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Effects of acidification on olfactorymediated behaviour in freshwater and
marine ecosystems: a synthesis
rstb.royalsocietypublishing.org
Antoine O. H. C. Leduc1, Philip L. Munday2, Grant E. Brown3
and Maud C. O. Ferrari4
1
Instistuto de Biologia, Universidade Federal da Bahia, Ondina, Salvador, Bahia, Brazil
ARC Centre of Excellence for Coral Reef Studies, School of Marine and Tropical Biology, James Cook University,
Townsville, Queensland, Australia
3
Department of Biology, Concordia University, 7141 Sherbrooke St. West, Montreal, Quebec, Canada H4B 1R6
4
Department of Biomedical Sciences, WCVM, University of Saskatchewan, Saskatoon, Saskatchewan,
Canada S7N 5B4
2
Review
Cite this article: Leduc AOHC, Munday PL,
Brown GE, Ferrari MCO. 2013 Effects of acidification on olfactory-mediated behaviour in
freshwater and marine ecosystems: a synthesis.
Phil Trans R Soc B 368: 20120447.
http://dx.doi.org/10.1098/rstb.2012.0447
One contribution of 10 to a Theme Issue
‘Ocean acidification and climate change:
advances in ecology and evolution’.
Subject Areas:
behaviour, ecology, environmental science,
physiology
Keywords:
climate change, ocean acidification, acid rain,
fish behaviour, olfaction, chemoreception
Author for correspondence:
Antoine O. H. C. Leduc
e-mail: [email protected]
For many aquatic organisms, olfactory-mediated behaviour is essential to
the maintenance of numerous fitness-enhancing activities, including foraging, reproduction and predator avoidance. Studies in both freshwater and
marine ecosystems have demonstrated significant impacts of anthropogenic
acidification on olfactory abilities of fish and macroinvertebrates, leading to
impaired behavioural responses, with potentially far-reaching consequences
to population dynamics and community structure. Whereas the ecological
impacts of impaired olfactory-mediated behaviour may be similar between
freshwater and marine ecosystems, the underlying mechanisms are quite
distinct. In acidified freshwater, molecular change to chemical cues along
with reduced olfaction sensitivity appear to be the primary causes of olfactory-mediated behavioural impairment. By contrast, experiments simulating
future ocean acidification suggest that interference of high CO2 with brain
neurotransmitter function is the primary cause for olfactory-mediated behavioural impairment in fish. Different physico-chemical characteristics
between marine and freshwater systems are probably responsible for these
distinct mechanisms of impairment, which, under globally rising CO2
levels, may lead to strikingly different consequences to olfaction. While fluctuations in pH may occur in both freshwater and marine ecosystems, marine
habitat will remain alkaline despite future ocean acidification caused by
globally rising CO2 levels. In this synthesis, we argue that ecosystem-specific
mechanisms affecting olfaction need to be considered for effective management and conservation practices.
1. Introduction
Anthropogenic acidification of lakes, rivers and the oceans can have dramatic and
far-reaching impacts on the structure and function of aquatic ecosystems [1–5].
Historically, the problem of acidification has mostly been associated with freshwater ecosystems affected by acid rain precipitation [6–8]. Decades of this
phenomenon have reduced the acid neutralizing capacity in many impacted
areas, leading to persisting vulnerability of freshwater ecosystems to future
changes of water pH [9,10]. However, attention has shifted towards the threat
of acidification in marine ecosystems, as increased CO2 uptake from the atmosphere is causing ocean pH to decline with a concomitant increase in dissolved
CO2 [5,11]. Although the mechanism of anthropogenic acidification differs
between freshwater and marine ecosystems (box 1), the underlying cause is the
same—the continued burning of fossil fuels (figure 1). Furthermore, the chemical
changes associated with acidification can lead to fundamental changes to biological and ecological processes in both freshwater and marine ecosystems,
including impacts on individual performance (e.g. reproductive output or
predator avoidance), species interactions and community structure [7,11,19].
& 2013 The Author(s) Published by the Royal Society. All rights reserved.
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2
For many aquatic organisms, one of the main consequences of non-lethal acidification of aquatic ecosystems
may be the disruption of olfaction and chemosensory abilities
[20,21]. The detection of chemical cues and signals by olfactory and gustatory receptors plays a central role in the
decision-making process [22], especially in structurally complex or turbid environments or under low light conditions
[23 –25]. For instance, homing [26,27], microhabitat choice
[28,29], mate selection [30,31], kin recognition [32], food
location [33], dominance interactions [34] and predator avoidance [35,36] are all mediated by the detection of chemical
cues, at least to some extent. Any interference with the functioning of normal chemosensory responses could reduce the
ability to perceive basic environmental stimuli or public
information that is critical for long-term survival. Consequently, impaired olfactory-mediated responses caused by
acidification in freshwater and marine ecosystems may have
significant impacts on the ecology and life histories of
many aquatic organisms. Experiments with freshwater fish
have demonstrated a range of behavioural and ecological
changes associated with the impairment of olfaction and
chemical cues detection under weakly acidified conditions
(approx. pH 6.0) [20,37,38]. Recently, a very similar range of
behavioural changes has been observed in experiments
with marine fish exposed to predicted future changes in
ocean pH due to rising atmospheric CO2 [39,40]. However,
despite the remarkable similarity in many of the behavioural
responses, the underlying mechanisms appear to be entirely
different [37,41]. In this review, we compare and contrast the
effects of acidification on olfactory-mediated behaviour in
freshwater and marine organisms and present evidence for
significant dissimilarities between the underlying mechanisms
of action. Numerous studies demonstrating these effects
have used fish as a model organism, whereas studies using
invertebrates are by comparison much rarer. Reflecting this
asymmetry, we mostly used fish examples to explore this question and included invertebrates examples when available. We
then consider how projected increases in atmospheric CO2
may affect marine and freshwater organisms. Identifying the
consequences of acidification on olfactory-mediated behaviour, along with an understanding of the mechanisms at play
become critical for applying effective management and
conservation practices in freshwater and marine ecosystems.
