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517
INTEG. AND COMP. BIOL., 42:517–525 (2002)
Stress in Fishes: A Diversity of Responses with Particular Reference to Changes in
Circulating Corticosteroids1
BRUCE A. BARTON2
Department of Biology and Missouri River Institute, University of South Dakota, Vermillion, South Dakota 57069
SYNOPSIS. Physical, chemical and perceived stressors can all evoke non-specific responses in fish, which
are considered adaptive to enable the fish to cope with the disturbance and maintain its homeostatic state.
If the stressor is overly severe or long-lasting to the point that the fish is not capable of regaining homeostasis,
then the responses themselves may become maladaptive and threaten the fish’s health and well-being. Phys-
iological responses to stress are grouped as primary, which include endocrine changes such as in measurable
levels of circulating catecholamines and corticosteroids, and secondary, which include changes in features
related to metabolism, hydromineral balance, and cardiovascular, respiratory and immune functions. In
some instances, the endocrine responses are directly responsible for these secondary responses resulting in
changes in concentration of blood constituents, including metabolites and major ions, and, at the cellular
level, the expression of heat-shock or stress proteins. Tertiary or whole-animal changes in performance,
such as in growth, disease resistance and behavior, can result from the primary and secondary responses
and possibly affect survivorship.
Fishes display a wide variation in their physiological responses to stress, which is clearly evident in the
plasma corticosteroid changes, chiefly cortisol in actinopterygian fishes, that occur following a stressful event.
The characteristic elevation in circulating cortisol during the first hour after an acute disturbance can vary
by more than two orders of magnitude among species and genetic history appears to account for much of
this interspecific variation. An appreciation of the factors that affect the magnitude, duration and recovery
of cortisol and other physiological changes caused by stress in fishes is important for proper interpretation
of experimental data and design of effective biological monitoring programs.
INTRODUCTION
Hans Selye once defined stress as ‘‘the nonspecific
response of the body to any demand made upon it’’
(Selye, 1973). A common misconception among fish-
ery biologists is that stress, in itself, is detrimental to
the fish. This is, however, not necessarily the case. The
response to stress is considered an adaptive mechanism
that allows the fish to cope with real or perceived
stressors in order to maintain its normal or homeostatic
state. Quite simply, stress can be considered as a state
of threatened homeostasis that is re-established by a
complex suite of adaptive responses (Chrousos, 1998).
If the intensity of the stressor is overly severe or long-
lasting, however, physiological response mechanisms
may be compromised and can become detrimental to
the fish’s health and well-being, or maladaptive, a state
associated with the term ‘‘distress’’ (Selye, 1974; Bar-
ton and Iwama, 1991) and the important concern of
managers and aquaculturists.
Physiological responses of fish to environmental
stressors have been grouped broadly as primary and
secondary (Fig. 1). Primary responses, which involve
the initial neuroendocrine responses, include the re-
lease of catecholamines from chromaffin tissue (Rand-
all and Perry, 1992; Reid et al., 1998), and the stim-
ulation of the hypothalamic-pituitary-interrenal (HPI)
axis culminating in the release of corticosteroid hor-
1 From the Symposium Stress—Is It More Than a Disease? A
Comparative Look at Stress and Adaptation presented at the Annual
Meeting of the Society for Integrative and Comparative Biology, 3–
7 January 2001, at Chicago, Illinois.
2 E-mail: bbarton@usd.edu
mones into circulation (Donaldson, 1981; Wendelaar
Bonga, 1997; Mommsen et al., 1999). Secondary re-
sponses include changes in plasma and tissue ion and
metabolite levels, hematological features, and heat-
shock or stress proteins (HSPs), all of which relate to
physiological adjustments such as in metabolism, res-
piration, acid-base status, hydromineral balance, im-
mune function and cellular responses (Pickering, 1981;
Iwama et al., 1997, 1998; Mommsen et al., 1999).
Additionally, tertiary responses occur (Fig. 1), which
refer to aspects of whole-animal performance such as
changes in growth, condition, overall resistance to dis-
ease, metabolic scope for activity, behavior, and ulti-
mately survival (Wedemeyer and McLeay, 1981; Wed-
emeyer et al., 1990). This grouping is simplistic, how-
ever, as stress, depending on its magnitude and dura-
tion, may affect fish at all levels of organization, from
molecular and biochemical to population and com-
munity (Adams, 1990).
Much of our present knowledge about physiological
responses of fish to stress has been gained from study-
ing the primary responses of the brain-chromaffin and
HPI axes to stressors and the subsequent or secondary
effects associated with neuroendocrine stimulation on
metabolism, reproduction, and the immune system
(Randall and Perry, 1992; Pickering, 1993; Iwama et
al., 1997; Reid et al., 1998; Mommsen et al., 1999).
The majority of past research on stress physiology in
fish during the last few decades has focused on aqua-
culture because of the interest in managing for stress
while maximizing production in artificial environ-
ments. Many reviews have been published in that con-
518 BRUCE A. BARTON
FIG. 1. Physical, chemical and other perceived stressors act on fish to evoke physiological and related effects, which are grouped as primary,
secondary and tertiary or whole-animal responses. In some instances, the primary and secondary responses in turn may directly affect secondary
and tertiary responses, respectively, as indicated by the arrows.
text (Barton and Iwama, 1991; Iwama et al., 1997;
Pickering, 1998) and a few have dealt with the nature
of stress responses and manipulations of stress-hor-
mone levels in fish (Mazeaud et al., 1977; Pickering,
1981; Gamperl et al., 1994; Wendelaar Bonga, 1997;
Mommsen et al., 1999). Comparatively less informa-
tion is available on physiological responses of fish to
environmental perturbations associated with natural or
anthropogenic stressors, particularly water-borne con-
taminants (Cairns et al., 1984; Adams, 1990; Niimi,
1990; Brown, 1993; Hontela, 1997). The purpose of
this paper is to illustrate the diversity of corticosteroid
stress responses that occurs among fishes in the con-
text of their genetic, developmental and environmental
history.
ENDOCRINE RESPONSES TO STRESS IN FISH
When fish are exposed to a stressor, the physiolog-
ical stress response is initiated by the recognition of a
real or perceived threat by the central nervous system
(CNS). The sympathetic nerve fibers, which innervate
the chromaffin cells, stimulate the release of catechol-
amines via cholinergic receptors (Reid et al., 1996,
1998). The chromaffin tissue (adrenal medulla homo-
logue) is located mainly in the anterior region of the
kidney in teleostean fishes (Reid et al., 1998). Because
catecholamines, predominantly epinephrine in teleos-
tean fishes, are stored in the chromaffin cells, their
release is rapid and the circulating levels of these hor-
mones increase immediately with stress (Mazeaud et
al., 1977; Randall and Perry, 1992; Reid et al., 1998).
