Phil. Trans. R. Soc.

B (2012) 367, 1607–1614

doi:10.1098/rstb.2012.0036

Introduction

Determining environmental causes of

biological effects: the need for a
mechanistic physiological dimension
in conservation biology
Frank Seebacher1,* and Craig E. Franklin2
1
School of Biological Sciences A08, University of Sydney, Sydney, New South Wales 2006, Australia
2
School of Biological Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia
The emerging field of Conservation Physiology links environmental change and ecological success
by the application of physiological theory, approaches and tools to elucidate and address conserva-
tion problems. Human activity has changed the natural environment to a point where the viability of
many ecosystems is now under threat. There are already many descriptions of how changes in bio-
logical patterns are correlated with environmental changes. The next important step is to determine
the causative relationship between environmental variability and biological systems. Physiology pro-
vides the mechanistic link between environmental change and ecological patterns. Physiological
research, therefore, should be integrated into conservation to predict the biological consequences
of human activity, and to identify those species or populations that are most vulnerable.
Keywords: global change; climate change; land clearing; adaptation; acclimation;
ecological success

systems and thereby maintain functioning ecosystems.

Conservation Physiology may be defined as the appli-
cation of physiological theory, approaches and tools
to elucidate and address conservation problems with
the aim to provide a mechanistic understanding of
how environmental disturbances and threatening pro-
cesses impact physiological responses and thereby
ecological function, population persistence, and
species survival.
1. INTRODUCTION
The importance of addressing conservation issues, such
as climate change, emerging diseases and habitat loss,
lies in preserving the integrity of ecosystems at local
and global scales. Biodiversity is essential to provide uti-
litarian ecosystems that can sustain human subsistence,
as well as cultural values that confer a sense of identity.
A well-functioning natural environment and mainten-
ance of biodiversity are thus fundamental to human
well-being [1]. Climate change and environmental
degradation has already resulted in negative conse-
quences for human subsistence and health and, hence,
economic success [2,3]. The regional decline of agri-
culture [4] and of some fisheries [5–8] are examples
of environmental and ecological problems that can
be attributed directly to human activity. The most cru-
cial issue is to slow anthropogenic impacts on natural
There is good evidence that conservation can work
[1,9], and our aim here is to help improve the effective-
ness of conservation measures by linking physiology and
ecology in a mechanistic framework, thereby providing a
stronger knowledge base for decision-making.
Any conservation measure requires sound scientific
information of the effects that habitat alterations
resulting from human activity have on natural systems
[10]. Even if the political will existed to curtail all
human impact, this is logistically impossible. Conser-
vation must therefore be selective and pragmatic.
Decisions must be based on an understanding of the
impacts that particular human activities have on eco-
systems, so that the benefits of remedial actions can
be maximized, while the costs to society are mini-
mized. In other words, there is an urgent need to
understand the link between the cause (i.e. human
activity) and its effect on biological function from indi-
viduals to ecosystems. We argue here that in many if
not most cases, the physiology of individuals provides
this link between cause and effect, and can thereby
explain ecological patterns. Physiological capacities
and responses act as a filter between environmental
change and ecological performance of individuals
and, hence, populations and species [11,12] (figure 1).

* Author for correspondence (frank.seebacher@sydney.edu.au). 2. HUMAN ACTIVITY MODIFIES THE ABIOTIC AND
One contribution of 13 to a Theme Issue ‘Conservation physiology:
BIOTIC ENVIRONMENTS
integrating physiological mechanisms with ecology and evolution to Environmental change is natural and occurs at different
predict responses of organisms to environmental change’. time scales. For example, natural forcing can cause
1607 This journal is q 2012 The Royal Society
1608 F. Seebacher and C. E. Franklin Introduction. Conservation physiology

P
H
Y

metabolism, growth, behaviour,

S

reproduction,
I ECOLOGY

etc.
ENVIRONMENTAL CHANGE PERSISTENCE
O BIODIVERSITY
global change
L
habitat destruction
temperature, pH, etc.
O
G
Y
Figure 1. Physiology acts as a filter between environmental changes, and ecology and biodiversity. Environmental changes
result from global change and habitat destruction, for example, which lead to changes in physical variables such as tempera-
ture, pH, etc. The physiological response of organisms to these changes will determine fitness-related functions, such as
metabolism, growth, behaviour and ultimately reproduction. These functions are key elements that determine ecological
relationships and the persistence of species in particular habitats, and thereby biodiversity. Photos J. Smith (left panels,
with permission) and F. Seebacher (right panel).