2. Ecological effects of acidification on olfaction
(a) Freshwater ecosystems
Experiments in freshwater have demonstrated that the ability
of fishes to detect and respond to chemical cues of injured
conspecifics (termed ‘alarm cues’ [24,25]) may be disrupted
under weakly acidified conditions. Alarm cues are particularly useful for studying chemosensory abilities in fishes as
they trigger innate, readily measurable overt responses
[24,42]. Exposure to alarm cues can elicit adaptive predator
avoidance behaviour, such as reduced activity levels and
increased hiding or tighter group cohesion [43]. These behavioural responses to alarm cues have been observed in a range
of freshwater fishes, including fathead minnows (Pimephales
promelas), finescale dace (Phoxinus neogaeus), pumpkinseed
(Lepomis gibbosus) and rainbow trout (Oncorhynchus mykiss)
[20,37,44]. However, predator avoidance behaviour was
diminished or absent when these alarm cues were presented
in experimental treatments acidified using a minute amount
of sulfuric acid (often a major contributor to freshwater acidification) [20,38,45]. Furthermore, behavioural responses to
basic chemical stimuli from food (amino acids) were significantly reduced under a similar range of pHs (e.g. 5.0–6.0)
in fathead minnows and Atlantic salmon (Salmo salar)
[38,46]. Under field conditions, experiments revealed a similar absence of response to chemosensory cues in brook
trout (Salvelinus fontinalis) and Atlantic salmon exposed to
conspecific alarm cues in acidic streams ( pH range; 5.8 –
6.3), whereas avoidance responses were retained in neutral
pH streams (pH range; 6.8–7.4) [20,45,47,48]. Likewise, episodic acidifying events may cause short-term loss of
chemosensory abilities in freshwater fish. Field tests demonstrated that following acid rain precipitations, the response of
Atlantic salmon to alarm cues did not differ from their
response to a control stimulus of stream water (at approx. pH
6.2) [45]. Following subsequent flushing of the acid pulses,
the response of the salmon returned to pre-acidification levels
Phil Trans R Soc B 368: 20120447
Acidification of rivers and lakes occurs chiefly as a result of acidified rain or snow depositions. The process that results in the
formation of acid depositions begins with emissions into the atmosphere of sulfur dioxides and nitrogen oxides. These gases
are typically released following fossil fuel combustion and combine with water vapour to form sulfuric and nitric acids
(figure 1). When such precipitations fall, they have become highly acidic, typically with pH values of 5.6 or lower. In the American Northeast and Eastern Europe, decades of acid precipitations have depleted the soil buffering capacities such that any
further acidic depositions may have rapid and long-lasting effects on ambient water pH [12]. While in these regions emissions
of sulfur dioxide have generally decreased when compared with previous decades [13], globally they remain at relatively constant levels (e.g. approx. 65 kton in 2000) from the increasing sulfur dioxide emitting countries [14,15]. As such, the problem of
acid rain is likely to expand to areas previously unaffected by this phenomenon.
Ocean acidification occurs through the uptake of additional CO2 from the atmosphere. Over 2 trillion tons of additional
CO2 (550 Gt carbon) has been released into the atmosphere by fossil fuel burning, cement production and land use changes
since the industrial revolution [16 –18]. The partial pressure of CO2 at the surface ocean is proportional to that in the atmosphere, consequently more CO2 is taken up by the ocean as atmospheric CO2 levels rise. Additional CO2 reacts with water to
form carbonic acid (H2CO3), which quickly disassociates to form Hþ ions and bicarbonate (HCO32) ions. Excess Hþ ions
bond with CO322 ions producing more HCO32. Adding more CO2 to sea water thus increases aqueous CO2, bicarbonate
and hydrogen ions, the latter having the observed effect of lowering sea water pH, and decreases the abundance of carbonate
ions (figure 1).
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Box 1. The acidifying processes.
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3
H2SO4
SO2 + H2O
HNO3
CO2
NOx
wet
dry
acid depositions
H2CO3
H+ + CO32–
HCO3–
lake
HCO3– + H+
Figure 1. Anthropogenic sources of marine (left) and freshwater ecosystem acidification (right). Ocean acidification occurs through the uptake of additional CO2 from the
atmosphere, the CO2 converting into carbonic acid as it reacts with seawater. In freshwater systems, acidifying depositions occur following the release of nitrogen oxides
(NOx) and sulfur dioxide (SO2) into the atmosphere, mainly from the combustion of fossil fuels, which then may fall in dry or wet form. (Online version in colour.)
(approx. pH 6.9) and they exhibited strong predator avoidance
behaviour in the presence of the alarm cues.
Together, these experiments and observations demonstrate
that even relatively small changes in pH (approx. 0.5 unit)
can dramatically affect both the feeding and antipredator
responses of freshwater fishes.
Such demonstrated loss of adaptive alarm behaviour
under weakly acidic conditions is probably due to an
inability to detect and thus respond to alarm cues. Indeed,
following the pairing of aversive alarm cues stimulus with
a novel odour, wild Atlantic salmon tested in neutral streams
subsequently responded to the novel odour as a dangerous
stimulus [49]. However, following the same procedure, similar learned responses did not occur for salmon conditioned
and tested in acidic streams, suggesting a pH-mediated
inability to perceive the information of risk that is normally
associated with the alarm cues [50]. Under acidified conditions, the lack of antipredator response towards the alarm
cues probably prevents the learned association of risk with
the novel predator odour, resulting in failed learning. Thus,
the retention of and the ability to generalize acquired predator recognition may be significantly impaired under weakly
acidic conditions [51,52].