The release of cortisol in teleostean and other bony
fishes is delayed relative to catecholamine release. The
pathway for cortisol release begins in the HPI axis
with the release of corticotropin-releasing hormone
(CRH), or factor (CRF), chiefly from the hypothala-
mus in the brain, which stimulates the corticotrophic
cells of the anterior pituitary to secrete adrenocorti-
cotropin (ACTH). Circulating ACTH, in turn, stimu-
lates the interrenal cells (adrenal cortex homologue)
embedded in the kidney to synthesize and release cor-
ticosteroids into circulation for distribution to target
tissues. The interrenal tissue is located in the anterior
kidney in teleosts and exhibits considerable morpho-
logical variation among taxonomic groups (Nandi,
1962), but is found throughout the kidney in chon-
drosteans (Idler and O’Halloran, 1970). Cortisol is the
principle corticosteroid in actinopterygian (i.e., tele-
ostean, other neopterygian and chondrostean) fishes
(Sangalang et al., 1971; Idler and Truscott, 1972; Han-
son and Fleming, 1979; Barton et al., 1998) whereas
1␣-hydroxycorticosterone is the major corticosteroid
in elasmobranchs (Idler and Truscott, 1966, 1967).
Cortisol synthesis and release from interrenal cells has
a lag time of several minutes, unlike chromaffin cells,
and, therefore, proper sampling protocol can allow
measurement of resting levels of this hormone in fish
(Wedemeyer et al., 1990; Gamperl et al., 1994). As a
result, the circulating level of cortisol is commonly
used as an indicator of the degree of stress experienced
by fish (Barton and Iwama, 1991; Wendelaar Bonga,
1997). Control of cortisol release is through negative
feedback of the hormone at all levels of the HPI axis
(Fryer and Peter, 1977; Donaldson, 1981; Bradford et
al., 1992; Wendelaar Bonga, 1997). Regulation of the
HPI axis is far more complicated than this description
implies, however. For additional details, Sumpter
(1997), Hontela (1997) and Wendelaar Bonga (1997)
provide more complete descriptions of the endocrine
stress axis in fish.
Other peripheral hormones can become elevated
during stress, including notably thyroxine (Brown et
519STRESS AND CORTICOSTEROIDS IN FISHES
TABLE 1. Examples of mean (Ϯ SE) plasma cortisol concentrations in selected juvenile freshwater fishes before and 1 hr after being subjected
to an identical 30-sec aerial emersion (handling stressor).*
Species
Cortisol (ng/ml)
Pre-stress Post-stress
Pallid sturgeon Scaphirhynchus albus
Hybrid sturgeon S. albus ϫ platorynchus
Paddlefish Polyodon spathula
Arctic grayling Thymallus arcticus
Rainbow trout (domestic) Oncorhynchus mykiss
Common carp Cyprinus carpio
2.3 Ϯ 0.3
2.2 Ϯ 0.4
2.2 Ϯ 0.6
1.1 Ϯ 0.3
1.7 Ϯ 0.5
7.4 Ϯ 2.9
3.0 Ϯ 0.3
3.2 Ϯ 0.3
11 Ϯ 1.8
26 Ϯ 4.4
43 Ϯ 3.5
79 Ϯ 14
Brook trout Salvelinus fontinalis
Yellow perch Perca flavescens
Bull trout Salvelinus confluentus
Brown trout Salmo trutta
Lake trout Salvelinus namaycush
Walleye Stizostedion vitreum
4.0 Ϯ 0.6
3.4 Ϯ 1.1
8.1 Ϯ 1.2
1.0 Ϯ 0.3
2.8 Ϯ 0.4
11 Ϯ 4.4
85 Ϯ 11
85 Ϯ 12
90 Ϯ 11
94 Ϯ 11
129 Ϯ 11
229 Ϯ 16
* All species were acclimated to their respective environmental preferenda and are listed in order of increasing magnitude of their plasma
cortisol concentration 1 hr after the disturbance (from Barton and Zitzow, 1995; Barton and Dwyer, 1997; Barton et al., 1998, 2000; Barton,
2000; and unpublished data for common carp [N. Ruane, Wageningen University], yellow perch [A. H. Haukenes, University of South Dakota]
and Arctic grayling [B. A. B. and W. P. Dwyer, U.S. Fish and Wildlife Service, Bozeman Fish Technology Center]).
al., 1978), prolactin (Avella et al., 1991; Pottinger et
al., 1992a) and somatolactin (Rand-Weaver et al.,
1993; Kakizawa et al., 1995). Also, stress may sup-
press reproductive hormones in circulation (Pickering
et al., 1987; Pankhurst and Dedual, 1994; Haddy and
Pankhurst, 1999), as does an elevated level of cortisol
(Carragher et al., 1989; Carragher and Sumpter, 1990).
However, these other hormones have not yet been
demonstrated to be useful stress indicators per se and,
therefore, are not discussed herein. Interest has focused
recently on the responses of central brain monoamines,
specifically the catecholamines and indoleamines in re-
sponse to stress (Winberg and Nilsson, 1993). Sero-
tonin, in particular, has been implicated in both epi-
nephrine and cortisol regulation in fish during stress
(Fritsche et al., 1993; Winberg and Nilsson, 1993;
Winberg et al., 1997).
FACTORS INFLUENCING CORTICOSTEROID STRESS
RESPONSES
Genetic factors
Fishes exhibit a wide variation in their responses to
stressors, particularly endocrine responses (Barton and
Iwama, 1991; Gamperl et al., 1994). Earlier studies on
corticosteroid stress responses tended to center on
freshwater fishes, particularly salmonids, because of
their importance in government and commercial aqua-
culture (Barton and Iwama, 1991; Barton, 1997), but
interest has focused recently on commercially impor-
tant marine species (Thomas and Robertson, 1991;
Pankhurst and Sharples, 1992; Morgan et al., 1996;
Waring et al., 1996; Barnett and Pankhurst, 1997; Ro-
tllant et al., 2000). Elevations in plasma cortisol range
at least as much as two orders of magnitude among
fishes following an identical stressor (Table 1) and can
be much higher, depending on species.
Characteristic cortisol elevations of fishes in re-
sponse to acute stressors tend to range within about 30
and 300 ng/ml (Wedemeyer et al., 1990; Barton and
Iwama, 1991) but there are notable exceptions. Barton
et al. (1998, 2000) observed that peak levels in cortisol
following an acute handling stressor were low (Table
1) in scaphirhynchid sturgeons (Scaphirhynchus spp.)
and paddlefish (Polyodon spathula). Their results sug-
gest a trend toward lower stress responses in those
chondrosteans compared with teleosts. Belanger et al.
(2001), however, found that peak plasma cortisol in
white sturgeon (Acipenser transmontanus) following
an acute disturbance was about 40 ng/ml, indicating
that a low corticosteroid stress response may not be a
universal phenomenon in this fish group.