regional climate change at time scales of 1–10 years
[13], and palaeoclimate records around the globe
show that regional climate fluctuation of as much as
8–168C occurred repeatedly at periods of less than 10
years [14]. These regional climate changes have had a
direct impact on human societies [2]. Importantly, for-
cing by human activity accelerates climate change at
regional and global scales. Human activity such as
extensive deforestation may have affected climate since
prehistoric times in Europe [15]. However, the recent
climate change induced by increased CO2 emissions
starting in the late twentieth century remains unprece-
dented [15,16]. The resulting increases in temperature
and acidification of marine systems are global [16],
although temperature increases can be much more pro-
nounced in climate change ‘hotspots’. For example, sea
temperatures in southeastern Australia have increased
much more rapidly (by 2–38C since the mid-twentieth
century) than the global average [17]. Regional and
small-scale changes in the environment are also driven
by local land-use practices [18]. Deforestation and
land clearing affect biodiversity by direct removal of
species. Direct removal of species, either as a result of
land clearing or of exploitation for human use, alters
resource availability, such as shelter and food, for
higher trophic levels. Land clearing causes climate
warming by adding CO2 to the atmosphere and decreas-
ing evaporation, but it may also have a cooling effect by
changing the surface albedo [18]. Removal of vegetation
cover affects the hydrologic dynamics of the soil and
may contribute to increased salinization of freshwater
systems [19,20].
Other major impacts on the physical environment
at global or regional scales result from pollution.
Phil. Trans. R. Soc. B (2012)
Dumping or spillage of industrial chemicals has a
direct impact on the environment. Examples of nega-
tive effects on biodiversity are chemical spillages
from mine tailing dams, such as in the otherwise
relatively pristine rivers of New Guinea [21]. The
military strategy of defoliation, whereby American
forces dumped hundreds of thousands of tonnes of
herbicides on forests in Vietnam in the 1960s and
1970s, has caused large-scale deforestation and pol-
lution, the effects of which are still present today
[22]. At a global scale, the increase in ultra-violet
(UV) radiation as a result of hydrofluorocarbon release
can affect ecosystems by disrupting different life-
history stages of vulnerable species, and its effect
may be compounded by other stressors such as
pollution [23,24].
3. ECOLOGICAL SUCCESS IS COUPLED TO
ENVIRONMENTAL CONDITIONS VIA THE
SENSITIVITY OF PHYSIOLOGICAL SYSTEMS
It is well established that changes in the abiotic
environment affect the physiology of organisms at mul-
tiple levels. A large proportion of reproductive success
and individual fitness is determined by physiology, so
that environmental change affects fitness by its effect
on physiology. Time to sexual maturity depends on
growth rate and therefore on the capacity of energy
assimilation and metabolism [25]. Foraging, compe-
tition and reproductive behaviour of animals are a
function of locomotor performance and therefore of
muscle physiology and metabolism [26,27].
The efficacy of metabolism and muscle physiology
as well as most other physiological systems depends
 Introduction. Conservation physiology
on the cellular environment (temperature, pH, acid–
base balance, etc.), which is influenced by the external
environment. Changes in body temperature, for
example, affect biochemical reaction rates and most
organisms function best within a relatively narrow
range of body temperatures. Because the thermal sensi-
tivities of individual reaction rates vary, the challenge for
organisms lies in maintaining the stoichiometry of their
complex cellular biochemistry, which will be disrupted
by a change in the thermal environment. Increases or
decreases in means or variability of operative environ-
mental temperatures change body temperature directly
in those organisms that do not thermoregulate,
or change the environmental context within which ani-
mals thermoregulate [28]. In endotherms, a decrease
in environmental temperatures will elicit an increase in
metabolic heat production and, conversely, increases in
temperature decrease metabolic heat production.
Ectotherms may respond to changes in environmental
temperature by selecting different microhabitats, such
as increased shelter use to minimize absorption of
solar radiation in warming environments [29]. In
addition to behavioural responses, many ectotherms
modulate their cellular biochemistry to compensate for
thermal effects by, for example, quantitatively or quali-
tatively changing the expression of rate-limiting
enzymes [30,31]. In all cases, the change in physiologi-
cal need that ensues from a change in the environment
will alter the resource use of individuals. In the examples
above, energy requirements and the utilization of the
structural environment change, both of which have
important ecological consequences by changing foraging
and predation, and competition for particular micro-
habitats. Similar relationships as discussed briefly
above for temperature exist for changes in other abiotic
environmental variables, such as UV-B radiation, CO2
levels, rainfall and dehydration, hypoxia and salinity.
Hence, physiological requirements are at the interface
between environmental change and ecology (figure 1).
Importantly, physiology also mediates biotic inter-
