Aquatic Toxicology 126 (2013) 365372

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Aquatic Toxicology
journal homepage: www.elsevier.com/locate/aquatox

Review

Climate change and ocean acidicationInteractions with aquatic toxicology

Mikko Nikinmaa
Department of Biology, University of Turku, FI-20014 Turku, Finland

a r t i c l e i n f o a b s t r a c t

Article history: The possibilities for interactions between toxicants and ocean acidication are reviewed from two angles.
Received 29 August 2012 First, it is considered how toxicant responses may affect ocean acidication by inuencing the car-
Received in revised form bon dioxide balance. Second, it is introduced, how the possible changes in environmental conditions
12 September 2012
(temperature, pH and oxygenation), expected to be associated with climate change and ocean acidi-
Accepted 12 September 2012
cation, may interact with the toxicant responses of organisms, especially sh. One signicant weakness
in available data is that toxicological research has seldom been connected with ecological and physio-
Keywords:
logical/biochemical research evaluating the responses of organisms to temperature, pH or oxygenation
Climate change
Carbon dioxide
changes occurring in the natural environment. As a result, although there are signicant potential inter-
Contaminant discharge actions between toxicants and natural environmental responses pertaining to climate change and ocean
Hypoxia acidication, it is very poorly known if such interactions actually occur, and can be behind the observed
pH disturbances in the function and distribution of organisms in our seas.
2012 Elsevier B.V. All rights reserved.

Contents

1. Introduction: why climate change and ocean acidication are not independent from aquatic toxicology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 365
2. The interactions between natural environmental variables and toxicant responses have been little studied . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 366
3. Major sources of pollutants in oceans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 366
4. How can pollutants inuence ocean acidication . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 367
4.1. Effects on primary productivity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 367
4.2. The formation of calcied structures and their circulation in oceans may affect carbon dioxidecarbonate balance . . . . . . . . . . . . . . . . . . . . . 367
4.3. Toxicant-induced changes in cellular respiration may affect carbon dioxide balance in marine environments . . . . . . . . . . . . . . . . . . . . . . . . . . . 368
5. The interactions between toxicant responses and natural environmental variables associated with climate change and ocean acidication . . . 368
5.1. Temperature and toxicant responses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 368
5.2. Interactions between toxicant responses and pH . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 369
5.3. Interactions between toxicant responses and water oxygenation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 370
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 370
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 370

1. Introduction: why climate change and ocean total global photosynthesis (Field et al., 1998; Falkowski, 2012).
acidication are not independent from aquatic toxicology Since photosynthesis is the major consumer of carbon dioxide,
any changes of phytoplankton abundance will affect the overall
Climate change and ocean acidication are largely thought to be carbon dioxide balance. Phytoplankton also affects carbon diox-
caused by increased atmospheric carbon dioxide level. While a lot ide balance via the oceanic carbon cycle and the predicted changes
of emphasis has gone on terrestrial plants, especially rain forests, would decrease the efciency of carbon dioxide removal from the
acting as carbon dioxide sinks because of their photosynthesis, atmosphere (Cermeno et al., 2008). Thus, any effect of toxicants on
little attention has been paid on what happens to a very impor- global phytoplankton abundance will affect carbon dioxide balance.
tant carbon dioxide consumer group, autotrophic phytoplankton. Notably, there has been a global decrease of oceanic phytoplankton
Recent estimates suggest that they account for nearly half of the in the last century (Boyce et al., 2010).
Any increase in atmospheric carbon dioxide level will shift the
carbon dioxidecarbonate equilibrium in water to acidic direction
Tel.: +358 23335731; fax: +358 23336598. (Fig. 1). Consequently, the ocean will be acidied (for reviews on
E-mail addresses: miknik@utu., mikko.nikinmaa@utu. ocean acidication, see e.g. Fabry et al., 2009; Feely et al., 2009).