Among teleosts, some species also exhibit low cor-
ticosteroid responses to acute stressors. Atlantic cod
(Gadus morhua), for example, had a peak increase in
plasma cortisol to Ͻ15 ng/ml after handling (Hemre
et al., 1991). At the high end of the response range,
Maule et al. (1988) during their physiological moni-
toring studies of migrating juvenile chinook salmon
(Oncorhynchus tshawytscha) found that peak post-dis-
turbance cortisol concentrations often reached 400 ng/
ml during and after transport. However, Congleton et
al. (2000) later measured cortisol titers in outmigrating
chinook salmon from the same system that were con-
siderably lower. Mazik et al. (1991) documented plas-
ma cortisol increases in striped bass (Morone saxatilis)
to nearly 2,000 ng/ml during recovery following 5 hr
of hauling, which represent some of the highest levels
reported.
Response differences to stressors are clearly evident
among closely related fish species and such differences
appear to be consistent. Barton (2000) and Ruane et
al. (1999) both showed that brown trout (Salmo trutta)
exhibited greater cortisol increases after brief handling
and short-term confinement, respectively, than did
rainbow trout (Oncorhynchus mykiss). This difference
was also consistent with glucose responses between
these two species. Similarly, both McDonald et al.
(1993) and Barton (2000) found that lake trout (Sal-
520 BRUCE A. BARTON
velinus namaycush) were more sensitive to a transport
stressor than brook trout (Salvelinus fontinalis), a
closely related char species.
A few studies have subjected fish to continuous se-
vere stressors in an attempt to characterize maximum
corticosteroid responses to stress. Plasma cortisol in
sturgeons and paddlefish reached maximum levels of
about 13 and 60 ng/ml, respectively, when subjected
to severe continuous confinement accompanied by
handling (Barton et al., 1998, 2000), but in juvenile
rainbow trout, this plateau was about 160 ng/ml using
the same experimental protocol (Barton et al., 1980).
In similar studies, peak plasma cortisol concentrations
exceeded 500 ng/ml in juvenile chinook salmon
(Strange et al., 1978) and approached 1,400 ng/ml in
striped bass (Noga et al., 1994), further emphasizing
the wide variations in stress responses apparent among
fish species.
Most fish species tested show their highest plasma
increase in cortisol within about 0.5–1 hr after a stress-
ful disturbance (Barton and Iwama, 1991), but there
are exceptions to this general pattern. Vijayan and
Moon (1994) found that circulating cortisol in the sea
raven (Hemitripterus americanus), a sedentary, ben-
thic marine fish, took about 4 hr to reach its peak level
of about 260 ng/ml following an acute stressor. Those
authors suggested that the slow rate of response to the
stressor may help conserve energy in a normally in-
active species having a slow metabolic rate.
Differences in corticosteroid stress responses also
exist among strains or stocks within the same species
(Iwama et al., 1992; Pottinger and Moran, 1993), their
hybrids (Noga et al., 1994), and between wild and
hatchery fish (Woodward and Strange, 1987). Within
a single strain or population, variation in stress re-
sponses also has a genetic component (Heath et al.,
1993) and some fish may be predisposed to consis-
tently exhibit high or low cortisol responses to stress-
ors (Pottinger et al., 1992b; Tort et al., 2001), a pattern
that appears to have a behavioral correlate (Øverli et
al., 2002). The tendency for major differences in stress
responses between and among taxa is a trait that ap-
pears to be at least partly heritable (Fevolden et al.,
1991; Fevolden and Røed, 1993; Pottinger et al.,
1994). Fevolden et al. (1999) estimated a heritability
value of 0.56 for the plasma cortisol increases mea-
sured in adult rainbow trout after being exposed to
three stressful events, each spaced more than 1 mo
apart. Similarly, Tanck et al. (2001) recently attempted
to calculate heritability estimates for stressor-induced
plasma cortisol elevations in common carp (Cyprinus
carpio) and determined, with reservation, a relatively
high mean heritability value of 0.60 for an androge-
netic stock. It is unclear, however, whether fishes that
display relatively high or low corticosteroid stress re-
sponses are actually ‘‘more or less stressed’’ than oth-
ers or simply have different capacities to respond to
stressors. Differences in physiological mechanisms
that would account for wide variations remain largely
unexplored, but Pottinger et al. (2000) found recently
that high cortisol levels exceeding 1,500 ng/ml in chub
(Leuciscus cephalus) following a disturbance were as-
sociated with low corticosteroid receptor affinity.
Developmental factors
The developmental stage of the fish can also affect
its responsiveness to a stressor. A fish’s ability to re-
spond to a disturbance develops very early in life. Lar-
val turbot (Scophthalmus maximus) at 23 days post-
hatch and before metamorphosis showed elevations of
whole-body cortisol after they were exposed to high
levels of crude oil in a laboratory setting (Stephens et
al., 1997). Pottinger and Mosuwe (1994) determined
that the HPI axis in both rainbow and brown trout was
responsive to an acute stressor as early as 5 wk post-
hatch. Barry et al. (1995a) subsequently determined
that rainbow trout could elicit a significant plasma cor-
tisol response to an acute stressor within 2 wk after
hatching, 1 wk before they started to feed. Barry et al.
(1995b) also noted that, although the fish did not re-
spond to the stressor immediately after hatching, the
interrenal tissue at this stage was capable of secreting
cortisol upon stimulation by ACTH in vitro, suggest-
ing there may be a brief post-hatch period at which
time the HPI axis is not yet functional. Fish with a
more rapid rate of development may be capable of
eliciting a stress response much earlier. Stouthart et al.
(1998) observed that the HPI axis in embryonic carp,
as measured by whole-body cortisol, was activated and
produced a cortisol response 50 hr after fertilization,
6 hr before hatching, when eggs were subjected to me-
chanical pressure. High cortisol content in embryos or
larvae may actually affect larval quality. McCormick
(1998, 1999) found that elevated cortisol in female
damselfishes (Pomacentrus amboinensis) transferred
to the egg yolk can result in smaller larvae at hatching.
Whether endogenously produced cortisol resulting
from stress at this life stage would have a similar neg-
ative effect on early growth of larvae is unknown al-
though Weil et al. (2001) demonstrated a positive cor-
relation between speed of recovery of circulating cor-
tisol and growth rate in juvenile rainbow trout.
Limited evidence exists to suggest that fish show a
consistent increase in stress responses as they develop,
but they do appear to have heightened responses dur-
ing periods of metamorphosis. Anadromous salmonid
fishes, for example, appear to be especially sensitive
to certain stressors, particularly physical disturbances,
during the period of parr-smolt transformation, a time
of physiological metamorphosis during which juvenile
salmon prepare for seawater entry. Barton et al.
(1985a) reported a two-fold increase in the response
of plasma cortisol at 1 hr following a brief handling
stressor in juvenile coho salmon (Oncorhynchus kis-
utch) during the 3–4-mo period of parr-smolt trans-
formation as the juvenile fish switch from a freshwater
to saltwater existence. Maule et al. (1987) noted that
coho salmon smolts also appear to be particularly sen-
sitive to stressors during this transformation and
Shrimpton and Randall (1994) concluded that addi-
521STRESS AND CORTICOSTEROIDS IN FISHES
tional stress on smolting fish may also impair certain
necessary physiological changes that occur at this
time. As fish mature, primary stress responses may
actually decrease in magnitude, possibly as a result of
a reduced threshold for regulatory feedback with the
onset of maturity (Pottinger et al., 1995).
