Download 5-Russel 2012

Mar Biol (2012) 159:2633–2639
DOI 10.1007/s00227-011-1863-8
ORIGINAL PAPER
Origins and consequences of global and local stressors:
incorporating climatic and non-climatic phenomena
that buVer or accelerate ecological change
Bayden D. Russell · Sean D. Connell
Received: 6 October 2011 / Accepted: 19 December 2011 / Published online: 5 January 2012
© Springer-Verlag 2012
Abstract With research into the ecological eVects of climatic change intensifying over the past decade, there has
been an eVort to increase the scale of experiments from a
focus on individual organisms to incorporate the eVects of
the structure and functioning of entire ecosystems. As the
scale of investigation becomes increasingly broad, however, the number of seemingly contradictory outcomes also
increases. In reality, however, change or persistence of ecological patterns represents interplay of processes across
diverse scales of space and time. At one extreme, non-climatic inXuences can dominate local and short-term processes that protect systems against change or accelerate
change. Here, we draw on case studies that demonstrate
such contrasting situations, presenting examples where
local conditions can either ameliorate or exacerbate the predicted eVects of climate change. By incorporating examples
of stressors that originate and manifest at diVerent spatial
scales, we also attempt to reWne some of the eVorts surrounding research into the eVects of climate change.
Introduction
The concept of scale has been central to ecological problem
solving for over four decades (e.g. Greig-Smith 1952;
MacArthur 1965). In the last 20 years, however, research
that explicitly recognises the scales at which ecological pat-
Communicated by U. Sommer.
B. D. Russell (&) · S. D. Connell
Southern Seas Ecology Laboratories, School of Earth
& Environmental Sciences, The University of Adelaide,
Adelaide, SA 5005, Australia
e-mail: [email protected]
terns, and the processes that drive them, has become
increasingly common (Wiens 1989; Levin 1992; Schneider
2001). Indeed, understanding the functioning of phenomena that occurs across diVerent scales of space and time is
essential to understand the processes that either buVer systems against change or facilitate change (Menge and Olson
1990; Denny et al. 2009). Nevertheless, it is often far from
simple to integrate scale-dependent phenomena across global (e.g. regional weather patterns), local (e.g. microclimates caused by rocky shore topography) to micro-scales
(e.g. temperature gradients around organisms). Yet, understanding how organisms respond to these diVerent environmental conditions, which act at diVerent scales, is needed if
we are to accurately account for seemingly counter-intuitive changes in ecosystems, in particular where human
activities alter environments (Folt et al. 1999; Crain et al.
2008).
Much of the focus of how environmental conditions
aVect the functioning of ecosystems has recently shifted to
research into climate change per se. Early research into the
ecological consequences of climate change reXected the
global scale of the problem and primarily attempted to Wt
broad-scale changes in environmental conditions, such as
average global temperatures, to responses of organisms or
populations. While observations of ecological responses to
changing climatic conditions are increasingly common, this
approach has lead to an increasing number of cases where
population responses to changing environmental conditions
are diVerent to what would be predicted. For example,
alpine vegetation is generally predicted to retreat to higher
altitudes with warming of global temperatures, yet in some
locations they are doing the opposite (Crimmins et al.
2011). Such cases often limit progress in understanding
what drives change in the distribution of species and the
mechanisms that are driving these shifts.
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Increasingly, it is being recognised that the extent to
which changes in ecosystems can be attributed to climate
change is contingent on local conditions (Helmuth et al.
2010). Some of these interactions between climatic and
local conditions are relatively intuitive, albeit with unexpected synergies. A good example of such predictions are
that warming of the oceans is more likely to drive ecosystem shifts (or phase-shifts) in locations that have reduced
resilience because of nutrient pollution (e.g. Carilli et al.
2009; Russell et al. 2009) or overWshing (e.g. Hughes et al.
2007; Ledlie et al. 2007). Some of these interactions are not
intuitive, however, and have until recently gone unrecognised. For example, wave splash and tidal height on rocky
shores can ameliorate the eVects of warming to reduce mortality below what would be predicted from regional average
temperatures (Helmuth et al. 2006a). Here, we argue such
seemingly discordant impacts of changing environmental
conditions can be reconciled by explicitly recognising the
scale of origin of environmental change and the spatial
scale at which the impact manifests. Further, recognising
the scale at which the impact of environmental change
manifests allows recognition of how the eVects of changes
that originate at the global scale can be altered by localscale conditions.