0166-445X/$ see front matter 2012 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.aquatox.2012.09.006
366 M. Nikinmaa / Aquatic Toxicology 126 (2013) 365372

Fig. 1. Principles of oceanic carbon dioxide balance and its disturbances. A major acidbase regulating system in the ocean is carbon dioxidebicarbonatecarbonate entity.
(1) An increase in atmospheric carbon dioxide tension tends to shift the carbon dioxidebicarbonatecarbonate equilibrium to acid direction. (2) The atmospheric carbon
dioxide tension is inuenced by terrestrial consumption and production. (3) Photosynthesis by oceanic plants and algae, and respiration by all marine organisms contributes
to the global carbon dioxide loading. (4) Release of carbonate from sediments shifts the carbon dioxidebicarbonatecarbonate equilibrium to alkaline direction. Ocean
acidication results if carbon dioxide loading and carbonate uptake of sediments exceed the use of carbon dioxide in photosynthesis and upwelling of carbonate from
sediments.

Ocean acidication will also affect the speciation of metals (Millero
et al., 2009) and nutrient cycles (Hutchins et al., 2009). During
the past century, there has been a pronounced eutrophication of
the marine environment, especially of the coastal zones (Jickells,
1998; Keeling et al., 2010). Together with eutrophication, any tem-
perature increase of marine areas, as has been observed (Belkin,
2004), will increase the metabolic rate of organisms with the net
consequence that the area of hypoxic zones of the marine environ-
ment will continue to increase as it has in the recent past (Diaz
and Rosenberg, 2008; Keeling et al., 2010). It should be noted
that while eutrophication increases primary production which con-
sumes carbon dioxide, it appears that overall respiration, producing
carbon dioxide, also increases markedly leading to a decrease in the
oxygen level (Diaz and Rosenberg, 2008). A temperature increase
further increases the mismatch between primary production and
respiration, so that the net primary production actually decreases
(Hoegh-Guldberg, 2010).
Consequently, when considering how climate change, ocean
acidication and aquatic toxicology interact, one needs to con-
sider the interactions of toxicants with three natural variables:
temperature, oxygenation and pH. Furthermore, as ocean acidi-
cation affects the speciation of metals (Diaz and Rosenberg, 2008;
Millero et al., 2009), metal toxicity will be markedly affected by the
ongoing increase in carbon dioxide level. It should be noted that
the responses to toxicants themselves can affect one or all of the
variables: if, e.g., the response to a toxicant changes the rate of pho-
tosynthesis differently from respiration rate, both carbon dioxide
and oxygen levels will be affected. Also, while temperature increase
affects many phenomena, any toxicant-dependent responses of
organisms to, and changes caused by them in oxygenation and pH
will also occur independently of temperature.
2. The interactions between natural environmental
variables and toxicant responses have been little studied
When I started writing this work, my aim was to contribute a
normal review. However, it soon became obvious that although
the possibilities for interactions between toxicant responses, cli-
mate change and ocean acidication are many, the occurrence of
these interactions has been little studied experimentally. Although
some consideration of interactions has been addressed with regard
to invertebrate development and other life history traits (Byrne,
2011, 2012), it is generally poorly understood at any level, how
toxicant responses may affect or be affected by changes predicted
to occur in environmental conditions (temperature, pH or oxy-
gen level) in the near future. This is largely due to the tradition in
mechanistic toxicology which has emphasized standardizing envi-
ronmental conditions to facilitate comparisons between toxicity
evaluations done in different places. On the downside it has meant
that interactions between responses to toxicants and ecologically
relevant environmental changes have been little studied. With cli-
mate change and ocean acidication becoming major concerns,
more mechanistic studies in aquatic toxicology are needed address-
ing the possibilities of interactions between toxicants and observed
or predicted changes in environmental conditions. This is required
to increase the general awareness of how environmental chemi-
cals in aquatic environments may affect the precious balance of
aquatic food webs with far-reaching consequences to earths car-
bon dioxide level, marine conditions, sheries and aquaculture.