Environmental factors
Almost all environmental factors tested can influ-
ence the degree to which fish respond to stressors. Ex-
ternal factors include acclimation temperature
(Strange, 1980; Davis et al., 1984; Barton and
Schreck, 1987; Davis and Parker, 1990), salinity
(Strange and Schreck, 1980; Mazik et al., 1991; Bar-
ton and Zitzow, 1995), time of day (Davis et al., 1984;
Barton et al., 1986), wave length of light (Volpato and
Barreto, 2001) and even background color of the tanks
(Gilham and Baker, 1985). Internal environmental fac-
tors, including the fish’s nutritional state (Barton et al.,
1988) and presence of disease (Barton et al., 1986),
may also affect the magnitude of the stress response.
In certain instances, stress-modifying factors that are
themselves chronically stressful, such as poor water
quality or toxicants, can actually exacerbate (Barton et
al., 1985b) or attenuate (Pickering and Pottinger, 1987;
Hontela, 1997; Wilson et al., 1998) the cortisol re-
sponse to a second stressor. Continual interrenal activ-
ity will down-regulate the HPI axis as a result of neg-
ative feedback by cortisol, which causes the attenua-
tion of the response to additional stressors. Thus, when
a second acute stressor subsequently challenges fish
exposed to a chronic stressor, the corticosteroid re-
sponse to the additional stressor may be reduced con-
siderably relative to controls (Hontela, 1997). Impaired
interrenal function from chronic stress has been dem-
onstrated in vivo by subjecting fish to an acute physical
disturbance after being exposed to various contami-
nants (Hontela et al., 1992; Wilson et al., 1998; Norris
et al., 1999; Laflamme et al., 2000).
This apparent interrenal dysfunction has also been
assessed by measuring the functional integrity of the
interrenal tissue in vitro as a bioassay approach for
environmental monitoring. Brodeur et al. (1997) de-
veloped a relatively simple perifusion protocol and,
more recently, Leblond et al. (2001) described a meth-
od of preparing and using interrenal cell suspensions
for quantifying the extent of in vitro steroidogenic in-
hibition of ACTH-stimulated interrenal tissue at the
cellular level. These and similar approaches have been
used by this group of investigators and others to eval-
uate the mechanisms involved in the depression of in-
terrenal capacity following exposure to contaminants
including heavy metals and organochlorine com-
pounds (Brodeur et al., 1998; Girard et al., 1998; Wil-
son et al., 1998; Leblond and Hontela, 1998; Benguira
and Hontela, 2000; Laflamme et al., 2000).
Repeated stressors
Fish can exhibit a cumulative response to repeated
stressors (Carmichael et al., 1983; Flos et al., 1988;
Maule et al., 1988). Barton et al. (1986) found that
when juvenile chinook salmon were given multiple
handling stressors, the peak cortisol responses after the
final disturbance were cumulative. This phenomenon
was demonstrated in this species at the secondary
physiological level with plasma glucose (Barton et al.,
1986; Mesa, 1994) and also at the whole-animal level
using response time to avoid a noxious stimulus or a
predator as an indicator (Sigismondi and Weber, 1988;
Mesa, 1994).
However, repeated exposures to mild stressors can
desensitize fish and attenuate the neuroendocrine and
metabolic responses to subsequent exposure to stress-
ors (Reid et al., 1998; see also last section). For ex-
ample, Barton et al. (1987) subjected juvenile rainbow
trout to one of three different brief handling stressors
once a day for 10 wk and at the end of that time,
measured their response to acute handling. The re-
sponse of plasma cortisol was about half of that ob-
served in naive, previously unstressed fish indicating
possible desensitization of the HPI axis to the repeated
disturbances. A matching and significant decline in the
response of plasma glucose in the treatment group,
which implies the involvement of the catecholamine
response, suggests a general habituation to the repeat-
ed stressor.
The length of time between discrete stressors, the
effect of multiple stressors, and the severity of contin-
uous stressors are important factors that will likely in-
fluence how fish respond. Unless stressors, singularly
or in combination, are severe enough to challenge the
fish’s homeostatic mechanisms beyond their compen-
satory limits or permanently alter them, which ulti-
mately may cause death, physiological processes gen-
erally adapt to compensate for the stress (Schreck,
1981, 2000). In these cases, blood chemistry features,
such as cortisol, used to evaluate stress may appear
‘‘normal’’ and alternative approaches, such as deter-
mining the magnitude of response to an additional
acute stressor, may be needed to assess the fish’s phys-
iological state.
SUMMARY
Knowledge and understanding of what constitutes
stress in fish has increased immensely in the past few
decades, notably in the area of physiological mecha-
nisms and responses that lead to changes in metabo-
lism and growth, immune functions, reproductive ca-
pacity, and normal behavior. Primary stress responses
in actinopterygian fishes include a number of hormon-
al changes, but particularly those in circulating levels
of cortisol and catecholamines. Secondary responses,
which may or may not be caused directly by the en-
docrine response, include measurable changes in blood
glucose, lactate or lactic acid, and major ions (e.g.,
chloride, sodium, and potassium), and tissue levels of
glycogen and HSPs. Tertiary responses, including
changes in growth, disease resistance and behavior,
may result directly or indirectly from these primary
and secondary responses. Many other apparent factors,
522 BRUCE A. BARTON
however, influence characteristic stress responses in
fish and include genetic (e.g., species, strain), devel-
opmental (e.g., life history stage), and environmental
(e.g., temperature, nutrition, water quality) factors.
Interpreting the changes that occur in physiological
variables can be more problematic than actually mea-
suring the responses for two reasons. First, various ge-
netic, developmental and environmental factors can
have a modifying effect on the magnitude and duration
of the stress response. Without knowing the extent to
which these other factors may have affected the re-
sponse, it is difficult to interpret the biological signif-
icance of that response in a specific context. A second
factor complicating data interpretation is the variation
and apparent inconsistency among fishes in the re-
sponses of different blood chemistry characteristics.
For example, a species that shows the greatest plasma
cortisol response increase compared with other taxa
may not be the same species that elicits the greatest
increase in a secondary response, such as glucose or
lactate, when subjected to the identical stressor. Thus,
a species or group that appears ‘‘most stressed’’ as
indicated by one particular indicator or level of re-
sponse may not necessarily reflect that same degree of
stress if measured by another aspect of the response.
The response to a stressor is a dynamic process and
physiological measurements taken during a time
course are only representative instantaneous ‘‘snap-
shots’’ of that process. A significant delay, depending
on the level and type of response, can occur from ini-
tial perception of the stressor by the CNS to the time
when plasma cortisol or other feature of interest reach-
es a peak level of response. Thus, the measurement of
plasma cortisol alone may not necessarily reflect the
degree of stress experienced by the fish at that instant
but more likely be representative of the extent of the
earlier or initial response.
