Temperature

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Effects of temperature on feeding and digestive

processes in fish

Helene Volkoff & Ivar Rønnestad

To cite this article: Helene Volkoff & Ivar Rønnestad (2020) Effects of temperature on feeding and
digestive processes in fish, Temperature, 7:4, 307-320, DOI: 10.1080/23328940.2020.1765950

To link to this article: https://doi.org/10.1080/23328940.2020.1765950

Published online: 18 May 2020.

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TEMPERATURE
2020, VOL. 7, NO. 4, 307–320
https://doi.org/10.1080/23328940.2020.1765950

PRIORITY REVIEW

Effects of temperature on feeding and digestive processes in fish

a b
Helene Volkoff and Ivar Rønnestad
a
Departments of Biology and Biochemistry, Memorial University of Newfoundland, St. John’s, NL, Canada; bDepartment of Biological
Sciences, University of Bergen, Bergen, Norway

ABSTRACT ARTICLE HISTORY

As most fish are ectotherms, their physiology is strongly affected by temperature. Temperature affects Received 12 March 2020
their metabolic rate and thus their energy balance and behavior, including locomotor and feeding Revised 29 April 2020
behavior. Temperature influences the ability/desire of the fish to obtain food, and how they process Accepted 3 May 2020
food through digestion, absorb nutrients within the gastrointestinal tract, and store excess energy. As KEYWORDS
fish display a large variability in habitats, feeding habits, and anatomical and physiological features, the Fish; temperature; feeding;
effects of temperature are complex and species-specific. The effects of temperature depend on the hormones; food intake;
timing, intensity, and duration of exposure as well as the speed at which temperature changes occur. metabolism; digestion
Whereas acute short-term variations of temperature might have drastic, often detrimental, effects on
fish physiology, long-term gradual variations might lead to acclimation, e.g. variations in metabolic and
digestive enzyme profiles. The goal of this review is to summarize our current knowledge on the effects
of temperature on energy homeostasis, with specific focus on metabolism, feeding, digestion, and how
fish are often able to “adapt” to changing environments through phenotypic and physiological changes.

Overall effects of temperature in fish Since biochemical reaction rates increase with tem-
perature, the standard metabolic rate (SMR, the meta-
Most fish are classified as ectotherms, i.e. their
bolic rate required to maintain life and routine
metabolic heat production, and retaining mechan-
activity) in the ectothermic fish also increases with
isms are insufficient to provide body warming [1].
temperature (Figure 1(a)). The maximum metabolic
They are therefore strict temperature conformers
rate (MMR or metabolic rate at maximum sustained
and obligate poikilotherms i.e. the ambient envir-
exercise) on the other hand, usually has a dome-
onmental temperature determines their body tem-
shaped response to temperature, where it increases,
peratures. As a consequence, in fish, temperature
and subsequently plateaus or decreases [9]. The meta-
sets the rates of virtually all biochemical reactions
bolic (or aerobic) scope, calculated as the difference
and thus the pace of physiological processes [2,3].
between MMR and SMR (plotted in Figure 1(b)), is
Since temperature has such a large impact on fish,
the surplus energy left after the basal maintenance
it is labeled the abiotic ecological master factor [4].
costs are met and is available for functions such as
When uncompensated, metabolic processes
digestion, locomotion, growth, and reproduction
increase 2- to 3-fold with a 10°C increase in environ-
[9,10]. Aerobic scope is used as a proxy for perfor-
mental temperature, the influence of temperature on
mance (Figure 1(b)).
physiological processes being described by the Q10
In all ectotherms, including fish, thermal perfor-
temperature coefficient (i.e. the rate at which
mance curves, i.e. performance (related to traits such
a physiological response changes with a 10°C
as growth, reproduction, and locomotion) as
increase in temperature) [5]. However, the magni-
a function of temperature is bell-shaped curves
tude of these changes varies with the temperatures
[11,12]. Performance is maximal within a range of
considered, as Q10 values are not constant for differ-
optimal temperatures, declines when outside that
ent 10°C increments and usually decrease at higher
optimal range, to become zero at the upper and
temperatures [5,6]. Consequently, enzymatic reac-
lower critical temperatures (Figure 1(b)), which define
tions, cellular respiration, oxygen consumption,
the organism’s thermal tolerance range [13].
and thus metabolic rates vary with temperature [7,8].