Because the actual interactions between toxicant responses and
abiotic environmental have been little studied, the following dis-
cusses, rst, the major sources of oceanic pollutants, second, how
toxicants can affect ocean acidication, and third, what can the
interactions between the responses to toxicants and to environ-
mental changes expected to occur during climate change and ocean
acidication be.
3. Major sources of pollutants in oceans
Schematically, the pollutants reach the sea in river runoff,
efuent pipes, atmospheric deposition or marine transport and
shipwrecks (Fig. 2). In addition, with an increasing proportion of oil
production occurring in off-shore platforms, it causes some leakage
of oil (or produced water oil component-contaminated water) to
the surrounding marine environment, and, at an extreme, causes
massive accidents, as exemplied by the oil leak of Deepwater
Horizon. Formerly, the major solution of getting rid of unwanted
efuents was to lead them via an outlet pipe to the sea. When the
coastal water started to get polluted, the solution was to increase
the length of the efuent pipe. Also, with regard to atmospheric
 M. Nikinmaa / Aquatic Toxicology 126 (2013) 365372
Fig. 2. Schematic representation of major pollution sources of the marine environ-
ment. The oval represents the sea. Contaminants can reach it as a result of riverine
deposition (1), or as industrial (2) or municipal (3) efuents led directly to the sea.
Water currents (4) can transport contaminants for long distances. Point contami-
nation (5) may result from shipwrecks, oil exploration or liberation of toxic wastes
(deposited earlier, e.g., in containers) from bottom sediments. Contaminants can
also reach the ocean as atmospheric deposition (6).
pollution, with the appearance of damage in nearby areas, chim-
neys were made longer, causing the distribution of harmful
chemicals to farther places. As a consequence, and because of the
action of air and water currents, one can nd foreign chemicals even
in the remotest parts of the world (Macdonald et al., 2005; Doney,
2010). While the effects of direct efuent disposal and direct river-
ine pollution on the oceans are easily appreciated, much of ocean
contamination is based on atmospheric deposition, as exemplied
for nitrogenous wastes (Paerl et al., 2002).
4. How can pollutants inuence ocean acidication
4.1. Effects on primary productivity
Since the net primary production (NPP = the rate of photosyn-
thesis vs. respiration rate) largely determines how much the seas
either consume or produce carbon dioxide (and what the recent
change in the ratio between production and consumption is), the
effects of pollutants on photosynthesis and abundance of photo-
synthetic organisms (in comparison to heterotrophs) are decisive
for evaluating the role of oceans autotrophs as carbon dioxide sinks
and their consecutive role in global carbon dioxide dynamics. Over-
all, the oceans are a net carbon dioxide sink (Macdonald et al., 2005).
However, it appears that net primary production is only possible
with external source of nutrients (Falkowski, 1994) such as riverine
deposition. The appearance of photoautotroph, e.g. cyanobacterial,
blooms occurs when nutrient availability in photosynthetic zone is
high (Falkowski, 1994). Notably, while cyanobacteria do not toler-
ate full-strength seawater, their blooms are expected to intensify
with predicted increasing temperature and carbon dioxide tension
in brackish water environments such as the Baltic Sea and estuaries
(Hutchins et al., 2009). Although the overall intensity of cyanobac-
terial blooms may increase, the toxicity of the blooms may decrease,
as it appears that toxic cyanobacterial strains are worse competitors
in high carbon dioxide environment than non-toxic strains (Van de
Waal et al., 2011).
Although it appears that the overall phytoplankton abundance
has decreased in the worlds oceans during the last hundred years
(Boyce et al., 2010), two types of increases may occur: rst, contin-
ued eutrophication will increase primary production in ever larger,
mainly coastal, areas (Jickells, 1998; Howarth, 2008), second, an
increase in temperature increases the productivity of temperate
367
and arctic (Antarctic) waters (Fabry et al., 2009). However, the tem-
perature effect may be masked. The availability of micronutrients
such as iron may regulate primary production (Sathyendranath and
Platt, 2001), and their availability may be decreased by a change in
nutrient cycles caused by increased temperature (Falkowski, 2012).
