Chamove, A.S., Moodie, E.M., 1990. Are alarming events good for captive monkeys? Appl. Anim. Behav. Sci. 27, 169–
Chiszar, D.S., Wellborn, S., Wand, M.A., Scudder, K.M., Smith, H.M., 1980. Investigatory behavior in snakes II: cage
cleaning and the induction of defecation in snakes. Anim. Learn. Behav. 8, 505–510.
Chrousos, G.P., 1997. The neuroendocrinology of stress: its relation to the hormonal milieu, growth, and development.
Growth Genet. Hormones 13, 1–8.
Clarke, A.S., Schneider, M.L., 1993. Prenatal stress has long-term effects on behavioral responses to stress in juvenile
rhesus monkeys. Develop. Psychobiol. 26, 293–305.
Cloutier, S., Weary, D.M., Fraser, D., 2000. Can ambient sound reduce distress in piglets during weaning and restraint? J.
Appl. Anim. Welfare Sci. 3, 107–116.
Clubb, R., Mason, G., 2003. Captivity effects on wide-ranging carnivores. Nature 425, 473–474.
Clubb, R., Mason, G., 2007. Natural behavioural biology as a risk factor in carnivore welfare: How analysing species
differences could help zoos improve enclosures. Appl. Anim. Behav. Sci. 102, 303–328.
Coile, D.C., Pollitz, C.H., Smith, J.C., 1989. Behavioral determination of critical ﬂicker fusion in dogs. Physiol. Behav.
Colburn, J.F., Tarte, R.D., 1976. The effect of rearing environments on the contrafreeloading phenomenon in rats. J. Exp.
Anal. Behav. 26, 289–294.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302290
Author's personal copy
Cooper, J.J., 2004. Consumer demand under commercial husbandry conditions: practical advice on measuring
behavioural priorities in captive animals. Anim. Welfare 13 (Suppl.), S47–S56.
Cooper, J.J., Appleby, M.C., 2003. The value of environmental resources to domestic hens: a comparison of the work-rate
for food and for nests as a function of time. Anim. Welfare 12, 39–52.
Cooper, J.J., Odberg, F., Nicol, C.J., 1996. Limitations on the effectiveness of environmental improvement in reducing
stereotypic behaviour in bank voles (Clethrionomys glareolus). Appl. Anim. Behav. Sci. 48, 237–248.
Cottereau, P., 1978. Effects of sonic boom from aircraft on wildlife and animal husbandry. In: Fletcher, J.L., Busnel, R.G.
(Eds.), Effects of Noise on Wildlife. Academic Press, New York, NY, pp. 63–79.
Coulton, L.E., Waran, N.K., Young, R.J., 1997. Effects of foraging enrichment on the behaviour of parrots. Anim. Welfare
Crockett, C.M., Bowers, C.L., Shimoji, M., Leu, M., Bowden, D.M., Sackett, G.P., 1995. Behavioral responses of
longtailed macaques to different cage sizes and common laboratory experiences. J. Compar. Psychol. 109, 368–383.
Cupp, A.S., Roberson, M.S., Stumpf, T.T., Wolfe, M.W., Werth, L.A., Kojima, N., Kittock, R.J., Kinder, J.E., 1993.
Yearling bulls shorten the duration of postpartum anestrus in beef cows to the same extent as do mature bulls. J. Anim.
Sci. 71, 306–309.
Cuthill, I.C., Partridge, J.C., Bennett, A.T.D., Church, S.C., Hart, N.S., Hunt, S., 2000. Ultraviolet vision in birds. Adv.
Studies Behav. 29, 159–214.
D’Amato, F.R., Moles, A., 2001. Ultrasonic vocalizations as an index of social memory in female mice. Behav. Neurosci.
Dantzer, R., 1991. Stress, stereotypies and welfare. Behav. Process. 25, 95–102.
Davey, A.K., Fawcett, J.P., Lee, S.E., Chan, K.K., Schoﬁeld, J.C., 2003. Decrease in hepatic drug-metabolizing enzyme
activities after removal of rats from pine bedding. Compar. Med. 53, 299–302.
Davis, H., Taylor, A., Norris, C., 1997. Preference for familiar humans by rats. Psychon. Bull. Rev. 4, 118–120.
Davis, N., Schaffner, C.M., Smith, T.E., 2005. Evidence that zoo visitors inﬂuence HPA activity in spider monkeys (Ateles
geoffroyii ruﬁventris). Appl. Anim. Behav. Sci. 90, 131–141.
Dawkins, M.S., 1990. From an animal’s point of view: motivation, ﬁtness, and animal welfare. Behav. Brain Sci. 13.
Dawkins, M.S., Cook, P.A., Whittingham, M.J., Mansell, K.A., Harper, A.E., 2003. What makes free-range broiler
chickens range? In situ measurement of habitat preference. Anim. Behav. 66, 151–160.
D’Eath, R.B., 1998. Can video images imitate real stimuli in animal behaviour experiments? Biol. Rev. 73, 267–292.
de Jong, I.C., Ekkel, E.D., Van de Burgwal, J.A., Lambooij, E., Korte, S.M., Ruis, M.A.W., Koolhaas, J.M., Blokhuis, H.J.,
1998. Effects of straw bedding on physiological responses to stressors and behavior in growing pigs. Physiol. Behav.
Dettmer, E., Fragaszy, D., 2000. Determining the value of social companionship to captive tufted capuchin monkeys
(Cebus apella). J. Appl. Anim. Welfare Sci. 3, 293–304.
Dielenberg, R.A., Carrive, P., McGregor, I.S., 2001. The cardiovascular and behavioral responses to cat odor in rats:
unconditioned and conditioned effects. Brain Res. 897, 2280237.
Dorries, K.M., Adkinsregan, E., Halpern, B.P., 1995. Olfactory sensitivity to the pheromone androstenone is sexually
dimorphic in the pig. Physiol. Behav. 57, 255–259.
Draper, W.A., 1965. Sensory stimulation and rhesus monkey activity. Percept. Motor Skills 21, 319–322.
Draper, W.A., Bernstein, I.S., 1963. Stereotyped behavior and cage size. Percept. Motor Skills 16, 23–234.
Duke, J.L., Zammit, T.G., Lawson, D.M., 2001. The effects of routine cage-changing on cardiovascular and behavioral
parameters in male Spraque-Dawley rats. Contemp. Topics Lab. Anim. Sci. 40, 17–20.
Ehret, G., 1980. Development of sound communication in mammals. In: Rosenblatt, J.S., Hinde, R.A., Beer, C., Busnel,
M.C. (Eds.), Advances in the Study of Behavior, vol. 11. Academic Press, New York, NY, pp. 179–225.
Eisner, A., Samples, J.R., 1991. Profound reductions of ﬂicker sensitivity in the elderly: can glaucoma involve the retina
distal to ganglion cells? Appl. Optomet. 30, 2121–2135.
Engelhart, A., Mullerschwarze, D., 1995. Responses of beaver (Castor canadensis Kuhl) to predator chemicals. J. Chem.
Ecol. 21, 1349–1364.
Epple, G., 1985. The prmates, I: order anthropoidia. In: Brown, R.E., MacDonald, D.W. (Eds.), Social Odor in Mammals.
Clarendon Press, Oxford, GB, pp. 732–739.
Epple, G., Niblick, H., Lewis, S., Nolte, D.L., Campbell, D.L., Mason, J.R., 1996. Pine needle oil causes avoidance
behaviors in pocket gophers. J. Chem. Ecol. 22, 1013–1025.
Faerevik, G., Andersen, I.L., Boe, K.E., 2005. Preferences of sheep for different types of pen ﬂooring. Appl. Anim. Behav.
Sci. 90, 265–276.
Ferrante, V., Canali, E., Mattiello, S., Verga, M., Sacerdote, P., Manfredi, B., Panerai, A.E., 1998. Preliminary study on the
effect of size of individual stall on the behavioural and immune reactions of dairy calves. J. Anim. Feed Sci. 7, 29–36.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 291
Author's personal copy
File, S.E., Zangrossi, H., Sanders, F.L., Mabbutt, P.S., 1995. Dissociation between behavioral and corticosterone
responses to repeated exposures to cat odor. Physiol. Behav. 54, 1109–1111.
Forthman, D.L., 1998. Toward optimal care for conﬁned ungulates. In: Shepherdson, D.J., Mellen, J.D., Hutchins, M.
(Eds.), Second Nature: Environmental Enrichment for Captive Animals. Smithsonian Institution Press, Washington,
DC, pp. 236–261.