CONTACT Helene Volkoff hvolkoff@mun.ca

© 2020 Informa UK Limited, trading as Taylor & Francis Group
308 H. VOLKOFF AND I. RØNNESTAD
a)
b)
Figure 1. (a) Changes in standard metabolic rate (SMR) and max-
imum metabolic rate (MMR) and aerobic scope (AS) as a function
of temperature in fish; (b) Performance curve as a function of
temperature. Performance is maximal at an optimal temperature
(Topt). Performance can no longer be sustained at temperatures
below the minimal critical temperature (CTmin) or beyond the
maximal critical temperature (CTmax) [based on [18]].
Fish live in species-specific temperature ranges
where they can optimize physiological perfor-
mance, so that performance curves vary among
species [14,15]. Fish living at low temperatures
have a left-shifted performance curve compared
to high-temperature adapted fish [6]. For example,
the maximum thermal tolerance varies from −1/
−2°C in Antarctic fish (Notothenioidei) [16] to
44.6°C for desert pupfish (Cyprinodon macularius,
C. salinus) [17]. In general, temperate ectothermic
species, inhabiting mid-latitudes where seasonal
differences in temperatures are largest, have
wider thermal performance ranges, lower optimal
temperatures, and are more cold-tolerant and less
heat-tolerant compared to tropical species [18,19].
Temperature preference also varies with other
intrinsic factors such as size (small animals have
a higher metabolic rate per unit weight than do
large animals) age, and developmental and repro-
ductive stages [9,20].
Individual fish exposed to moderate tempera-
ture changes are usually able to maintain close to
optimal performance by altering either their beha-
vior (preference/avoidance) or their physiology by
acclimatization/acclimation (i.e. reversible physio-
logical plasticity, responses without changes in
genotype) [1]. Acclimatory responses act to keep
biological processes functioning at an acceptable
rate [5] and include changes in the synthesis of
isozymes and modification of cell membrane
structure. Longer exposures over several genera-
tions result in evolutionary changes and genetic
adaptation [6]. Metabolic acclimation requires
time and is valuable as an adaptation to seasonal
or slow changes in temperature, while it fails to
enable the fish to respond to rapid episodic
changes such as those due to heat waves in the
summer. In addition, concurrent factors such as
heat waves and bloom of toxic algae may interact
with detrimental synergistic effects on survival: for
example, in larval cobia, survival is reduced by
16% in fish exposed to either heat or algae toxin,
but drops by 60% when both stressors are pre-
sent [21].
Temperature tolerance and performance curves
shift with acclimation and lethal thermal limits are
affected by the temperatures that fish are placed in
prior to exposure [22]. With this as a starting
point, two types of lethal thermal limits can be
defined: incipient (or chronic) and ultimate
(acute) lethal temperatures [5]. Incipient lethal
temperature is the temperature at which signifi-
cant mortality (50% of the group is often the
standard, TL50) occurs, following continuous expo-
sure of fish to this temperature for a long time
period. Exposure time is critical, and fish will
survive exposure to higher/lower temperatures if
that exposure is shorter. The acute lethal tempera-
ture is the temperature at which death occurs