The overall recent decrease of phytoplankton abundance may also
be associated with the eutrophication and temperature-dependent
deoxygenation of the worlds oceans (Keeling et al., 2010), which
may limit the growth of also autotrophs.
Apart from nutrients reaching the sea, different levels of oil pol-
lution are the most general changes observed. Different degrees of
oil pollution exist from cleaning of tanks to massive ship wrecks
or accidents in oil-producing platforms (Baker, 2001; Torres et al.,
2008). The toxic responses to oil components are affected by the
contact area of the organism to oil. As a result, oil dispersants
often increase the toxicity of oil to aquatic biota (Hsiao et al., 1978;
Yamane et al., 1984; Wolfe et al., 1998). Generally, oil components
both decrease the growth rate and inhibit photosynthesis of phy-
toplankton (Dennington et al., 1975; Hsiao, 1978; Gaur and Kumar,
1981; Yamane et al., 1984; Tukaj, 1987; Hing et al., 2011), although
also opposite results have been obtained. Rare, spontaneous muta-
tions occur in oil-contaminated sites enabling the continuation of
photosynthesis by phytoplankton even in highly oil-contaminated
sites (Carrera-Martinez et al., 2010, 2011).
Because some metal ions, such as those of iron, copper and zinc,
are essential in small amounts, their availability may be limiting the
growth of phytoplankton. However, at high concentrations they are
all toxic, and inuence both growth and photosynthesis. Decreased
growth rate and decreased rate of photosynthesis are common
responses to metal contamination (Stebbing and Santiago-Fandio,
1983; Stauber and Florence, 1985a,b; Goudey, 1987; Thompson and
Couture, 1991; Gerringa et al., 1995; Hassler et al., 2005; Hiriart-
Baer et al., 2006; Miao and Wang, 2006; Hadjoudja et al., 2009;
Takami et al., 2012; Wu et al., 2012b). Consequently, an overall
effect of metal pollution in aquatic environment is to decrease the
carbon dioxide removal from the atmosphere.
In addition to the eutrophication-inducing pollutants, oil com-
ponents and metals, various forms of contaminants, such as
pesticides and pharmaceuticals, are found not only as point con-
tamination but all over the marine environment (Doney, 2010).
Both the point and overall contamination may affect the phy-
toplankton growth and carbon dioxide dynamics of the marine
environments. However, it is beyond the scope of the present work
to evaluate the effects of all the hundreds of possible different con-
taminants.
4.2. The formation of calcied structures and their circulation in
oceans may affect carbon dioxidecarbonate balance
With regard to climate change and ocean acidication, corals
have been most in headlines, because of their bleaching at increased
temperatures (Hughes et al., 2003; Pandol et al., 2011) and
because calcium carbonate-dependent reef building may be dis-
turbed (Cohen and Holcomb, 2009). Effects on overall carbon
dioxidecarbonate balance and ocean acidication can result rst
from disturbances that toxicants cause on reef building and sec-
ond from effects on calcied structure circulation in the oceans:
the death of the organism results on downward drift of calcium
carbonate to sea bottom. Thus, base is removed from the marine
circulation, and it contributes to pH decrease. Presently virtually all
surface waters of oceans are supersaturated with the major forms
of calcium carbonate, aragonite and calcite (Feely et al., 2009),
but changes are expected to occur primarily in Arctic and Antarc-
tic areas during the 21st century (Fabry et al., 2009; Feely et al.,
2009).
368 M. Nikinmaa / Aquatic Toxicology 126 (2013) 365372
Fig. 3. The effects of lipophilic weak acids on respiration. Oxidative phosphorylation in mitochondria generates charge and proton gradients between the interior of mito-
chondria and the space between inner and outer mitochondrial membranes. The proton gradient generated is utilized by proton pump (1) in energy (ATP) production.