Francis, D.A., Christison, G.I., Cymbaluk, N.F., 1996. Uniform or heterogeneous weight groups as factors in mixing
weanling pigs. Can. J. Anim. Sci. 76, 171–176.
Fraser, D., 1985. Selection of bedded and unbedded areas by pigs in relation to environmental temperature and behaviour.
Appl. Anim. Behav. Sci. 14, 117–126.
Fraser, S., Phillips, P.A., Thompson, B.K., Tennessen, T., 1991. Effect of straw on the behavior of growing pigs. Appl.
Anim. Behav. Sci. 30, 307–318.
Friend, T.H., 1999. Behavior of picketed circus elephants. Appl. Anim. Behav. Sci. 62, 73–88.
Friend, T.H., 1991. Behavioral aspects of stress. J. Dairy Sci. 74, 292–303.
Friend, T.H., 1989. Recognizing behavioral needs. Appl. Anim. Behav. Sci. 22, 151–158.
Fullard, J.H., Barclay, R.M.R., Thomas, D.W., 1993. Echolocation in free-ﬂying atiu swiftlets (Aerodramus sawtelli).
Biotropica 25, 334–339.
Galef Jr., B.F., 2002. Social learning of food preferences in rodents: rapid appetitive learning. Curr. Protocol Neurosci.
Gamble, M.R., 1982. Sound and its signiﬁcance for laboratory-animals. Biol. Rev. Cambr. Philosoph. Soc. 57, 395–421.
Gelez, H., Fabry-Nys, C., 2004. The ‘‘male effect’’ in sheep and goats: a review of the respective roles of the two olfactory
systems. Hormone Behav. 46, 257–271.
Genaro, G., Schmidek, W., Franci, C.R., 2004. Social condition affects hormone secretion and exploratory behavior in
rats. Braz. J. Med. Biol. Res. 37, 833–840.
Geverink, N.A., Bu
¨hnemann, A., Van de Burgwal, J.A., Lambooij, E., Blokhuis, H.J., Wiegant, V.M., 1998. Responses of
slaughter pigs to transport and lairage sounds. Physiol. Behav. 63, 667–673.
Glatston, A.R., Geiloet-Soeteman, E., Hora-Pacek, E., van Hooff, J.A.R.A.M., 1984. The inﬂuence of the zoo
environment on social behavior of groups of cotton-top tamarins, Saguinus oedipus. Zoo Biol. 3, 241–253.
Gliner, J.A., 1972. Predictable versus unpredictable shock: preference behavior and stomach ulceration. Physiol. Behav. 9,
Goerke, B., Fleming, L., Creel, M., 1987. Behavioral changes of a juvenile gorilla after transfer to a more naturalistic
environment. Zoo Biol. 6, 283–295.
Goliszek, A.G., Crawford, G.E., Lawrence, H.S., Bennett, J., Williams, F., Hurley, S.L., 1996. Effects of prepubertal stress
on subsequent ACTH response to novel stress and CRH in male versus female rats. Stress Med. 12, 199–204.
Goodwin, D., Davidson, H.P.B., Harris, P., 2005. Sensory varieties in concentrate diets for stabled horses: effects on
behaviour and selection. Appl. Anim. Behav. Sci. 90, 337–349.
Gordon, C.J., 2004. Effect of cage bedding on temperature regulation and metabolism of group housed female mice.
Compar. Med. 54, 63–68.
Gordon, C.J., Becker, P., Ali, J.S., 1998. Behavioral thermoregulatory responses of single- and group-housed mice.
Physiol. Behav. 65, 255–262.
Grandin, T., Johnson, C., 2005. Animals in Translation. Scribner, New York, NY.
Greenberg, G., 1972. The effects of ambient temperature and population density on aggression in two inbred strains of
mice, Mus musculus. Behaviour 42, 119–130.
Greenman, D.L., Bryant, P., Kodell, R.L., Sheldon, W., 1982. Inﬂuence of cage shelf level on retinal atrophy in mice. Lab.
Anim. Sci. 32, 353–356.
Greenwood, V.J., Smith, E.L., Goldsmith, A.R., Cuthill, I.C., Crisp, L.H., Walter-Swan, M.B., Bennett, A.T.D., 2003.
Does the ﬂicker frequency of ﬂuorescent lighting affect the welfare of captive European starlings? Appl. Anim.
Behav. Sci. 86, 145–159.
Grifﬁn, D.R., Webster, F.A., Michael, C.R., 1960. The echolocation of ﬂying insects by bats. Anim. Behav. 8, 141–154.
Gronli, J., Murison, R., Fiske, E., Bjorvatn, B., Sorensen, E., Portas, C.M., Ursin, R., 2005. Effects of chronic mild stress
on sexual behavior, locomotor activity and consumption of sucrose and saccharine solutions. Physiol. Behav. 84, 571–
Gunter, R., 1995. The absolute threshold for vision in the cat. J. Physiol. 114, 8–15.
Haberstroh, L.I., Ullrey, D.E., Silkarskie, J.G., Richter, N.A., Colmery, B.H., Meyers, T.D., 1984. Diet and oral health in
captive Amur tigers (Pantera tigris altaica). J. Zoo Anim. Med. 15, 142–146.
Hagerman, I., Rasmanis, G., Blomkvist, V., Ulrich, R., Eriksen, C.A., Theorell, T., 2005. Inﬂuence of intensive coronary
care acoustics on the quality of care and physiological state of patients. Int. J. Cardiol. 98, 267–270.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302292
Author's personal copy
Hall, E., Morgan, K.N., Marchese, C., 2005. Effect of feeding enrichment on grey-cheeked mangabeys. In: Paper
presented at the 7th International Conference on Environmental Enrichment, New York, NY, 31 July–5 August.
Haller, J., Fuchs, E., Hala
´sz, J., Makara, G.B., 1999. Defeat is a major stressor in males while social instability is stressful
mainly in females: towards the development of a social stress model in female rats. Brain Res. Bull. 50, 33–39.
Hansen, L.T., Berthelsen, H., 2000. The effect of environmental enrichment on the behaviour of caged rabbits
(Oryctolagus cuniculus). Appl. Anim. Behav. Sci. 68, 163–178.
Hanson, J.P., Larson, M.E., Snowdon, C.T., 1976. The effects of control over high intensity noise on plasma cortisol levels
in rhesus monkeys. Behav. Biol. 16, 333–340.
Hargreaves, A.L., Hutson, G.D., 1990. Changes in heart rate, plasma cortisol and haemocrit of sheep during a shearing
procedure. Appl. Anim. Behav. Sci. 26, 91–101.
Harlow, H.F., Harlow, M.K., 1971. Psychopathology in monkeys. In: Kimmel, H.D. (Ed.), Experimental Psychopathol-
ogy: Recent Research and Theory. USnc, San Diego, CA, pp. 203–229.
Hauser, M.D., Caffrey, C., 1994. Antipredator response to raptor calls in wild crows, Corvus brachyrhunochos Hesperis.
Anim. Behav. 48, 1469–1471.
Hazlett, B.A., Schoolmaster, D.R., 1999. Responses of cambarid crayﬁsh to predator odor. J. Chem. Ecol. 24, 1757–1770.
Hediger, H., 1964. Wild Animals in Captivity: An Outline of the Biology of Zoological Gardens. Dover Publications, New
Hediger, H., 1955. Studies of the Psychology and Behavior of Captive Animals in Zoos and Circuses. Criterion Press, New
Heffner, R.S., Heffner, H.E., Contos, C., Kearns, D., 1994. Hearing in prairie dogs: transition between surface and
subterranean rodents. Hear. Res. 73, 185–189.
Hemsworth, P.H., 2003. Human–animal interactions in livestock production. Appl. Anim. Behav. Sci. 81, 185–198.
Hemsworth, P.H., Barnett, J.L., Hansen, C., 1987. The inﬂuence of inconsistent handling by humans on the behaviour,
growth and corticosteroids of young pigs. Appl. Anim. Behav. Sci. 17, 245–252.
Hemsworth, P.H., Barnett, J.L., Hansen, C., 1986a. The inﬂuence of handling by humans on the behaviour, reproduction
and corticosteroids of male and female pigs. Appl. Anim. Behav. Sci. 15, 303–314.
Hemsworth, P.H., Barnett, J.L., Hansen, C., Winﬁeld, C.G., 1986b. Effects of social environment on welfare status and
behaviour of female pigs: II. Effects of space allowance. Appl. Anim. Behav. Sci. 16, 259–267.
