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CONCEPTS & THEORY Climate change impacts on connectivity in the ocean: Implications for conservation LEAH R. GERBER,1, MARIA DEL MAR MANCHA-CISNEROS,1 MARY I. O’CONNOR,2 AND ELIZABETH R. SELIG3 1 Ecology, Evolution and Environmental Science, School of Life Sciences, Arizona State University, Box 874501, Tempe, Arizona 85287-4501 USA 2 Department of Zoology and Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia V6T 1Z4 Canada 3 Betty and Gordon Moore Center for Science and Oceans, Conservation International, 2011 Crystal Drive, Suite 500, Arlington, Virginia 22202 USA Citation: Gerber, L. R., M. Del Mar Mancha-Cisneros, M. I. O’Connor, and E. R. Selig. 2014. Climate change impacts on connectivity in the ocean: Implications for conservation. Ecosphere 5(3):33. http://dx.doi.org/10.1890/ES13-00336.1 Abstract. Effective spatial management in the ocean requires a network of conservation areas that are connected by larval and adult dispersal. We propose a conceptual framework for including the likely impacts of a changing climate on marine connectivity, and synthesize information on the relationships between changing ocean temperature and acidification, connectivity and conservation tools. Our framework relies on concepts of functional connectivity, which depends on an organism’s biological and behavioral responses to the physical environment, and structural connectivity, which describes changes in the physical and spatial structure of the environment that affect connectivity and movement. Our review confirms that ocean climate change likely reduces potential dispersal distance and therefore functional connectivity. Structural connectivity in the ocean will inevitably change with the spatial arrangement of biogenic habitats resulting from disturbance as well as enhanced growth and mortality due to climate change. Climate change will also likely reduce the spatial scale of connectivity, suggesting that we will need more closely spaced protected areas. Key words: climate change; connectivity; dispersal; marine reserves; marine spatial planning; ocean acidification; warming. Received 21 October 2013; revised 20 January 2014; accepted 22 January 2014; final version received 21 February 2014; published 24 March 2014. Corresponding Editor: D. P. C. Peters. Copyright: Ó 2014 Gerber et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. http://creativecommons.org/licenses/by/3.0/ E-mail: [email protected] INTRODUCTION (IPCC 2007). Most areas of the ocean have warmed, albeit with considerable spatial variation in the magnitude of change (Hansen et al. 2006, Rayner et al. 2006, Hoegh-Guldberg et al. 2007). Increases in ocean temperature are accompanied by changes in ocean chemistry—specifically ocean acidification (OA) resulting from increasing dissolution of atmospheric CO2 in the sea (Orr et al. 2005, Hoegh-Guldberg et al. 2007, Guinotte and Fabry 2008). Climate change The rate of anthropogenic carbon dioxide (CO2) emissions has increased from ;280 ppm prior to the industrial revolution to more than 400 ppm in 2013 and is predicted to increase to ;700 ppm in 2100 (Sabine et al. 2004). Such levels of atmospheric CO2 influence global sea surface temperatures, which have already risen by 0.768C, on average, since pre-industrial times v www.esajournals.org 1 March 2014 v Volume 5(3) v Article 33 CONCEPTS & THEORY GERBER ET AL. has also been implicated as a primary cause of sea level rise, increased frequency and intensity of storms, and changing ocean circulation patterns (Meehl et al. 2005, IPCC 2007). In coming decades, the pace of these changes is expected to accelerate, which will alter the processes underlying connectivity in marine populations. However, the implications of ocean change for marine conservation planning are just beginning to be explored (Gaines et al. 2010, McLeod et al. 2012, Rau et al. 2012). In this paper, we propose a general framework to understand the impacts of warming and acidification on the connectivity of marine organisms. Over the past decade, the number of studies on the effects of climate change on connectivity of marine organisms has increased dramatically, incorporating the effects of numerous physical and biological climatic stressors as well as multiple experimental, statistical, and modeling approaches. Most studies have focused on impacts on larval or juvenile stages of marine animal populations (e.g., 81% of 110 studies reviewed by Wernberg et al. [2012]), with benthic invertebrates being the most studied groups. Changes in ocean temperatures may influence biological processes such as dispersal and survival (Munday et al. 2009c, Johnson and Welch 2010). For example, O’Connor et al. (2007) demonstrated a relationship between temperature and a reduction in pelagic larval duration (PLD) across 69 marine species. In addition, ocean acidification has strong, negative effects on calcified organisms (e.g., calcified algae, corals, mollusks, and larval stages of echinoderms) while other taxa (e.g., crustaceans, and fleshy algae, seagrasses, and diatoms) are more resilient to ocean acidification (Kroeker et al. 2010, Kroeker et al. 2013). Much of this work documents physiological effects at the individual level, and focuses less on ecological impacts at the population or community levels. Furthermore, 65% of experimental studies conducted between 2000 and 2009 involve single-factor manipulations of either warming or acidification (Wernberg et al. 2012), with most temperature studies showing significant negative effects of warming, but acidification responses exhibiting a great degree of variability (Kroeker et al. 2010, Wernberg et al. 2012, Kroeker et al. 2013). There have been fewer v www.esajournals.org studies examining the effects of two or more climate change stressors at once (e.g., Wernberg et al.’s [2012] review in which 30% of the studies looked at two stressors and only ,5% of studies looked at more than two stressors), and these show even higher variation in responses. Increased ocean temperatures have been shown to both increase and decrease the severity of ocean acidification, and the potential interaction effects are likely significant (Gooding et al. 2009). In this paper, we develop a conceptual framework based on the concepts of structural and functional connectivity and use this framework to evaluate cumulative impacts of warming and acidification on marine connectivity (Kindlmann and Burel 2008). We use this framework to synthesize existing data on the effects of temperature and ocean acidification stress on marine organisms. We then discuss how our findings relate to developing effective marine conservation strategies to mitigate climate change impacts on marine ecosystems. A FRAMEWORK FOR UNDERSTANDING IMPACTS OF CLIMATE CHANGE ON CONNECTIVITY While there are many physical symptoms of climate change on ocean ecosystems (e.g., sea level rise, altered storm regimes [Meehl et al. 2005, Macreadie et al. 2011]), we focus specifically on changing temperature and pH for our review due to the increased uncertainty in their predictions and the lack of literature on their impacts. We relate empirical estimates of effect size of temperature and OA to functional connectivity, which describes the suite of biological or behavioral responses of individuals to the physical environment, and structural connectivity, which describes the physical and spatial structure of the environment (Kindlmann and Burel 2008, Turgeon et al. 2010). We use these concepts to characterize our theoretical and empirical understanding of the effects of climate on the biological and spatial processes underlying connectivity. This framework unites two very different effects of climate change: direct effects on the biology of dispersing individuals (functional connectivity), and emergent changes to the spatial structure of the landscape that influence the probability of population persistence (structural connectivity). By integrating individual and 2 March 2014 v Volume 5(3) v Article 33 CONCEPTS & THEORY GERBER ET AL. Fig. 1. Climate change impacts on marine connectivity with implications for Marine Spatial Planning (MSP); (a) Climate change could reduce functional connectivity by altering the duration of, trajectory and survival during the larval life cycle. Bold arrows represent organism dispersal; (b) Climate change could reduce structural connectivity by reducing habitat (dotted arrows). Grey patches represent pre-climate change habitat extent and blue patches represent habitat after climate-related change. population-level responses to climate change, our framework can be populated with empirical data that are relevant to conservation objectives, such as probability of