Lipophilic weak acids bind to the membrane (2) and can dissipate the proton gradient, whereby energy production is decreased.
4.3. Toxicant-induced changes in cellular respiration may affect
carbon dioxide balance in marine environments
As a result of the general eutrophication of especially the coastal
zones, the biomass and consequently also respiration of aquatic
organisms has increased markedly in the last century (Nixon and
Buckley, 2002), with the net result that the hypoxic areas in the
marine environments have increased (Keeling et al., 2010). In addi-
tion to heterotrophs, even the growth of photoautotrophs in the
nearly anoxic areas is decreased (Wu et al., 2012a). The gen-
eral increase in oxygen consumption includes both biological and
chemical oxygen demand. The biological oxygen demand includes
both prokaryotic and eukaryotic oxygen consumption. Oxygen
utilization occurs especially as a result of bacterial oxidation of
sinking organic particles (Keeling et al., 2010), and is highly depth-
dependent with up to 50-fold decrease from 100 to 1000 m (Keeling
et al., 2010). While much of what we know about the effects of tox-
icants on (cellular) respiration in aquatic organisms is based on
animals, especially sh, many of the basic principles are the same
regardless of the type of organism. Thus, the observed effects can
often be generalized across organism types.
Since aerobic respiration is much more effective (in terms of
energy produced from a given substrate) than anaerobic, organisms
rely on aerobic respiration whenever possible. This is not possible
whenever hypoxic conditions ensue. With regard to animals, respi-
ration of sh in oxygen-limiting conditions has been discussed by
Nilsson and Renshaw (2004) and that of invertebrates by Schmitz
and Harrison (2004).
A major effect on aerobic respiration is the effect of lipid-soluble
weak acids. They accumulate in all biological membranes and act
as protonophores shufing protons across membranes (Fig. 3).
Because actively maintained proton gradient is the basis of aerobic
energy production in, e.g., mitochondria, enabling proton pumps
(ATP synthases) to convert ADP to ATP, this effect occurs in all aer-
obically energy-producing organisms. Examples of such weak acids
are different phenols, the toxicity of which correlates with the lipid
solubility (Saarikoski and Viluksela, 1982), and organic tin com-
pounds (e.g. tributyl tin, tripropyl tin and triphenyl tin chloride) for
which effects on intracellular pH have been described for a cell type
which maintains intracellular pH actively (lamprey erythrocytes)
(Tufts and Boutilier, 1990). Although organic tin chlorides cause
endocrine disruption (Horiguchi, 2006), and their use in antifoul-
ing paints has been banned largely because of that, the endocrine
disruption effect cannot be behind the general toxic effect of the
organic tin compound-containing paints, because organisms (e.g.
plants) not having the animal-like sexual hormone system are simi-
larly affected. In contrast, a membrane-level effect affecting energy
production would take place in virtually all organisms.
Another general effect affecting aerobic energy production
regardless of the organism type is if the toxicant affects any of
the proteins in the electron transport chain setting up the proton
gradient used for energy production. Examples of such toxicants
are cyanides, which inhibit cytochrome C oxidase, rotenone, which
acts by inhibiting the transfer of electrons from complex 1 to
ubiquinone, hydrogen sulphide, which both affects cytochrome
C oxidase function and reactive oxygen species production, and
reactive oxygen species, which affect various steps of the electron
transport chain (Esposti, 1998; Borisov et al., 2011; Bouillaud and
Blachier, 2011).
On the whole, toxicants cause inhibition of respiration. Thus, the
production of carbon dioxide will be decreased. This will diminish
ocean acidication, but because general eutrophication increases
respiration and thereby carbon dioxide production and since tox-
icants generally decrease rate of photosynthesis, the overall effect
of toxicants tends to increase ocean acidication.