Hemsworth, P.H., Coleman, G.J., Barnett, J.L., Jones, R.B., 1994. Behavioural-responses to humans and the productivity
of commercial broiler-chickens. Appl. Anim. Behav. Sci. 41, 101–114.
Hemsworth, P.H., Gonyou, H.W., Dzuik, P.J., 1986c. Human communication with pigs: the behavioural response of pigs
to speciﬁc human signals. Appl. Anim. Behav. Sci. 15, 45–54.
Hemsworth, P.H., Pedersen, V., Cox, M., Cronin, G.M., Coleman, G.J., 1999. A note on the relationship between the
behavioural response of lactating sows to humans and the survival of their piglets. Appl. Anim. Behav. Sci. 65, 43–52.
Henderson, J.V., Waran, N.K., 2001. Reducing equine stereotypies using an Equiball
. Anim. Welfare 10, 73–80.
Hendrie, C.A., Neill, J.C., 1991. Exposure to the calls of predators of mice activates defensive mechanisms and inhibits
consumatory behavior in an inbred mouse strain. Neurosci. Biobehav. Rev. 15, 479–482.
Henkin, R.I., Knigge, C.M., 1963. The effects of sound on the hypothalamic-pituitary-adrenal axis. Am. J. Physiol. 204,
Henning, C.W., Dunlap, W.P., 1978. Tonic immobility in Anolis carolinensis: effects of time and conditions of captivity.
Behav. Biol. 23, 75–86.
Herbers, J.M., 1981. Time resources and laziness in animals. Oecologia 49, 252–262.
Herbert, M., Sluckin, W., 1969. Acquisition of colour preferences by chicks at different temperatures. Anim. Behav. 17,
Herskin, M.S., Jensen, K.H., 2000. Effects of different degrees of social isolation on the behaviour of weaned piglets kept
for experimental purposes. Anim. Welfare 9, 237–249.
Hester, P.Y., 1994. The role of the environment and management on leg abnormalities in meat type fowl. Poult. Sci. 73,
Hetts, S., Clark, J.D., Calpin, J.P., Arnold, C.E., Mateo, J.M., 1992. Inﬂuence of housing conditions on beagle behavior.
Appl. Anim. Behav. Sci. 34, 137–155.
Hillmann, E., Mayer, C., Schon, P.C., Puppe, B., Schrader, L., 2004b. Vocalisation of domestic pigs (Sus scrofa domestica)
as an indicator for their adaptation towards ambient temperatures. Appl. Anim. Behav. Sci. 89, 195–206.
Hillman, E., Mayer, C., Schroder, L., 2004a. Lying behavior and adrenocortical response as indicators of the thermal
tolerance of pigs of different weights. Anim. Welfare 13, 329–335.
Holm, L., Jensen, M.B., Jeppesen, L.L., 2002. Calves’ motivation for access to two different types of social contact
measured by operant conditioning. Appl. Anim. Behav. Sci. 79, 175–194.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 293
Author's personal copy
Horton, G.M.J., Malinowski, K., Burgher, C.C., Palatini, D.D., 1991. The effect of space allowance and sex on blood
catecholamines and cortisol, feed consumption, and average daily weight gain in growing lambs. Appl. Anim. Behav.
Sci. 32, 197–204.
Hosey, G.R., 2005. How does the zoo environment affect the behaviour of captive primates? Appl. Anim. Behav. Sci. 90,
Hosey, G.R., Druck, P.L., 1987. The inﬂuence of zoo visitors on the behaviour of captive primates. Appl. Anim. Behav.
Sci. 18, 19–29.
Hubrecht, R.C., Serpell, J.A., Poole, T.B., 1992. Correlates of pen size and housing conditions on the behaviour of
kenneled dogs. Appl. Anim. Behav. Sci. 34, 365–383.
Hughes, B.O., Duncan, I.J.H., 1988. Behavioral needs: can they be explained in terms of motivational models? Appl.
Anim. Behav. Sci. 19, 352–355.
Hughes, R.N., 1969. Social facilitation of locomotion and exploration in rats. Brit. J. Psychol. 60, 385–388.
Hultgren, J., 2001. Effects of two stall ﬂooring systems on the behaviour of tied dairy cows. Appl. Anim. Behav. Sci. 73,
Hutchins, M., Hancocks, D., Crockett, C., 1984. Naturalistic solutions to behavioral problems of captive animals. Der
Zoologische Garten 54, 28–42.
Huynh, T.T.T., Aarnink, A.J.A., Spoolder, H.A.M., Verstegen, M.W.A., Kemp, B., 2004. Effects of ﬂoor cooling during
high ambient temperatures on the lying behavior and productivity of growing ﬁnishing pigs. Trans. ASAE 47,
Ikeda, M., Dagara, M., Inoue, S., 2000. Continuous exposure to dim illumination uncouples temporal patterns of sleep,
body temperature, locomotion and drinking behaviour in the rat. Neurosci. Lett. 279, 185–189.
Inglis, I.R., Ferguson, N.J.K., 1986. Starlings search for food rather than eat freely available, identical food. Anim. Behav.
Inglis, I.R., Shepherd, D.S., 1994. Rats work for food they then reject: support for the information-primacy approach to
learned industriousness. Ethology 98, 154–164.
International Primatological Society, 1989. International guidelines for the acquisition, care, and breeding of nonhuman
primates. Codes of practice 1–3. Primate Report, 35, 3–29.
Issac, W., De Vito, J.L., 1958. Effect of sensory stimulation on the activity of normal and prefrontal-lobectomized
monkeys. J. Compar. Physiol. Psychol. 51, 172–174.
Jachner, A., 1995. Changes in feeding-behavior of bleak (Alburnus alburnus L.) in response to visual and chemical stimuli
from predators. Archiv Fur Hydrobiologie 133, 305–314.
Jensen, P., Toates, F.M., 1993. Who needs ‘‘behavioural needs’’? Motivational aspects of the needs of animals. Appl.
Anim. Behav. Sci. 37, 161–181.
Jildge, B., 1991. The rabbit—a diurnal or a nocturnal animal. J. Exp. Anim. Sci. 34, 170–183.
Johnson, S.R., Patterson-Kane, E.G., Niel, L., 2004. Foraging enrichment for laboratory rats. Anim. Welfare 13, 305–312.
Johnston, R.E., 1992. Vomeronasal and or olfactory mediation of ultrasonic calling and scent marking by female golden
hamsters. Physiol. Behav. 51, 437–448.
Jones, R.B., 1985. Fear responses of individually caged laying hens as a function of cage level and aisle. Appl. Anim.
Behav. Sci. 14, 63–74.
Jones, R.B., 1987. Fearfulness of caged laying hens: the effects of cage level and type of rooﬁng. Appl. Anim. Behav. Sci.
Jones, R.B., Facchin, L., McCorquodale, C., 2002. Social dispersal by domestic chicks in a novel environment: reassuring
properties of a familiar odourant. Anim. Behav. 63, 659–666.
Kanitz, E., Tuchscherer, M., Puppe, B., Tuchscherer, A., Stabenow, B., 2004. Consequences of repeated early isolation in
domestic piglets (Sus scrofa) on their behavioural, neuroendocrine, and immunological responses. Brain Behav.
Immun. 18, 35–45.
Kastelein, R.A., Wiepkema, P.R., 1989. A digging trough as occupational therapy for Paciﬁc Walruses (Odobenus
rosmarus divergens) in human care. Aquat. Mammal 15, 9–17.
Kaufman, B.M., Pouliot, A.L., Tiefenbacher, S., Novak, M.A., 2004. Short and long-term effects of a substantial change in
cage size on individually housed, adult male rhesus monkeys (Macaca mulatta). Appl. Anim. Behav. Sci. 88, 319–330.
Kemble, E.D., Bolwahnn, B.L., 1997. Immediate and long-term effects of novel odors on risk assessment in mice. Physiol.
Behav. 61, 543–549.
Kimchi, T., Terkel, J., 2002. Seeing and not seeing. Curr. Opin. Neurobiol. 12, 728–734.
Kleiman, D.G., 1994. Mammalian sociobiology and zoo breeding programs. Zoo Biol. 13, 423–432.
Konkle, A.T.M., Baker, S.L., Kentner, A.C., Barbagallo, L.S-M., Merali, Z., Bielajew, C., 2003. Evaluation of the effects
of chronic mild stressors on hedonic and physiological responses: sex and strain compared. Brain Res. 992, 227–238.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302294
Author's personal copy
Korte, S.M., 2001. Corticosteroids in relation to fear, anxiety, and psychopathology. Neurosci. Biobehav. Rev. 25,
Krebs, H., Weyers, P., Macht, M., Weijers, H.-G., Janke, W., 1997. Scanning behavior of rats eating under stressful noise.