population persistence (Fig. 1). and survival probability while dispersing), and the aggregate of individual activity at the population level. Ocean conditions influence the timing and location of cues for reproduction and settlement (Munday et al. 2009b), potential dispersal distances and survival (O’Connor et al. 2007, Munday et al. 2009c), and feeding and predation opportunities during dispersal periods. Here we summarize empirical examples and research approaches to studying the effects of ocean temperature and acidification on functional connectivity. FUNCTIONAL CONNECTIVITY: LINKING ENVIRONMENTAL CONDITIONS WITH INDIVIDUAL MOVEMENT Functional connectivity may be used to describe an organism’s biological and behavioral responses to individual elements in the physical environment as well as the spatial configuration of the entire landscape (Kindlmann and Burel 2008). This includes individual activity and performance (e.g., time available for dispersal v www.esajournals.org Empirical examples In marine systems, over 70% of species have a planktonic larval stage that is subject to dispersal 3 March 2014 v Volume 5(3) v Article 33 CONCEPTS & THEORY GERBER ET AL. (Lockwood et al. 2002, Levin 2006, Munday et al. 2009c). Furthermore, most dispersal and mortality occurs during this pelagic development stage (Morgan 1995, Levin 2006). The eggs, larvae or spores of benthic adult fish, invertebrates or seaweeds may travel tens or hundreds of kilometers before settling and transitioning to juvenile life stages (Kinlan and Gaines 2003, Siegel et al. 2003), yet mortality during the pelagic stage is also extremely high (Morgan 1995). Early life stages in the organisms’ complex life cycle thus can be critical for the maintenance of functional connectivity in marine ecosystems. Studying individual larval activity is notoriously challenging because direct observations of dispersal (e.g., movement of larvae) for most species are rare (but see Mora and Sale 2002, Planes et al. 2009). However, there has been a recent increase in research on larval retention (self-recruitment) within and dispersal (connectivity) among coral reef populations, as well as a wide range of techniques and approaches for their study, from larval tagging and paternity analyses at small scales, to biophysical models at larger scales (Jones et al. 2009). Table 1 summarizes a few examples of approaches with the potential to examine the effects of climate change on life history and functional connectivity. Connectivity can also be mediated by behavioral traits that determine settlement time and location, and these traits can be affected by changing ocean conditions. The effect of ocean acidification on larval behavior and their sensory systems has been studied experimentally most extensively on tropical coral reef fish fishes. High CO2 levels may have significant effects on the habitat selection process involved with attraction to olfactory cues, which can bring about changes in population connectivity patterns (Munday et al. 2009b). At near-future levels of CO2, orange clownfish (Amphiprion percula) tended to avoid positive settlement cues that would normally lead to the location of suitable adult settlement sites. Instead, larvae were attracted to negative stimuli that led to suboptimal locations for settlement or even locations devoid of settlement habitat, which they normally avoided in today’s CO2 conditions (Munday et al. 2009b). Exposure to elevated CO2 has also been shown to affect the timing of settlement in damselfishes (Pomacentrus spp.) with different patterns of habitat use, v www.esajournals.org potentially leading to detrimental effects on larval survival and population replenishment if settlement occurs at unfavorable times (Devine et al. 2012a). Acidification has also been shown to significantly affect adult fish homing behavior. Devine et al. (2012b) tested the effects of nearfuture levels of CO2 on the ability of adult cardinal fish (Cheilodipterus quinquelineatus) to home to their diurnal resting site after nocturnal feeding, and they detected an impaired ability to distinguish between home and foreign sites as well as increased activity level. These studies provide evidence to suggest that ocean acidification has an effect on fish brain functioning and fish behaviors (larval and adult) that may negatively impact population connectivity patterns. Statistical approaches In addition to empirical approaches quantifying key aspects of functional connectivity, efforts to characterize and model the probability of dispersal can also be used to study potential changes in the scale of functional connectivity (Box 1). Dispersal kernel functions represent the probability of dispersing a particular distance from a source location over repeated dispersal events (Lockwood et al. 2002), and capture average patterns in pre-settlement processes, but not post settlement mortality and selection (Almany et al. 2007, Graham et al. 2008). Thus for many species, dispersal kernels relate the spatial scales of dispersal to those of demographic population connectivity. Dispersal kernels can also be used to relate distributions of dispersal distances to the larval development period (Fig. 2). The average dispersal distance from one population to another can determine the scale of demographic processes, such as recolonization after disturbance. In contrast, the long tails of a dispersal distribution may be the most important determinant of migration rate and genetic connectivity (Clark 1998, Neubert and Caswell 2000, Palumbi 2004). Generalized dispersal kernels have played a central role in the development of marine reserve theory (Botsford 2001, Lockwood et al. 2002, Botsford et al. 2003, Gerber et al. 2003) and are potentially a useful tool for relating the effects of climate change to population-level responses (Munday et al. 2009a, Munday et al. 2009c). Dispersal kernels can also be 4 March 2014 v Volume 5(3) v Article 33 CONCEPTS & THEORY GERBER ET AL. Table 1. Review on the current state of knowledge of the effects of temperature and ocean acidification stress on marine organisms with respect to functional and structural connectivity. Climate change impact Functional Ocean acidification (high CO2 conditions) Increased ocean temperatures Approach Taxa Findings Experimental manipulation of CO2 levels þ settlement cues Experimental manipulation of CO2 levels Orange clownfish (larvae) Induced attraction to suboptimal or non-existent settlement habitat Munday et al. (2009c) Damselfishes (larvae) Unfavorable timing of settlement Devine et al. (2012a) Cardinalfish (adult) Altered homing behavior: impaired distinction between home and foreign sites Significant changes in spawning patterns in the southern Benguela Upwelling system. Reduced PLD has large impact on dispersal at large scales, and spawning location and temporal variability explains connectivity patterns in the Bay of Biscay. Devine et al. (2012b) Evolutionary physical model Small pelagic fish (larvae) Coupled physicalbiological model (IBM) using Lagrangian particle tracking models and dispersal kernel descriptors European anchovy (larvae) Modeling framework explicitly simulating larval behavior Coupled 3-D hydrodynamic model-IBM (Lagrangian) and dispersal kernels Coupled oceanographic model-IBM Weakly swimming fish larvae Generic benthic invertebrate (larvae) Striped trumpeter (larvae) Shifts in major ocean currents Passive particle dispersion modeling Generic larvae Reduced (THC) Coupled hydrodynamic model-IBM Arcto-Norwegian cod Region-wide analysis of changes in reef architectural complexity Coral reefs Regional analysis of SST anomaly and coral bleaching reports Coral reefs Structural Increased ocean temperatures v www.esajournals.org Hydrodynamic spatio-temporal variability causing stronger stratification can concentrate particles in the surface where they can be affected by THC changes. Shortened PLD increased selfrecruitment rate in coastal environments. Decreased PLD induced selfretention and increased local connectivity while decreasing dispersal distance and thus regional connectivity. Positive minor effect on survival by 2050, but decreased performance and dispersal outside thermal niche by 2100, increasing mortality in Tasmania, Australia. Southerly shifts in the South Equatorial Current caused particles to shift advection patterns. Larval and juvenile transport patterns shift in response to a slowed-down THC in the NE Atlantic. The architectural complexity of coral reefs has declined drastically in the last 40 years due in part to climateinduced bleaching events, affecting both coral abundance and community composition in the Caribbean region. Positive correlation between the spatial extent and coral bleaching intensity with SST anomalies in the Caribbean over the last two decades. 