when water temperature is raised rapidly. At the
ultimate (acute) lethal temperature mortality is
almost instantaneous (<10 min) [5].
The thermal limits for fish acclimated to specific
temperatures can be summarized graphically as
a temperature tolerance polygon [23]. Pioneering
studies by Fry and coworkers used these thermal
tolerance polygons to compare eight salmonid spe-
cies [see refs in [24]]. The incipient lethal levels
were defined within a tolerance zone where sal-
mon survived over 7 days. The data for Atlantic
salmon (Salmo salar), the most robust of these
species [24], are shown in Figure 2. Resistance to
thermal stress outside the tolerance zone was
a function of time: the ultimate lethal level
(defined as survival for 10 min) increased with
acclimation temperature to a maximum of 33°C,
whilst the minimum value remained close to 0°C.
Fish with poor swimming ability are sometimes
forced to adapt to habitats where temperature fluc-
tuations are large. For example, fish faced with harsh
winter conditions become dormant and down-
regulate metabolic enzyme activity [e.g. cunner
Figure 2. Thermal tolerance polygon for Atlantic salmon. The
purple area outlines the tolerance zone while the blue area is
the limit for food intake. The incipient lethal temperature (incipi-
ent Ct) is the temperature where 50% of individuals acclimated to
a certain temperature can survive for a long time, in this study
defined as 7 days. The ultimate lethal temperature (Ultimate Ct) is
the highest temperature to which fish can acclimate [123]. Note
that both lower and upper limits for food intake, incipient, and
ultimate lethal temperatures are positively correlated with accli-
mation temperature [modified from [24]].
TEMPERATURE 309
Tautogolabrus adspersus [25,26]] or are freeze toler-
ant [e.g. winter flounder Pseudopleuronectes ameri-
canus, sculpins [27]]. Interestingly, the temperature
sensors in fish remain to be described. Fish do not
seem to have the TRPM8 gene, which encodes for the
principal molecular receptor of cold temperatures in
mammals. However, there is evidence in zebrafish
that they possess TRPV1, a cation-selective ion chan-
nel activated by hot temperatures [28] (and also by
noxious chemicals like capsaicin, although this may
not be relevant in fish). However, there is ample
evidence that fish sense and react to temperature,
as they are capable of behavioral thermoregulation
[4,29]. High temperatures induce frantic activity
which assists fish in nature to flee [30] and can
cause apparent panic and intense swimming activity,
as seen in Atlantic salmon treated against salmon
louse during short-term exposure, i.e. 30 s in water at
34–36°C [31]. Low temperatures most likely are also
sensed, but cold induces lethargy which might pre-
vent fish from escaping very low temperatures [30].
The close relationships between water tempera-
ture and the rates of physiological processes also
affect the food intake required to meet the demands
for chemical energy and substrates necessary for
survival. Ingested food, following processing by the
gastrointestinal tract (GIT), provides the chemical
energy used for basal maintenance and the excess is
allocated to activity/locomotion, somatic growth or
reproduction and storage/reserves [32]. Some of the
ingested energy is also lost during processing of
nutrients via specific dynamic action (SDA), the
increase in metabolic rate in response to feeding
resulting from ingestion, digestion, absorption, and
assimilation of a meal (Figure 3(a)). Temperature,
through its effects on metabolism, affects this energy
budget by influencing nutrient digestion and assim-
ilation and the investment of surplus energy into
reproduction and growth, and the intake of energy
via feeding [9]. However, although this relationship
has often been described using an energetics
approach, the mechanisms underlying some of the
observed changes are poorly understood. It has been
speculated that food intake ultimately is a function of
energy requirements, including the energy required
to grow. However, this assumption lacks empirical
support not only in fish but also in mammals, and, to
date, there is no convincing demonstration that
energy expenditure influences within-day appetite
310 H. VOLKOFF AND I. RØNNESTAD

Figure 3. (a) Dynamic energy budget in a fish. Energy is provided by ingestion of food, which is processed in the gastrointestinal
tract (GIT). Food undergoes digestion and portion of the digesta is absorbed, and some is not absorbed and is lost via the feces
(egestion). Absorbed nutrients provide energy that is used for basal maintenance (SMR). Energy in excess is allocated to activity/
locomotion, storage/reserves, somatic growth, or reproduction. Energy is also lost during processing of nutrients via SDA and some
due to excretion of N-containing compounds, i.e. NH3 [based on [124] and [125]]. (b) General effects of temperature on performance
(conversion efficiency) and rates of food intake, metabolic rate, and growth in fish. Numbers (1–3) indicate maxima (optima) in
relation to temperature [modified from [126]].

