Thermal Tolerance of Nearshore Fishes Across Seasons: Implications for Coastal Fish Communities in a Changing Climate

Mar Biol (2016) 163:83 DOI 10.1007/s00227-016-2858-2 ORIGINAL PAPER Thermal tolerance of nearshore fishes across seasons: implications for coastal fish communities in a changing climate Aaron D. Shultz1,2 · Zachary C. Zuckerman2 · Cory D. Suski1,2 Received: 10 June 2015 / Accepted: 2 March 2016 / Published online: 21 March 2016 © Springer-Verlag Berlin Heidelberg 2016 Abstract Global climate change is predicted to increase maximum temperatures beyond the TSM of all nearshore the variability in weather patterns with more extreme fish in this study. Distribution of fishes in the nearshore weather conditions occurring on a more frequent basis. environment in the future will depend on available thermal Little information exists on thermal limits of fishes from refuge, cost of migrating, and food web interactions. Over- highly variable environments. This study evaluated the all, the thermal landscape in the nearshore environment thermal maximum and minimum of checkered puffers, yel- in the future will likely benefit species with positive ther- lowfin mojarra, schoolmaster snapper, and bonefish across mal safety margins that are capable of acclimatizing (e.g., seasons. Thermal scope (i.e., CTmax–CTmin) of nearshore schoolmaster snapper), while relatively intolerant species fishes ranged from 24 to 28.6 °C across seasons, with (e.g., bonefish) may inhabit these systems less frequently thermal scopes typically being larger in the winter (Janu- or will be absent in the future. ary 1, 2012–March 22, 2012) than in the summer (June 26, 2012–November 9, 2012). Acclimatization response ratios 1 1 (AZRR; ΔCTmax ΔT− and ΔCTmin ΔT− ) were typically Introduction greater than 0.60 for all species, a value greater than most previously reported for fish species from variable thermal Global climate change due to anthropogenic sources has environments. Present-day maximum and minimum tem- altered weather patterns, the physical characteristics of the peratures in the nearshore environment are approximately oceans, and the distribution of species (Roessig et al. 2005). equal to or exceed the thermal tolerance limits of the fish In the next 100 years, marine temperatures are expected in this study, making thermal safety margins (TSM; i.e., to increase by as much as 2 °C (IPCC 2013). Moreover, the difference between thermal tolerance limit and extreme extreme weather events, such as major storms (i.e., tropical environmental temperature) very small or negative for cyclones), floods, heat waves, and cold spells are expected nearshore fishes (TSM upper 4.9 to 0.5; lower 0.2 to increase in both intensity and frequency as the climate = − = − to 0.4). The IPCC’s worse-case scenario will push changes (Knutson et al. 2010; Kerr 2011). Temperature is one of the main drivers behind the distribution of ectother- mic species (e.g., fish) in the ocean (Somero 2010), and Responsible Editor: H.-O. Pörtner. recent evidence indicates that climate change has altered the distribution and community interactions of some Reviewed by undisclosed experts. marine species (Perry et al. 2005; Poloczanska et al. 2013). * Aaron D. Shultz For example, an extreme weather event increased seawater [email protected] temperatures 3–5 °C above normal for more than 10 weeks along the West Coast of Australia, altering the distribu- 1 Department of Natural Resources and Environmental Sciences, University of Illinois, 1102 S. Goodwin Ave., MC tion and abundance of demersal fish, sessile invertebrates, 047, Urbana, IL 61801, USA and seaweeds in habitats throughout this region (Wernberg 2 Flats Ecology and Conservation Program, Cape Eleuthera et al. 2012). On the whole, environmental temperature may Institute, Eleuthera, Bahamas 1 3 83 Page 2 of 10 Mar Biol (2016) 163:83 exceed the physiological limits of species in the future, planet (Valiela et al. 2001; Barbier et al. 2011). Nearshore thereby affecting their biogeographical distributions. habitats are characterized by dynamic abiotic conditions, The proximity of animals to their thermal limits, coupled such as temperature, pH, and pCO2, that fluctuate over diur- with their potential to acclimatize to future environmen- nal, tidal, and seasonal scales (Lam et al. 2006). Though tal conditions, will both be factors influencing the reshap- many species of nearshore fishes demonstrate an ability ing of ecosystems as the climate changes (Stillman 2003; to cope with these dynamic conditions (Lam et al. 2006; Somero 2012). Ectotherms in the tropics are expected to Shultz et al. 2014), it is unknown if they have evolved simi- be adapted to a relatively narrow range of temperatures lar physiological limits that will allow them to cope with due to relatively small seasonal variation in temperature extreme