Physiol. Behav. 62, 151–154.
Krohn, T.C., Hansen, A.K., Dragsted, N., 2003. Telemetry as a method for measuring the impact of housing conditions on
rats’ welfare. Anim. Welfare 12, 53–62.
Kuehn, B.M., 2002. Zoo animal welfare boosted by environmental enrichment, positive reinforcement training. J. Am.
Vet. Med. Assoc. 221, 1532.
Kyngdon, D.J., Minot, E.O., Stafford, K.J., 2003. Behavioural responses of captive common dolphins Delphinus delphis
to a ‘‘swim-with-dolphin’’ programme. Appl. Anim. Behav. Sci. 81, 163–170.
Lambeth, S.P., Bloomsmith, M.A., Alford, P.L., 1997. Effects of human activity on chimpanzee wounding. Zoo Biol. 16,
Lammers, G.J., Schouten, G.P., 1985. Effect of pen size on the development of agonistic behaviour in piglets. Netherl. J.
Agric. Sci. 33, 305–307.
Lammers, M.O., Au, W.W.L., Herzing, D.L., 2003. The broadband social acoustic signaling behavior of spinner and
spotted dolphins. J. Acoust. Soc. Am. 114, 1629–1639.
Langman, V.A., Rowe, M., Forthman, D., Whitton, N., Langman, T., Roberts, T., Huston, K., Boling, C., Maloney, D.,
1996. Thermal assessment of zoological exhibits 1: sea lion enclosure at the Audubon zoo. Zoo Biol. 15, 403–411.
Lefcort, H., Thomson, S.M., Cowles, E.E., Harowicz, H.L., Livaudais, B.M., Robers, W.E., Ettinger, W.F., 1999.
Ramiﬁcations of predator avoidance: predator and heavy-metal-mediated competition between tadpoles and snails.
Ecol. Appl. 9, 1477–1489.
Levy, D.M., 1944. On the problem of movement restraintics, stereotyped movements, hyperactivity. Am. J. Orthop-
sychiat. 14, 644–671.
Lindburg, D.G., 1998. Enrichment through provisioning. In: Shepherdson, S.J., Mellen, J.D., Hutchins, M. (Eds.),
Second Nature: Environmental Enrichment for Captive Animals. Smithsonian Institution Press, Washington, DC,
Lindsey, S.L., Bennett, C.L., Fried, J.J., Prichard, J.K., 1993. Functional analysis of infrasound in the okapi (Okapia
johnstoni): mother–infant communication. Am. Assoc. Zool. Parks Aquariums Ann. Conf. Proc. 299–305.
Line, S.W., Markowitz, H., Morgan, K.N., Strong, S., 1991. Effects of cage size and environmental enrichment on
behavioral and physiological responses of rhesus macaques to the stress of daily events. In: Novak, M.A., Petto, A.J.
(Eds.), Through the Looking Glass: Issues of Psychological Well-Being in Captive Non-human Primates. American
Psychological Association, Washington, DC, pp. 160–179.
Line, S.W., Morgan, K.N., Markowitz, H., Strong, S., 1990. Increased cage size does not alter heart rate or behavior in
female rhesus monkeys. Am. J. Primatol. 20, 107–113.
Line, S.W., Morgan, K.N., Markowitz, H., Strong, S., 1989. Heart rate and activity of rhesus monkeys in response to
routine events. Lab. Primate Newslett. 28, 9–12.
Lipman, E.A., Grassi, J.R., 1942. Comparative auditory sensitivity of man and dog. Am. J. Psychol. 55, 84–89.
Lutz, C.K., Novak, M.A., 1995. Use of foraging racks and shavings as enrichment tools for groups of rhesus monkeys
(Macaca mulatta). Zoo Biol. 14, 463–474.
Mack, A.L., Jones, J., 2003. Low-frequency vocalizations by cassowaries (Casuarius spp.). Anim. Behav. 120, 1062–
Maddocks, S.A., Bennett, A.T.D., Hunt, S., Cuthill, I.C., 2002a. Context-dependent visual preferences in starlings and
blue tits: mate choice and light environment. Anim. Behav. 63, 69–75.
Maddocks, S.A., Cuthill, I.C., Goldsmith, A.R., Sherwin, C.M., 2001. Behavioural and physiological effects of absence of
ultraviolet wavelengths for domestic chicks. Anim. Behav. 62, 1013–1019.
Maddocks, S.A., Goldsmith, R., Cuthill, I.C., 2002b. Behavioural and physiological effects of absence of ultraviolet
wavelengths on European starlings Sturnus vulgaris. J. Avian Biol. 33, 103–106.
Maier, J.A.K., Murphy, S.M., White, R.G., Smith, M.D., 1998. Responses of caribou to overﬂights by low-altitude jet
aircraft. J. Wildlife Manage. 62, 752–766.
Maier, S.F., Seligman, M.E., 1976. Learned helplessness: theory and evidence. J. Exp. Psychol.: Gen. 105, 3–46.
Malinow, M.R., Hill, J.D., Ochsner, A.J., 1974. Heart rate in caged rhesus monkeys (Macaca mulatta). Lab. Anim. Sci. 24,
Mallapur, A., Chellam, R., 2002. Environmental inﬂuences on stereotypy and the activity budget of Indian leopards
(Panthera pardus) in four zoos in Southern India. Zoo Biol. 21, 585–595.
Mann, D.A., Higgs, D.M., Tavolga, W.N., Souza, M.J., Popper, A.N., 2001. Ultrasound detection by clupeiform ﬁshes. J.
Acoust. Soc. Am. 109, 3048–3054.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 295
Author's personal copy
Manninen, E., de Passille
´, A.M., Rushen, J., Norring, M., Saloniemi, H., 2002. Preferences of dairy cows kept in unheated
buildings for different kinds of cubicle ﬂooring. Appl. Anim. Behav. Sci. 75, 281–292.
Manser, C.E., Broom, D.M., Overend, P., Morris, T.H., 1998. Investigations into the preferences of laboratory rats for
nest-boxes and nesting materials. Lab. Anim. 32, 23–35.
Manser, C.E., Morris, T.H., Broom, D.M., 1995. An investigation into the effects of solid or grid cage ﬂooring on the
welfare of laboratory rats. Lab. Anim. 29, 353–363.
Mansour, A.A.H., Zakaria, A.-H., Fraser, A.F., 2000. Effect of enclosure quality on reactivity and welfare of captive
Soemmerring’s gazelle (Gazella soemmerringii). J. Appl. Anim. Welfare Sci. 3, 335–343.
Marai, I.F.M., Rashwan, A.A., 2004. Rabbits’ behavioural response to climatic and managerial conditions: a review. Arch.
Anim. Breed. 47, 469–482.
Marashi, V., Barnekow, A., Ossendorf, E., Sachser, N., 2003. Effects of different forms of environmental enrichment on
behavioral, endocrinological, and immunological parameters in mice. Hormone Behav. 43, 281–292.
Markowitz, H., 1975. Analysis and control of behavior in the zoo. In: National Academy of Sciences, Research in Zoos
and Aquariums. Washington, D.C., pp. 77–90.
Markowitz, H., 1982. Behavioral Enrichment in the Zoo. Van Nostrand Reinhold, New York, NY.
Markowitz, H., 1997. The conservation of species-typical behaviors. Zoo Biol. 16, 1–2.
Markowitz, H., Aday, C., Gavazzi, A., 1995. Effectiveness of acoustic prey for a captive African leopard (Panthera
pardus). Zoo Biol. 14, 371–379.
Markowitz, H., Spinelli, J.S., 1986. Environmental engineering for primates. In: Benirschke, K. (Ed.), Primates: The
Road to Self-Sustaining Populations. Springer–Verlag, New York, NY, pp. 489–498.
Marriner, L.M., Drickamer, L.C., 1994. Factors inﬂuencing stereotyped behavior of primates in a zoo. Zoo Biol. 13,
Martrenchar, A., 1999. Animal welfare and intensive production of turkey broilers. World Poult. Sci. J. 55,
Mason, G.J., 1993. Forms of stereotypic behaviour. In: Lawrence, A.B., Rushen, J. (Eds.), Stereotypic Animal Behaviour:
Fundamentals and Applications to Welfare. CAB International, Oxon, UK, pp. 7–40.
