Defining and observing stages of climate-mediated range shifts in marine systems
Introduction
In order to persist in the face of environmental change, species cope, adjust in situ or shift their geographical distribution (Maggini et al., 2011). Understanding this trade-off has inspired decades of research addressing the implications of long-term responses of populations, communities and biodiversity to global change, with species redistribution receiving significant research effort (Root et al., 2003, Hickling et al., 2006, Hawkins et al., 2008, Hawkins et al., 2009, Wernberg et al., 2011, Bellard et al., 2012, Cahill et al., 2012, La Sorte and Jetz, 2012, Parmesan and Yohe, 2003). Climate change has altered the spatial distributions of species by changing the balance between colonization and extinction, leading to geographic shifts in the location of species’ range edges (Gaston, 2003, Sinervo et al., 2010, Cheung et al., 2013, Poloczanska et al., 2013). The rapid pace of climate change means that range shifts are expected to be the dominant impact on ecosystem function and structure (Dawson et al., 2011, Doney et al., 2012), and thus range shifts are the focus of this contribution.
Geographic shifts have been well documented at range peripheries, and in particular, at the leading edges of latitudinal and elevational ranges (Hickling et al., 2006, Sunday et al., 2012). For example, when range edges are limited by a species’ cold tolerance, warming is expected to increase organismal performance (e.g., activity, growth and immune response), survivorship and fecundity (Pörtner and Farrell, 2008), and ultimately lead to population increase. With ongoing warming, locations that were historically too cold for survival will become increasingly suitable for colonists. Range extension can be a direct response to physical parameters, such as temperature, and on land, precipitation and soil moisture (Bonebrake and Mastrandrea, 2010, Chen et al., 2011a). Extension can also be facilitated by indirect processes, for instance the arrival of a critical habitat-forming species that subsequently facilitates colonization by individuals of a dependent species (Yamano et al., 2011). By contrast, range contractions at trailing range edges are driven by population decline from areas of a species’ historical range (Helmuth et al., 2006). Sub-lethal and lethal effects of high temperature in populations at range edges occur when physiological thresholds are exceeded as environmental temperature increases, and are well-documented (e.g., Beukema et al., 2009, Jones et al., 2010, Smale and Wernberg, 2013). Indirect drivers (although less studied), such as declining food availability, have also been implicated in geographic contractions, but do not appear to be more important than temperature (Cahill et al., 2012, Cahill et al., 2014).
Species with cold range edges that are presently limited by habitat availability will be particularly vulnerable to reductions in their environmental niche caused by climate change (Burrows et al., 2011, Burrows et al., 2014, Mair et al., 2014). Examples include species that are currently threatened or constrained by habitat availability, including species from polar or alpine habitats, isolated islands or the edges of continents (Pörtner et al., 2009, Wernberg et al., 2011, Cahill et al., 2012). However, for many species, climate change will lead to both positive and negative population-level effects, as determined by local climate across their range, presenting complexities at community scales that are challenging to anticipate.
Predicting how species’ ranges will respond to climate variability is limited by our capacity to observe and establish mechanisms for both geographic extensions and contractions. This is in part because evaluating range shifts comes with at least four practical challenges. First, preliminary stages of range shifts occur as a progressive sequence that can resemble or be confounded by the stochastic dynamics of range edges (Sexton et al., 2009). Attributing shifts to long-term climate trends is difficult if historical data are inadequate to quantify the portion of variability in the observed location of the range edge due to processes unrelated to climate change. Second, what constitutes a range shift can be difficult to define – range shifts can occur for different life history stages, such as larvae or adults, and new or remnant peripheral populations may represent viable self-recruiting or immigration-dependent populations. Third, the mechanisms setting range edge boundaries differ among species and therefore rates of range shift responses will also vary among species (Brown et al., 1996, Gaston, 2003, Sexton et al., 2009, Doak and Morris, 2010). Fourth, extension and contraction processes are underpinned by evolutionary, physiological, and demographic processes (Lenoir and Svenning, 2013). Such detailed biological information is rarely available at the community level and tracking distributions through time remains elusive for many species, limiting our power to predict range shifts from climate data alone.
Theoretical understanding of biological responses to climate change has been developed for terrestrial systems (e.g., Bellard et al., 2012, Lenoir and Svenning, 2013). We seek to translate this understanding to develop a framework for categorizing marine range shifts into discrete stages. We focus primarily on warming-related range shifts because the distributions of marine species generally correspond more closely to their environmental niche and have been directly responsive to climate warming (Sunday et al., 2012). In fact, the primary role of temperature in setting distributional limits has long been recognized for marine species (Hutchins, 1947). A notable example comes from 70 years of abundance data from intertidal invertebrates and plankton from the western English Channel. Periods of range extension by warm-water species corresponded with periods with warmer ocean temperatures, and contraction in these same species occurred during cooler periods, while the reverse occurred for cold affinity species (Southward et al., 1995). Indeed, temperature has been implicated as a pervasive driver of geographic range extension and contraction in diverse marine fauna and flora, e.g., seaweeds (e.g., Root et al., 2003, Tanaka et al., 2012, Smale and Wernberg, 2013, Nicastro et al., 2013), invertebrates (e.g., Sagarin et al., 1999, Helmuth et al., 2006, Mieszkowska et al., 2006), and fishes (e.g., Perry et al., 2005, Dulvy et al., 2008, Last et al., 2011). For these reasons, marine systems provide the opportunity to examine the progression of range shifts in species that span large-scale environmental gradients, where many species have been, and will continue to be, highly responsive to ocean warming (Cheung et al., 2013).