control [33]. Several models for physiological control
of appetite mainly developed for mammals do not
involve energy expenditure, but rather describe food
intake as a function of signals arising from adipose
tissue and the GIT [34,35]. The experimental evi-
dence for making such thorough assessment does
not exist in fish, due to the current lack of available
methods for assessing the parameters required.
However, several of the key factors involved in sig-
naling pathways in the regulation, particularly at the
gene expression levels have been explored in several
studies over the last few years (see sections below).
Effects of temperature on feeding
Effects of temperature on feeding behavior and
food intake
The impacts of temperature on feeding vary depend-
ing on species, but usually, voluntary food intake
increases with moderate temperature increases, and
decreases when temperatures are outside the fish opti-
mal temperature range (Figure 3(b)); [e.g. Sockeye
salmon Oncorhynchus nerka [4]; channel catfish
Ictalurus punctatus [36]; walking catfish Clarias
batrachus [37]; cobia Rachycentron canadum [38];
Indian major carp Catla catla [39]; Atlantic salmon
[40,41]; goldfish Carassius auratus [42]; perch fry
Perca fluviatilis [43]].
The available data show that fish will lose appe-
tite, cease, and finally stop ingesting food at tem-
peratures well before the ultimate maximal critical
temperature for the species [44]. This can also be
seen in thermal tolerance polygons in Atlantic
salmon [45], for which the temperature limits for
food intake increase slightly with acclimation tem-
perature to upper and lower mean values of 22.5°C
and 7.0°C, but these values are well below the
incipient lethal temperature (Figure 2).
Successful food consumption depends on the avail-
ability of appropriate food items, adequate sensory
perception, and the capacity for locomotion. Food
intake is closely linked to feeding behavior, which
includes a series of steps including food detection,
capture, and ingestion and ultimately swallowing
[46,47]. Temperature might independently affect and
modulate several of these processes and factors.
Food is detected via a wide range of chemical
(olfaction and taste), visual (eyes), and mechanical
(lateral line) stimuli. In most species, olfaction