5 Reference Lett et al. (2009) Huret et al. (2010) Lett et al. (2010) Irisson (2008) Ayata et al. (2010) Tracey et al. (2012) Munday et al. (2009c) Vikebø et al. (2007) Alvarez-Filip et al. (2009) McWilliams et al. (2005) March 2014 v Volume 5(3) v Article 33 CONCEPTS & THEORY GERBER ET AL. Table 1. Continued. Climate change impact Ocean acidification (high CO2 conditions) Approach Taxa Findings Empirical fish abundance estimates coupled with on-site temperature data over 6 years and long-term SST analysis Juvenile coral reef fish Meta-analyses of experimental evidence Coral reefs Natural in situ investigations Coral and seagrass communities in cool volcanic seeps Experimental manipulations of CO2 conditions Coral and seaweed communities The increasing temperate incursion of the East Australian Current (EAC) is shown to allow increased connectivity with the Great Barrier Reef. Present warming trends are shown to steadily increase the frequency of warm, survivable winters, thus allowing potential range expansions. Coral calcification expected to decline by ;15–22% on average by the end of the century. Reduced coral diversity, recruitment, abundances, and shifts in competitive interactions. Increase in seagrass cover and noncalcareous macroalgae and reduction in crustose coralline algal cover. Increased coral mortality through enhanced seaweed ability to kill and potentially outcompete corals in contact with seaweed communities. Suppressed larval oxygen consumption and reduced metamorphosis rate. Reduced coral settlement and crustose coralline algal cover. Increased sensitivity to OA under warm conditions. Coral reefs (larvae) Coral reefs Both increased ocean acidification and temperature Experimental manipulation of CO2 and temperature conditions Crustose coraline algae Algal turfs and kelp beds In non-calcifying organisms. Turfs had positive enhanced abundance and were shown to inhibit kelp recruitment. Reference Figueira and Booth (2010) Chan and Connolly (2013) Fabricius et al. (2011) Diaz-Pulido et al. (2011) Nakamura et al. (2011) Doropoulos et al. (2012) Doropoulos et al. (2012) Connell and Russell (2010) Note: Abbreviations are: THC ¼ thermohaline circulation; IBM ¼ individual based model; PLD ¼ pelagic larval duration; OA ¼ ocean acidification. applied to coupled circulation and population models (Neubert and Caswell 2000). mortality, and settlement processes of larvae, and are particularly relevant to questions related to the effects of climate change on connectivity because connectivity patterns are usually determined by both physical and biological processes (Werner et al. 2007). A small number of these coupled models have been explicitly used to look at the effects of climate change on connectivity (Lett et al. 2010). For example, by using a biophysical modeling approach and dispersal kernels to describe spatial distributions of larvae, Huret et al. (2010) found that variability in PLD can have a major impact on dispersal at large Analytical approaches: biophysical modeling Biophysical modeling approaches are increasingly being used to understand the dispersal of single-species pelagic larval stages by coupling biological properties of the organism with realistic hydrodynamic conditions (Miller 2007, Werner et al. 2007, Treml et al. 2008, Cowen and Sponaugle 2009, Lett et al. 2009, Metaxas and Saunders 2009) (Box 1, Table 2). Such biophysical models typically represent transport, behavior, v www.esajournals.org 6 March 2014 v Volume 5(3) v Article 33 CONCEPTS & THEORY GERBER ET AL. Box 1 The Gulf of California as an Illustrative Case Study To examine how temperature and pH change may influence conservation planning, we model directional changes in functional connectivity with climate change by linking an abiotic change (e.g. temperature, pH) to the rate of a biological process (larval development and related dispersal). We examine the implications of a change in mean dispersal distance resulting from climate change for spatial prioritization of conservation actions in the Gulf of California (GoC). We focus on the GoC because (1) data on larval spawning locations are available (Soria et al. 2010), (2) a circulation model is available (Marinone et al. 2008), and (3) a spatial prioritization effort has been conducted to identify conservation sites (Ulloa et al. 2006), but this effort did not account for connectivity or climate change. Here we explore whether our framework suggests that future adaptation of the prioritization scheme might be necessary. We focus on how climate change may impact dispersal and connectivity of a key species in the Northern Gulf, the rock scallop Spondylus calcifer. Rock scallops are highly sought after in artisanal fisheries, and have been recently protected by a network of marine reserves (CudneyBueno et al. 2009). Planktonic larvae of S. calcifer drift with ocean currents for several weeks following spawning and fertilization (Soria et al. 2010). Using our understanding of the potential magnitude and spatial variability in changes in connectivity and abundance resulting from potential changes in pH-value and temperature, we map potential changes in functional connectivity that could result from local climate change using a published circulation model (Marinone et al. 2008). We do not consider changes in structural connectivity because we have no reason to forecast change to habitat for rock scallop. In the absence of a downscaled general circulation model (GCM) for this region, we apply general climate change projections of 38C warming and 0.4 pH units as a simple illustration of our approach (Soria et al. 2010). We consider these changes in the context of the current configuration of priority areas identified in the Gulf of California Ecoregional Assessment (Ulloa et al. 2006), specifically focusing on the Rocas Consag priority area (Fig. 3). Our results suggest that the current spatial extent of potential settling larvae is larger than the range for future settling with ocean warming and acidification (Fig. 3). In the northern areas, current settlement extends further south and in the eastern areas, settlement stretches further west than in a þ38C warming scenario (Fig. 3). In addition, there is greater larval density within a smaller area in the future temperature scenario. How the impacts of climate change on functional connectivity affect the potential success of conservation areas depends on whether a single priority area or a network is considered (Fig. 3). Rocas Consag (Graham et al. 2008) is the biggest priority area in the Northern Gulf. Our climate change scenarios dramatically affect scallop settlement in Rocas Consag, reducing it by nearly half. However, when the entire priority area network in the Northern Gulf is considered, the impact of warming on settlement locations is negligible (Fig. 3, Table 2). This suggests that the greater coverage and spatial distribution of priority areas in the network would be more resilient to changes in mean dispersal distance of rock scallop. abilities by shortening the development time, thus increasing local retention and self-recruitment rate (Irisson 2008). The breadth of modeling approaches that have been developed in the past 20 years represents a significant increase in our understanding of the scales and vertical behavior at smaller scales, with a reduction in PLD having the potential to reduce the dispersal distance. Other approaches have explicitly simulated larval behavior and focused on the effect of increased water temperatures accelerating development of swimming v www.esajournals.org 7 March 2014 v Volume 5(3) v Article 33 CONCEPTS & THEORY GERBER ET AL. Fig. 2. Basic properties of dispersal kernels (A) vary predictably with the planktonic larval duration (PLD) and mortality (Siegel et al. 2003). (B) Mean absolute displacement of larvae relative to parental source increases with PLD, (C) variance in dispersal distances increases nonlinearly with PLD, (D) survival at the modal dispersal distance declines with PLD and (E) daily mortality rate. in oceanic currents as an additional variable (but see Munday et al. 2009c). Nonetheless, the modeling studies described in this section (see Table 1) have proven useful tools to test hypotheses about how climate change may impact connectivity patterns (Lett et al. 2010). interaction between the characteristics of the physical environment (e.g., temperature and circulation) and changes in organismal life history traits that are ultimately responsible for survival and dispersal (e.g., PLD). However, only a few studies have explicitly considered changes Table 2. Proportion of larval trajectoriesthat settle in conservation