Failure to appropriately respond to chemical cues could
significantly increase mortality rates of prey and potentially
alter population dynamics. The ecological consequence of
pH-mediated chemosensory impairment to chemical alarm
cues was demonstrated in staged encounters between rainbow
trout prey and a predator, the largemouth bass (Micropterus
salmoides). Bass captured trout faster and in greater proportion
when trout alarm cues introduced in test tanks were acidified
(pH 6.0) compared with treatments were alarm cues were
introduced using neutral pH water [45]. Thus, prey ‘naivety’
arising from acid-mediated chemosensory impairment led to
greater predation cost. In addition to alarm behaviour, weak
acidification may affect other behavioural activities in freshwater fishes. Suppression of spawning [53], nest digging [54]
and migration behaviour [55] were demonstrated in landlocked sockeye salmon (Oncorhynchus nerka) exposed to
weak levels of acidification (i.e. pH 6.1–6.3). Thus, non-lethal
anthropogenic acidification may affect a wide range of behaviour in freshwater fishes, with significant effects on their life
histories and role in the ecosystem. Although providing
important insights to the potential ecological consequences of
acidity-mediated maladaptive behaviour, the studies mentioned above were conducted under controlled laboratory
conditions. Future studies would further this knowledge,
while providing ecologically relevant data, by conducting
investigations under field conditions.
Akin to fish olfaction abilities, experimental evidence
demonstrated that freshwater invertebrates may, likewise,
be affected by acidification. In crayfishes, Orconectes virilis
and Procambarus acutus, weakly acidified conditions ( pH
5.8) had no effect on feeding behaviour to an amino acids
mixture but more severe acidification levels ( pH 4.5 and
3.5) led to significant reductions of this response [56]. Interestingly, in this experiment the amount of food consumed
was not affected by acidification, suggesting that compared
with fishes, these crustaceans may have higher tolerance
towards acidification. Similar olfaction impairment was
also demonstrated in the crayfish Cambarus baroni, which
showed reduced ability to detect a food source at pH 4.5 [57].
(b) Marine ecosystems
Atmospheric CO2 has increased from approximately 280 ppm
at the start of the industrial revolution to over 390 ppm today,
and there has been a corresponding 0.1 pH unit decline in
ocean pH [16]. Depending on emission scenarios, CO2 levels
in the atmosphere could exceed 900 ppm by the end of the century [58]. This would cause the pH of the ocean to drop another
0.3–0.4 units. Under such scenarios of future oceanic acidification, the ability of larval orange clownfish (Amphiprion percula)
to discriminate between olfactory cues involved in the selection
of suitable settlement sites was tested [21]. Larval clownfish
reared in control seawater (today’s pH of 8.15) had the
ability to discriminate between chemical cues of suitable
versus unsuitable settlement sites and between kin and nonkin. However, when larvae were reared from hatching under
conditions simulating near-future CO2-induced ocean acidification (pH 7.8 and 1050 ppm CO2), this discriminatory
ability was lost and larvae became attracted to olfactory stimuli
that they normally avoided. Similarly, five-lined cardinalfish
(Cheilodipterus quinquelineatus) exposed to future conditions
Phil Trans R Soc B 368: 20120447
ocean
CO2 + H2O
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NOx+ H2O
SO2
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3. Mechanisms of behavioural impairment
Although olfaction impairment in freshwater and marine
organisms exposed to acidified conditions may have very
similar consequences on behaviour (table 1), translating into
equivalently significant ecological costs (e.g. increased predation, reduced recruitment), given the different modes of
acidification between freshwater and marine habitat, the mechanisms affecting olfactory/chemosensory response appear to
be entirely distinct.
(a) Freshwater ecosystems
In freshwater, acidification may affect fish olfaction by two
non-mutually exclusive mechanisms. First, reduced chemosensory abilities observed in acidified conditions can stem
from molecular change to chemical cues, essentially rendering them as ‘non-functional’ [37]. For example, the alarm
cues of Ostariophysan fishes probably consist of a suite of
active compounds such as purine-N-oxides [30,68] and glycosaminoglycan chondroitins [79]. Analytical chemical work
has suggested that under acidic conditions, one of these
active components, hypoxanthine-3-N-oxide is converted to
6,8-dioxypurine with a loss of the 3-N-oxide functional
group [80,81] (figure 2). This suggests that acute exposures
to acidic conditions might result in the non-reversible loss of
the N–O functional group, reducing the effectiveness of the
alarm cue to elicit an adaptive alarm response [82]. It is
4
Phil Trans R Soc B 368: 20120447
more attracted to male olfactory cues when pH was raised
from 8.0 to 9.5 using NaOH [70]. In pipefish (Syngnathus
typhle), a similar pH increase through Na2CO3 addition
reduced the number of pregnant males [71]. Reducing seawater
pH to 7.5 with CO2 had no effect on mating propensity in the
pipefish [71], however the duration of exposure to acidified
conditions (less than 5 h total) was probably insufficient for
any behavioural effects of elevated CO2 to be induced [61].
While these examples demonstrated effects of seawater alkalinization through eutrophication, rather than its acidification by
rising CO2 levels, they underscore that changes in seawater
pH may alter important processes in sexual selection. At present, a gap in knowledge exists limiting our ability to predict
if near-future ocean acidification scenarios will have similar
effects on mate choice.
In marine invertebrates, acidification has been shown to
detrimentally affect behavioural choices at very low pH. In
hermit crabs (Pagurus bernhardus), finding and selecting the
gastropod shells they inhabit is conducted via tactile, visual
and chemical assessment. Choosing an optimal shell is vital
as it provides protection against environmental extremes
and predators. Under highly acidified conditions (pH 6.8 and
12 000 ppm CO2), crabs were less likely to change from a suboptimal to an optimal shell than those in untreated seawater,
while the time required to change shells significantly increased
[72]. Additionally, at this reduced pH level, hermit crabs were
less successful in locating an odour source and had lower
locomotory activity compared with hermit craps in untreated
seawater [73]. Thus, reductions in seawater pH may have disruptive consequence on resource assessment and gathering along
with the decision-making processes of hermit crabs. Whether
these impaired response patterns occur at more representative
future levels of ocean acidification (CO2 levels , 1000 ppm)
and are generalizable in marine invertebrates is unknown.