An appreciation of the factors that affect the mag-
nitude, duration and recovery of cortisol and other
physiological changes in fishes during the stress re-
sponse is important for proper interpretation of exper-
imental data and design of effective biological moni-
toring programs. Moreover, understanding trends in
changes that occur in fish in response to stressors can
often provide clues that help relate the physiological
responses of individuals with changes in performance
manifested at the population level that could affect
their health and survivorship.
ACKNOWLEDGMENTS
I thank Neil Ruane, Wageningen University, and Alf
Haukenes, University of South Dakota, for permission
to use their unpublished data in Table 1. I also thank
James Carr and Cliff Summers for organizing this
symposium and am grateful to the Society of Integra-
tive and Comparative Biology and the University of
South Dakota Office of Research and Graduate Edu-
cation for their support.
REFERENCES
Adams, S. M. (ed.) 1990. Biological indicators of stress in fish.
American Fisheries Society Symposium Series 8, Bethesda,
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endokrinologi stree in fish

  • 1. 517 INTEG. AND COMP. BIOL., 42:517–525 (2002) Stress in Fishes: A Diversity of Responses with Particular Reference to Changes in Circulating Corticosteroids1 BRUCE A. BARTON2 Department of Biology and Missouri River Institute, University of South Dakota, Vermillion, South Dakota 57069 SYNOPSIS. Physical, chemical and perceived stressors can all evoke non-specific responses in fish, which are considered adaptive to enable the fish to cope with the disturbance and maintain its homeostatic state. If the stressor is overly severe or long-lasting to the point that the fish is not capable of regaining homeostasis, then the responses themselves may become maladaptive and threaten the fish’s health and well-being. Phys- iological responses to stress are grouped as primary, which include endocrine changes such as in measurable levels of circulating catecholamines and corticosteroids, and secondary, which include changes in features related to metabolism, hydromineral balance, and cardiovascular, respiratory and immune functions. In some instances, the endocrine responses are directly responsible for these secondary responses resulting in changes in concentration of blood constituents, including metabolites and major ions, and, at the cellular level, the expression of heat-shock or stress proteins. Tertiary or whole-animal changes in performance, such as in growth, disease resistance and behavior, can result from the primary and secondary responses and possibly affect survivorship. Fishes display a wide variation in their physiological responses to stress, which is clearly evident in the plasma corticosteroid changes, chiefly cortisol in actinopterygian fishes, that occur following a stressful event. The characteristic elevation in circulating cortisol during the first hour after an acute disturbance can vary by more than two orders of magnitude among species and genetic history appears to account for much of this interspecific variation. An appreciation of the factors that affect the magnitude, duration and recovery of cortisol and other physiological changes caused by stress in fishes is important for proper interpretation of experimental data and design of effective biological monitoring programs. INTRODUCTION Hans Selye once defined stress as ‘‘the nonspecific response of the body to any demand made upon it’’ (Selye, 1973). A common misconception among fish- ery biologists is that stress, in itself, is detrimental to the fish. This is, however, not necessarily the case. The response to stress is considered an adaptive mechanism that allows the fish to cope with real or perceived stressors in order to maintain its normal or homeostatic state. Quite simply, stress can be considered as a state of threatened homeostasis that is re-established by a complex suite of adaptive responses (Chrousos, 1998). If the intensity of the stressor is overly severe or long- lasting, however, physiological response mechanisms may be compromised and can become detrimental to the fish’s health and well-being, or maladaptive, a state associated with the term ‘‘distress’’ (Selye, 1974; Bar- ton and Iwama, 1991) and the important concern of managers and aquaculturists. Physiological responses of fish to environmental stressors have been grouped broadly as primary and secondary (Fig. 1). Primary responses, which involve the initial neuroendocrine responses, include the re- lease of catecholamines from chromaffin tissue (Rand- all and Perry, 1992; Reid et al., 1998), and the stim- ulation of the hypothalamic-pituitary-interrenal (HPI) axis culminating in the release of corticosteroid hor- 1 From the Symposium Stress—Is It More Than a Disease? A Comparative Look at Stress and Adaptation presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3– 7 January 2001, at Chicago, Illinois. 2 E-mail: bbarton@usd.edu mones into circulation (Donaldson, 1981; Wendelaar Bonga, 1997; Mommsen et al., 1999). Secondary re- sponses include changes in plasma and tissue ion and metabolite levels, hematological features, and heat- shock or stress proteins (HSPs), all of which relate to physiological adjustments such as in metabolism, res- piration, acid-base status, hydromineral balance, im- mune function and cellular responses (Pickering, 1981; Iwama et al., 1997, 1998; Mommsen et al., 1999). Additionally, tertiary responses occur (Fig. 1), which refer to aspects of whole-animal performance such as changes in growth, condition, overall resistance to dis- ease, metabolic scope for activity, behavior, and ulti- mately survival (Wedemeyer and McLeay, 1981; Wed- emeyer et al., 1990). This grouping is simplistic, how- ever, as stress, depending on its magnitude and dura- tion, may affect fish at all levels of organization, from molecular and biochemical to population and com- munity (Adams, 1990). Much of our present knowledge about physiological responses of fish to stress has been gained from study- ing the primary responses of the brain-chromaffin and HPI axes to stressors and the subsequent or secondary effects associated with neuroendocrine stimulation on metabolism, reproduction, and the immune system (Randall and Perry, 1992; Pickering, 1993; Iwama et al., 1997; Reid et al., 1998; Mommsen et al., 1999). The majority of past research on stress physiology in fish during the last few decades has focused on aqua- culture because of the interest in managing for stress while maximizing production in artificial environ- ments. Many reviews have been published in that con-