priority areas. Results from analysis of effects of temperature and pH on potential larval dispersal distance in the Gulf of California (Fig. 3). Rocas Consag Network Scenario Number Percentage of total Number Percentage of total Current þ38C þ38C, 0.4 pH 465 270 273 4.0 2.3 2.3 4061 4054 3997 35 34.9 34.5 v www.esajournals.org 8 March 2014 v Volume 5(3) v Article 33 CONCEPTS & THEORY GERBER ET AL. Furthermore, an increasing number of approaches solely focusing on how modeling population connectivity can be modified by ocean currents (i.e., under current conditions) are becoming available for specific regions (Marinone et al. 2008, Treml et al. 2008). Despite their widespread application, however, using such approaches remains difficult since assessing climate change impacts still requires extensive computing power and sophisticated models (e.g., coupled climate ocean general circulation models). The capacity to run them at the appropriate spatial resolution and in conjunction with relevant biological processes is still in its infancy (Munday et al. 2009c). The success of most of these models has strongly relied on approaches that focus at small, very local scales, which makes the use of these models heavily site-specific. substantially affect total settlement. Variation in responses could also reflect species-specific sensitivities and local adaptation to different environmental conditions (Kroeker et al. 2013). Nonetheless, the apparent trend of decreased mean dispersal distance and reduced survival probability remains crucial and useful when considering the framework proposed here (Fig. 1a). Variability may be incorporated into estimates of functional connectivity for particular cases using dispersal kernels. Despite the fact that approaches quantifying particular trajectories for the study of functional connectivity are still under development, we can nonetheless continue to study changes to the dispersal process with the use of dispersal kernels (Fig. 2). Even without specifically quantifying dispersal trajectories, we can consider how changes to the ocean influence functional connectivity by relating properties of the ocean environment to outcomes of individual movement such as dispersal distance and survival. Synthesis of functional connectivity framework As seen from the few examples mentioned here, increasing evidence suggests direct effects of changes in ocean climate on individual dispersal biology. Increasing ocean temperatures are likely to accelerate larval and egg development, leading to reduced time in the water column (Hirst and López-Urrutia 2006, O’Connor et al. 2007) allowing earlier habitat-seeking behavior (Munday et al. 2009c), changes in dispersal distance (Lett et al. 2009, Ayata et al. 2010, Huret et al. 2010, Lett et al. 2010), changes in transport processes and thus settlement location (Vikebø et al. 2007, Munday et al. 2009c, Huret et al. 2010, Tracey et al. 2012), and modifications of local versus regional connectivity (Irisson 2008, Ayata et al. 2010). Additionally, even though there remains considerable variability in responses among taxa, the combined effect of increased ocean temperatures and acidification shows a trend towards lower survival, growth, and development (Findlay et al. 2010, Lischka et al. 2011, Kroeker et al. 2013). These relationships between temperature, acidification and mortality could be mediated by direct physiological impacts, or indirectly through changes in size at age, morphology or feeding efficiency (Kurihara 2008, Dupont and Thorndyke 2009, Kroeker et al. 2010, Kroeker et al. 2013). This combination of stressors can also potentially impact other biological sources of mortality, such as predation and starvation, and changes to mortality could v www.esajournals.org Structural connectivity: relating environmental conditions to habitat area Structural connectivity reflects the spatial structure of the environment and the influence of spatial structure on the likelihood of individuals from one habitat reaching another habitat (Kindlmann and Burel 2008). In contrast to functional connectivity, which can be used to describe the effect of ocean conditions, such as temperature, on the dispersal potential of individuals via physiological mechanisms, structural connectivity describes the effect of habitat size, proximity, and quality on the connectivity of individuals inhabiting that habitat (Kindlmann and Burel 2008). For some marine species, the spatial arrangement of their habitat is determined by other species, referred to as foundation species. In such biogenic habitats, species like coral reefs, kelp, marine algae, and seagrasses host a vast biodiversity of associated invertebrates, fish, and seaweeds (Thompson et al. 2002, O’Hara et al. 2008, Hewitt and Thrush 2010, Perry et al. 2011). Structural connectivity in the ocean will inevitably respond to changes in the spatial rearrangement of biogenic habitats resulting from climate change. The following section summarizes a few examples of the impacts of increased ocean temperatures and ocean acidifi9 March 2014 v Volume 5(3) v Article 33 CONCEPTS & THEORY GERBER ET AL. cation on foundation species that maintain structural connectivity. Although we focus mostly on coral reef systems given the breadth of evidence available for them, the framework could be applied to other systems with major foundation species. The effects of acidification could be modified by concurrent warming. Some species of coralline crustose algae have been shown to be particularly sensitive to ocean acidification under warm conditions in manipulative experiments (Kleypas and Yates 2009, Doropoulos et al. 2012). In general, acidification is expected to reduce calcification rates in crustose coralline algae, potentially reducing the amount of suitable coral settlement habitat (Kleypas and Yates 2009, Doropoulos et al. 2012). Predicted end of the century CO2 levels have also been demonstrated through experimental manipulations to significantly reduce crustose coralline algal cover and consequently coral settlement, suggesting acidification may also reduce coral population recovery (Doropoulos et al. 2012). These combined impacts will likely affect structural connectivity for species dependent on biogenic habitats like coral reefs (Hoegh-Guldberg et al. 2007). Many habitat-forming species are also likely to be affected by ocean acidification through shifts in relative abundances that could lead to changes in community composition. Acidification is expected to increase productivity of autotrophic foundation species such as seagrasses, especially in cold climates (Guinotte and Fabry 2008), with positive effects on meadow size, the number of meadows, and their isolation. In tropical systems, natural in situ field studies detected an eightfold increase in seagrass cover and a doubling in noncalcareous macroalgae (Guinotte and Fabry 2008). Although structural connectivity of coral reefs may be reduced, connectivity among seagrass meadows seems likely to increase. This emerging evidence suggests both positive and negative responses of marine foundation species to ocean change, with the direction of effect depending in part on local environmental conditions, species composition, acclimation and adaptation capacity, physiological responses to interacting factors such as temperature, acidification, and nutrients (Pandolfi et al. 2011, Chan and Connolly 2013). The effects of temperature increases and acidification on the spatial arrangement of foundation species will contribute to changes in structural connectivity. Reduced habitat area could decrease structural connectivity, reducing immigration or metapopulation dynamics that might enable patch size to be maintained. In addition, chances for successful Empirical examples Ocean warming may impact habitat patch area directly through effects on foundation species’ growth, survival, and resilience potential. For example, climate change is expected to increase the frequency and severity of extreme temperature events, which may lead to increased rates of coral bleaching and subsequent decreases in coral cover (McWilliams et al. 2005, Vivekanandan et al. 2009, Anthony et al. 2011, HoeghGuldberg 2011, Hoeke et al. 2011). Even when corals acclimatize to increasing temperatures, they experience reduced growth rates (Cantin et al. 2010, Jones and Berkelmans 2010). The combination of mortality from bleaching and slower growth rates can lead to an overall reduction in coral habitat (Alvarez-Filip et al. 2009, Cantin et al. 2010, Pandolfi et al. 2011). Reduced habitat area implies increased isolation between some remaining habitats, and these changes in area and configuration could reduce dispersal, colonization and alter community