Mason, M.J., Narins, P.M., 2002. Seismic sensitivity in the desert golden mole (Eremitalpa granti): a review. J. Compar.
Psychol. 116, 158–163.
Mason, W.A., 1991b. Effects of social interaction on well-being: developmental aspects. Lab. Anim. Sci. 41, 323–328.
Mason, W.A., Fitz-Gerald, F.L., 1962. Intellectual performance of an isolation-reared rhesus monkey. Percept. Motor
Skills 15, 594.
McComb, K., Reby, D., Baker, L., Moss, C., Sayialel, S., 2003. Long-distance communication of acoustic cues to social
identity in African elephants. Anim. Behav. 65, 317–329.
McEwen, B.S., 2000. The neurobiology of stress: from serendipity to clinical relevance. Brain Res. 886, 172–189.
McGlone, J.J., Curtis, S.E., 1985. Behavior and performance of weanling pigs in pens equipped with hide areas. J. Anim.
Sci. 60, 20–24.
McGreevy, P.D., Cripps, P.J., French, N.P., Green, L.E., Nicol, C.J., 1995. Management factors associated with stereotypic
and redirected behaviour in the thoroughbred horse. Equine Vet. J. 27, 86–91.
McLean, I.G., Schmitt, N.T., Jarman, P.J., Duncan, C., Wynne, C.D.L., 2000. Learning for life: training marsupials to
recognize introduced predators. Behaviour 137, 1361–1376.
McPhee, M.E., 2002. Intact carcasses as enrichment for large felids: effects on on- and off exhibit behaviors. Zoo Biol. 21,
Mench, J., 1998. Why it is important to understand animal behavior. ILAR On-line, 39, Retrieved on 8/25/05 from http://
Menzel, E.W., 1991. Chimpanzee (Pan troglodytes): problem-solving versus the bird-in-the hand, least-effort strategy.
Primates 32, 497–508.
Meyer-Holzapfel, M., 1968. Abnormal behavior in zoo animals. In: Fox, M.W. (Ed.), Abnormal Behavior in Animals.
Saunders, Philadelphia, PA, pp. 476–502.
Michelson, D., Licinio, J., Gold, P.W., 1995. Mediation of the stress response by the hypothalamic-pituitary-adrenal axis.
In: Friedman, M.J., Charney, D.S., Deutch, A.Y. (Eds.), Neurobiological and Clinical Consequences of Stress: From
Normal Adaptation to PTSD. Lippincott-Raven Publishers, Philadelphia, PA, pp. 225–238.
Miller, P.E., Murphy, C.J., 1995. Vision in dogs. J. Am. Vet. Med. Assoc. 207, 1623–1634.
Milligan, S.R., Sales, G.D., Khirnykh, K., 1993. Sound levels in rooms housing laboratory animal: an uncontrolled daily
variable. Physiol. Behav. 53, 1067–1076.
Mineka, S., Kelly, K.A., 1989. The relationship between anxiety, lack of control and loss of control. In: Steptoe,
A., Appels, E. (Eds.), Stress, Personal Control, and Health. Oxford University Press, Oxford, GB, pp. 163–191.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302296
Author's personal copy
Mineur, Y.S., Prasol, D.J., Belzung, C., Crusio, W.E., 2003. Agonistic behavior and unpredictable chronic mild stress in
mice. Behav. Genet. 33, 513–519.
Mitchell, G., Herring, G., Obradovich, S., Tromborg, C.T., Dowd, B., Neville, L.E., Field, L., 1991. Effects of visitors and
cage changes on the behavior of mangabeys. Zoo Biol. 10, 417–423.
Mitchell, G., Herring, F., Tromborg, C.T., Dowd, B., Steiner, S., Obradovich, S., 1992a. Targets of aggressive facial
displays by golden bellied mangabeys (Cercocebus galeritus chrysogaster) at the Sacramento zoo. Appl. Anim.
Behav. Sci. 33, 249–259.
Mitchell, G., Tromborg, C.T., Kaufman, J., Bargabus, S., Simoni, R., Geissler, V., 1992b. More on the ‘‘inﬂuence’’ of zoo
visitors on the behaviour of captive primates. Appl. Anim. Behav. Sci. 35, 189–198.
Mizisin, A.P., Kalichman, M.W., Garrett, R.S., Dines, K.C., 1998. Tactile hyperesthesia, altered epidermal innervation
and plantar nerve injury in the hindfeet of rats housed on wire grates. Brain Res. 788, 13–19.
Moinard, C., Lewis, P.D., Perry, G.C., Sherwin, C.M., 2001. The effects of light intensity and light source on injuries due
to pecking of male domestic turkeys (Meleagris gallopavo). Anim. Welfare 10, 131–139.
Moodie, E.M., Chamove, A.S., 1990. Brief threatening events beneﬁcial for captive tamarins. Zoo Biol. 9, 275–286.
Moore, I.T., Jessop, T.S., 2003. Stress, reproduction, and adrenocortical modulation in amphibians and reptiles. Hormone
Behav. 43, 39–47.
Morgan, K.N., Milton, M.M., Brederson, J.D., 1999. Prenatal stress affects performance in the Morris water maze. In:
Poster presented at the Boston Area Neuroscience Group Annual Meeting, Boston, MA, February.
Morgan, K.N., Mondesir, F.L., Buell, K., Guy, P., Carmella, V., Hunt, C., Pizarro, S., 2002. Changes in chimp behavior,
visitor behavior, and visitor attitude with a change in exhibit. In: Paper presented at the Animal Behaviour Society
Annual Meeting, Bloomington, IN, June.
Morgan, K.N., Schwartzman, I.N., Ward, K.A., 1997. Social facilitation of diet preference in prenatally stressed rats: a
preliminary report. In: Poster presented at the International Society for Developmental Psychobiology, New Orleans,
Morgan, K.N., Thayer, J.E., 1997. Prenatal stress affects emotional responses to an escape task. In: Poster presented at the
American Psychological Society, Biology and Behavior Symposium, Washington, DC, May.
Morris, D., 1964. The responses of animals to a restricted environment. Symp. Zool. Soc. Lond. 13, 99–118.
Napolitano, F., de Rosa, G., Grasso, F., Pacelli, C., Bordi, A., 2004. Inﬂuence of space allowances on the welfare of
weaned buffalo (Bubalus bubalis) calves. Livestock Prod. Sci. 86, 117–124.
National Research Council, 1996. Guide for the Care and Use of Laboratory Animal, 7th ed. National Academy Press,
Newberry, R.C., Shackleton, D.M., 1997. Use of visual cover by domestic fowl: a Venetian blind effect? Anim. Behav. 54,
Nishio, H., Kasuga, S., Ushijima, M., Harada, Y., 2001. Prenatal stress and postnatal development of neonatal rats:
sex-dependent effects on emotional behavior and learning ability of neonatal rats. Int. J. Develop. Neurosci. 19,
Nogueira, S.S.C., Bernadi, L.G., Nogueira, S.L.G., 2004. A note on comparative enclosure facility usage by wild and
captive-born capybaras (Hydrochoerus hydrochaeris). Appl. Anim. Behav. Sci. 89, 139–143.
Novak, M.A., Kinsey, J.H., Jorgensen, M.J., Hazen, T.J., 1998. Effects of puzzle feeders on pathological behavior in
individually housed rhesus monkeys. Am. J. Primatol. 46, 213–227.
Nuboer, J.F.W., Coemans, M.A.J.M., Vos, J.J., 1992. Artiﬁcial lighting in poultry houses: do hens perceive the modulation
of ﬂuorescent lamps as ﬂicker? Brit. Poult. Sci. 33, 122–123.
Ogden, J.J., Lindburg, D.G., Maple, T.L., 1994. A preliminary study of the effects of ecologically relevant sounds on the
behaviour of captive lowland gorillas. Appl. Anim. Behav. Sci. 39, 163–176.
Olsen, A.W., Simonsen, H.B., Dybkjaer, L., 2002. Effect of access to roughage and shelter on selected behavioural
indicators of welfare in pigs housed in a complex environment. Anim. Welfare 11, 75–87.
O’Neill, P., 1989. A room with a view for captive primates: issues, goals, related research and strategies. In: Segal, E.F.
(Ed.), Housing, Care, and Psychological Wellbeing of Captive and Laboratory Primates. Noyes Publications, Park
Ridge, NJ, pp. 135–160.
Overmeier, J.B., 2002. On learned helplessness. Integr. Physiol. Behav. Sci. 37, 4–8.