  • 2. 518 BRUCE A. BARTON FIG. 1. Physical, chemical and other perceived stressors act on fish to evoke physiological and related effects, which are grouped as primary, secondary and tertiary or whole-animal responses. In some instances, the primary and secondary responses in turn may directly affect secondary and tertiary responses, respectively, as indicated by the arrows. text (Barton and Iwama, 1991; Iwama et al., 1997; Pickering, 1998) and a few have dealt with the nature of stress responses and manipulations of stress-hor- mone levels in fish (Mazeaud et al., 1977; Pickering, 1981; Gamperl et al., 1994; Wendelaar Bonga, 1997; Mommsen et al., 1999). Comparatively less informa- tion is available on physiological responses of fish to environmental perturbations associated with natural or anthropogenic stressors, particularly water-borne con- taminants (Cairns et al., 1984; Adams, 1990; Niimi, 1990; Brown, 1993; Hontela, 1997). The purpose of this paper is to illustrate the diversity of corticosteroid stress responses that occurs among fishes in the con- text of their genetic, developmental and environmental history. ENDOCRINE RESPONSES TO STRESS IN FISH When fish are exposed to a stressor, the physiolog- ical stress response is initiated by the recognition of a real or perceived threat by the central nervous system (CNS). The sympathetic nerve fibers, which innervate the chromaffin cells, stimulate the release of catechol- amines via cholinergic receptors (Reid et al., 1996, 1998). The chromaffin tissue (adrenal medulla homo- logue) is located mainly in the anterior region of the kidney in teleostean fishes (Reid et al., 1998). Because catecholamines, predominantly epinephrine in teleos- tean fishes, are stored in the chromaffin cells, their release is rapid and the circulating levels of these hor- mones increase immediately with stress (Mazeaud et al., 1977; Randall and Perry, 1992; Reid et al., 1998). The release of cortisol in teleostean and other bony fishes is delayed relative to catecholamine release. The pathway for cortisol release begins in the HPI axis with the release of corticotropin-releasing hormone (CRH), or factor (CRF), chiefly from the hypothala- mus in the brain, which stimulates the corticotrophic cells of the anterior pituitary to secrete adrenocorti- cotropin (ACTH). Circulating ACTH, in turn, stimu- lates the interrenal cells (adrenal cortex homologue) embedded in the kidney to synthesize and release cor- ticosteroids into circulation for distribution to target tissues. The interrenal tissue is located in the anterior kidney in teleosts and exhibits considerable morpho- logical variation among taxonomic groups (Nandi, 1962), but is found throughout the kidney in chon- drosteans (Idler and O’Halloran, 1970). Cortisol is the principle corticosteroid in actinopterygian (i.e., tele- ostean, other neopterygian and chondrostean) fishes (Sangalang et al., 1971; Idler and Truscott, 1972; Han- son and Fleming, 1979; Barton et al., 1998) whereas 1␣-hydroxycorticosterone is the major corticosteroid in elasmobranchs (Idler and Truscott, 1966, 1967). Cortisol synthesis and release from interrenal cells has a lag time of several minutes, unlike chromaffin cells, and, therefore, proper sampling protocol can allow measurement of resting levels of this hormone in fish (Wedemeyer et al., 1990; Gamperl et al., 1994). As a result, the circulating level of cortisol is commonly used as an indicator of the degree of stress experienced by fish (Barton and Iwama, 1991; Wendelaar Bonga, 1997). Control of cortisol release is through negative feedback of the hormone at all levels of the HPI axis (Fryer and Peter, 1977; Donaldson, 1981; Bradford et al., 1992; Wendelaar Bonga, 1997). Regulation of the HPI axis is far more complicated than this description implies, however. For additional details, Sumpter (1997), Hontela (1997) and Wendelaar Bonga (1997) provide more complete descriptions of the endocrine stress axis in fish. Other peripheral hormones can become elevated during stress, including notably thyroxine (Brown et
  • 3. 519STRESS AND CORTICOSTEROIDS IN FISHES TABLE 1. Examples of mean (Ϯ SE) plasma cortisol concentrations in selected juvenile freshwater fishes before and 1 hr after being subjected to an identical 30-sec aerial emersion (handling stressor).* Species Cortisol (ng/ml) Pre-stress Post-stress Pallid sturgeon Scaphirhynchus albus Hybrid sturgeon S. albus ϫ platorynchus Paddlefish Polyodon spathula Arctic grayling Thymallus arcticus Rainbow trout (domestic) Oncorhynchus mykiss Common carp Cyprinus carpio 2.3 Ϯ 0.3 2.2 Ϯ 0.4 2.2 Ϯ 0.6 1.1 Ϯ 0.3 1.7 Ϯ 0.5 7.4 Ϯ 2.9 3.0 Ϯ 0.3 3.2 Ϯ 0.3 11 Ϯ 1.8 26 Ϯ 4.4 43 Ϯ 3.5 79 Ϯ 14 Brook trout Salvelinus fontinalis Yellow perch Perca flavescens Bull trout Salvelinus confluentus Brown trout Salmo trutta Lake trout Salvelinus namaycush Walleye Stizostedion vitreum 4.0 Ϯ 0.6 3.4 Ϯ 1.1 8.1 Ϯ 1.2 1.0 Ϯ 0.3 2.8 Ϯ 0.4 11 Ϯ 4.4 85 Ϯ 11 85 Ϯ 12 90 Ϯ 11 94 Ϯ 11 129 Ϯ 11 229 Ϯ 16 * All species were acclimated to their respective environmental preferenda and are listed in order of increasing magnitude of their plasma cortisol concentration 1 hr after the disturbance (from Barton and Zitzow, 1995; Barton and Dwyer, 1997; Barton et al., 1998, 2000; Barton, 2000; and unpublished data for common carp [N. Ruane, Wageningen University], yellow perch [A. H. Haukenes, University of South Dakota] and Arctic grayling [B. A. B. and W. P. Dwyer, U.S. Fish and Wildlife Service, Bozeman Fish Technology Center]). al., 1978), prolactin (Avella et al., 1991; Pottinger et al., 1992a) and somatolactin (Rand-Weaver et al., 1993; Kakizawa et al., 1995). Also, stress may sup- press reproductive hormones in circulation (Pickering et al., 1987; Pankhurst and Dedual, 1994; Haddy and Pankhurst, 1999), as does an elevated level of cortisol (Carragher et al., 1989; Carragher and Sumpter, 1990). However, these other hormones have not yet been demonstrated to be useful stress indicators per se and, therefore, are not discussed herein. Interest has focused recently on the responses of central brain monoamines, specifically the catecholamines and indoleamines in re- sponse to stress (Winberg and Nilsson, 1993). Sero- tonin, in particular, has been implicated in both epi- nephrine and cortisol regulation in fish during stress (Fritsche et al., 1993; Winberg and Nilsson, 1993; Winberg et al., 1997). FACTORS INFLUENCING CORTICOSTEROID STRESS RESPONSES Genetic factors Fishes exhibit a wide variation in their responses to stressors, particularly endocrine responses (Barton and Iwama, 1991; Gamperl et al., 1994). Earlier studies on corticosteroid stress responses tended to center on freshwater fishes, particularly salmonids, because of their importance in government and commercial aqua- culture (Barton and Iwama, 1991; Barton, 1997), but interest has focused recently on commercially impor- tant marine species (Thomas and Robertson, 1991; Pankhurst and Sharples, 1992; Morgan et al., 1996; Waring et al., 1996; Barnett and Pankhurst, 1997; Ro- tllant et al., 2000). Elevations in plasma cortisol range at least as much as two orders of magnitude among fishes following an identical stressor (Table 1) and can be much higher, depending on species. Characteristic cortisol elevations of fishes in re- sponse to acute stressors tend to range within about 30 and 300 ng/ml (Wedemeyer et al., 1990; Barton and Iwama, 1991) but there are notable exceptions. Barton et al. (1998, 2000) observed that peak levels in cortisol following an acute handling stressor were low (Table 1) in scaphirhynchid sturgeons (Scaphirhynchus spp.) and paddlefish (Polyodon spathula). Their results sug- gest a trend toward lower stress responses in those chondrosteans compared with teleosts. Belanger et al. (2001), however, found that peak plasma cortisol in white sturgeon (Acipenser transmontanus) following an acute disturbance was about 40 ng/ml, indicating that a low corticosteroid stress response may not be a universal phenomenon in this fish group. Among teleosts, some species also exhibit low cor- ticosteroid responses to acute stressors. Atlantic cod (Gadus morhua), for example, had a peak increase in plasma cortisol to Ͻ15 ng/ml after handling (Hemre et al., 1991). At the high end of the response range, Maule et al. (1988) during their physiological moni- toring studies of migrating juvenile chinook salmon (Oncorhynchus tshawytscha) found that peak post-dis- turbance cortisol concentrations often reached 400 ng/ ml during and after transport. However, Congleton et al. (2000) later measured cortisol titers in outmigrating chinook salmon from the same system that were con- siderably lower. Mazik et al. (1991) documented plas- ma cortisol increases in striped bass (Morone saxatilis) to nearly 2,000 ng/ml during recovery following 5 hr of hauling, which represent some of the highest levels reported. Response differences to stressors are clearly evident among closely related fish species and such differences appear to be consistent. Barton (2000) and Ruane et al. (1999) both showed that brown trout (Salmo trutta) exhibited greater cortisol increases after brief handling and short-term confinement, respectively, than did rainbow trout (Oncorhynchus mykiss). This difference was also consistent with glucose responses between these two species. Similarly, both McDonald et al. (1993) and Barton (2000) found that lake trout (Sal-