structure. Much of the research on the effects of acidification on foundation species has focused on corals. The general mechanism by which corals or other calcifying organisms are affected by ocean acidification is through the increase in atmospheric CO2 altering the current dissolved inorganic carbon distribution in seawater and reducing its pH (Cohen and Holcomb 2009, Findlay et al. 2010). The reduction of carbonate ions (CO32) slows the rate at which calcifying organisms produce CaCO3 (calcification) to a point where rates of erosion exceed rates of skeletal accretion, most likely due to the fact that calcification is very energetically costly (Cohen and Holcomb 2009). Quantitative syntheses of the available experimental evidence on the sensitivity of coral calcification to ocean acidification have suggested that under business-asusual emissions scenarios, coral calcification could decline by ;15–22% on average by the end of the century (Chan and Connolly 2013). v www.esajournals.org 10 March 2014 v Volume 5(3) v Article 33 CONCEPTS & THEORY GERBER ET AL. recruitment and population persistence could be reduced because of an increase in the number of smaller habitat patches and increased distance between them (structural connectivity; Fig. 1b; Guinotte et al. 2003, Munday et al. 2009a, Hendriks et al. 2010). Decreases in suitable habitat may not only reduce overall coral reef area, but also decrease resilience to future disturbances because new larval recruits will be less likely to reach new areas to settle. Metapopulation theory suggests that changes to habitat area will have disproportionate effects on population size and persistence (Kininmoth et al. 2010, Kininmonth et al. 2011). With less available habitat, particularly of foundation species, there will not only be less larvae produced, but also potentially longer distances for settlers to travel. Recent work has used regionally downscaled climate change models that include ocean circulation together with models that include habitat type and foundation species to estimate changes in connectivity (Mumby 1999, Mumby et al. 2011). In the future, these modeling exercises should incorporate changes in functional connectivity for a more complete estimation of connectivity changes due to climate change (Fig. 1). RESERVE SIZE SPACING Determining adequate reserve size depends on management goals. One approach is to make the reserve larger than the mean dispersal distance to ensure that the reserve persists independent of dynamics in other reserves or fished areas (Botsford et al. 2001, White et al. 2010). With increasing reserve size there is eventually a tradeoff in terms of reduced spillover (Gaines et al. 2010). Our review suggest that with reduced structural connectivity, reserves may need to be larger to compensate for habitat loss (Fig. 1b), consistent with previous suggestions (McLeod et al. 2009). In terms of spacing, network designs must consider the mean larval dispersal distance of target species (Botsford et al. 2001, Lockwood et al. 2002, Botsford et al. 2003). Marine reserves are thought to benefit fisheries primarily through adult spillover to unprotected areas and larval export from protected areas to other protected areas as well as unprotected areas (Gaines and Bertness 1992, Botsford et al. 2001, Botsford et al. 2003, Gerber et al. 2003, Gaines et al. 2010). If reserves are spaced so that there is sufficient connectivity among them, then persistence of the entire network is possible even if no reserve is self-persistent (Kaplan 2006). With variability in dispersal distances, reserve spacing is less important than size (Kaplan 2006); yet spacing must be close enough relative to dispersal distance to allow network persistence (Moffitt et al. 2009). Ocean warming and acidification may alter the spatial scale of connectivity, potentially increasing connectivity among nearby habitats and reducing connectivity among already distant habitats. Thus, marine reserve networks may need to be designed either with a spatial arrangement that can accommodate changes in the scale of connectivity (McLeod et al. 2009), or with future flexibility that could allow for the creation of additional reserves to serve as stepping stones (Treml et al. 2008) to connect distant habitats that are increasingly isolated. Optimal reserve size and spacing will clearly depend on the dispersal distance of the target species, which may be related to PLD. Shorter PLDs will require reserves to be spaced closer together, but may also mean that reserve size can be relatively small and still maintain IMPLICATIONS OF CHANGING CONNECTIVITY FOR MARINE CONSERVATION Understanding how to incorporate climate change into marine conservation strategies such as marine reserve design and marine spatial planning is critical to sustainably managing marine populations. One common approach to marine conservation is the establishment of marine reserves, which can be planned based on three general principles: (1) reserve size and spacing must be scaled to mean dispersal distance of target species, (2) reserves must capture an adequate fraction of larvae of target species, and (3) networks of reserves have distinct advantages over single reserves (Botsford et al. 2003, Gerber et al. 2003, Gruss et al. 2011). Here we discuss implications of our conceptual framework and synthesis for marine reserve theory. v www.esajournals.org AND 11 March 2014 v Volume 5(3) v Article 33 CONCEPTS & THEORY GERBER ET AL. Fig. 3. Weighted mean density of larvae at (A) current temperature, (B) current temperature þ38C, and (C) þ38C and acidification of 0.4 pH units. Passive larval trajectories were modeled using a three-dimensional, baroclinic numerical model, and final location was determined using a temperature-dependent larval duration (Eq. 1). Conservation priority areas including Rocas Consag (Graham et al. 2008) are indicated by black lines. Values were calculated on a 1-km grid with a 5 3 5 km smoothing algorithm. export. Longer PLDs will likely require larger reserves, but the space between them can also be greater. CAPTURING OF LARVAE AN Identifying where these places may persist in a changing climate is critical to future reserve design. During spatial planning exercises, particular attention could be given to protecting places that support high levels of larval export as the climate changes (i.e., ‘‘core areas’’). Including smaller, but spatially closer reserves may ensure connectivity even to more distant habitats. In places where warming is expected to be greater, these distances may need be relatively short. In Box 1, we use a coupled bio-physical model for the Gulf of California to illustrate implications for reserve design (Table 2). ADEQUATE FRACTION Our review suggests that warming and OA could reduce larval survival, changing total larval output for several taxa (Anthony et al. 2008, Kroeker et al. 2010, Talmage and Gobler 2010). Botsford et al. (2001) propose a numerical threshold of 35% of natural larval settlement in a population that must be captured by reserves. This value was derived for a case of no reproduction outside reserves and for a settlerrecruit relationship that has a slope of 1/0.35 at the origin (reflecting groundfish stocks off the California and Oregon coasts). While 35% is not a universal or absolute number (White et al. 2010), reduced larval survival from increasing pH could represent a threat for any minimum threshold based on a healthy, non-exploited or otherwise impacted population. To accommodate climatedriven increases in mortality, targets for minimum larval retention should be greater than 35%. Although larger reserves could compensate for reduced larval retention, there would be tradeoffs in the amount of larval export. Reserves designed to protect key life stages where the target species aggregate may be sufficient. v www.esajournals.org IMPLICATIONS FOR MARINE SPATIAL PLANNING In the context of a framework based on structural and functional connectivity, the evidence we have reviewed suggests that connectivity could be reduced in warmer, more acidic oceans. We illustrate how these changes could impact the effectiveness of the design of marine conservation areas for a benthic marine invertebrate in the Gulf of California (Box 1, Fig. 3). Understanding the precise impacts of warming and acidification on marine connectivity will require detailed studies aimed at quantitatively determining scaling relationships and thresholds between climate factors and critical demographic parameters. It is important to quantitatively consider the potential for general changes in the 12 March 2014 v Volume 5(3) v Article 33 CONCEPTS & THEORY GERBER ET AL. size and spacing of reserves (Almany et al. 2009, McLeod et