Owen, M.A., Swaisgood, R.R., Czekela, N.M., Steinman, K., Lindburg, D.G., 2004. Monitoring stress in captive giant
pandas (Ailuropoda melanoleuca): behavioral and hormonal responses to ambient noise. Zoo Biol. 23, 147–164.
Patterson-Kane, E.G., 2003. Shelter enrichment for rats. Contemp. Topics Lab. Anim. Sci. 42, 46–48.
Patterson-Kane, E.G., Hunt, M., Harper, D., 2002. Rats demand social contact. Anim. Welfare 11, 327–332.
Paulk, H.H., Dienske, H., Ribbens, L.G., 1977. Abnormal behavior in relation to cage size in rhesus monkeys. J. Abnormal
Psychol. 86, 87–92.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 297
Author's personal copy
Pearce, G.P., Patterson, A.M., 1993. The effect of space restriction and provision of toys during rearing on the behavior,
productivity, and physiology of male pigs. Appl. Anim. Behav. Sci. 36, 11–28.
Pearson, J., 2002. On a roll: novel objects and scent enrichment for Asiatic lions. Shape Enrich. 11, 7–10.
Pepperberg, I.M., 2004. Cognitive and communicative capacities of Grey parrots—implications for the enrichment of
many species. Anim. Welfare 13 (Suppl.), S203–S208.
Perkins, L.A., 1992. Variables that inﬂuence the activity of captive orangutans. Zoo Biol. 11, 177–186.
Pern, S.M., Bennett, A.T.D., Cuthill, I.C., 2003. The role of ultraviolet-A reﬂectance and ultraviolet-A-induced
ﬂuorescence in budgerigar mate choice. Ethology 109, 961–970.
Perrot-Sinal, T.S., Ossenkopp, K.P., Kavaliers, M., 1999. Effects of repeated exposure to fox odor on locomotor activity
levels and spatial movement patterns in breeding male and female meadow voles (Microtus pennsylvanicus). J. Chem.
Ecol. 25, 1567–1584.
Perrot-Sinal, T., Petersen, K., 1997. Exposure to predator odor reduces locomotor activity levels in adult male rats: lack of
effect of hippocampal lesion. J. Chem. Ecol. 23, 2175–2186.
Peterson, E.A., 1980. Noise and laboratory animal. Lab. Anim. Sci. 30, 422–439.
Pfaff, J., Stecker, M., 1976. Loudness level and frequency contect of noise in the animal house. Lab. Anim. 10, 111–117.
Phillips, P.A., Fraser, D., Pawluczuk, B., 2000. Floor temperature preference of sows at farrowing. Appl. Anim. Behav.
Sci. 67, 59–65.
Pollard, J.C., Littlejohn, R.P., 1994. Behavioural effects of light conditions on red deer in a holding pen. Appl. Anim.
Behav. Sci. 41, 127–134.
Poltyrev, T., Keshet, G.I., Kay, G., Weinstock, M., 1996. Role of experimental conditions in determining differences in
exploratory behavior of prenatally stressed rats. Develop. Psychobiol. 29, 453–462.
Price, E.O., 1984. Behavioral aspects of domestication. Quarter. Rev. Biol. 59, 1–32.
Pytte, C.L., Ficken, M.S., Moiseff, A., 2004. Ultrasonic singing by the blue-throated hummingbird: a comparison between
production and perception. J. Compar. Physiol. 190, 665–673.
Quine, D.B., 1979. Infrasound detection and frequency discrimination by the homing pigeon. Dissert. Abstr. Int. 40, 2492.
Rabin, L.A., 2003. Maintaining behavioural diversity in captivity for conservation: natural behaviour management. Anim.
Welfare 12, 85–94.
Rao, G.N., 2001. Light intensity-associated eye lesions of Fischer-334 rats in long-term studies. Toxicol. Pathol. 19, 148–
Ratnasabapathi, D., Burns, J., Souchek, R., 1992. Effects of temperature and prior residence on territorial aggression in the
convict cichlid Cichlastoma nigrofasciatum. Aggress. Behav. 18, 365–372.
Rees, P.A., 2004. Low environmental temperature causes an increase in stereotypic behaviour in captive Asian elephants
(Elephas maximus). J. Thermal Biol. 29, 37–43.
Reinhardt, V., 1994. Caged rhesus macaques voluntarily work for ordinary food. Primates 35, 95–98.
Reinhardt, V., Reinhardt, A., 2000. The lower row monkey cage: an overlooked variable in biomedical research. J. Appl.
Anim. Welfare Sci. 3, 141–149.
Reinhardt, V., Rossell, M., 2001. Self-biting in caged macaques: cause, effect, and treatment. J. Appl. Anim. Welfare Sci.
Rickards, S.L., Job, R.F.S., Boakes, R.A., 1997. Effects of acute shock on body weight are mediated by changes in food
intake. Anim. Learn. Behav. 25, 437–445.
Robinson, I., Dowdall, R., Meert, T.F., 2004. Development of neuropathic pain is affected by bedding texture in two
models of peripheral nerve injury in rats. Neurosci. Lett. 368, 107–111.
Rutherford, K.M.D., Haskell, M.J., Glasbey, C., Jones, R.B., Lawrence, A.B., 2004. Fractal analysis of animal behaviour
as an indicator of animal welfare. Anim. Welfare 13 (Suppl.), S99–S103.
Saibaba, R., Sales, G.D., Stodulski, G., Hau, J., 1996. Behaviour of rats in their home cages: daytime variations and effects
of routine husbandry procedures analyzed by time sampling techniques. Lab. Anim. 30, 13–21.
Saito, T.R., Motomura, N., Taniguchi, K., Hokao, R., Arkin, A., Takahashi, K.W., Sato, N.L., 1996. Effect of cage size on
sexual behavior pattern in male rats. Contemp. Topics Lab. Anim. Sci. 35, 80–82.
Sales, G.D., Milligan, S.R., Khirnykh, K., 1999. Sources of sound in the laboratory animal environment: a survey of the
sounds produced by procedures and equipment. Anim. Welfare 8, 97–115.
Sales, G.D., Wilson, K., Spencer, K.E.V., Milligan, S.R., 1988. Environmental ultrasound in laboratories and animal
houses: a possible cause for concern in the welfare and use of laboratory animal. Lab. Anim. 22, 369–375.
Salvetti, F., Chelli, B., Gesi, M., Pellegrini, A., Giannaccini, G., Lucacchini, A., Martini, C., 2000. Effect of noise
exposure on rat cardiac peripheral benzodiazapine receptors. Life Sci. 66, 1165–1175.
Sambrook, T.D., Buchanan-Smith, H.M., 1997. Control and complexity in novel object enrichment. Anim. Welfare 6,
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302298
Author's personal copy
Sanchez, C., 2003. Stress-induced vocalizationin adult animals: a validmodel of anxiety? Eur. J.Pharmacol. 463, 133–143.
Sandberg, R., Muth, R., Pfabe, C., Wiltschko, R., Wiltschko, W., 1999. Staying in plastic containers interferes with the
orientation of clock-shifted homing pigeons. Animal Behav. 57, 695–704.
Sanford, A.N., Clark, S.E., Talham, G., Sidelsky, M.G., Cofﬁn, S.E., 2002. Inﬂuence of bedding type on mucosal immune
responses. Compar. Med. 52, 429–432.
Sapolsky, R., 1996. Stress, glucocorticoids, and damage to the nervous system: the current state of confusion. Stress 1,
Sapolsky, R., Armanini, M., Packan, D., Tombaugh, G., 1987. Stress and glucocorticoids in aging. Endocrinol. Metab.
Clin. North Am. 16, 965–980.
Sapolsky, R., Plotsky, P.M., 1990. Hypercortisolism and its possible neural bases. Biol. Psychiat. 27, 937–952.
Sapolsky, R.M., Uno, H., Rebert, C.S., Finch, C.E., 1990. Hippocampal damage asociated with prolonged glucocorticoid
exposure in primates. J. Neurosci. 10, 2897–2902.
¨fer, H.J., Schmidt, U., Brzoska, J., Hubl, L., 1978. Temperature dependence of visual fusion frequency in Rana
lessonae Cam., Bufo bufo L. and Bombina bombina (L.) (Amphibia). Behav. Process. 3, 259–264.
Schlingmann, F., de Rijk, S.H.L.M., Pereboom, W.J., Remie, R., 1994. ‘‘Avoidance’’ as a behavioural parameter in the
determination of distress among albino and pigmented rats at various light intensities. Anim. Technol. 44, 87–96.