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of CO2 demonstrated significantly reduced abilities to discriminate between odours of their home site versus a foreign site
[59]. In another study, aquarium-reared larval clownfish
under acidified conditions became attracted to the odour of predators and were unable to distinguish between the chemical
cues of predators and non-predators [60]. Further experiments
demonstrated that clownfish and wild-caught damselfish
(Pomacentrus wardi) reared under high CO2 treatments (700
and 850 ppm CO2) for only 2–4 days also displayed impaired
olfactory-mediated behaviour, whereby CO2-treated fish
initially avoided predator odour, as did control fish, but subsequently became attracted to this odour [61].
Similar to the loss of alarm response in freshwater fishes,
laboratory tests revealed that juvenile damselfish exposed to
CO2-acidified conditions for 4 days exhibited a decreased
response to conspecific chemical alarm cues [62]. The response
of predators to prey alarm cues was also affected, with a
common predator of juvenile damselfishes, the brown dottyback (Pseudochromis fuscus), spending approximately 20% less
time in a water stream containing prey odour following
exposure to near-future CO2-acidification conditions [62,63].
Reduced attraction to prey odour by the predator did not, however, offset an increased risk of predation in prey fish exposed
to elevated CO2. Mortality rates of small damselfishes were
almost twice that of controls when a high CO2-exposed dottyback interacted with high CO2-exposed damselfish in a
mesocosm experiment [62].
Field tests conducted in natural habitat revealed significant ecological outcomes of behavioural changes caused by
predicted ocean acidification. Juvenile damselfish exposed
to CO2-acidified conditions and then placed on patches of
coral habitats were more active and ventured further from
shelter than juveniles exposed to current-day CO2 levels
[61,62]. This riskier behaviour was associated with increased
mortality from predation when compared with control fish
[61,62]. Reduced olfaction abilities and other cognitive
impairment that occurs at elevated CO2 levels [41,64,65]
also appear to affect navigation and homing of reef fish
under natural conditions. For instance, cardinalfish uses
olfactory cues and visual landmarks to aid in navigation to
daytime resting sites after nocturnal foraging, but cardinalfish reared under elevated CO2 treatments displayed a
22– 31% reduction in homing success compared with control
fish when released at 200 m from home sites [66]. Despite
showing home-site fidelity, high CO2-treated fish were
more active and ventured further from the reef compared
with control fish [66], which would be likely to increase their
risk of predation. Given that the persistence of most coastal
species depends on the ability of larvae to find suitable settlement sites and avoid predators at the end of their pelagic phase,
the effects of ocean acidification on habitat selection and predator avoidance behaviour may have significant consequences
for the replenishment of fish populations. Furthermore, variation in sensitivity to acidification among prey species [67]
and shifts in prey preference by predators [62] could lead to
far-reaching effects on reef fish community structure.
In addition to predator–prey interactions and homing
behaviour, changes in seawater pH may also have consequences on mate choice and reproductive behaviour. For
instance, females may choose between males using major
histocompatibility complex (MHC) alleles, which may be
perceivable through scent [68,69]. In a laboratory choice experiment, gravid female stickleback (Gasterosteus aculeatus) were
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Table 1. Effects of acidification/alkalinization on olfactory/chemosensory abilities and its consequences in fish and invertebrate species. PC, post-conditioning;
RTE, reciprocal transfer experiment.
type of cue
food stimulus
food searching
treatment/
environmental
change and range
consequence
references
freshwater
Pimephales promelas
food stimulus
food searching
pH 6.0
acidification (H2SO4)
pH 6.0
pH 5.0
Salmo salar
L-serine
odour
discrimination
Onchorynchus mykiss
alanine
L-serine
—
electrophysiological
[38]
neutral
negative
[74]
neutral
negative
[46]
acidification (HNO3 and
H2SO4)
pH 5.1
negative
pH 5.1
acidification (H2SO4)
positive
[75]
2
metal dilution (Al )
response
Orconectes virilis a
Procambarus acutus a
Cambarus bartoni a
amino acids
mixture
food stimulus
food searching
food searching
pH 4.7
negative
pH 4.7,
20 mmol l21 Al2
negative
acidification (H2SO4)
pH 6.8
pH 5.8
neutral
pH 4.5
pH 3.5
negative
negative
acidification (H2SO4)b
pH 7.5
pH 4.5
S. salar
testosterone,
ovulated female
urine
electrophysiological
response
[56]
neutral
[57]
neutral
negative
pH 7.5
acidification (H2SO4)
intermediate
pH 6.5 – 3.5
increasingly
negative
[76]
alkalinization (NaOH)
pH 8.5 – 9.5
Pimephales promelas,
Phoxinus neogaeus
conspecific skin
extract,
alarm response
hypoxanthine-3-Noxide
Lepomis gibbosus
conspecific skin
—
acidification (H2SO4)
pH 6.0
—
increasingly
negative
negative
[37]
negative
alarm response
acidification (H2SO4)
negative
extract,
congener skin
—
pH 6.0
—
negative
extract,
hypoxanthine-3-N-
—
—
negative
[44]
oxide
(Continued.)
Phil Trans R Soc B 368: 20120447
Poecilia sphenops
acidification (H2SO4)
pH 6.5
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species
behavioural
response
5
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6
Table 1. (Continued.)