detects the most distant stimuli while touch and
gustation detect the closest ones and vision plays
the most prominent role in prey/food detection
[48]. However, there is variation among fish spe-
cies. For example, plaice Pleuronectes platessa is
mostly dependent on vision for feeding but sole
Solea solea relies principally on chemoreception
and mechanoreception [49]. In Chinese perch
Siniperca chuatsi, blocking of olfaction, but not
vision or lateral line, decreases feeding behavior
[50]. Similarly, in goldfish, destruction of the eyes
[51] or reduced visibility (increased water turbid-
ity) [42] does not affect food intake, although it
increases locomotion and the time taken to reach
food, whereas impairment of olfaction decreases
feeding behavior [52]. In red drum Sciaenops ocel-
latus, blocking vision alone or olfaction alone does
affect predation, whereas fish with the lateral line
system blocked exhibited low predation rate [53].
Some fish species are also reliant on hearing for
detection of predators and prey, particularly in
muddy or dark habitats when vision is lim-
ited [54].
Temperature has been shown to influence the
sensitivity of sensory systems, including vision,
hearing, and olfaction/taste, likely affecting feed-
ing behavior. For example, in rockfish (Sebastes
sp.), the low-light sensitivity of the retina
decreases tenfold with a 10°C increase in tem-
perature [55]. In channel catfish Ictalurus punc-
tatus, hearing sensitivity is lowest at 10°C and
increases between 10°C and 26°C [54], and the
average life span of taste bud cells on the barbels
is on the order of 40, 30, 15, and 12 days at 14°C,
18°C, 22°C, and 30°C, respectively [56]. These
changes in perception might explain why tem-
perature can affect taste preferences in some fish.
For example, in stellate sturgeon Acipenser stel-
latus, palatability of some amino acids (L-gluta-
mic acid, L-alanine, L-tryptophan, L-valine, and
L-leucine) changes with temperature [57,58].
Temperature can also affect fish cognitive abil-
ities, perhaps also disturbing their ability to forage
for food. In wild-type zebrafish, extreme tempera-
tures (18°C and 34°C, 26°C being control) have
been shown to not only affect energy metabolism
but also to down-regulate the expression of pro-
teins associated to synapses and neurotransmitter
release, resulting in reduced interest for the novel
TEMPERATURE 311
environment and an impairment of cognitive abil-
ities during behavioral tests [59].
Furthermore, temperature can affect locomotor
performance of fish and their ability to capture
food (and also to escape from predators), with an
increase up to an optimal temperature and a rapid
decrease as temperatures increase above that opti-
mal value. For example, the best swimming per-
formances for goldfish are attained at
temperatures from 20°C to 30°C, with lower values
at 5°C, 10°C, 15°C, 35°C, and 38°C [60]. Similar
curves are seen in other fish such as Atlantic cod
Gadus morhua [61], channel catfish [36], five-
banded damsel-fish A. vaigiensis and A. whitleyi
[62], yellow catfish Pelteobagrus fulvidraco [63].
Similarly, decreases in locomotor performance
negatively affect the ability of prey to survive an
attack from a predator [64].
It is not clear to what extent these temperature-
dependent changes in swimming performances are
due to physiological changes in fish muscle and neu-
rons or to variations in the physical properties of
water. Fish propulsion is driven by muscular contrac-
tions controlled by the nervous system. Temperature
strongly affects muscle physiology [for example, mus-
cle takes twice as long to contract and relax when
temperature drops by 10°C and have faster contractile
properties in warmer waters [65]] and nerve conduc-
tion is reduced by temperature [66]. Changes in tem-
perature also cause variations in the physical
properties of water, which may affect fish movements,
as a decrease in temperature induces increases in
viscosity and density, and thus drag. For example, in
Atlantic herring Clupea harengus, swimming speed
increases by 60% in fish as temperature is increased
from 6°C to 13°C and reduced viscosity accounts for
54% of this increase [67].
Effects of temperature on appetite-regulating
endocrine factors
In fish, as in mammals, the control of food intake is
affected by a number of endocrine factors that are
produced by the brain or peripheral organs (such as
the intestine, pancreas, liver, and possibly adipose
tissue and muscle) (Figure 4), which influence feed-
ing centers in the brain and thus inhibit (anorexi-
genic factors) or stimulate (orexigenic factors)
feeding [68,69]. Peripheral endocrine factors are