5. The interactions between toxicant responses and natural
environmental variables associated with climate change
and ocean acidication
5.1. Temperature and toxicant responses
Hitherto the discussion has concentrated on global effects and
mainly on how ocean acidication and associated phenomena can
be affected by toxicant responses. The rest of the review discusses
how the changes associated with ocean acidication can affect
the responses of individuals, mainly sh, to toxic challenges. With
regard to temperature changes, most studies are not very rele-
vant, as large, rapid changes have been studied, and they cannot be
expected. The environmental relevance of any marked temperature
changes will be related to their probability increasing. In marine
environments, this would only happen in shallow coastal areas and
tidal pools (Bridges, 1988). Most of the temperature changes which
can be expected are small, maximally a few degrees centigrade, and
slow. Such changes are either not normally associated with any
measurable physiological responses or the responses get hidden
 M. Nikinmaa / Aquatic Toxicology 126 (2013) 365372 369

Fig. 4. Schematic representations on how toxicants may affect the temperature responses of poikilothermic organisms. (a) The maximal oxygen consumption increases
with increasing temperature until a maximum is reached, whereafter the maximum decreases. The resting oxygen consumption of poikilotherms increases with increasing
temperature. The difference between maximal and resting oxygen consumption gives the scope of activity which is maximal at optimum temperature. (b) Hypothetical effects
of toxicants on the scope of activitytemperature relationship. (A) Hypothetical example of normal scope of activitytemperature dependence. (B) The toxicant decreases
optimal temperature (temperature at which the highest scope of activity is reached). (C) The toxicant increases the optimal temperature. (D) The toxicant decreases the
maximal value of the scope of activity.

among the individual variation, which is characteristic of individ-
ual function (Nikinmaa and Waser, 2007). However, although no
measurable effects are easily observed in the short term, in the long
run species distributions can be affected, and temperature effects
on sh populations have been extensively discussed (Portner et al.,
2001, 2006, 2008; Portner, 2008, 2010; Portner and Peck, 2010).
One thing that should be noted is the seasonality of responses
(Lecklin and Nikinmaa, 1999): the temperature effects on a given
life stage can be different depending on the time of measurement.
Because the changes in season are most pronounced at high lati-
tudes where also temperature changes are expected to be largest,
the seasonality of responses, which probably occurs mainly in shal-
low water species, must always be taken into account. Also both the
temperature and toxicant effects may vary between different life
stages. It is further possible that the responses of a given stage of
sh (and other organisms) to toxicants vary in the different seasons
at the same temperature.
A schematic representation of how temperature and responses
to toxicants may interact is given in Fig. 4. Effects of tempera-
ture on species and their abundance are likely to occur particularly
for stenothermal species. Among sh these include cod and its
relatives, several salmonids and Antarctic sh. The temperature
responses of these groups are better studied than those of most
shes. In addition to directly affecting the toxicity of a compound,
temperature has a pronounced inuence on the uptake and excre-
tion of chemicals across membranes. The inux and efux rates
of toxicants across membranes increase with increasing tempera-
ture. This is of major inuence to temperature-dependent changes
on toxicant levels in the body of organisms, as the uptake of many
chemicals is largely via the gills and they form the majority of the
uptake area of organisms, e.g., sh (Gray, 1954). With an increase of
lipophilicity of chemicals, the uptake route becomes increasingly
via food and alimentary channel. Temperature affects active inux
and efux more than passive uxes: the Q10 values of the former are
in excess of 2, the apparent values for secondarily active transport
can even be close to 10 (Cossins and Kilbey, 1990), and for the lat-
ter 1. Thus, the temperature-dependent changes in the steady-state
level of an unmetabolized compound depend on the relationship
of active and passive uxes in the uptake and excretion. Also, the
metabolism and its temperature dependence vary depending the
chemical and its metabolization pathway. An additional compli-
cating factor results from temperature adaptation (Cossins and
Raynard, 1987; Hazel, 1984): it is usually considered that three
weeks after the temperature change adaptation has taken place.