O. mykiss
type of cue
behavioural
response
conspecific skin
alarm response
acidification (H2SO4)
consequence
references
negative
[20]
pH 6.0
extract
conspecific skin
extract
—
stream acidificationc
pH 6.1
negative
S. salar
conspecific skin
extract
alarm response
acidic rainc
pH 6.2
negative
O. mykiss
—
survival to
predator
acidification (H2SO4)
pH 6.0
negative
S. salar
conspecific skin
alarm response
stream acidificationc
negative
S. salar
extract
conspecific skin
acquired predator
pH 5.8 – 6.1
stream acidificationc
extract, lemon
odour
O. mykiss
conspecific skin
extract, predator
odour
pH 6.1
negative
1 day PC
—
negative
acidification (H2SO4)
conditioning
2 days PC
pH 6.0
—
7 days PC
S. salar
conspecific skin
extract
alarm response
RTE
—
[47]
[50]
recognition
conditioning
acquired predator
recognition
[45]
[51]
negative
negative
—
negative
c
stream acidification
pH 6.1
pH 7.3
[77]
negative
neutral
marine
Gasterosteus aculeatus
male odour
mate choice
alkalinization (NaOH)
pH 9.5
positive
Pomacentrus moluccensis,
habitat odour
habitat choice
elevated carbon dioxide
negative
[59]
[66]
P. amboinensis,
P. chrysurus
[70]
700, 850 ppm CO2
Cheilodipterus
quinquelineatus
habitat odour
habitat choice
elevated carbon dioxide
550– 950 ppm CO2
negative
—
habitat odour
homing response
elevated carbon dioxidec
negative
habitat choice/
550– 950 ppm CO2
acidification, elevated
Amphiprion percula
habitat odour,
Pagurus bernhardus
a
Pagurus bernhardus
b
conspecific
odour
homing
gastropod shell
cues
resources
assessment
carbon dioxide
pH 7.8, 1050 ppm CO2
A. percula
food searching
predator odour
avoidance
negative
acidification, elevated
carbon dioxide
pH 6.8, 12 000 ppm CO2
food odour
[21]
[72]
negative
acidification, elevated
carbon dioxide
pH 6.8, 12 000 matmCO2
acidification, elevated
[73]
negative
[60]
carbon dioxide
pH 7.8, 1000 ppm CO2
negative
(Continued.)
Phil Trans R Soc B 368: 20120447
Salvelinus fontinalis
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species
treatment/
environmental
change and range
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Table 1. (Continued.)
Plectropomus leopardus
type of cue
behavioural
response
predator odour
antipredator
elevated carbon dioxide
consequence
references
negative
[78]
negative
[41]
700– 850 matm CO2
A. percula
predator odour
predator
discrimination
elevated carbon dioxide
900 matm CO2
A. percula
Pomacentrus wardi
P. moluccensis,
predator odour
live predators
live predator
P. amboinensis,
antipredator
antipredator
predator
avoidance
neutral
elevated carbon dioxide
550 ppm CO2
[61]
neutral
700, 850 ppm CO2
negative
elevated carbon dioxidec
700 ppm CO2
neutral
850 ppm CO2
elevated carbon dioxide
negative
negative
[62]
700 matm CO2
P. nagasakiensis,
P. chrysurus
Pseudochromis fuscus
live prey
prey selection
elevated carbon dioxide
700 matm CO2
reversed
preferred
size
selection
P. moluccensis,
P. chrysurus,
conspecific skin
extract
antipredator
elevated carbon dioxide
700– 850 ppm CO2
negative
live predators
survival
elevated carbon dioxidec
negative
prey odour
700– 850 ppm CO2
acidification, elevated
[67]
P. amboinensis
P. nagasakiensis
P. chrysurus
Pseudochromis fuscus
prey skin extract
discrimination
Pomacentrus amboinensis
conspecific skin
extract, predator
acquired predator
recognition
odour
[63]
carbon dioxide
pH 8.0, 630 matm CO2
negative
pH 7.8, 950 matm CO2
negative
acidification, elevated carbon
dioxide
pH 8.0, 700 ppm CO2
pH 7.9, 850 ppm CO2
[65]
negative
negative
a
Invertebrate.
Conducted sequentially.
c
Experiments conducted under field conditions.
b
unknown, but likely that changes in pH also affect chondroitin functionality as well. In keeping with the hypothesis of
an irreversible molecular change to the chemical cue, shortterm (48 h) changes in water pH, from neutral to weakly
acidic and back to neutral, were well matched with the ability
of fish to detect and respond to the alarm cues [37]. This experimental design suggested that no permanent olfactory damage
or significant stress could account for the loss of response
observed at the acidity level tested (pH 6.0). Similarly, a
reverse transplant experiment, in which Atlantic salmon
from either neutral or acidic streams were alternatively tested
in their natal stream or in a stream of a different pH, demonstrated that the rearing pH was not directly affecting salmon
chemosensory detection abilities. After a 24 h period of acclimation in stream enclosures, the response to chemical alarm cues
was detectable in all salmon (reared in neutral or acidic
streams) when tested under neutral but not under acidic
streams [77]. Thus, under acidic condition, the alarm cues
Phil Trans R Soc B 368: 20120447
900 matm CO2, GABA-A
receptor antagonist
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species
treatment/
environmental
change and range
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(a)
O
O
O
+ N
H
–
N
N
N
+ N
(b)
H
N
N
N
H
OH
(i)
(ii)
GABA
future seawater:
elevated pCO2
elevated H+
regulatory
changes in fish:
elevated HCO3–
reduced Cl–
maintained H+
hyperpolarizing current
when binding of GABA to the
GABA-A receptor leads to
inflow of Cl– and/or HCO3–
into neurons
altered
gradients of Cl–
and/or HCO3–
over neuronal
membranes
depolarizing current when
Cl–
binding of GABA to the
GABA-A receptor leads to HCO –
3
outflow of Cl– and/or HCO3–
from neurons
Figure 2. Potential mechanisms leading to olfactory-mediated behavioural impairment in freshwater (a) and marine fishes (b). (a) In the Ostariophysi alarm cue
molecule (hypoxanthine-3-N-oxide), at neutral pH the acid – base equilibrium heavily favours the deprotonated (N – O2) form (i). However, as the pH decreases, the
acid – base equilibrium shifts in favour of the hydroxy form (ii), decreasing the relative concentration of the deprotonated active form of the chemical signal.