312 H. VOLKOFF AND I. RØNNESTAD
Figure 4. General overview of the endocrine regulation of
feeding in fish. Information on the presence and composition
of food in the gastrointestinal tract (GIT) is transmitted to the
brainstem and subsequently the brain feeding centers via
receptors [GIT hormone receptors as well as mechanoreceptors
(stretch) and chemoreceptors] located on vagal afferents. Some
GIT hormones also act via the circulation and cross the blood-
brain barrier and affect the secretion of brain appetite hor-
mones, which in turn affect feeding centers. AgRP, agouti-
related peptide; CART, cocaine- and amphetamine-regulated
transcript; CCK, cholecystokinin; CRF, corticotropin-releasing fac-
tor; GHRL, ghrelin; GLP, glucagon-like peptide; MCH, melano-
cyte-concentrating hormone; NPY, neuropeptide Y; OX, orexin;
POMC, proopiomelanocortin; PYY, peptide YY. Hormones are
characterized as orexigenic (green) or anorexigenic (red) if they
stimulate or inhibit feeding, respectively.
released in the blood and cross the blood-brain bar-
rier and have a direct action on receptors on complex
neural networks that act as feeding centers. Sensory
information (chemical, sensed by chemoreceptors,
and mechanical, such as distension, sensed by
mechanoreceptors) from the GIT is also carried by
the vagus nerve and will also affect feeding centers,
via innervation from the brainstem [69,70]. Recent
evidence suggests that plasma concentrations of glu-
cose can be directly sensed by the brain and appetite-
controlling centers, and the existence of comparable
mechanisms for other nutrients is currently being
explored [71]. The major endocrine brain factors
include neuropeptide Y (NPY), orexin, cocaine-
and amphetamine-regulated transcript (CART),
Agouti-related protein peptide, melanocyte-
stimulating hormone [post-translatory cleavage pro-
duct from the proopiomelanocortin] and corticotro-
pin-releasing factor (CRF), while major peripheral
endocrine factors include cholecystokinin (CCK),
peptide YY and glucagon-like peptide (intestine),
ghrelin (intestine/stomach), and leptin (liver)
[68,69,72].
Similar to mammals, food consumption in fish
may be viewed in terms of short- and long-term
signals. However, the large variability in feeding
habits, food availability, ecology, and anatomical fea-
tures, such as the lack of stomach in some fish, adds
much complexity to this view. In the short term,
initiation of food consumption during a meal is
believed to be regulated by sensory stimuli, gut
mechanical and chemical sensors, nutrient concentra-
tions in the plasma, and levels of gut hormones
secreted by specialized enteroendocrine cells [34].
Dynamic changes in these stimuli eventually induce
“satiation,” leading to a decrease and termination of
food intake while food is present in the anterior part
of the GIT. In many species, there will be a period of
“satiety” that is characterized by an inhibition of
further ingestion and minimal hunger. For example,
in rainbow trout Oncorhynchus mykiss, appetite stops
shortly after feeding and returns when 70–80% of the
previous meal has been evacuated from the stomach
[73]. The long-term regulation of feeding in fish is
more controversial. Fish can survive for long periods
of time without food, and fasting periods are part of
the natural life cycle of many fish species, as it is the
case during winter months and spawning migrations.
In mammals, leptin, secreted by adipose tissue, acts as
a lipostatic signal which relays information regarding
energy status to the brain and allows animals to
maintain a relatively constant body weight [74]. It is
still unclear if and how any adiposity signal (i.e. leptin
in mammals), modulates hunger, satiation, and feed-
ing behavior in fish. While there are indications that
leptin may act as a “the lipostatic signal” in fish [74],
thus providing a potential negative feedback for the
regulation of adipose tissue, it has also been suggested
that leptin is mainly involved in glucose homeostasis
and/or maintenance of adequate energy stores for
survival during periods of energy deficit [74,75].
In fish, the argument for a long-term homeostatic
control of energy, in particular in the context of body
weight stability, is not convincing, since many fish
continue to grow their whole life. Overfeeding does
not lead to any significant down-regulation of energy
intake as would be predicted in a homeostatic system,
but rather the fish grow faster and continue to allocate
more of the ingested energy into fat deposits in body.
Similar to mammals, there is no complete generic or
species-specific model that describes the signaling
pathways and factors involved in the control of