Scale: origin versus impact
Early research into climate change focussed not on the
eVects of changing environmental conditions in ecosystems, but rather how climatic conditions themselves were
likely to change and whether these changes could be attributed to human activities. As such, the scale of these investigations was both spatially and temporally large,
investigating changes to global weather patterns across millennia. From an ecosystem perspective, the general view
was that this ‘climate change’ is a global stressor, leading
to predictions of impacts over very broad spatial scales.
Therefore, early predictions of shifts in the geographical
range of species focussed on contractions towards the poles
(or higher altitudes) across hundreds of kilometres without
consideration of the Wne scale variation in environmental
conditions. Yet, it rapidly became apparent that many of
these predictions were inaccurate and that the realised distribution of populations was being driven by Wner scale processes (Helmuth et al. 2010). As a result, it is increasingly
being recognised that the scale of climate predictions is
often discordant with the scale at which organisms experience environmental conditions. While overall warming is
anticipated at the global scale, there will be substantial
small-scale diVerences in the degree of warming both spatially and temporally (Easterling et al. 2000). Moreover,
local conditions will either ameliorate or amplify the eVects
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Mar Biol (2012) 159:2633–2639
of this warming (Denny et al. 2009). For example, contrary
to expectations, intertidal mussels on the western coast of
the USA can experience more extreme summer temperatures at more poleward locations than at lower latitudes
because of the timing of low tides (Helmuth et al. 2006a).
This apparent lack of agreement between predictions and
observations occurs as a function of the disconnection
between the scale of origin of the stressor (global) and the
scale at which it manifests or impacts (local). By necessity,
many of the predictions of future conditions are based on an
‘average’, which ignores Xuctuations around this mean and
how local conditions will aVect it (Denny et al. 2009). Yet,
the eVects of these stressors will be experienced at the level
of the organism and therefore have ramiWcations at the
scale of individuals and populations. While changes to
environmental conditions may be at the global scale, such
as increasing concentrations of carbon dioxide and temperature, how these changes will manifest in biological systems will be in part determined by the local context.
Context dependency
The way in which stressors originating at global scales
manifest at local scales may be contingent on the physical
conditions in that locality. In turn, heterogeneity in the
physical environment at small spatial scales, even down to
centimetres, can manifest in seemingly stochastic and often
unpredictable biological responses (PandolW et al. 2011).
While this type of complexity initially challenged our
capacity to predict the ecological consequences of these
interacting conditions, there is an increasing body of literature that demonstrates both the potential positive and the
potential negative outcomes (e.g. reviews by Hawkins et al.
2009; Helmuth et al. 2010). For example, the seemingly
random eVect of temperature stress in driving mortality of
mussels on rocky shores can be reconciled by the identiWcation of micro-climates based on shore topography (Helmuth
and Hofmann 2001). Even well-understood interactions
between species, such as the rate at which Pisaster ochraceus consumes Mytilus californianus, cannot be predicted
based on broad-scale temperatures, but rather require
knowledge of site-speciWc environmental conditions (Broitman et al. 2009). In the open ocean, the reduced calciWcation of the coccolithophore Emiliania huxleyi under
elevated concentrations of carbon dioxide is further
reduced by ammonia, suggesting that the eVects of ocean
acidiWcation will be contingent on local nutrient pollution
(Lefebvre et al. 2011). Indeed, in some regions, the
increased biomass associated with nutrient pollution has
increased the acidiWcation of coastal waters (because of
increased respiration, Cai et al. 2011), meaning that ecosystem responses may be diVerent in areas of oligotrophic
Mar Biol (2012) 159:2633–2639
versus eutrophic waters. Therefore, recognising the scale
at which diVerent stressors manifest (rather than the scale at
which they originate) allows incorporation of conditions
at that scale (both natural and anthropogenic) to be incorporated into models to forecast potential responses by ecosystems.