Schneider, M.L., Moore, C.F., Kramer, G.W., Roberts, A.D., DeJesus, O.T., 2002. The impact of prenatal stress, fetal alcohol
exposure, or both on development: perspectives from a primate model. Psychoneuroendocrinology 27, 285–298.
Schouten, W.G.P., Wiegant, V.M., 1997. Individual responses to acute and chronic stress in pigs. Acta Physiol. Scand. 161,
Schultz, E.F., Tapp, J.T., 1973. Olfactory control of behavior in rodents. Psychol. Bull. 79, 21–44.
Seligman, M.E., Beagley, G., 1975. Learned helplessness in the rat. J. Compar. Physiol. Psychol. 88, 534–541.
Seligman, M.E., Maier, S.F., Geer, J.H., 1968. Alleviation of learned helplessness in the dog. J. Abnormal Psychol. 73,
Selye, H., 1976. The Stress of Life. McGraw-Hill Book Company, New York, NY.
Shah, R., Shine, R., Hudson, S., Kearney, M., 2004. Experimental analysis of retreat-site selection by thick-tailed geckos
Nephrurus milii. Austr. Ecol. 29, 547–552.
Shah, B., Shine, R., Hudson, S., Kearney, M., 2003. Sociality in lizards: why do thick-tailed\geckos (Nephrurus milii)
aggregate? Behaviour 140, 1039–1052.
Shair, H.N., Brunelli, S.A., Masmela, J.R., Boone, E., Hofer, M.A., 2003. Social, thermal, and temporal inﬂuences
on isolation-induced and maternally potentiated ultrasonic vocalization of rat pups. Develop. Psychobiol. 42, 206–222.
Shapiro, S.J., Stavisky, R., Hook, M., 2000. The lower row cage may be dark, but behavior does not appear to be affected.
Lab. Primate Newslett. 39, 4–6.
Sharp, J., Zammit, T., Azar, T., Lawson, D., 2003a. Stress-like responses to common procedures in individually and group-
housed female rats. Contemp. Topics Lab. Anim. Sci. 42, 9–18.
Sharp, J., Zammit, T., Azar, T., Lawson, D., 2003b. Are ‘‘bystander’’ female Sprague-Dawley rats affected by
experimental procedure? Contemp. Topics Lab. Anim. Sci. 42, 19–27.
Shepherdson, D.J., Carlstead, K., Mellen, J.D., Reynolds, S., 1989. Auditory enrichment for Lar gibbons. Int. Zoo
Yearbook 28, 256–260.
Shepherdson, D.J., Carlstead, K., Mellen, J.D., Seidensticker, J., 1993. The inﬂuence of food presentation on the behavior
of small cats in conﬁned environments. Zoo Biol. 12, 203–216.
Shepherdson, D.J., Mellen, J.D., Hutchins, M. (Eds.), 1998. Second Nature: Environmental Enrichment for Captive
Animals. Smithsonian Institution Press, Washington, DC.
Sherwin, C.M., Olsson, I.A.S., 2004. Housing conditions affect self-administration of anxiolytic by laboratory mice.
Anim. Welfare 13, 33–38.
Shyan, M.R., Merritt, D., Kohlmeier, N.M., Barton, K., Tenge, J., 2002. Effects of pool size on free-choice selections by
Atlantic bottlenosed dolphins at one zoo facility. J. Appl. Anim. Welfare Sci. 5, 215–225.
Slotnick, B., Schellinck, H., Brown, R., 2005. Olfaction. In: Whishaw, I.Q., Kolb, B. (Eds.), The Behavior of the
Laboratory Rat. Oxford University Press, New York, NY, pp. 90–104.
Smith, A., Lindburg, D.G., Vehrencamp, S., 1989. Effect of food preparation on feeding behavior of lion-tailed macaques.
Zoo Biol. 8, 57–65.
Smith, A.T., 1991. A review of the non-auditory effects of noise on health. Work Stress 5, 49–62.
Sneddon, I.A., Beattie, V.E., 1995. Improving the welfare of pigs. Irish J. Psychol. 16, 418–425.
Sobrian, S.K., Vaughn, V.T., Ashe, W.K., Markovic, B., Djuric, V., Jankovic, B.D., 1997. Gestational exposure to loud
noise alters the development and postnatal responsiveness of humoral and cellular components of the immune system
in offspring. Environ. Res. 73, 227–241.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 299
Author's personal copy
Sorensen, D.B., Ottesen, J.L., Hansen, A.K., 2004. Consequences of enhancing environmental complexity for laboratory
rodents: a review with emphasis on the rat. Anim. Welfare 13, 193–204.
Stoinski, T.A., Hoff, M.P., Lukas, K.E., Maple, T.L., 2001. A preliminary behavioral comparison of two captive all-male
gorilla groups. Zoo Biol. 20, 27–40.
Stoinski, T.A., Hoff, M.P., Maple, T.L., 2002. The effect of structural preferences, temperature, and social factors on
visibility in western lowland gorillas (Gorilla G-gorilla). Environ. Behav. 34, 493–507.
Stoskopf, M.K., 1983. The physiological effects of psychological stress. Zoo Biol. 2, 179–190.
Sumpter, C.E., Temple, W., Foster, T.M., 1999. The effects of differing response types andprice manipulations on demand
measures. J. Exp. Anal. Behav. 71, 329–354.
Swaid, H., 1991. Nocturnal variation of air surface-temperature gradients for typical urban and rural surfaces. Atmos.
Environ. Part B—Urban Atmos. 25, 333–341.
Swaisgood, R.R., Lindburg, D.G., Zhou, X.P., Owen, M.A., 2000. The effects of sex, reproductive condition and context
on discrimination of conspeciﬁc odours by giant pandas. Anim. Behav. 60, 227–237.
Swaisgood, R.R., White, A.M., Zhou, X.P., Zhang, H.M., Zhang, G.Q., Wei, R.P., Hare, V.J., Tepper, E.M., Lindburg,
D.G., 2001. A quantitative assessment of the efﬁcacy of an environmental enrichment programme for giant pandas.
Anim. Behav. 61, 447–457.
Szymanski, M.D., Bain, D.E., Kiehl, K., Pennington, S., Wong, S., Henry, K.R., 1999. Killer whale (Orcinus orca)
hearing: auditory brainstem response and behavioral audiograms. J. Acoust. Soc. Am. 106, 1134–1141.
Tarlow, E.M., Blumstein, D.T., 2007. Evaluating methods to quantify anthropogenic stressors on wild animals. Appl.
Anim. Behav. Sci. 102, 429–451.
Taylor, P.E., Coerse, N.C.A., Haskell, M., 2001. The effects of operant control over food and light on the behaviour of
domestic hens. Appl. Anim. Behav. Sci. 71, 319–333.
Thiessen, D.D., Graham, M., Perkins, J., Marcks, S., 1977. Temperature regulation and social grooming in the Mongolian
gerbil (Meriones unguiculatus). Behav. Neural Biol. 19, 279–288.
Thompson, V.D., 1989. Behavioral responses of 12 ungulate species in captivity to the presense of humans. Zoo Biol. 8,
Tilbrook, A.J., Turner, A.I., Clarke, I.J., 2002. Stress and reproduction: central mechanisms and sex differences in non-
rodent species. Stress 5, 83–100.
Townsend, P., 1997. Use of in-cage shelters by laboratory rats. Anim. Welfare 6, 95–103.
Tromborg, C.T., 1993. Behavioral effects of exposing captive cotton top tamarins to controlled auditory stimuli.
Unpublished Master’s Thesis, California State University, San Franscisco.
Tromborg, C.T., Coss, R.C., 1995. Denizens, decibels, and dens. In: Annual Proceedings of the American Association of
Zoos and Aquariums, Seattle, WA, pp. 521–528.
Tsigos, C., Chrousos, G.P., 1995. Stress, endocrine manifestations, and diseases. In: Cooper, C.L. (Ed.), Handbook of
Stress Medicine. CRC Press, Boca Raton, FL, (Chapter 3), pp. 61–65.
United States Department of Agriculture, 1991. Title 9, CFR (Code of Federal Register), Part 3: Animal Welfare,
Standards, Final Rule. Federal Register, 56, 6426–6505.