Modified from Brown et al. [61]. (b) In marine fish, physiological interferences arising from the hyperpolarization of the neurotransmitter membrane of the
GABA-A receptor occur when exposed to elevated CO2-acidified conditions. Adapted from Nilsson et al. [39]. (Online version in colour.)
appear to undergo molecular changes and become either completely degraded (i.e. non-functional) and unrecognizable, or
the concentration of its active component is reduced below a
threshold necessary to trigger an adaptive alarm response [44].
A second mechanism by which olfaction and chemosensory abilities may be affected stems from physiological
disruptions of the fishes’ olfactory organs, whereby reduced
sensitivity or affinity to fish olfactory receptors may occur
[74,76,83]. In rainbow trout, fathead minnow and Atlantic
salmon, reduced abilities to respond to amino acids or ovulated
female urine were demonstrated at approx. pH 6.0 [38,46,76].
Similar to the pH-dependent response observed for chemical
alarm cues, the feeding response to amino acids was well
matched with short-term changes in water pH. Indeed, Atlantic salmon were attracted to glycine under neutral pH (7.6) but
became indifferent under lower tank pH (5.1), while following
a return to neutrality, salmon olfactory attraction towards
glycine was re-activated [46]. Importantly, these short-term
effects may be magnified in heavily acidified conditions (i.e.
pH , 6.0) under which the release of monomeric ions (Al2,
Cuþ) may further interfere with olfactory epithelia, leading to
lasting chemosensory impairment [75,76].
Intriguingly, in freshwater systems, the ability of fishes to
detect chemical cues may not be steadily affected by acidification. For instance, the time required of gold mollies (Poecilia
sphenops) to locate food sources was not significantly different
between pH 6.0 and pH 7.9 [74]. Likewise, the pH of a novel
odour was not a critical factor for its subsequent recognition
as a danger stimulus by juvenile rainbow trout, as long as it
was paired with chemical alarm cues that were left unacidified
[84]. Thus, in freshwater, acidification does not appear to systematically affect fish chemosensory abilities and olfactory
receptor sensitivity. However, as described earlier, the chemical
nature of the alarm cues appears to be modified, thereby reducing their effectiveness to trigger a response [37]. For this later
mechanism of impairment, a threshold for chemosensory detection has been shown to occur at a pH of approximately 6.3,
whereby rainbow trout failed to respond to chemical alarm
cues [85]. Likewise, electro-physiological recordings of Atlantic
salmon olfactory epithelia were significantly reduced at a pH of
5.5 [76]. Several variables could affect such a potential threshold
of chemosensory impairment, including the species under
investigation along with the chemical compounds tested. However, experimental results performed close to these thresholds
indicate that chemosensory impairment may be readily
reversed following a return of ambient water to neutral pH
[37,46,76,85], thereby suggesting that weak acidification does
not have lasting physiological consequences to fish olfaction.
(b) Marine ecosystems
In contrast to the findings in freshwater fishes, CO2-induced
acidification affects the behavioural response of marine fish
to chemical cues, but does not appear to affect the cue
itself. Orange clownfish larvae reared in control conditions
( pH 8.15) but immediately tested in acidified conditions
( pH 7.6) exhibited the same odour choices as larvae reared
and immediately tested in control water. Larvae reared at
pH 7.6 but tested in control water did not respond to any
olfactory stimuli, just as larvae reared and tested at pH 7.6
water did not respond to odours [21]. This demonstrates
that rearing the fish in acidified conditions causes the behavioural changes, and that the pH of seawater does not seem to
affect the cue, at least for a change in pH of 0.5 unit. Likewise,
using a classical conditioning design, pre-settlement damselfish (Pomacentrus amboinensis) reared in control water were
Phil Trans R Soc B 368: 20120447
GABA binding can be
antagonized experimentally
with gabazine
Cl–
HCO3–
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H
8
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4. Why the difference in response mechanisms?
A critical question arising from the research conducted to date
in freshwater and marine ecosystems is why different mechanisms should be responsible for otherwise similar effects of
acidification on olfactory responses in these two ecosystems.
In what way are freshwater and marine ecosystems fundamentally different in their respective acidification processes that
affect olfactory functions in aquatic organisms? Answering
these questions is important for predicting the effects of different forms of anthropogenic acidification in aquatic systems.
A useful way to contextualize the cause of an apparently
similar impairment to chemosensory functions between
freshwater and marine ecosystems involves comparing their
inherent characteristics of acidification. Freshwater ecosystems often have a pH that is near neutrality but can also be
acidic or alkaline. By contrast, seawater always remains alkaline. Thus, it might not be the change in pH level but rather
the absolute pH value that determines the non-reversible
changes in chemical alarm cues and impairs olfactory neurons in freshwater fishes, but not in marine fishes. In
freshwater systems, behavioural impairment has been
shown to start occurring in mildly acidic conditions (6.3 –
6.5), becoming very evident as pH decreases [38,76,87]. By
contrast, predicted ocean acidification will bring seawater
pH to a more acidic value, but it will still remain alkaline
(i.e. above pH 7.0). In fact, ocean acidification experiments
never get close to the pH levels under which olfaction is
impaired in freshwater. Thus, compared with marine fishes,
freshwater fishes may tend to live in more acidic conditions
and therefore closer to the threshold under which the structure of the chemical alarm cues is changed [37,85] or the
sensitivity of olfactory neurons is affected [38,46,76]. The
chemical bonds of alarm cue molecules, and probably other
odour molecules, are probably sensitive to the absolute pH
they experience, not just a change in pH per se [51,52]. Therefore, the reason why studies on acidification in freshwater
have found that changes to chemical stimuli are responsible
for altered behaviour, whereas this does not appear to be
the case in marine studies, is probably that they are working
in different parts of the pH scale (i.e. weakly acidic freshwater
versus weakly alkaline ocean water).