Interacting stressors and synergies
The eVects of changing global environmental conditions
will manifest at similar scales to stressors that originate at
local scales and have a long history of study, such as nutrient pollution or over-exploitation of herbivores. These
local-scale stressors have produced environmental conditions that are diVerent to those naturally experienced by
ecosystems (Lotze and Worm 2002) and have led to the
well-documented loss of the dominant habitat-forming taxa
across tropical and temperate ecosystems (e.g. Hughes
1994; Eriksson et al. 2002; Bellwood et al. 2004; Fabricius
2005; Thibaut et al. 2005; Airoldi and Beck 2007; Connell
et al. 2008). In tropical systems, it is likely that the interaction between increasing concentrations of carbon dioxide,
temperature and local-scale stressors will cause a synergistic negative eVect on coral reefs from two directions, the
negative eVect on corals and the positive eVect on non-calcareous macroalgae (Langer et al. 2006; KuVner et al.
2008; Fabricius et al. 2011). Greater nutrient concentration
on coastal reefs promotes overgrowth and smothering of
reef-building corals by macroalgae (Fabricius 2005) and
reduces the resilience of corals to bleaching at warmer temperatures (Carilli et al. 2009). In addition, over-exploitation
of herbivorous Wsh allows macroalgae to dominate space
following bleaching events (Hughes et al. 2007; Ledlie
et al. 2007). The combination of these stressors is broadly
predicted to cause a shift of coral reef ecosystems to be
dominated by algae (Bellwood et al. 2004).
In temperate marine systems, canopies of algae (c.f.
reef-building corals) are the dominant habitat-formers that
provide structure, survival of associated species and economic beneWt for human societies (Tegner and Dayton 2000;
Steneck et al. 2002). On many coasts of the world, however,
increasing nutrients from land-derived sources are driving
phase-shifts where these canopies are replaced by small Wlamentous algal turfs (Eriksson et al. 2002; Airoldi and Beck
2007; Connell et al. 2008; Gorman et al. 2009). Recent
research has demonstrated that increasing concentration of
carbon dioxide and temperature alone may be suYcient to
increase the productivity of these non-calcareous algae
(Kubler et al. 1999; Connell and Russell 2010; Russell et al.
2011b). When these environmental conditions are increased
concurrently with nutrients, however, the growth of opportunistic algae increases at a greater rate than would be expected
from the addition of their independent eVects (Russell et al.
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2009). Superimposed upon this interaction between stressors
of global and local origin is the observed poleward contraction of these canopy-forming algae (Ladah et al. 2003;
Wernberg et al. 2011b) that may accelerate in regions where
human activities have increased nutrient concentrations
(Eriksson et al. 2002; Thibaut et al. 2005; Airoldi and Beck
2007; Connell et al. 2008).
While organisms may show some resistance to independent stressors, their sensitivity is often altered under the
concurrent application of multiple changes, resulting in
eVects of a larger magnitude than anticipated from the
study of independent stressors (Folt et al. 1999; Reynaud
et al. 2003; Feely et al. 2004; Przeslawski et al. 2005).
Therefore, on both tropical and temperate reefs, it is likely
that the combination of stressors of global origin (e.g.
increasing concentration of carbon dioxide and temperature) will interact with stressors of local origin (e.g. nutrient
pollution and over harvesting) to reduce the resilience of
these systems and to increase the frequency of ecosystem
shifts from domination by one set of taxa to another, such
as the shift from corals to macroalgae. Nevertheless, much
work remains to be done on understanding which local biological and non-climatic processes buVer systems against
broader scale changes in climate.
Biological and physical amelioration
Just as the interaction among multiple stressors can combine to have greater negative impacts on ecosystems, the
presence of certain species or environmental conditions can
ameliorate stressors. Individual organisms will respond to
the local physical environment, not the average conditions
over broader spatial scales (Hallett et al. 2004). In terrestrial systems, the eVects of regional climate on mortality of
trees (Crimmins et al. 2011) and sheep (Hallett et al. 2004)
are reduced by localised rainfall. Similarly, in marine systems, when maximum daily air temperatures coincide with
high tides, the physiological stress experienced by intertidal
organisms is reduced (Helmuth et al. 2002). Further, angle
of the substratum can play a large role in determining the
body temperature of intertidal organisms, vastly reducing
physiological stress in some cases (Helmuth and Hofmann
2001). Therefore, seemingly large heterogeneity in the survival of individuals, and populations, can often be reconciled by physical amelioration over smaller scales (e.g.
metres).