Vanbetteray, J.N.F., Vossen, J.M.H., Coenen, A.M.L., 1991. Behavioural characteristics of sleep in rats under different
light dark conditions. Physiol. Behav. 50, 79–82.
van der Meer, E., Van Loo, P.L.P., Baumans, V., 2004. Short-term effects of a disturbed light dark cycle and environmental
enrichment on aggression and stress-related parameters in male mice. Lab. Anim. 38, 376–383.
van der Tol, P.P., Metz, J.H., Noordhuizen-Stassen, E.N., Back, W., Braam, C.R., Weijs, W.A., 2005. Frictional forces
required for unrestrained locomotion in dairy cattle. J. Dairy Sci. 88, 615–624.
van de Weerd, H.A., vandenBroek, F.A.R., Baumans, F., 1996. Preference for different types of ﬂooring in two rat strains.
Appl. Anim. Behav. Sci. 46, 251–261.
van de Weerd, H.A., Van Loo, P.L.P., Van Zutphen, L.F.M., Koolhaas, J.M., Baumans, V., 1998. Preferences for nest boxes
as environmental enrichment for laboratory mice. Anim. Welfare 7, 11–25.
van Loo, P.L.P., Kruitwagen, C.L.J.J., Van Zutphen, L.F.M., Koolhaas, J.M., Baumans, V., 2000. Modulation of aggression
in male mice: inﬂuence of cage cleaning regime and scent marks. Anim. Welfare 9, 281–295.
van Rooijen, J., 1984. Impoverished environments and welfare. Appl. Anim. Behav. Sci. 12, 3–13.
van Rooijen, J., 1991. Predictability and boredom. Appl. Anim. Behav. Sci. 31, 283–287.
van Wagenberg, A.V., Aerts, J.M., Van Brecht, A., Vranken, E., Leroy, T., Berckmans, D., 2005. Climate control based on
temperature measurement in the animal-occupied zone of a pig room with ground channel ventilation. Trans. ASAE
Veasey, J.S., Waran, N.K., Young, R.J., 1996. On comparing the behaviour of zoo housed animals with wild conspeciﬁcs
as a welfare indicator, using the giraffe (Giraffa camelopardalis) as a model. Anim. Welfare 5, 139–153.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302300
Author's personal copy
Vickery, S., Mason, G., 2004. Stereotypic behavior in Asiatic black and Malayan sun bears. Zoo Biol. 23, 409–430.
Vieuille-Thomas, C., Signoret, J.P., 1992. Pheromonal transmission of an aversive experience in domestic pig. J. Chem.
Ecol. 18, 1551–1557.
Vinke, C.M., Eenkhoorn, N.C., Netto, W.J., Fermont, P.C.J., Spruijt, B.M., 2002. Stereotypic behaviour and tail biting in
farmed mink (Mustela vison) in a new housing system. Anim. Welfare 11, 231–245.
Vliet, K.A., 1989. Social displays of the American alligator (Alligator mississippiensis). Am. Zool. 29, 1019–1031.
von Muggenthaler, E., 1992. Infrasound from the Rhinocerotidae. In: Proceedings from the International Conference of
Rhinoceros Biology and Conservation. pp. 136–140.
von Muggenthaler, E., 2000. Low frequency and infrasonic vocalizations from tigers. In: Paper presented at the Acoustic
Society of America Conference, Newport Beach, CA, 6 December.
von Muggenthaler, E., Baes, C., Hill, D., Fulk, R., Lee, A., 1999. Infrasound and low frequency vocalizations from the
giraffe. Retrieved no. 8/25/05 from http://www.animalvoice.com/Giraffe.htm.
Vosburgh, K.M., Barbiers, R.B., Silkarskie, J.G., Ullrey, D.E., 1982. A soft versus hard diet and oral health in captive
timber wolves (Canis lupus). J. Zoo Anim. Med. 13, 104–107.
Vyas, A., Chattaji, S., 2004. Modulation of different states of anxiety-like behavior by chronic stress. Behav. Neurosci.
Waiblinger, E., Ko
¨nig, B., 2004. Reﬁnement of gerbil housing and husbandry in the laboratory. Anim. Welfare 13,
Waiblinger, S., Menke, C., Coleman, G., 2002. The relationship between attitudes, personal characteristics and
behaviour of stockpeople and subsequent behaviour and production of dairy cows. Appl. Anim. Behav. Sci. 79,
Waitt, C., Buchanan-Smith, H.M., 2001. What time is feeding? How delays and anticipation of feeding schedules affect
stump-tailed macaque behavior. Appl. Anim. Behav. Sci. 75, 75–85.
Waitt, C., Buchannan-Smith, H.M., Morris, K., 2002. The effects of caretaker-primate relationships on primates in the
laboratory. J. Appl. Anim. Welfare Sci. 5, 309–319.
Waldman, B., Bishop, P.J., 2004. Chemical communication in an archaic anuran amphibian. Behav. Ecol. 15, 88–93.
Wallace, R.A., 1979. Animal Behavior: Its Development, Ecology, and Evolution. Goodyear Publishing Company, Santa
Waples, K.A., Gales, N.J., 2002. Evaluating and minimizing social stress in the care of captive bottlenose dolphins
(Tursiops aduncus). Zoo Biol. 21, 5–26.
Ward, J.F., MacDonald, D.W., Doncaster, C.P., Mauget, C., 1996. Physiological response of the European hedgehog to
predator and nonpredator odor. Physiol. Behav. 60, 1469–1472.
Waser, P.M., Brown, C.H., 1986. Habitat acoustics and primate communication. Am. J. Primatol. 10, 135–154.
Waynert, D.F., Stookey, J.M., Schwartzkopf-Genswein, K.S., Watts, J.M., Waltz, C.S., 1999. The response of beef cattle to
noise during handling. Appl. Anim. Behav. Sci. 62, 27–42.
Weisenberger, M.E., Krausman, P.R., Wallace, M.C., DeYoung, D.W., Maughan, O.E., 1996. Effects of simulated jet
aircraft noises on hear rate and behavior of desert ungulates. J. Wildlife Manage. 60, 52–61.
Weiss, I.C., Pryce, C.R., Jongen-Relo, A.L., Nanz-Bahr, N.I., Feldon, J., 2004. Effect of social isolation on stress-related
behavioural and neuroendocrine state in the rat. Behav. Brain Res. 152, 279–295.
Wells, D.L., Egli, J.M., 2004. The inﬂuence of olfactory enrichment on the behaviour of captive black-footed cats, Felis
nigripes. Appl. Anim. Behav. Sci. 85, 107–119.
Wenker, C.J., Stich, H., Mu
¨ller, M., Lussi, A., 1999. A retrospective study of dental conditions of captive brown bears
(Ursus arctos spp.) compared with free-ranging Alaskan grizzlies (Ursus arctos horribilis). J. Zoo Wildlife Med. 30,
Widowski, T.M., Keeling, L.J., Duncan, I.J.H., 1992. The preferences of hens for compact ﬂuorescent over incandescent
lighting. Can. J. Anim. Sci. 72, 203–211.
Wiedenmayer, C., 1997. Causation of the ontogenetic development of stereotypic digging in gerbils. Anim. Behav. 53,
Wiegand, R.M., Gonyou, H.W., Curtis, S.E., 1994. Pen shape and size: effects on pig behavior and performance. Appl.
Anim. Behav. Sci. 39, 49–61.
Wilson, D.R., Hare, J.F., 2004. Ground squirrel uses ultrasonic alarms. Nature 430, 523.
Wilson, S.F., 1982. Environmental inﬂuences on the activity of captive apes. Zoo Biol. 1, 201–209.
Wolﬂe, T.L., 1989. Dog socialization. In: Animal Care and Use: Policy Issues in the 1990’s. NIH, OPRR, OACU
Conference, Bethesda, Maryland, pp. 43–45.
Wommack, J.C., Salinas, A., Melloni, R.H., Delville, Y., 2004. Behavioural and neuroendocrine adaptations to repeated
stress during puberty in male golden hamsters. J. Neuroendocrinol. 16, 767–775.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302 301
Author's personal copy
Wood, W., 1998. Interactions among environmental enrichment, viewing crowds, and zoo chimpanzees (Pan troglodytes).
Zoo Biol. 17, 211–230.
Wurbel, H., Chapman, R., Rutland, C., 1998. Effect of feed and enrichment on development of stereotypic wire-gnawing
in laboratory mice. Appl. Anim. Behav. Sci. 60, 69–81.
Zulkiﬂi, I., Rasedee, A., Syaadah, O.N., Norma, M.T.C., 1998. Daylength effects on stress and fear responses in broiler
chickens. Asian-Austr. J. Anim. Sci. 11, 751–754.
K.N. Morgan, C.T. Tromborg / Applied Animal Behaviour Science 102 (2007) 262–302302