weather patterns predicted to occur in the future and, therefore, may not have the capacity to acclimatize to due to climate change. The duration and number of heat warming seas (Ghalambor et al. 2006). However, a recent waves and cold snaps are expected to increase as the cli- meta-analysis indicates that the capacity to acclimatize to mate changes (Kerr 2011). For example, a record-break- thermal environments in marine ectotherms is not depend- ing sea surface temperature anomaly in the Caribbean of ent on latitude or thermal seasonality (Gunderson and Still- 29.5 °C was recorded in September of 2010 (Trenberth and man 2015). Rather, tropical ectotherms from thermally sta- Fasullo 2012), and a 12-day cold snap in January of 2010, ble environments are suspected to be vulnerable to climate Florida, USA, decreased nearshore water temperatures by change because they live closer to their thermal limits rela- 11.2 °C in Butternut Key, Florida from 19.3 °C on Janu- tive to organisms in temperate regions (i.e., smaller ther- ary 1 to 8.1 °C on January 12 (NOAA 2010). Considering mal safety margins; Pörtner and Farrell 2008; Nilsson et al. the proximity of fish to their thermal limits across seasons, 2009; Pörtner and Peck 2010). However, recent evidence coupled with understanding the physiological plasticity of indicates that organisms from variable environments (e.g., fish to abiotic variables when acclimatized to seasonal con- intertidal zones) may be in closer proximity to their thermal ditions, will be important tools for evaluating the response limits relative to organisms from stable environments (e.g., of fish to the future oceanic conditions and extreme weather coral reefs), making them vulnerable to temperature fluctu- events associated with climate change (Pörtner 2002). ations associated with climate change (Madeira et al. 2012; Moreover, fish from highly variable environments, such as Seebacher et al. 2014; Norin et al. 2014). Defining which nearshore marine ecosystems and latitudes between 20 and species currently live near their upper thermal limit can 35 (i.e., subtropical regions), are underrepresented in the provide a basis for evaluating how marine ecosystems will thermal tolerance literature (Sunday et al. 2011). change in the future, especially during extreme weather Based on this background, the objective of this study events, and which species will be most vulnerable to local was twofold: (1) determine the critical thermal tolerance extinction (Somero 2010). Similarly, the ability of organ- limits of four nearshore fishes across seasons, (2) relate isms to acclimatize (i.e., seasonal or long-term phenotypic these limits to current and projected thermal environ- alterations to new abiotic conditions) will play a role in ments in the ocean. To do this, we defined the critical ther- buffering species against climate change (Hofmann et al. mal maxima (CTmax) and minima (CTmin), and estimated 2010). Previous research on fish acclimatized to the same thermal scope (CTmax–CTmin), acclimatization response temperature across different seasons has demonstrated dif- ratios (AZRR), and thermal safety margins (TSM) of four ferences in metabolic rates, indicating that seasonal shifts common nearshore fishes across summer and winter sea- in physiological traits can occur (Evans 1984; Chipps et al. sons. Collectively, the outcomes of this research will help 2000). In addition, the upper thermal tolerance of several improve predictions of how species, fish communities, and subtropical species of fish has been determined to be sig- ultimately ecosystems will respond to climate change. nificantly higher during summer compared to winter, dem- onstrating a seasonal component to tolerance limits for these species (Fangue and Bennett 2003; Murchie et al. Methods 2011). Species that have relatively high thermal maxima are expected to have a limited capacity to acclimatize to This study was conducted at The Cape Eleuthera Insti- new conditions (Stillman 2003; Magozzi and Calosi 2014), tute (CEI) in Eleuthera, The Bahamas (N 24°50′05″ W but this assumption has not been tested on species found 76°20′32″). All research conformed to the University of in variable thermal environments in nearshore subtropical Illinois Institutional Animal Care and Use Committee pro- ecosystems. tocol (Protocol # 09160). Fish [adult checkered puffer, Nearshore ecosystems provide a number of important Sphoeroides testudineus (Linnaeus, 1758) and adult bone- ecosystem services such as protecting coasts, sequestering fish, Albula vulpes (Linnaeus, 1758), and juvenile yellow- carbon, and acting as nursery areas, yet they are some of fin mojarra, Gerres cinereus (Walbaum, 1792) and juvenile the most anthropogenically disturbed ecosystems on the schoolmaster snapper, Lutjanus

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