Many physiological functions are under environmental
control. In particular, rates of consumption can be strongly
determined by physical conditions (Sanford 1999;
O’Connor 2009) and may alter the predicted eVects of climate
in determining ecological functions (Helmuth et al. 2006b;
Gaedke et al. 2010). Where predictions of phase-shifts from
domination by habitat-forming species in response to
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2636
environmental stressors centre on increased productivity in
the taxa that replace them, this increase in consumption by
herbivores may ameliorate the eVects of changing climatic
conditions (O’Connor 2009; Connell et al. 2011); for
example, in southern Australia, predictions of phase-shifts
from kelp forests to small Wlamentous turf-forming algae
centre on increased productivity and domination by turfs
with increased carbon dioxide, temperature and nutrients
(Connell and Russell 2010; Russell et al. 2011a, b). With
this increase in temperature, however, there should theoretically be an increase in herbivory, potentially leading to
consumption of this additional primary productivity, thus
enabling the system to resist the phase-shift. Therefore,
recognising that production and consumption are often at
least partly controlled by abiotic conditions (Sanford 2002;
Lopez-Urrutia et al. 2006; O’Connor 2009) may allow
measures of local environmental conditions to be integrated
into predictions of how changes to environmental conditions will manifest at diVerent scales, from the physiology
of individuals up to the functioning of ecosystems (Helmuth
et al. 2006b).
Implementing conservation measures to protect habitatforming species may also have a positive feedback that
ameliorates the eVects of stressors over local scales. Habitatformers, or biogenic habitats, are often seen as ecosystem
engineers (sensu Jones et al. 1994, 1997) because they can
substantially alter the physical conditions in close proximity to their populations. Importantly, habitat-formers can Wll
this role across environmental gradients, reducing environmental stress for other organisms that rely on them for
habitat (Crain and Bertness 2006). In terrestrial systems,
habitats such as forests, which alter regimes of light, temperatures and can even create their own localised weather
patterns, are readily recognised to Wll this function (review
by McAlpine et al. 2009). In marine systems, habitats such
as kelp forests, seagrass beds and coral reefs also alter
physical conditions, Wlling the same role as that of terrestrial forests. For example, in intertidal habitats, canopies of
algae, such as Ascophyllum nodosum, retain moisture at
low tide and ameliorate desiccation stress for benthic invertebrates (Bertness et al. 1999). In subtidal systems, algal
canopies can reduce the eVects of eutrophication by limiting the growth of alternative taxa that are their competitors
(Eriksson et al. 2006). Furthermore, it also seems that large
stands of canopy-forming algae may have the capacity to
buVer against some of the negative eVects associated with
increased concentrations of carbon dioxide, such as ocean
acidiWcation, using carbon dioxide in photosynthesis and
increasing pH over small scales (Middelboe and Hansen
2007; Hurd et al. 2009). Likewise, primary productivity on
coral reefs can increase the pH by »0.4 units during daylight hours (e.g. Jokiel et al. 2008). While this buVering
eVect is likely to be over small spatial scales, probably only
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Mar Biol (2012) 159:2633–2639
metres to tens of metres, they may be disproportionately
positive on species that inhabit these locations, especially
for particularly susceptible life stages (e.g. larvae and juveniles).
Scale dependency
Most experimental studies on the eVects of climate change
to date have understandably focused on the most easily
manipulated life stage of species in controlled laboratory or
mesocosm experiments. There have been multiple criticisms levelled at such laboratory experiments, especially
that the organisms within the experiments are thought not
to function as they would in their natural environment.
Therefore, while such experiments are informative on one
scale, such as the physiological responses of individuals to
microclimates, they cannot replicate the scales over which
diVerent environmental conditions dominate local ecologies. Indeed, the diVerent processes that determine ecosystem function vary over a range of spatial and temporal
scales, and caution must be used when ‘scaling-up’ experiments of limited spatial or temporal extent to make inferences about ecosystem processes (Thrush et al. 1997).
Therefore, because much of our understanding of the functioning of ecosystems is based on laboratory or Weld experiments with experimental units that are limited in size, how
these experimental outcomes add to our understanding of
generality in ecology requires an understanding of the
regional context surrounding the experiments (Thrush et al.
2000; Connell and Irving 2008). For example, seemingly
contradictory outcomes among multiple spatially constrained experiments on the drivers of loss of kelp forests in
Australia (dominated by Ecklonia radiata) can be reconciled by incorporating the diVerent biogeographic regions
and ocean current systems into explanatory models; elevated nutrient concentrations are more likely to drive loss
of kelp forests on the southern coast (Russell et al. 2005;
Connell and Irving 2008; Wernberg et al. 2011a), while
increased herbivory drive canopy loss on the east coast
(Connell and Vanderklift 2007; Ling 2008; Wernberg et al.