al. 2010), particularly for foundation or target species that are experiencing changes in ocean temperature and acidification. While it is well-established that a network of marine protected areas is needed to manage marine species with a bipartite life cycle, reserves should be closer together and larger in size to mitigate climate change impacts (McLeod et al. 2009). In fact, climate change could lead to some predictable (directional) changes in patterns. For example, our review suggests that conservation areas may need to be closer together and larger in area than previously thought. Increasing the proportion of habitats covered by reserves by increasing reserve size and putting reserves closer together would increase the likelihood for success. Ensuring that connectivity is maintained through stepping stones that may not necessarily increase the total proportion of area under reserves is also possible. Protection of areas of greater resilience or resistance is often cited as an element of mitigating the effects of climate change for marine ecosystems (West and Salm 2003, Grimsditch and Salm 2005), although identifying these areas is challenging (Chollett et al. 2010). Furthermore, because many fish species migrate to warmer water for reproduction, shortened PLDs could actually increase MPA retention and therefore benefit single MPA persistence. In recent years, Marine Spatial Planning (MSP) has become a popular approach to marine conservation (Foley et al. 2010) because of its focus on sustainable use for a wide range of stakeholders. Most MSP efforts are spatially explicit to account for a range of biological, social, and economic factors (Crowder and Norse 2008, Ogden 2010). Some efforts include connectivity in the design framework (Beger et al. 2010a, Beger et al. 2010b), but they rarely consider how connectivity may change in coming decades. Given that the potential effects of climate change and ocean acidification on connectivity are significant, ignoring these variations may compromise the long-term effectiveness of management and conservation actions. In light of uncertainty about how ecosystem services associated with multi-use marine zones are going to change with climate change, flexible zoning will be essential in a changing world. In the spirit of v www.esajournals.org adaptive management, regular (e.g., decadal) assessment of social and ecological patterns should be conducted and spatial management can be modified based on the best available data. In addition to considering habitat and species in conservation planning, spatial planning should also include areas that are predicted to exhibit different responses to climate change (Ackerly et al. 2010). Incorporating this type of ‘‘climate heterogeneity’’ into marine spatial planning offers the opportunity to zone for higher levels of protection in key areas that are not predicted to change while enforcing some restriction in places that may become key larval settling areas over time. Considering the full range of uses that are typically included in MSP is important to understand the relevance of climate change and ocean acidification for conservation prioritization. CONCLUSION Even in the absence of desired data, developing a framework for predicting changes in the spatial distribution of marine organisms not only highlights insights from available data and models (Fig. 1), but also underscores the importance of improving our fundamental understanding of climate change impacts on marine systems. Data on the interactive effects of ocean acidification and temperature as well as habitat data at fine-scales may enable us to better assess how changes in functional and structural connectivity may affect marine populations and ultimately, design conservation strategies aimed at maintaining their persistence. Our framework can be used to incorporate other dimensions of climate change, such as altered circulation patterns, sealevel rise, and frequency and intensity of storms as these data become available. Integrating fundamental insights of climate change impacts on marine organisms into conservation planning is critical to the future of marine biodiversity. ACKNOWLEDGMENTS We are grateful to Guido Marinone for providing outputs from his circulation model and to Robert Wildermuth for insightful comments on this manuscript. 13 March 2014 v Volume 5(3) v Article 33 CONCEPTS & THEORY GERBER ET AL. Slows Coral Growth in the Central Red Sea. Science 329:322–325. Chan, N. C. S. and S. R. Connolly. 2013. Sensitivity of coral calcification to ocean acidification: a metaanalysis. Global Change Biology 19:282–290. Chollett, I., P. J. Mumby, and J. Cortes. 2010. Upwelling areas do not guarantee refuge for coral reefs in a warming ocean. Marine Ecology Progress Series 416:47–56. Clark, J. S. 1998. Why trees migrate so fast: Confronting theory with dispersal biology and the paleorecord. American Naturalist 152:204–224. Cohen, A. L. and M. Holcomb. 2009. Why corals care about ocean acidification: Uncovering the mechanism. Oceanography 22:118–127. Connell, S. D. and B. D. Russell. 2010. The direct effects of increasing CO2 and temperature on noncalcifying organisms: increasing the potential for phase shifts in kelp forests. Proceedings of the Royal Society B 277:1409–1415. Cowen, R. K. and S. Sponaugle. 2009. Larval Dispersal and Marine Population Connectivity. Annual Review of Marine Science 1:443–466. Crowder, L. and E. Norse. 2008. The role of marine spatial planning in implementing ecosystem-based, sea use management. Marine Policy 32:772–778. Cudney-Bueno, R., M. F. Lavin, S. G. Marinone, P. T. Raimondi, and W. W. Shaw. 2009. Rapid effects of marine reserves via larval dispersal. PLoS One 4:e4140. Devine, B. M., P. L. Munday, and G. P. Jones. 2012b. Homing ability of adult cardinalfish is affected by elevated carbon dioxide. Oecologia 168:269–276. Devine, B. M., P. M. Munday, and G. P. Jones. 2012a. Rising CO2 concentrations affect settlement behaviour of larval damselfishes. Coral Reefs 31:229–238. Diaz-Pulido, G., M. Gouezo, B. Tilbrook, S. Dove, and K. R. N. Anthony. 2011. High CO2 enhances the competitive strength of seaweeds over corals. Ecology Letters 14:156–162. Doropoulos, C., S. Ward, G. Diaz-Pulido, O. HoeghGuldberg, and P. J. Mumby. 2012. Ocean acidification reduces coral recruitment by disrupting intimate larval-algal settlement interactions. Ecology Letters 15:338–346. Dupont, S. and M. C. Thorndyke. 2009. Impact of CO2driven ocean acidification on invertebrates early life-history: What we know, what we need to know and what we can do. Biogeosciences Discussions 6:3109–3131. Fabricius, K. E., C. Langdon, S. Uticke, C. Humphrey, S. Noonan, G. De’ath, R. Okazaki, N. Muehllehner, M. S. Glas, and J. M. Lough. 2011. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nature Climate Change 1:165–169. Figueira, W. F. and D. J. Booth. 2010. Increasing ocean LITERATURE CITED Ackerly, D. D., S. R. Loarie, W. K. Cornwell, S. B. Weiss, H. Hamilton, R. Branciforte, and N. J. B. Kraft. 2010. The geography of climate change: implications for conservation biogeography. Diversity and Distributions 16:476–487. Almany, G. R., M. L. Berumen, S. R. Thorrold, S. Planes, and G. P. Jones. 2007. Local replenishment of coral reef fish populations in a marine reserve. Science 316:742–744. Almany, G. R., S. R. Connolly, D. D. Heath, J. D. Hogan, G. P. Jones, L. J. McCook, M. Mills, R. L. Pressey, and D. H. Williamson. 2009. Connectivity, biodiversity conservation and the design of marine reserve networks for coral reefs. Coral Reefs 28:339–351. Alvarez-Filip, L., N. K. Dulvy, J. A. Gill, I. M. Cote, and A. R. Watkinson. 2009. Flattening of Caribbean coral reefs: region-wide declines in architectural complexity. Proceedings of the Royal Society B 276:3019–3025. Anthony, K. R. N., D. I. Kline, G. Diaz-Pulido, S. Dove, and O. Hoegh-Guldberg. 2008. Ocean acidification causes bleaching and productivity loss in coral reef builders. Proceedings of the National Academy of Sciences USA 105:17442–17446. Anthony, K. R. N., J. A. Maynard, G. Diaz-Pulido, P. J. Mumby, P. A. Marshall, L. Cao, and O. HoeghGuldberg. 2011. Ocean acidification and warming will lower coral reef resilience. Global Change Biology 17:1798–1808. Ayata, S. D., P. Lazure, and E. Thiebaut. 2010. How does the connectivity between populations mediate range limits of marine invertebrates? A case study of larval dispersal between the Bay of Biscay and the English Channel (North-East Atlantic). Progress in Oceanography 87:18–36. Beger, M., H. S. Grantham, R. L. Pressey, K. A. Wilson, E. L. Peterson, D. Dorfman, P. J. Mumby, R. Lourival, D. R. Brumbaugh, and H. P. Possingham. 