As an important acclimatory mechanism is maintaining the uid-
ity of membranes (homeoviscous adaptation), any pollutants, such
as ethanol, affecting membrane uidity, disturb temperature accli-
mation.
One temperature effect observed in all poikilotherms is an
increase in oxygen consumption with increasing temperature. If
an animal is close to the high (or low) end of its preferred temper-
ature range, even a small temperature increase and disturbance in
regulation of energy production by environmental pollutants may
decrease its scope of activity and thereby affect the ecological suc-
cess of an organism (Fig. 4). Another temperature-dependent effect
is the haemoglobin function. With increasing temperature the
haemoglobin oxygen afnity usually decreases (exceptions being
heterothermic tuna and several billsh, which have haemoglobins
showing inverse temperature dependence in physiological condi-
tions, Carey, 1973; Carey and Gibson, 1977; Weber et al., 2010;
Weber and Campbell, 2011). The most detailed evaluation of pos-
sible climate change-induced effects on haemoglobin function
has been done with cod (Portner et al., 2001, 2008). Toxicants
which affect haemoglobin function are especially nitrite and free
radicals containing nitrogen (Jensen, 2003), and any compounds
which cause stabilization of either deoxy- or oxyconformation
(Bogdanova et al., 2009). However, so far interactions between
realistic temperature changes and environmentally relevant tox-
icant levels have not, to my knowledge, been investigated. The
situation concerning temperaturetoxicant interactions becomes
even more complicated in brackish water areas, as marked salinity
changes may occur there because of changes in both precipitation
and evaporation (Schlenk and Lavado, 2011).
5.2. Interactions between toxicant responses and pH
The toxicity of all weak acids and bases varies markedly with
their dissociation status: usually the undissociated form is more
toxic than the charged form (Saarikoski and Viluksela, 1982).
The uptake of chemicals in organisms depends mainly on their
lipophilicity which is much higher for the acid than base forms
of weak acids/bases (Erickson et al., 2006a,b). Consequently, they
also distribute more readily to membranes than cytoplasma and
can, e.g., exert membrane-dependent toxicity as described above.
In addition to weak-acid/-base toxicants the function of virtually
all enzymes, many membrane transporters and, e.g., haemoglobin
is pH-sensitive at physiologically relevant pH area 78, whereby all
the toxicants affecting their function will respond to pH variations.
The reason why pH changes are very important in the regulation of
protein function stems from the fact that histidine residues change
their charge on protonation (histidine imidazole charge) at physi-
ological pH range, and the charge of the active group of protein is a
major regulator of its activity. In fact, the so called imidazole alpha-
stat hypothesis, based on the maintenance of histidine-imidazole
charge, was formulated to explain the acidbase regulation of ani-
mals (Reeves, 1972).
370 M. Nikinmaa / Aquatic Toxicology 126 (2013) 365372
5.3. Interactions between toxicant responses and water
oxygenation
Two different types of hypoxic conditions occur in marine areas:
in shallow eutrophic areas within photosynthetic zone low oxygen
levels vary rhythmically (in 24 h cycles) with hyperoxic condi-
tions. Under the photic zone hypoxic or even anoxic areas occur
whenever the consumption of oxygen exceeds its diffusion. This
may happen even if the oxygen consumption is minimal as in
the oxygen-minimum zones of oceans (Keeling et al., 2010). The
changes in oxygen level are aggravated by an increase in temper-
ature. Aquatic organisms are thus a prime choice for studying any
oxygen-dependent responses (Nikinmaa, 2002).