actions. These interactions may be nested within the
effect of abiotic drivers as in the example above
where energetic needs for thermoregulation change
in different environmental contexts. Nutrition, with
respect to both energetic and macronutrient require-
ments, in particular determines interactions between
organisms [32,33]. At a quantitative level, density of
prey will determine predator numbers [34], but this
relationship will change with environmentally driven
changes in energy requirements, such as for thermo-
regulation. Different abiotic contexts can also change
the macronutrient requirements of individuals and
therefore change the need for prey quality in addition
to quantity. For example, temperature affects the rela-
tive macronutrient requirements in trout, and fish at
warm temperatures require relatively more protein
than at cooler temperatures [35]. As a result, foraging
behaviour must be adjusted to meet intake targets, and
predation pressures shift to different prey species,
potentially leading to a change in community structure
and interactions [33].
Similarly, decreases in aquatic oxygen levels in
freshwater river systems can impact on the diving ecol-
ogy of bimodally respiring turtles, requiring them to
Phil. Trans. R. Soc. B (2012)
F. Seebacher and C. E. Franklin 1609
expend greater energy to surface more frequently to
acquire oxygen from the air, but also increasing the
risk of predation, especially in hatchlings as they
swim through the water column [36]. Changes in
salinity of freshwater systems also change the activities
of ATPases for ion regulation [37] and therefore mod-
ulate energy intake, and thereby the impact that
individuals have on their ecological community.
Most species possess a degree of plasticity that permits
persistence across a range of environmental conditions.
However, there is a limit to physiological compensation
for environmental variability [38,39]. If environmental
conditions become too extreme, direct cellular damage
may ensue and animals will become more susceptible
to disease [40], and ultimately extinctions will occur.
4. PHYSIOLOGICAL SYSTEMS CAN
COMPENSATE FOR ENVIRONMENTAL
CHANGE—UP TO A POINT
The effect of environmental variation on physiological
function (phenotype) may be modulated by compensa-
tory responses. Such responses can occur at different
time scales: between generations (genetic adaptation)
[41], during development (developmental plasticity)
[42,43] so that phenotypes are matched to prevailing
environmental conditions, and within the adult lifespan
as reversible plasticity (acclimation and acclimatization)
[44–46] and migration [47,48].
The optimal ‘adaptive strategy’ of organisms
depends on the patchiness or ‘grain’ of the environ-
ment [49]. A coarse-grained environment fluctuates
between distinct states, and an individual is exposed
to only one. Performance and fitness in a coarse-
grained environment may be maximized by genetic
adaptation if environmental conditions remain stable
across generations, and by developmental plasticity if
the environment remains stable during the lifetime of
the organism [49,50]. In a fine-grained environment,
an individual experiences numerous patches, so that
total fitness will be the sum of the individual fitness
components of each patch, and reversible acclimation
would enhance performance and fitness [30,51].
In theory [49,52], coarse-grained environments will
produce phenotypes that are specialized (adapted) to
the relatively stable conditions experienced, while
fine-grained environments produce generalists that
perform well over a wider range of environmental con-
ditions albeit at a reduced level; in other words,
generalists trade-off maximal performance for per-
formance breadth. However, this need not be the
case if reversible acclimation can compensate for
environmental variation experienced during the life-
time, effectively leading to ‘specialized generalists’ in
which the conditions at which performance optima
occur track changes in environmental conditions
without loss of performance [51,53].
Most species experience both fine- and coarse-
grained variation at several temporal (e.g. day, season
and geological) and spatial (e.g. microhabitat and lati-
tude) dimensions, as well as the interaction of the two
resulting from animal movement within habitats [54],
between geographically separated habitats [48], or as a
consequence of life-history stages occupying different
1610 F. Seebacher and C. E. Franklin Introduction. Conservation physiology
habitats [55]. Hence, fine-scale patchiness at a short
temporal scale is added to coarse scale variation at
longer periods. Patchiness of the environment changes
naturally, for example, with season or latitude. However,
conservation issues may arise when human activities
alter patchiness and thereby disrupt evolutionary strat-
egies. Local land-use patterns such as deforestation
and agricultural activities, and anthropogenic climate
change, for example, can alter fine- and coarse-grained
patchiness of the environment, respectively.
The relative importance of plasticity and adaptation
will depend firstly on the relationship between lifespan
and rate of environmental change and, secondly, on
the rate of phenotypic change relative to environ-
mental change. The importance of lifespan is that
species with very short lifespans may experience only
one distinct (coarse-grained) environment, so that
genetic adaptation between generations and possibly
developmental plasticity will be the most important
responses. Many species, however, will also experience