2010a. Conservation planning for connectivity across marine, freshwater, and terrestrial realms. Biological Conservation 143:565–575. Beger, M., S. Linke, M. Watts, E. Game, E. Treml, I. Ball, and H. P. Possingham. 2010b. Incorporating asymmetric connectivity into spatial decision making for conservation. Conservation Letters 3:359–368. Botsford, L., A. Hastings, and S. D. Gaines. 2001. Dependence of sustainability on the configuration of marine reserves and larval dispersal distance. Ecology Letters 4:144–150. Botsford, L. W., F. Micheli, and A. Hastings. 2003. Principles for the design of marine reserves. Ecological Applications 13:S25–S31. Cantin, N. E., A. L. Cohen, K. B. Karnauskas, A. M. Tarrant, and D. C. McCorkle. 2010. Ocean Warming v www.esajournals.org 14 March 2014 v Volume 5(3) v Article 33 CONCEPTS & THEORY GERBER ET AL. temperatures allow tropical fishes to survive overwinter in temperate waters. Global Change Biology 16:506–516. Findlay, H. S., M. A. Kendall, J. I. Spicer, and S. Widdicombe. 2010. Post-larval development of two intertidal barnacles at elevated CO2 and temperature. Marine Biology 157:725–735. Foley, M. M., B. S. Halpern, F. Micheli, M. H. Armsby, M. R. Caldwell, C. M. Crain, E. Prahler, N. Rohr, D. Sivas, M. W. Beck, M. H. Carr, L. B. Crowder, J. E. Duffy, S. D. Hacker, K. L. McLeod, S. R. Palumbi, C. H. Peterson, H. M. Regan, M. H. Ruckelshaus, P. A. Sandifer, and R. S. Steneck. 2010. Guiding ecological principles for marine spatial planning. Marine Policy 34:955–966. Gaines, S. D. and M. D. Bertness. 1992. Dispersal of juveniles and variable recruitment in sessile marine species. Nature 360:579–580. Gaines, S. D., C. White, M. H. Carr, and S. R. Palumbi. 2010. Designing marine reserve networks for both conservation and fisheries management. Proceedings of the National Academy of Sciences USA 107:18286–18293. Gerber, L. R., L. W. Botsford, A. Hastings, H. P. Possingham, S. D. Gaines, S. R. Palumbi, and S. Andelman. 2003. Population models for marine reserve design: a retrospective and prospective synthesis. Ecological Applications 13:S47–S64. Gooding, R. A., C. D. G. Harley, and E. Tang. 2009. Elevated water temperature and carbon dioxide concentration increase the growth of a keystone echinoderm. Proceedings of the National Academy of Sciences USA 106:9316–9321. Graham, N. A. J., T. R. McClanahan, M. A. MacNeil, S. K. Wilson, N. V. C. Polunin, S. Jennings, P. Chabanet, S. Clark, M. D. Spalding, Y. Letourneur, L. Bigot, R. Galzin, M. C. Öhman, K. C. Garpe, A. J. Edwards, and C. R. C. Sheppard. 2008. Climate warming, marine protected areas and the oceanscale integrity of coral reef ecosystems. PLoS One 3:e3039. Grimsditch, G. D. and R. V. Salm. 2005. Coral reef resilience and resistance to bleaching. IUCN, Gland, Switzerland. Gruss, A., D. M. Kaplan, S. Guenette, C. M. Roberts, and L. W. Botsford. 2011. Consequences of adult and juvenile movement for marine protected areas. Biological Conservation 144:692–702. Guinotte, J. M., R. W. Buddemeier, and J. A. Kleypas. 2003. Future coral reef habitat marginality: temporal and spatial effects of climate change in the Pacific basin. Coral Reefs 22:551–558. Guinotte, J. M. and V. J. Fabry. 2008. Ocean acidification and its potential effects on marine ecosystems. Pages 320–342 in Year in ecology and conservation biology. Annals of the New York Academy of Sciences. v www.esajournals.org Hansen, J., M. Sato, R. Ruedy, K. Lo, D. W. Lea, and M. Medina-Elizade. 2006. Global temperature change. Proceedings of the National Academy of Sciences USA 103:14288–14293. Hendriks, I. E., C. M. Duarte, and M. Álvarez. 2010. Vulnerability of marine biodiversity to ocean acidification: A meta-analysis. Estuarine, Coastal and Shelf Science 86:157–164. Hewitt, J. E. and S. F. Thrush. 2010. Empirical evidence of an approaching alternate state produced by intrinsic community dynamics, climatic variability and management actions. Marine Ecology Progress Series 413:267–276. Hirst, A. and A. López-Urrutia. 2006. Effects of ecolution on egg development time. Marine Ecology Progress Series 326:29–35. Hoegh-Guldberg, O. 2011. Coral reef ecosystems and anthropogenic climate change. Regional Environmental Change 11:S215–S227. Hoegh-Guldberg, O., P. J. Mumby, A. J. Hooten, R. S. Steneck, P. Greenfield, E. Gomez, C. D. Harvell, P. F. Sale, A. J. Edwards, K. Caldeira, N. Knowlton, C. M. Eakin, R. Iglesias-Prieto, N. Muthiga, R. H. Bradbury, A. Dubi, and M. E. Hatziolos. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742. Hoeke, R. K., P. L. Jokiel, R. W. Buddemeier, and R. E. Brainard. 2011. Projected changes to growth and mortality of Hawaiian corals over the next 100 years. PLoS One 6. Huret, M., P. Petitgas, and M. Woillez. 2010. Dispersal kernels and their drivers captured with a hydrodynamic model and spatial indices: A case study on anchovy (Engraulis encrasicolus) early life stages in the Bay of Biscay. Progress in Oceanography 87:6–17. IPCC. 2007. Summary for policymakers. IPCC, Cambridge, UK. Irisson, J. O. 2008. Behavioural approach to larval dispersal in marine systems. Ecole doctorale de l’Ecole Pratique des Hautes Etudes. Johnson, J. E. and D. J. Welch. 2010. Marine fisheries management in a changing climate: a review of vulnerability and future options. Reviews in Fisheries Science 18:106–124. Jones, A. and R. Berkelmans. 2010. Potential costs of acclimatization to a warmer climate: growth of a reef coral with heat tolerant vs. sensitive symbiont types. PLos One 5:e10437. Jones, G. P., G. R. Almany, G. R. Russ, P. F. Sale, R. S. Steneck, M. J. H. Oppen, and B. L. Willis. 2009. Larval retention and connectivity among populations of corals and reef fishes: history, advances and challenges. Coral Reefs 28:307–325. Kaplan, D. M. 2006. Alongshore advection and marine reserves: consequences for modeling and management. Marine Ecology Progress Series 309:11–24. 15 March 2014 v Volume 5(3) v Article 33 CONCEPTS & THEORY GERBER ET AL. Kindlmann, P. and F. Burel. 2008. Connectivity measures: a review. Journal of Landscape Ecology 23:879–890. Kininmonth, S., M. Beger, M. Bode, E. Peterson, V. M. Adams, D. Dorfman, D. R. Brumbaugh, and H. P. Possingham. 2011. Dispersal connectivity and reserve selection for marine conservation. Ecological Modelling 222:1272–1282. Kininmoth, S., M. Drechsler, K. Johst, and H. P. Possingham. 2010. Metapopulation mean life time within complex networks. Marine Ecology Progress Series 417:139–149. Kinlan, B. P. and S. D. Gaines. 2003. Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020. Kleypas, J. A. and K. K. Yates. 2009. Coral reefs and ocean acidification. Oceanography 22:108–117. Kroeker, K. J., R. L. Kordas, R. Crim, I. E. Hendriks, L. Ramajo, G. S. Singh, C. M. Duarte, and J. P. Gattuso. 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Global Change Biology, in press. Kroeker, K. J., R. L. Kordas, R. N. Crim, and G. S. Singh. 2010. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecology Letters 13. Kurihara, H. 2008. Effects of CO 2-driven ocean acidification on the early developmental stages of invertebrates. Marine Ecology Progress Series 373:275–284. Lett, C., S. D. Ayata, M. Huret, and J. O. Irisson. 2010. Biophysical modelling to investigate the effects of climate change on marine population dispersal and connectivity. Progress in Oceanography 87:106– 113. Lett, C., K. A. Rose, and B. Megrey. 2009. Biophyisical models. Pages 88–111 in D. M. Checkley, J. Alheit, Y. Oozeki, and C. Roy, editors. Climate change and small pelagic fish. Cambridge University Press, Cambridge, UK. Levin, L. A. 2006. Recent progress in understanding larval dispersal: new directions and digressions. Integrative and Comparative Biology 46:282–297. Lischka, S., J. Büdenbender, T. Boxhammer, and U. Riebesell. 2011. Impact of ocean acidification and elevated temperatures on early juveniles of the polar shelled pteropod Limacina helicina: mortality, shell degradation, and shell growth. Biogeosciences 8:919–932. Lockwood, D. R., A. Hastings, and L. W. Botsford. 2002. The effects of dispersal patterns on marine reserves: does the tail wag the dog? Theoretical Population Biology 61:297–309. Macreadie, P. I., M. J. Bishop, and D. J. Booth. 2011. Implications of climate change for macrophytic rafts and their hitchhikers. Marine Ecology Pro- v www.esajournals.org gress Series 443:285–291. Marinone, S. G., M. J. Ulloa, A. Parés-Sierra, M. F. Lavı́n, and R. Cudney-Bueno. 2008. Connectivity in the northern Gulf of California from particle tracking in a three-dimensional numerical model. Journal of Marine Systems:149–158. McLeod, E., A. Green, E. Game, K. Anthony, J. Cinner, S. F. Heron, J. Kleypas, C. E. Lovelock, J. M. Pandolfi, R. L. Pressey, R. Salm, S. Schill, and C. Woodroffe. 