appetite and growth in fish. Again, similar to mam-
mals [34] the current conceptualization in fish should
not be regarded as permanent but rather as an evol-
ving representation based on the current state of
understanding.
Very few studies have examined the effects of
temperature on the endocrine factors controlling
feeding in fish mentioned above.
In goldfish, higher temperatures increase orexin
mRNA levels and decrease CART mRNA levels in
the hypothalamus and decrease peptide YY and CCK
mRNA levels in the intestine [42]. In Atlantic cod,
low temperatures inhibit food intake, and this inhi-
bition is in part mediated by increases in CART
transcript expression [76]. In Atlantic salmon, tem-
perature-induced variations in feeding have been
correlated to changes in plasma concentrations of
ghrelin [41,77] and leptin [78]. In cunner, orexin,
NPY, CART, and CCK mRNA levels decrease dur-
ing natural torpor (when fish are exposed to low
temperatures and do not feed) as compared to fed
summer fish, suggesting these hormones mediate
different physiological responses to torpor-induced
long-term fasting [79].
The hypothalamic–pituitary–interrenal axis has
also been shown to be involved in temperature-
mediated changes in feeding. Stressful environmen-
tal conditions such an increase in temperature or
extremely high and low water temperatures induce
the release of CRF and cortisol, which both inhibit
feeding in fish [e.g. rainbow trout [80], grouper
Epinephelus akaara [81]; Atlantic salmon [40];
carp [82]].
Effects of temperature on digestive processes
Digestion consists of a series of complex series of
processes with the overall aim to maximize absorption
of dietary nutrients (Figure 5). After ingestion, food is
mainly degraded by digestive enzymes and to some
extent mechanically by muscular movements of the
GIT. Among fish species, different feeding habits (e.g.
herbivore, omnivore, carnivore) result in different
GIT morphologies. Carnivores usually have short
and straight intestines, most often with the presence
of a true stomach and pyloric ceca (finger-like appen-
dages in the proximal intestine, which increase the
overall intestinal absorptive surface area) whereas
herbivores tend to have longer intestines without
TEMPERATURE 313
Figure 5. Processes involved in digestion. After food is ingested
(1), digestive juices are secreted (2) and allow enzymes to
digest food to very simple molecules (3) that are transported
across the intestinal epithelium into the blood (4). The food is
actively transported through the gastro-intestinal tract (GIT) by
smooth muscular movements (5). The remaining indigestible
food is eventually evacuated (6). The gut transit time is the time
from ingestion (1) to elimination (6). Digestion consists of
closely orchestrated processes (7) that are integrated in ways
that is believed to optimize efficiency and maximize absorption.
*The GIT also has a very important function as a barrier to
prevent entry of vectors for disease. Structural and enzymatic
barriers are characteristic of the entire GIT. Microbiota and
symbiotic digestion may occur not only in posterior section,
but also in the anterior sections. Interactions between the
digesta, microbiota, and gut tissue likely also occur.
ceca and sometimes no true stomach [83]. Agastric
fish may possess an intestinal bulb or an enlargement
in the anterior intestine that might somewhat increase
retention time [84]. A number of gastrointestinal
factors (hormones, neurotransmitters) act locally to
regulate digestive processes [85]. Temperature affects
the secretory activity of digestive juices (by its effect
on food ingestion), GIT motility, the activity of diges-
tive enzymes, and digestion and absorption rates [86].
Temperature influences gut transit time and
digestion/absorption rates
Cooler water temperatures may reduce nutrient
digestibility, by reducing digestion rates, increas-
ing gut transit time (time for all digesta to be
voided from the fish), and lowering gastrointest-
inal evacuation rates [87]. For example, in yellow-
tail kingfish (Seriola lalandi), gut transit time is
12–16 h in the summer compared to 36–48 h at
winter temperatures [87]. Similarly, gastric evacua-
tion rates are higher at ≥20°C than under ≤15°C in
the delicate loach Niwaella delicata [88], at 20°C
314 H. VOLKOFF AND I. RØNNESTAD
than at 10°C in horse mackerel [89], at 30°C than
22°C in mahseer Tor tambroides [90], 30°C than
22°C in the hybrid grouper Epinephelus fuscogut-
tatus ×E. lanceolatus [91] and blood snapper
Lutjanus malabaricus [92], 34°C than at 30°C in
cobia Rachycentron canadum [93].
Temperature might also change environmental
conditions in the GIT. For example, in cobia,
increasing temperature from 30°C to 34°C
increases the acidity levels in the intestine [93],
and in several seasonal species, intestinal pH
decreases in summer and increases during the
cold season [94]. This suggests that temperature-
and species-dependent pH changes in the intestine
may be necessary to optimize the activity of diges-
tive enzymes. The fatty acid composition of lipids
in the intestinal mucosa of goldfish has also been
shown to be temperature-dependent [95], which
might modify transport processes (e.g. lipid solu-
bility of amino acids and the rate at which they
cross the intestinal membranes). Temperature also
affects the composition of the intestinal microbiota
[96,97], which in turn might affect digestive pro-
cesses [98].
SDA (the increase in metabolic rate in response
to feeding resulting from ingestion, digestion,
absorption, and assimilation of a meal) is also
affected by temperature. Higher temperatures
usually induce higher increases in metabolic
rates and decreased durations of SDA, as seen in
lionfish Pterois ssp [99]., Southern catfish Silurus
meridionalis [100], Atlantic cod [101], Caribbean
neon goby Elacatinus lobeli [102], goldfish
Carassius auratus [103] and yellowfin tuna
Thunnus albacares [104].
Temperature affects digestive enzymes
Digestive processes and nutrient/energy digestibil-
ity usually decrease at temperatures outside the
optimal range [e.g. brook trout Salvelinus fontina-
lis [105]]. These changes are due in part to the
effects of temperature on digestive enzyme activ-
ities. Efficient degradation of nutrients in the
digestive tract of fish largely depends on the avail-
ability and activity of digestive enzymes, although
a longer gut transit time will increase the time
during which enzymes can work.
Most fish possess the similar main digestive
enzymes, i.e. proteolytic enzymes (i.e. trypsin,
carboxypeptidases), carbohydrate enzymes (i.e.
maltase, amylase), lipolytic enzymes (i.e. lipase),
and phosphatases (i.e. alkaline phosphatase)
[106,107]. Some enzyme may have several forms
within one species, forms that differ in specificity
and activity [e.g. trypsin/trypsinogen in Atlantic
salmon [108], Atlantic cod [109], albacore tuna
Thunnus alalunga [110], anchovy Engraulis japo-
nicus [111]]. Digestive enzyme profiles and activ-
ities vary between species, depending on food
preferences. Carnivorous species have higher
levels of proteolytic enzyme activity whereas car-
bohydrases are predominant in herbivorous and
omnivorous fish [112,113].
The nature of digestive enzymes also varies
depending on the habitat/climate fish live in.
Temperature adaptation of enzymes is genetically
determined and can involve phenotypic changes.
These include differences in structure, affinity to
substrates and activation energy, as well as
changes in rate of secretion and production of
isozymes – which catalyze the same reaction but
with optimal efficiencies at different temperatures
[114]. For example, digestive enzymes from fish
adapted to cold environments, such as the
Atlantic cod [115] and the Antarctic icefish
(Chionodraco hamatus) [116], have higher cataly-
tic efficiencies at low and moderate temperatures,
compared to mammals or fish living in warmer
temperatures.
The effects of water temperature on fish digestive
enzyme activities seem species-specific, as the opti-
mal temperature for enzyme activity usually falls
within the temperature range corresponding to the
fish habitats, as seen for example, in some subtropi-
cal/tropical species: in seabass (Dicentrarchus labrax,
carnivorous, range 8–24°C), α-amylase and lipase
activities peak at 23°C and trypsin at 17°C [117], in
threespine stickleback (Gasterosteus aculeatus, carni-
vorous, 4–20°C), highest levels of amylase and tryp-
sin activity occur at 18°C [118], in walking catfish
(Clarias batrachus, omnivore, 10–30°C) protease
activities are higher at 25°C and lipase activity is
higher at 30°C compared to 10°C, 15°C, 20°C, 25°
C, 30°C, and 35°C, with lowest enzyme activities
were recorded at 10°C [37] and in Catla catla (omni-
vore, 18–28°C) fish exposed at 10°C show reduced