at least some variation within their lifetime. In this
case, the optimal adaptive strategy will be a plastic
phenotype that can acclimate to each of the predict-
able extremes, in addition to genetic adaptation to
latitudinal and altitudinal gradients [12,56,57].
Ideally, fitness is maximized when organisms can
perform at a constant level despite environmental varia-
bility. It is impossible, however, that the phenotype can
change at the same time as the environment, if the
environmental change provides the signal for phenoty-
pic change. Hence, there will always be a lag between
the two. The lag in the phenotypic response may pre-
clude plasticity, when the rate of environmental
change is greater than the potential for phenotypic
change. Hence, an environmental fluctuation with a
period that is much shorter than the physiological
response time could not act as a stimulus for phenotypic
change. For example, it will take several weeks for
changes in metabolic gene expression and enzyme
activities to compensate for a chronic change in temp-
erature [58,59] so that daily temperature fluctuation
will not affect metabolic capacity. Generally, acute
changes in temperature resulting from movement
through different microclimates, weather changes and
diurnal fluctuations may affect real-time physiological
rates, but do not affect capacities. Similarly, genetic
adaptation will occur only when the rate of environ-
mental change is slower than that of genotypic
change. Human activity is often rapid relative to the
rate of adaptive processes and even relative to the life-
span of many organisms. Hence, genetic adaptation
may play a lesser role in responding to human-induced
environmental changes than developmental- and revers-
ible plasticity. This means that capacity for acclimation
will play a predominant role in determining the vulner-
ability of organisms to environmental change. Human
activity will affect species within the same habitat differ-
entially, depending on their capacity for physiological
plasticity and lifespan; the latter characteristics alone
can provide valuable background data informing
conservation decisions.
Even in the most plastic organisms, however, the
capacity to compensate for environmental change has
it limits [38]. These limits may be set by inadequate
Phil. Trans. R. Soc. B (2012)
environmental resources such as energy and nutrient
supply, which may curtail growth, locomotion and
other energy-consuming processes [32,60,61]. Limits
may also be set by biochemical constraints such as
an increased inefficiency of mitochondria in producing
chemical energy (ATP), or by the production of
reactive oxygen species, which cause damage to
membranes and proteins [31,62,63]. Beyond these
limits, fitness will decrease as a result of declining
performance, and accumulated damage and disease.
Successful conservation must predict these limits
and, if possible, maintain the range of environmental
fluctuations within the limits of effective organismal
responses. An understanding of the capacity for indi-
vidual plasticity that may compensate for human-
induced changes is of particular importance in the
light of rapidly changing environments. It is unlikely
that all species or populations within a region will
have the same capacities and limitations. However,
knowing the limits of physiological responses to
environmental perturbations will make it possible to
identify the elements of the ecosystem that are most
vulnerable to particular human activities.
5. PHYSIOLOGY CAN DETECT CAUSE AND
EFFECT TO DETERMINE VULNERABILITIES TO
ENVIRONMENTAL CHANGE
To date, most information regarding biological
responses to anthropogenic environmental changes,
and in particular to climate change, consists of cor-
relations between environmental and biological
variables [64,65]. For example, northward shifts in
the distributions of marine and terrestrial organisms
in the Northern Hemisphere have been associated
with the avoidance of increasing temperatures at
lower latitudes caused by anthropogenic climate
change [66,67]. Shorter winters and mild springs
resulting from global warming have been correlated
with the earlier flowering of plants and other shifts in
phenology [68]. These correlational data are essential
to understanding the potential impact of climate
change on biological systems. However, correlations
are not sufficient to determine whether climate
change has caused the observed changes in distri-
bution or phenology. Invariably, any biological
pattern will be correlated with a large number of abio-
tic and biotic patterns—some known, many unknown.
To determine whether or not a change in the environ-
ment can cause the observed change in pattern
requires experimental evidence [69]. It would be
necessary to demonstrate experimentally, with ade-
quate controls, replication and elucidation of the
underlying pathways, that the environmental variable
in question can effect the observed biological changes.
For example, in one of the first studies that related
global warming to a change in distribution, Parmesan
et al. [66] showed a northward shift in distribution of
butterflies in Britain between 1910 and 1997. However,
over that time frame, there were many changes in the
British landscape, and one very obvious one was the
decline and collapse of the coal industry in northern
England and Scotland (figure 2). Plotting the abun-
dance of butterflies in Scotland (i.e. the northernmost
 Introduction. Conservation physiology F. Seebacher and C. E. Franklin 1611