In addition to absolute pH levels, the absolute pCO2 level
experienced is also critical for understanding the potential
causal mechanism of olfactory-mediated maladaptive behaviour detected in fish. In ocean acidification studies, both the
pH and pCO2 are manipulated, whereas in freshwater acidification studies only pH is manipulated. This reflects the
9
Phil Trans R Soc B 368: 20120447
effects of acidification on olfactory-mediated behaviour. European eels (Anguilla Anguilla) demonstrated a surprisingly
high level of physiological tolerance towards hypercapnia
[89,90]. Although these experiments were conducted in freshwater, such tolerance to hypercapnia is greater than what
can be expected from most teleost fish. Studies conducted on
Atlantic salmon demonstrated that osmotic stress might be
amplified when exposed to acidification [91–93]. As such, it
is not well known how the chemosensory ability of organisms
found in brackish waters will be affected by acidification.
Likewise, for aquatic invertebrates little is known regarding
the mechanisms affecting chemosensorial abilities under
freshwater or marine acidification.
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able to associate a novel predator odour as a stimulus of
danger when the novel odour was paired with innately aversive alarm cues. However, this ability was compromised in
damselfish larvae reared in acidified water for 4 days, despite
holding the recognition phases of the novel predator odour in
control water [86]. Overall, these results show that exposures
to CO2-acidified water affect the olfactory system and that
the observed changes are not caused by an immediate interference to the fishes’ olfactory capabilities or chemical
modification of the odour cues.
The mechanism accounting for a loss of olfaction and
chemosensory abilities in marine fishes exposed to acidified
conditions appears to stem from a disruption of the normal
Cl – and/or HCO3– gradients over neuronal membranes,
causing some GABA-A receptors to become excitatory (depolarizing) rather than inhibitory (hyperpolarizing) [41]. The
GABA-A receptor, which is the major inhibitory neurotransmitter receptor in vertebrate brains, normally hyperpolarizes
neuronal membranes by opening a channel that leads to
an influx of Cl – and HCO3– . When exposed to high CO2,
marine fishes regulate their acid–base balance by accumulating
HCO3– , with compensatory reductions in Cl – [87]. In the brain,
this may lead to disturbances of the normal Cl2 and/or HCO3–
gradients in some neurons, resulting in gradients that favour
influx rather than out flux of these anions. Changes in HCO3–
and Cl – levels during high CO2 exposures thereby affect
behaviour and cause dramatic shifts in sensory choices [41].
Consequently, it is not the change in seawater pH that impairs
olfaction and chemosensory abilities in marine fishes but
rather the long-term exposure to elevated levels of environmental CO2. This is a critical distinction between the effects of
acidification in freshwater systems that occurs as a result of mineral acids, and acidification in marine systems, which is
occurring owing to increased uptake of atmospheric CO2.
Aside from olfaction, neurotransmitter disruption caused
by elevated CO2 levels has far-ranging effects on fishes’ behaviour. For instance, elevated CO2 levels led to increased
activity levels in fish [61,78] and interfered with auditory
preferences, whereby no avoidance behaviour occurred
during playbacks of predator-rich daytime reef recordings
[88]. Furthermore, elevated CO2 repressed the degree of behavioural lateralization, with individual propensity to turn
left or right becoming random under elevated CO2 [64].
Interestingly, treatments using a specific GABA-A receptor
antagonist (gabazine) administered 30 min before behavioural assays restored behavioural responses in clownfish,
(A. percula) that had been reared for 11 days in acidified conditions. When tested prior to administration of the receptor
antagonist, the fish exhibited abnormal responses to chemical
cues for a predatory fish. By contrast, they displayed similar
olfaction abilities as fish reared in control conditions following the administration of the receptor antagonist, indicating
that altered GABA-A receptor activity mediates the effects
of high CO2 on neural function in marine fishes, including
reversal of olfactory responses [41]. Although neurophysiological stress triggered by high CO2 may lead to olfactory-mediated
maladaptive behaviour, it is unknown to what extent the
concomitant changes in pH predicted under future ocean acidification scenarios may directly affect the chemosensory cues.
Behavioural tests conducted under a range of pH while keeping
CO2 constant would resolve this question.
As it pertains to organisms living in brackish conditions
(e.g. estuarine ecosystems), little is known about the potential
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In order to understand the potential consequences of anthropogenic acidification on olfactory functions of freshwater and
marine organisms, it is necessary to consider the spatial and
temporal variation of pH and pCO2 in their native habitats.
Species living in environments that naturally experience significant variation in pH and/or pCO2 may be adapted to
this variation, and thus may be more tolerant of anthropogenic acidification compared with species living in more
stable pH and pCO2 environments [96,97]. In freshwater ecosystems, the magnitude of pH changes may be substantial.
For example, short-term rainfall events (i.e. approx. 30 mm)
may be sufficient to reduce ambient acidity by 0.2–0.6 pH
units [45,98] whereas major rain precipitation events may
have more drastic effects on ambient acidity levels [99].