Changes in oxygen level are intimately associated with redox
status: hypoxic/anoxic conditions are reducing and hyperoxic oxi-
dizing. As a result, both hydrogen sulphide (Olson et al., 2006),
stable in reducing conditions (which hypoxia/anoxia is), and reac-
tive oxygen species, associated with high oxygen levels (Halliwell
and Gutteridge, 2007), play a role in the responses of organisms
to variation in oxygen levels. Both ROS and H2 S are toxicants
and oxidative stresses, which are characterized by elevated ROS
levels, are important mechanisms causing toxicity (Halliwell and
Gutteridge, 2007). Changes in ROS levels are also implicated in
responses to acute temperature increase of at least stenothermal
sh (Heise et al., 2006). Thus, any toxicants affecting ROS levels will
also inuence both hypoxia and temperature responses.
Redox changes are also implicated in the regulation of oxygen-
dependent gene expression by hypoxia-induced factor (HIF) in
general and teleost sh in particular (Nikinmaa et al., 2004). The HIF
pathway is the major regulator of hypoxia-induced gene expression
(Semenza, 2010). HIFs belong to the bHLH-PAS group of proteins,
which include many environmentally regulated transcription fac-
tors, e.g., aryl hydrocarbon receptor (AhR), the starting point of
xenobiotically induced gene expression (Kewley et al., 2004), i.e.
the most commonly studied biotransformation pathway. Both HIF
and AhR have ARTN (aryl hydrocarbon nuclear translocator) as the
dimerization partner. Dimerization is required before the factors
cause transcriptional induction (Nikinmaa and Rytkonen, 2011).
This competition for common dimerization partner can cause inter-
action between toxicant and hypoxia responses (Hofer et al., 2004).
Since daily rhythms are regulated by proteins of the same fam-
ily as AhR, it is no surprise that also AhR level can be inuenced
by light cycles (Rannug and Fritsche, 2006). Despite these obvious
possibilities of interactions between marine pollution and environ-
mental oxygen level or rhythmic changes in either oxygen level
or temperature, these ecologically relevant questions have, to my
knowledge, not been investigated in detail in any organism. The
lack of mechanistic information here is all the more dissatisfy-
ing, as it has recently become clear that thermal responses of
sh are often oxygen-limited indicating that oxygen-limited ther-
mal tolerance is of major importance in the responses of marine
organisms, such as sh, to climate change (Portner, 2010). One
of the factors affecting the responses of animals with circulation
to temperature changes is the changes occurring in microcircu-
lation (Nikinmaa et al., 1981). Since it is now known that CO,
NO, H2 S and ROS can regulate microvascular behaviour (Olson,
2005; Singel and Stamler, 2005; Bertuglia, 2008; Drenjancevic-
Peric et al., 2009; Morikawa et al., 2012), any toxicant-induced
effects on the levels of these molecules will affect the behaviour
of microcirculation, important for both temperature and hypoxia
responses.
An important component of respiration is the transfer of oxy-
gen from water to the organism. Gills have developed to ensure
adequate oxygenation of tissues in aquatic animals: they increase
the gas exchange area and with their development the diffusion
distance between the environment and the animal is minimized.
The diffusion distance between water and blood of active teleost
sh is only a couple of micrometers (Soivio and Tuurala, 1981). The
respiratory area of gills is inuenced both structurally (Sollid et al.,
2003) and via circulatory arrangements (Soivio and Tuurala, 1981)
by oxygen tension. Since the gills are, in addition, the primary route
for unwanted uptake of toxicants (and ions) or loss of materials, the
thinning of gill epithelium or increase of its area in hypoxic condi-
tions increases the unwanted uptake/loss of compounds. This is
often called the osmo-respiratory compromise (Matey et al., 2011).
Many toxicants, both metals and organic compounds, affect the
diffusion distance from water to blood (Tuurala and Soivio, 1982;
Lappivaara et al., 1995), which affects the arterial oxygen tension
(Tuurala, 1983). However, although effects of hypoxic conditions
and toxicants on the epithelial thickness have both been described,
their interactions or how ecologically relevant changes in ambi-
ent oxygen level affect the uptake/loss of chemicals have not been
studied.
Acknowledgements
The authors work is supported by the Academy of Finland
(Grant No. 258078). The valuable comments of anonymous review-
ers are acknowledged.
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