2012. Integrating climate and ccean change vulnerability into conservation planning. Coastal Management 40:651–672. McLeod, E., R. Moffitt, A. Timmermann, R. Salm, L. Menviel, M. J. Palmer, E. R. Selig, K. S. Casey, and J. F. Bruno. 2010. Warming seas in the coral triangle: coral reef vulnerability and management implications. Coastal Management 38:518–539. McLeod, E., R. Salm, A. Green, and J. Almany. 2009. Designing marine protected area networks to address the impacts of climate change. Frontiers in Ecology and the Environment 7:362–370. McWilliams, J. P., I. M. Côté, J. A. Gill, W. J. Sutherland, and A. R. Watkinson. 2005. Accelerating impacts of temperature-induced coral bleaching in the Caribbean. Ecology Letters 86:2055–2060. Meehl, G. A., W. M. Washington, W. D. Collins, J. M. Arblaster, A. Hu, L. E. Buja, W. G. Strand, and H. Teng. 2005. How much more global warming and sea level rise? Science 307:1769–1772. Metaxas, A. and M. Saunders. 2009. Quantifying the ‘‘bio-’’ components in biophysical models of larval transport in marine benthic invertebrates: advances and pitfalls. Biological Bulletin 216:257–272. Miller, T. J. 2007. Contribution of individual-based coupled physical-biological models to understanding recruitment in marine fish populations. Marine Ecology Progress Series 347:127–138. Moffitt, E. A., L. W. Botsford, D. M. Kaplan, and M. R. O’Farrell. 2009. Marine reserve networks for species that move within a home range. Ecological Applications 19:1835–1847. Mora, C. and P. F. Sale. 2002. Are populations of coral reef fish open or closed? Trends in Ecology & Evolution 17:422–428. Morgan, S. G. 1995. Life and death in the plankton: Larval mortality and adaptation. In L. R. McEdward and P. L. Lutz, editors. Ecology of marine invertebrate larvae. CRC Press, Boca Raton, Florida, USA. Mumby, P. J. 1999. Can Caribbean coral populations be modelled at metapopulation scales? Marine Ecology-Progress Series 180:275–288. Mumby, P. J., I. A. Elliott, C. M. Eakin, W. Skirving, C. B. Paris, H. J. Edwards, S. Enriquez, R. IglesiasPrieto, L. M. Cherubin, and J. R. Stevens. 2011. Reserve design for uncertain responses of coral reefs to climate change. Ecology Letters 14:132–140. 16 March 2014 v Volume 5(3) v Article 33 CONCEPTS & THEORY GERBER ET AL. Munday, P. L., N. E. Crawley, and G. E. Nilsson. 2009a. Interacting effects of elevated temperature and ocean acidification on the aerobic performance of coral reef fishes. Marine Ecology Progress Series 388:235–242. Munday, P. L., D. L. Dixson, J. M. Donelson, G. P. Jones, M. S. Pratchett, G. V. Devitsina, and K. B. Doving. 2009b. Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proceedings of the National Academy of Sciences USA 106:1848–1852. Munday, P. L., J. M. Leis, J. M. Lough, C. B. Paris, M. J. Kingsford, M. L. Berumen, and J. Lambrechts. 2009c. Climate change and coral reef connectivity. Coral Reefs 28:379–395. Nakamura, M., S. Ohki, A. Suzuki, and K. Sakai. 2011. Coral larvae under ocean acidification: Survival, metabolism, and metamorphosis. PLoS One 6:e14521. Neubert, M. G. and H. Caswell. 2000. Demography and dispersal: Calculation and sensitivity analysis of invasion speed for structured populations. Ecology 8:1613–1628. O’Connor, M. I., J. F. Bruno, S. D. Gaines, S. E. Lester, B. S. Halpern, B. P. Kinlan, and J. M. Weiss. 2007. Temperature control of larval dispersal and implications for marine ecology, evolution, and conservation. Proceedings of the National Academy of Sciences USA 104:1266–1271. Ogden, J. C. 2010. Marine spatial planning (MSP) A first step to ecosystem-based management (EBM) in the Wider Caribbean. Revista de Biologia Tropical 58:71–79. O’Hara, T. D., A. A. Rowden, and A. Williams. 2008. Cold-water coral habitats on seamounts: Do they have a specialist fauna? Diversity and Distributions 14:925–934. Orr, J. C., V. J. Fabry, O. Aumont, L. Bopp, S. C. Doney, R. A. Feely, A. Gnanadesikan, N. Gruber, A. Ishida, F. Joos, R. M. Key, K. Lindsay, E. Maier-Reimer, R. Matear, P. Monfray, A. Mouchet, R. G. Najjar, G.-K. Plattner, K. B. Rodgers, C. L. Sabine, J. L. Sarmiento, R. Schlitzer, R. D. Slater, I. J. Totterdell, M.-F. Weirig, Y. Yamanaka, and A. Yool. 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686. Palumbi, S. R. 2004. Marine reserves and ocean neighborhoods: The spatial scale of marine populations and their management. Annual Review of Environment and Resources 29:31–68. Pandolfi, J. M., S. R. Connolly, D. J. Marshall, and A. L. Cohen. 2011. Projecting coral reef futures under global warming and ocean acidification. Science 333:418–422. Perry, C. T., M. A. Salter, A. R. Harborne, S. F. Crowley, H. L. Jelks, and R. W. Wilson. 2011. Fish as major v www.esajournals.org carbonate mud producers and missing components of the tropical carbonate factory. Proceedings of the National Academy of Sciences USA 108:3865–3869. Planes, S., G. P. Jones, and S. R. Thorrold. 2009. Larval dispersal connects fish populations in a network of marine protected areas. Proceedings of the National Academy of Sciences USA 106:5693–5697. Rau, G. H., E. McLeod, and O. Hoegh-Gudberg. 2012. The need for new ocean conservation strategies in a high-carbon dioxide world. Nature Climate Change 2:720–724. Rayner, N. A., P. Brohan, D. E. Parker, C. K. Folland, J. J. Kennedy, M. Vanicek, T. J. Ansell, and S. F. B. Tett. 2006. Improved analyses of changes and uncertainties in sea surface temperature measured in situ since the mid-nineteenth century: the HadSST2 dataset. Journal of Climate 19:446–469. Sabine, C. L., R. A. Feely, N. Gruber, R. M. Key, K. Lee, J. L. Bullister, R. Wanninkhof, C. S. Wong, D. W. Wallace, B. Tilbrook, F. J. Millero, T. H. Peng, A. Kozyr, T. Ono, and A. F. Rios. 2004. The oceanic sink for anthropogenic CO2. Science 305:367–371. Siegel, D. A., B. P. Kinlan, B. HGaylord, and S. D. Gaines. 2003. Lagrangian description of marine larval disperson. Marine Ecology Progress Series 260:83–96. Soria, G., J. Tordecillas-Guillen, R. Cudney-Bueno, and W. Shaw. 2010. Spawning induction, fecundity estimation, and larval culture of Spondylus calcifer (Carpenter 1857) (Bivalvia: Spondylidae). Journal of Shellfish Research 29:143–149. Talmage, S. C. and C. J. Gobler. 2010. Effects of past, present, and future ocean carbon dioxide concentrations on the growth and survival of larval shellfish. Proceedings of the National Academy of Sciences USA 107:17246–17251. Thompson, R. C., T. P. Crowe, and S. J. Hawkins. 2002. Rocky intertidal communities: past environmental changes, present status and predictions for the next 25 years. Environmental Conservation 29:168–191. Tracey, S. R., K. Hartmann, and A. J. Hobday. 2012. The effect of dispersal and temperature on the early life history if a temperate marine fish. Fisheries Oceanography 21:336–347. Treml, E. A., P. N. Halpin, D. L. Urban, and L. F. Pratson. 2008. Modeling population connectivity by ocean currents, a graph-theoretic approach for marine conservation. Landscape Ecology 23:19–36. Turgeon, K., A. Robillard, J. Gregoire, V. Duclos, and D. L. Kramer. 2010. Functional connectivity from a reef fish perspective: behavioral tactics for moving in a fragmented landscape. Ecology 91:3332–3342. Ulloa, R., J. Torre, L. Bourillón, A. Gondor, and N. Alcantar. 2006. Planeación ecoregional para la conservación marina: Golfo de California y costa occidental de Baja California Sur. Informe final a The Nature Conservancy. Comunidad y Biodiver- 17 March 2014 v Volume 5(3) v Article 33 CONCEPTS & THEORY GERBER ET AL. Werner, F. E., R. K. Cowen, and C. B. Paris. 2007. Coupled biological and physical models: present capabilities and necessary developments for future studies of population connectivity. Oceanography 20:54–69. West, J. M. and R. V. Salm. 2003. Resistance and resilience to coral bleaching: implications for coral reef conservation and management. Conservation Biology 17:956–967. White, J. W., L. W. Botsford, A. Hastings, and J. L. Largier. 2010. Population persistence in marine reserve networks: incorporating spatial heterogeneities in larval dispersal. Marine Ecology Progress Series 398:49–67. sidad, A. C., Guaymas, Mexico. Vikebø, F. B., S. Sundby, B. Ådlandsvik, and O. H. Otterå. 2007. Impacts of a reduced thermohaline circulation on transport and growth of larvae and pelagic juveniles of Arcto-Norwegian cod (Gadus morhua). Fisheries Oceanography 16:216–228. Vivekanandan, E., M. H. Ali, B. Jasper, and M. Rajagopalan. 2009. Vulnerability of corals to warming of the Indian seas: a projection for the 21st century. Current Science 97:1654–1658. Wernberg, T. S., D. A. Smale, and M. S. Thomsen. 2012. A decade of climate change experiments on marine organisms: procedures, patterns and problems. Global Change Biology 18:1491–1498. v www.esajournals.org 18 March 2014 v Volume 5(3) v Article 33