600

no. coalmines in Scotland

150 400

200

butterfly sightings
100
0
1880 1923 1945 1997 2007
year

50

0 200 400 600

no. coalmines
Figure 2. Correlation between butterfly distribution and coal mining. Butterfly distributions (from Parmesan et al. [66]) in
Scotland were plotted against the number of coalmines in the area during the same time periods (inset). The strong correlation
presents the alternative hypothesis that butterfly distributions are constrained by coal pollution rather than by climate change
as suggested by Parmesan et al. [66]).

distribution) given in fig. 1 of Parmesan et al. [66] unlikely to reveal the mechanistic basis of changes in
against the number of coalmines in the area (data distribution [74].
from the UK Coal Authority) gives a perfect correlation Correlations are essential to propose hypotheses
of r ¼ 1 (figure 2). Apart from the inherent limitation of that could explain the observed patterns. Hence,
only three data-points, figure 2 clearly presents an the studies cited above and many other correlational
alternative hypothesis explaining distributional range studies are extremely important. Over-interpretations
shifts of butterflies in the UK in the last century. of correlations, however, are detrimental to conservation
Which explanation is correct, global warming or coal because a misrepresentation of the cause underlying a
pollution, if any? The only way to determine the correct biological pattern means that conservation efforts are
answer is by experimentation. Another example is the misguided. This is where the importance of physiology
perceived northward shift of fish in the North Sea [67] lies: it can detect the cause. Even in the absence of a
as a result of mean water temperature increases in the positive result, fairly standard physiological studies can
southern North Sea. At least for some species such as eliminate possible explanations. In the cod example
cod (Gadus morhua), published data [70–72] show above, physiological studies have shown that locomotor
that the fish are well able to acclimate to temperatures performance [72], metabolism and growth of larvae
over the observed temperature increase in mean surface [70,72], and even food supply [75] are not negatively
temperature from 11.78C to 13.08C in the North Sea affected by the observed temperature increase. Hence,
between 1980 and 2006. In fact, the fish are more temperature increases per se can be ruled out in
likely to be limited by cold at those temperatures than explaining the observed distributional shift. It is now
to be heat stressed. Hence, what is known about the clear that overfishing is the most likely candidate to
physiology of the fish does not support the conclusions have caused the pattern [5]. We would like to emphasize
drawn from the correlational study that temperature that we do not wish to downplay the importance of
per se caused shifts in distribution. Plausible alternative climate change. Instead, we advocate a more stringent
explanations that could explain the changed distribution assessment of its effects to increase the efficacy of conser-
pattern include overfishing, and a decline in copepod vation measures. Physiological research provides a tool
abundance which is the main food source of larval cod to identify causes of biological change, and to eliminate
[73]. Cod are a good example of the challenges facing others that may be correlated but not causative.
marine conservation, because the complex responses The environment interacts with physiological
to environmental variability within individuals and capacities of individuals. Growth rates, as well as
between populations [8] make it difficult to manage other fitness-related functions such as locomotion
the resource. Conservation physiology can make a [76], are directly dependent on individual physiologi-
significant contribution, because understanding the cal capacities such as for aerobic metabolic energy
plasticity of physiological responses of the species will production. Population growth—either positive or
permit modelling of ecological responses [8] and predic- negative—is the sum total of the growth and perform-
tions of the impact of future environmental change. ance of individuals. A shift in the environment that
Finally, correlations between climate change and bird causes a mismatch between environmental conditions
distribution patterns lack predictive power and are and optimal temperatures for individual physiological
Phil. Trans. R. Soc. B (2012)
1612 F. Seebacher and C. E. Franklin Introduction. Conservation physiology
performance can therefore cause population declines
and extinctions if performance optima are fixed
within populations. Hence, there is a need to under-
stand individual responses to changing environments
and then translate these to populations, species and
communities [8,11,12].
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