digestive enzyme (amylase, protease, lipase, trypsin)
activities compared to fish held at 25°C [39].
Species-specific seasonal variations in enzymatic
activities are also seen, likely related to not only
temperature effects on enzymes but also changes in
diet. In Atlantic salmon, trypsin activity levels are
lower during the winter months compared to spring
months [119]. In yellowtail kingfish (Seriola
lalandi), intestinal protease and lipase activity levels
are higher in winter, possibly as a compensation to
slower gut motility at colder water temperatures
[87]. In cunner, low temperatures induce
a reduction in feeding and in the activities of intest-
inal trypsin, alkaline phosphatase, and lipase [26]. In
the Japanese grenadier anchovy Coilia nasus (plank-
tivore), water temperature affects pepsin activity
during the spawning migration [120]. One seasonal
species can also produce different isozymes depend-
ing on the season, each form being adapted for
specific temperature ranges [114].
As water temperature affects the activity of all
enzymes, it directly affects the digestibility and
metabolism of nutrients such as proteins and lipids
[121]. For example, in spotted seabass (Lateolabrax
maculatus), the optimal dietary protein level is
higher at 27°C than at 33°C, and higher water tem-
perature lead to higher serum triglyceride concen-
tration, the differences being related to differentially
expressed hepatic genes involved in the metabolism
of amino acids, fatty acids, and glucose [122].
Conclusion
Temperature is likely the major physical environ-
mental factors affecting the physiology of fish
through effects on overall metabolism and energy
balance Temperature determines how much energy
fish obtains (through regulation of feeding behavior
and food intake), how much of that energy is
acquired (through digestion and absorption) and
how much of it can be allocated to key processes
such as activity, growth (including development in
larvae and juveniles), and reproduction. Each species
usually has a range of temperatures for which phy-
siological processes are optimized, and any deviation
from these optimal temperatures might have dra-
matic effects on the overall health of fish and their
survival. To date, our knowledge on the effects of
temperature on fish energy homeostasis is still very
TEMPERATURE 315
limited, in particular given the high diversity of fish
with regards to feeding habits and habitats and capa-
city to “adapt” to changing temperatures. A better
understanding of temperature-dependent is crucial
for fish conservation and aquaculture, in particular
in view of future global environmental changes.
List of abbreviations
CART Cocaine- and amphetamine-regulated transcript
CCK Cholecystokinin
CRF Corticotropin releasing factor
GIT Gastrointestinal tract
MMR Maximum metabolic rate
NPY Neuropeptide Y
SMR Standard metabolic rate
Acknowledgments
HV acknowledges funds from the Natural Sciences and
Engineering Research Council (NSERC, grant # 261414-03). IR
acknowledges funds from the Regional Research Fund West
(grant # 259183 Greenbag), Research Council of Norway, RCN
(grants # 267626 LeuSense; # 261753 ExcelAQUA; # 311627
Gut2Brain2020), Norwegian Programme for Capacity
Development in Higher Education and Research for
Development (grant # QZA-0485 SRV-13/0010), and Mobility
grants from Meltzer Foundation and University of Bergen.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
This work was supported by the Natural Sciences and
Engineering Research Council of Canada [261414-03];
Norwegian Programme for Capacity Development in Higher
Education and Research for Development [QZA-0485 SRV-13/
0010]; Regional Research Fund West [259183]; Research
Council of Norway [267626].
ORCID
Helene Volkoff http://orcid.org/0000-0003-1344-3428
Ivar Rønnestad http://orcid.org/0000-0001-8789-0197
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