  • 4. 520 BRUCE A. BARTON velinus namaycush) were more sensitive to a transport stressor than brook trout (Salvelinus fontinalis), a closely related char species. A few studies have subjected fish to continuous se- vere stressors in an attempt to characterize maximum corticosteroid responses to stress. Plasma cortisol in sturgeons and paddlefish reached maximum levels of about 13 and 60 ng/ml, respectively, when subjected to severe continuous confinement accompanied by handling (Barton et al., 1998, 2000), but in juvenile rainbow trout, this plateau was about 160 ng/ml using the same experimental protocol (Barton et al., 1980). In similar studies, peak plasma cortisol concentrations exceeded 500 ng/ml in juvenile chinook salmon (Strange et al., 1978) and approached 1,400 ng/ml in striped bass (Noga et al., 1994), further emphasizing the wide variations in stress responses apparent among fish species. Most fish species tested show their highest plasma increase in cortisol within about 0.5–1 hr after a stress- ful disturbance (Barton and Iwama, 1991), but there are exceptions to this general pattern. Vijayan and Moon (1994) found that circulating cortisol in the sea raven (Hemitripterus americanus), a sedentary, ben- thic marine fish, took about 4 hr to reach its peak level of about 260 ng/ml following an acute stressor. Those authors suggested that the slow rate of response to the stressor may help conserve energy in a normally in- active species having a slow metabolic rate. Differences in corticosteroid stress responses also exist among strains or stocks within the same species (Iwama et al., 1992; Pottinger and Moran, 1993), their hybrids (Noga et al., 1994), and between wild and hatchery fish (Woodward and Strange, 1987). Within a single strain or population, variation in stress re- sponses also has a genetic component (Heath et al., 1993) and some fish may be predisposed to consis- tently exhibit high or low cortisol responses to stress- ors (Pottinger et al., 1992b; Tort et al., 2001), a pattern that appears to have a behavioral correlate (Øverli et al., 2002). The tendency for major differences in stress responses between and among taxa is a trait that ap- pears to be at least partly heritable (Fevolden et al., 1991; Fevolden and Røed, 1993; Pottinger et al., 1994). Fevolden et al. (1999) estimated a heritability value of 0.56 for the plasma cortisol increases mea- sured in adult rainbow trout after being exposed to three stressful events, each spaced more than 1 mo apart. Similarly, Tanck et al. (2001) recently attempted to calculate heritability estimates for stressor-induced plasma cortisol elevations in common carp (Cyprinus carpio) and determined, with reservation, a relatively high mean heritability value of 0.60 for an androge- netic stock. It is unclear, however, whether fishes that display relatively high or low corticosteroid stress re- sponses are actually ‘‘more or less stressed’’ than oth- ers or simply have different capacities to respond to stressors. Differences in physiological mechanisms that would account for wide variations remain largely unexplored, but Pottinger et al. (2000) found recently that high cortisol levels exceeding 1,500 ng/ml in chub (Leuciscus cephalus) following a disturbance were as- sociated with low corticosteroid receptor affinity. Developmental factors The developmental stage of the fish can also affect its responsiveness to a stressor. A fish’s ability to re- spond to a disturbance develops very early in life. Lar- val turbot (Scophthalmus maximus) at 23 days post- hatch and before metamorphosis showed elevations of whole-body cortisol after they were exposed to high levels of crude oil in a laboratory setting (Stephens et al., 1997). Pottinger and Mosuwe (1994) determined that the HPI axis in both rainbow and brown trout was responsive to an acute stressor as early as 5 wk post- hatch. Barry et al. (1995a) subsequently determined that rainbow trout could elicit a significant plasma cor- tisol response to an acute stressor within 2 wk after hatching, 1 wk before they started to feed. Barry et al. (1995b) also noted that, although the fish did not re- spond to the stressor immediately after hatching, the interrenal tissue at this stage was capable of secreting cortisol upon stimulation by ACTH in vitro, suggest- ing there may be a brief post-hatch period at which time the HPI axis is not yet functional. Fish with a more rapid rate of development may be capable of eliciting a stress response much earlier. Stouthart et al. (1998) observed that the HPI axis in embryonic carp, as measured by whole-body cortisol, was activated and produced a cortisol response 50 hr after fertilization, 6 hr before hatching, when eggs were subjected to me- chanical pressure. High cortisol content in embryos or larvae may actually affect larval quality. McCormick (1998, 1999) found that elevated cortisol in female damselfishes (Pomacentrus amboinensis) transferred to the egg yolk can result in smaller larvae at hatching. Whether endogenously produced cortisol resulting from stress at this life stage would have a similar neg- ative effect on early growth of larvae is unknown al- though Weil et al. (2001) demonstrated a positive cor- relation between speed of recovery of circulating cor- tisol and growth rate in juvenile rainbow trout. Limited evidence exists to suggest that fish show a consistent increase in stress responses as they develop, but they do appear to have heightened responses dur- ing periods of metamorphosis. Anadromous salmonid fishes, for example, appear to be especially sensitive to certain stressors, particularly physical disturbances, during the period of parr-smolt transformation, a time of physiological metamorphosis during which juvenile salmon prepare for seawater entry. Barton et al. (1985a) reported a two-fold increase in the response of plasma cortisol at 1 hr following a brief handling stressor in juvenile coho salmon (Oncorhynchus kis- utch) during the 3–4-mo period of parr-smolt trans- formation as the juvenile fish switch from a freshwater to saltwater existence. Maule et al. (1987) noted that coho salmon smolts also appear to be particularly sen- sitive to stressors during this transformation and Shrimpton and Randall (1994) concluded that addi-