Here, we present a generalized framework for defining successive stages of geographic extension and contraction at range edges. We next consider differences in our capacity to observe these stages, and how limitations may be influencing our understanding of climate-mediated range shifts. Each range extension and contraction stage can be integrated within a confidence framework that considers the type and amount of evidence, and consensus among diverse lines of evidence, to provide an overall confidence score. We also explore how different biological traits and extrinsic factors can influence how quickly populations at range edges may transition through extension and contraction stages. Finally, we identify pragmatic directions for testing, observing and predicting range shift mechanisms and dynamics in marine systems.
Formulating range extensions and contractions as a series of well-defined stages facilitates: (1) the use of different types of data, (2) application across diverse species, (3) appropriate quantification of range shift rates so that early extension stages are not compared to late contraction stages, and (4) data objectives for monitoring programmes that will improve the capacity to make globally comparable assessments of community changes in response to warming.
Section snippets
Stages of range extension and contraction
Identification of range extension and contraction stages can be used to advance comparative analyses so that rates of change across systems and regions are standardized. A large body of research on range dynamics indicates that range extension can be compared to the final three stages of an invasion pathway, where non-native species move long distances to a novel geographic location, colonize, establish and spread (Theoharides and Dukes, 2007, Sorte et al., 2010). Similarly, range extensions
Variability in range edge locations
A key challenge to classifying species and events with this extension and contraction framework is the risk of misclassifying events due to background variability in distribution and abundance patterns that arise, for example, in species with vagrant individuals or species undergoing distribution change due to confounding human activities (Helmuth et al., 2006, Sexton et al., 2009, Fenberg and Rivadeneira, 2011). Moreover, in cases where species range boundaries are at equilibrium with climate,
Multiple sources of evidence for range shifts and confidence classification
The pragmatic use of multiple evidence sources for assessing range shifts generally represents the best approach, at least until biological monitoring programmes are implemented at the spatial resolution and sampling frequency to accurately capture range dynamics. For example, changes in a range boundary over two or more time points may provide information on the distance a range boundary has shifted; but even greater understanding can be gleaned from information on the life-history stages
Observing range shifts
One of the key complicating factors in climate change ecology is that many species have not undergone range changes or have moved in the opposite direction to isotherm shifts. Some of these non-shifting species may be falsely classified as responding to climate change while other shifting species may appear stable. Here we discuss three general issues of detectability that may result in misclassifications of range shift stages and may hinder recognition of patterns of change that are important
Are range extending and contracting species distinguished by their traits?
Some marine species have displayed stable distributions or shifted in a direction opposite to isotherms (Lima et al., 2007, Przeslawski et al., 2012), even in ocean warming hotspots (Last et al., 2011, Pitt et al., 2010, Poloczanska et al., 2011, Poloczanska et al., 2013). While this lack of range shift may be due in part to the challenges associated with accurately measuring changes in geographic location of range edges, as discussed earlier, an open question is whether species displaying
Why have so few species responded in the same direction as isotherms?
While biological traits of species will presumably shape the sensitivity of species to environmental change, in some cases extrinsic factors may exacerbate or constrain extension or contraction processes (Helmuth et al., 2006).
Here we highlight, among many, four mechanisms that are commonly explored in the literature (e.g., Gaston, 2003, Svenning and Skov, 2004, Sunday et al., 2012).
First, in many species, the current range edge may not be at equilibrium with climate and may even temporarily
Recommendations for a future in which range shifts can be observed and predicted with high confidence
Increasing our power to identify the underlying drivers of distribution change will advance our forecasting capacity. Given the potential impacts of range shifts, including significant changes to global resources and ecosystem services, identifying mechanisms for distribution change and developing predictive capacity are vital for conservation and management. Here, we identify approaches for monitoring, assigning confidence, and modelling range shifts that will contribute to a future with a
Conclusions
The underlying mechanisms of range shift processes are multi-layered, but can be classified into sequential steps. Species’ responsiveness to climate change involves all levels of biological organization and interactions with various biotic and abiotic factors (Cahill et al., 2012, Grigaltchik et al., 2012, Kordas et al., 2011). A consistent framework to define and assess range shifts will therefore facilitate global comparisons of species at each stage of range change and should advance
Acknowledgements
The Australian National Network in Marine Science, a collaborative funding initiative between James Cook University, The University of Tasmania, and The University of Western Australia, supported this study. T.W. was supported by an Australian Research Council (ARC) Future Fellowship (FT110100174), J.S. was supported by the NSERC Michael Smith Foreign Study Supplements Program, and G.J.E. by ARC Grant LP100200122. We thank T.J. Bird for comments on manuscript drafts and to A. Cooper, R.
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