Additionally, in fresh and brackish water with poor buffering
capacity, daily fluctuations of nearly 1 pH unit may occur as a
function of changing dissolved CO2 concentrations driven by
algal metabolism and growth [100,101]. Likewise, in some
marine habitats, pH gradients can be quite steep. For example,
pH typically fluctuates on a diel cycle in shallow coral reef
habitats, changing by more than 0.5 units in some locations
[102,103]. The cause of this variation in pH is a change in the
balance between the respiratory CO2 production and photosynthetic CO2 consumption of reef organisms, including
corals and their symbiotic algae. On shallow reef flats that
have restricted water exchange with the open ocean, pCO2
may vary by over 1000 matm over 24 h, driving the variation
in pH seen in these habitats [104,105]. Variations in pH and
pCO2 are generally much less in reef habitats with greater
water exchange, but may still shift by more than 0.2 units
within a few hours [106], whereas areas of upwelling and
coastal habitats can see sharp pH declines that last for days
to weeks (approx. 0.4 pH units) [102,107]. Thus, significant
10
Phil Trans R Soc B 368: 20120447
5. Environmental variability and adaptations
shifts in pH may occur in many freshwater and some marine
habitats, and this could influence the tolerance to acidification
of species living within these particular habitats.
There is evidence for adaptation to acidified habitats in
freshwater ecosystems. Natural factors (e.g. rain or snowmelt,
high decomposition rates, sulfur oxides/sulfuric acids
released from volcanic activity and forest fires) may create
extended or even permanent acidification of many freshwater
habitats [3,12,108,109]. Associated with these conditions,
several freshwater fish species have evolved physiological
tolerance towards extreme acidification levels [108,110].
Whether fish in these habitats also experience impaired
olfactory-mediated behavioural responses or have evolved
tolerance is yet to be tested. Interestingly, a shift in sensitivity
of other sensory modalities was shown to occur in juvenile
Atlantic salmon inhabiting weakly acidic streams, displaying
greater reliance on vision to mediate local predation risks
[48]. This suggests that differences in antipredator responses
may occur and be linked to the perceived level of information
available from different sensory modalities (e.g. from losing
chemical information under acidic conditions). However, it
might not simply be the range over which pH varies that is
important for tolerance to acidification, but also the duration
of pH and pCO2 shifts might be critically important. For
example, considerable fluctuations in pH and pCO2 may
take place in shallow coral reef habitat, but they occur on a
regular diel cycle. Low pH and high pCO2 occur at night
for a few hours, and the opposite takes place during the
day [103–105]. These short-term environmental fluctuations
appear to be of insufficient duration to have led to the evolution of tolerance to low pH or high CO2 for extended
periods (days) [41,111]. Indeed, maladaptive olfactorymediated behaviour only starts to occur after at least 24 h
exposure to high CO2 [61] in marine fishes. Consequently, a
few hours of high CO2 exposure overnight [104,112] is
probably of insufficient duration to lead to any discernable
effects. A 2–4 day exposure to CO2 conditions similar to
that briefly experienced overnight is enough to cause
impaired behavioural responses in fish [61], indicating that
these short-term exposures to elevated CO2 have not produced adaptations that overcome longer term exposure to
elevated pCO2.
Unlike most marine systems, fluctuations in pCO2 may
occur for extended periods (e.g. weeks to months) in some
freshwater systems. In large rivers and lakes, O2 saturation
may naturally range from anoxia to super-saturation as a
result of seasonal phenomena [113,114]. Environmental
hypercapnia is common in some freshwater systems, with
the most extreme examples being tropical aquatic environments [115]. Many freshwater fish have become tolerant to
these O2 fluctuations. In highly productive systems in
which CO2 and O2 are usually inversely related [116], it is
likely that they may also have become tolerant to high CO2.
Thus, if freshwater fish can tolerate periods of lower O2 tension than most marine fishes, then they may also have
become more tolerant to higher pCO2 tension [117]. Although
complete or significant degrees of physiological pH compensation during hypercapnia have been demonstrated in both
freshwater and marine fish species [118–120], freshwater
fishes were shown to have adapted to the most extreme conditions [117]. Therefore, compared with marine ecosystems,
the extended periods of pH and pCO2 shifts occurring in
freshwater may have set the stage for greater tolerance of
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different mechanism of acidification in these two ecosystems,
and there are important considerations that emerge from
these differences in experimental approach. First, although
the pH of seawater is usually much higher than that of freshwater when both are in equilibrium with the atmosphere
(and thus have approximately the same pCO2), freshwater
studies have not manipulated pCO2 levels. Consequently, it
is impossible to conclude that freshwater fishes are more tolerant to acidification than marine fishes simply because their
behaviour is not affected at the pH levels at which marine
fishes are highly affected. Secondly, if pCO2 remains relatively unchanged in freshwater that is acidified by acids,
because any CO2 generated is rapidly equilibrated with the
atmosphere, then a similar mechanism of behavioural
change cannot be expected to occur in freshwater fishes compared with marine fishes that are exposed to increased pCO2.
At identical pH levels, there is evidence that CO2 has greater
negative impacts on aquatic organisms when compared with
mineral acids [94,95]. However, further research is needed to
carefully elucidate the various effects of pH and pCO2 in
ocean acidification research. Considering freshwater fishes,
it is unknown whether their sensitivity to increasing pCO2
is the same as in marine fishes. It is possible that freshwater
fishes might be less sensitive to future changes in pCO2
than marine fishes, but to our knowledge this hypothesis
has not been tested.
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6. Management implications and conclusions
Acknowledgements. The authors wish to thank Howard Browman for
organizing ‘Workshop on acidification in aquatic environments:
what can marine science learn from limnological studies of acid
rain?’ from which this work stemmed. We also wish to thank the
reviewers of this manuscript for providing constructive comments.
Funding statement. This work was supported by a grant from Coordenação de Aperfeiçoamento de Pessoal de Nı́vel Superior (CAPES) PVE
to A.O.H.C.L. P.L.M. is supported by the Australian Research Council. M.C.O.F. is supported by the Natural Sciences and Engineering
Research Council of Canada.
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