  • 5. 521STRESS AND CORTICOSTEROIDS IN FISHES tional stress on smolting fish may also impair certain necessary physiological changes that occur at this time. As fish mature, primary stress responses may actually decrease in magnitude, possibly as a result of a reduced threshold for regulatory feedback with the onset of maturity (Pottinger et al., 1995). Environmental factors Almost all environmental factors tested can influ- ence the degree to which fish respond to stressors. Ex- ternal factors include acclimation temperature (Strange, 1980; Davis et al., 1984; Barton and Schreck, 1987; Davis and Parker, 1990), salinity (Strange and Schreck, 1980; Mazik et al., 1991; Bar- ton and Zitzow, 1995), time of day (Davis et al., 1984; Barton et al., 1986), wave length of light (Volpato and Barreto, 2001) and even background color of the tanks (Gilham and Baker, 1985). Internal environmental fac- tors, including the fish’s nutritional state (Barton et al., 1988) and presence of disease (Barton et al., 1986), may also affect the magnitude of the stress response. In certain instances, stress-modifying factors that are themselves chronically stressful, such as poor water quality or toxicants, can actually exacerbate (Barton et al., 1985b) or attenuate (Pickering and Pottinger, 1987; Hontela, 1997; Wilson et al., 1998) the cortisol re- sponse to a second stressor. Continual interrenal activ- ity will down-regulate the HPI axis as a result of neg- ative feedback by cortisol, which causes the attenua- tion of the response to additional stressors. Thus, when a second acute stressor subsequently challenges fish exposed to a chronic stressor, the corticosteroid re- sponse to the additional stressor may be reduced con- siderably relative to controls (Hontela, 1997). Impaired interrenal function from chronic stress has been dem- onstrated in vivo by subjecting fish to an acute physical disturbance after being exposed to various contami- nants (Hontela et al., 1992; Wilson et al., 1998; Norris et al., 1999; Laflamme et al., 2000). This apparent interrenal dysfunction has also been assessed by measuring the functional integrity of the interrenal tissue in vitro as a bioassay approach for environmental monitoring. Brodeur et al. (1997) de- veloped a relatively simple perifusion protocol and, more recently, Leblond et al. (2001) described a meth- od of preparing and using interrenal cell suspensions for quantifying the extent of in vitro steroidogenic in- hibition of ACTH-stimulated interrenal tissue at the cellular level. These and similar approaches have been used by this group of investigators and others to eval- uate the mechanisms involved in the depression of in- terrenal capacity following exposure to contaminants including heavy metals and organochlorine com- pounds (Brodeur et al., 1998; Girard et al., 1998; Wil- son et al., 1998; Leblond and Hontela, 1998; Benguira and Hontela, 2000; Laflamme et al., 2000). Repeated stressors Fish can exhibit a cumulative response to repeated stressors (Carmichael et al., 1983; Flos et al., 1988; Maule et al., 1988). Barton et al. (1986) found that when juvenile chinook salmon were given multiple handling stressors, the peak cortisol responses after the final disturbance were cumulative. This phenomenon was demonstrated in this species at the secondary physiological level with plasma glucose (Barton et al., 1986; Mesa, 1994) and also at the whole-animal level using response time to avoid a noxious stimulus or a predator as an indicator (Sigismondi and Weber, 1988; Mesa, 1994). However, repeated exposures to mild stressors can desensitize fish and attenuate the neuroendocrine and metabolic responses to subsequent exposure to stress- ors (Reid et al., 1998; see also last section). For ex- ample, Barton et al. (1987) subjected juvenile rainbow trout to one of three different brief handling stressors once a day for 10 wk and at the end of that time, measured their response to acute handling. The re- sponse of plasma cortisol was about half of that ob- served in naive, previously unstressed fish indicating possible desensitization of the HPI axis to the repeated disturbances. A matching and significant decline in the response of plasma glucose in the treatment group, which implies the involvement of the catecholamine response, suggests a general habituation to the repeat- ed stressor. The length of time between discrete stressors, the effect of multiple stressors, and the severity of contin- uous stressors are important factors that will likely in- fluence how fish respond. Unless stressors, singularly or in combination, are severe enough to challenge the fish’s homeostatic mechanisms beyond their compen- satory limits or permanently alter them, which ulti- mately may cause death, physiological processes gen- erally adapt to compensate for the stress (Schreck, 1981, 2000). In these cases, blood chemistry features, such as cortisol, used to evaluate stress may appear ‘‘normal’’ and alternative approaches, such as deter- mining the magnitude of response to an additional acute stressor, may be needed to assess the fish’s phys- iological state. SUMMARY Knowledge and understanding of what constitutes stress in fish has increased immensely in the past few decades, notably in the area of physiological mecha- nisms and responses that lead to changes in metabo- lism and growth, immune functions, reproductive ca- pacity, and normal behavior. Primary stress responses in actinopterygian fishes include a number of hormon- al changes, but particularly those in circulating levels of cortisol and catecholamines. Secondary responses, which may or may not be caused directly by the en- docrine response, include measurable changes in blood glucose, lactate or lactic acid, and major ions (e.g., chloride, sodium, and potassium), and tissue levels of glycogen and HSPs. Tertiary responses, including changes in growth, disease resistance and behavior, may result directly or indirectly from these primary and secondary responses. Many other apparent factors,
  • 6. 522 BRUCE A. BARTON however, influence characteristic stress responses in fish and include genetic (e.g., species, strain), devel- opmental (e.g., life history stage), and environmental (e.g., temperature, nutrition, water quality) factors. Interpreting the changes that occur in physiological variables can be more problematic than actually mea- suring the responses for two reasons. First, various ge- netic, developmental and environmental factors can have a modifying effect on the magnitude and duration of the stress response. Without knowing the extent to which these other factors may have affected the re- sponse, it is difficult to interpret the biological signif- icance of that response in a specific context. A second factor complicating data interpretation is the variation and apparent inconsistency among fishes in the re- sponses of different blood chemistry characteristics. For example, a species that shows the greatest plasma cortisol response increase compared with other taxa may not be the same species that elicits the greatest increase in a secondary response, such as glucose or lactate, when subjected to the identical stressor. Thus, a species or group that appears ‘‘most stressed’’ as indicated by one particular indicator or level of re- sponse may not necessarily reflect that same degree of stress if measured by another aspect of the response. The response to a stressor is a dynamic process and physiological measurements taken during a time course are only representative instantaneous ‘‘snap- shots’’ of that process. A significant delay, depending on the level and type of response, can occur from ini- tial perception of the stressor by the CNS to the time when plasma cortisol or other feature of interest reach- es a peak level of response. Thus, the measurement of plasma cortisol alone may not necessarily reflect the degree of stress experienced by the fish at that instant but more likely be representative of the extent of the earlier or initial response. An appreciation of the factors that affect the mag- nitude, duration and recovery of cortisol and other physiological changes in fishes during the stress re- sponse is important for proper interpretation of exper- imental data and design of effective biological moni- toring programs. Moreover, understanding trends in changes that occur in fish in response to stressors can often provide clues that help relate the physiological responses of individuals with changes in performance manifested at the population level that could affect their health and survivorship. ACKNOWLEDGMENTS I thank Neil Ruane, Wageningen University, and Alf Haukenes, University of South Dakota, for permission to use their unpublished data in Table 1. 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