2011a). Similarly, understanding the environmental drivers
of loss and recovery of giant kelp (Macrocystis pyrifera)
forests in the north-eastern PaciWc can only be reconciled
by understanding regional oceanography (e.g. upwelling
and El Nino, Dayton et al. 1992; Edwards and Estes 2006).
An understanding of how regional biogeography aVects
environmental conditions can also aid in reconciling both
the currently observed and potential future eVects of climate change. At its most simple, environmental conditions,
such as temperature, are likely to change at diVerent rates
depending on regional conditions (Easterling et al. 2000),
altering rates of biological change. For example, observed
Mar Biol (2012) 159:2633–2639
warming of coastal waters on the east and west coasts of
Australia over the past 50 years seems to be related to the
relative strength of the two main continental boundary currents and has driven diVerential rates of poleward shifts of
algal assemblages (Wernberg et al. 2011b). More complex
interactions among processes of diVerent scale are, however, also likely. For instance, increasing concentrations of
carbon dioxide, and therefore more acidic water, has been
shown to be detrimental to a broad range of taxa (e.g. invertebrates, review by Fabry et al. 2008; calcareous algae, Gao
et al. 1993, Martin and Gattuso 2009, Russell et al. 2009).
Kelp forests can, however, locally increase pH (Middelboe
and Hansen 2007), potentially buVering these negative
eVects over small scales. Yet, to predict the ability of kelp
forests to buVer the eVects of climate change over broad
scales, we also need an understanding of processes under
which kelp forests are likely to persist or decline. The
mechanisms that drive loss of kelp canopies diVer between
regions (e.g. the diVerent bioregions in Australia and New
Zealand, upwelling dynamics in the USA), but tend to be
meso-scale processes. Therefore, to gain a full understanding of the small-scale dynamics among locations, we also
need to know the broader scale processes that will modify
them (Connell and Irving 2008).
We argue that the value of experiments may be
improved by including information on the context dependency of the outcomes. Explicit recognition of this scaledependent information progresses our understanding of
impacts in ecosystems in two ways. First, knowledge of the
scale of the environmental conditions which cause the
greatest impact in a system will then also allow identiWcation of the key organisms and life stages that will be
aVected (Russell et al. 2011a). Second, recognition of the
scale at which diVerent stressors manifest allows explicit
incorporation of a range of stressors into the experiments
and models. Such multi-factorial studies would then allow
identiWcation of the relative strength of stressors, originating at global- (thousands of kilometres) to meso- (hundreds
to tens of kilometres) to local-scales (hundreds of metres to
kilometres), in either the maintenance or degradation of
diVerent systems. Therefore, while the study of climatic
stressors on small scales provides insights into how well
single species will respond, an understanding of local-toglobal scale interactions between multiple stressors in biological communities is required to identify how ecosystems
will function under predicted changes in our climate.
Conclusions
The scales of observation for environmental stressors may
need more consideration than we currently allow (Hallett
et al. 2004). Much of the recent discussion on the eVects of
2637
climate change in biological systems focuses on broadscale conditions, yet this often leads to the failure to detect
and predict ecological dependences at medium to small
spatial and temporal scales. Importantly, forecasts of ecological responses over large geographical scales require an
understanding of how environmental conditions vary at
relevant scales. Therefore, forecasts that incorporate interactions between climatic and non-climatic impacts, demonstrating how these eVects vary according to context (i.e.
variation in abiotic and biotic conditions), will be essential
to accurately predict the ecological consequences of changing environmental conditions. Demonstrations of an eVect
of one or two climate variables (e.g. elevated carbon dioxide and temperature) without showing the local conditions
in which these eVects occur are diYcult to interpret because
they lack realism and context. Importantly, by recognising
that the scale at which a stressor originates is often discordant from the scale at which it manifests (or scale of
impact), more accurate predictions will be possible. Finally,
ecologists are increasingly being asked to advise on the
most eVective local-scale adaptations to future climates. To
incorporate both regional ecology and the management of
non-climate impacts (e.g. Wshing and pollution), this advice
will necessarily draw on knowledge of the regional to
local-scale contingencies of non-climatic impacts and their
interactions with a changing climate.
Acknowledgments Fellowships to SDC and grants to SDC and BDR
were funded by the Australian Research Council.
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