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Variation in Thermal Tolerances of Native Freshwater Fishes in South Received: 10 August 2018 Accepted: 14 November 2018 DOI: 10.1111/jfb.13866 FISH REGULAR PAPER Variation in thermal tolerances of native freshwater fishes in South Africa's Cape Fold Ecoregion: examining the east–west gradient in species' sensitivity to climate warming Jody-Lee Reizenberg1 | Lesley E. Bloy2,3 | Olaf L. F. Weyl3,4 | Jeremy M. Shelton4,5 | Helen F. Dallas5,6 1Department of Biological Science, University of Cape Town, Rondebosch, South Africa The Cape Fold Ecoregion (CFE) is a biodiversity hotspot with high levels of endemism in its 2Department of Ichthyology and Fisheries freshwater fish fauna. This study examined inter and intra-specific variation in critical thermal Science, Rhodes University, Grahamstown, maxima (TCmax) for eight native species of freshwater fish from the CFE. Cape galaxias Galaxias South Africa zebratus, Breede River redfin Pseudobarbus burchelli, Berg River redfin Pseudobarbus burgi, Clan- 3 Center for Invasion Biology, South African william redfin Pseudobarbus calidus and fiery redfin Pseudobarbus phlegethon were the most ther- Institute for Aquatic Biodiversity (SAIAB), – Grahamstown, South Africa mally sensitive (TCmax = 29.8 32.8 C). Clanwilliam rock-catfish Austroglanis gilli, Eastern Cape 4DST/NRF Research Chair in Inland Fisheries redfin Pseudobarbus afer and Cape kurper Sandelia capensis were moderately sensitive and Freshwater Ecology, South African (TCmax = 33.0–36.8 C). An increase in intra-specific thermal sensitivity of S. capensis was Institute for Aquatic Biodiversity (SAIAB), observed from east to west. The results were related to in situ water temperature, which influ- Grahamstown, South Africa enced TCmax for all species, suggesting that thermal history is a major driver of variation in ther- 5Freshwater Research Centre, Scarborough, mal tolerance amongst populations. These thermal tolerance data for freshwater fishes in the South Africa CFE demonstrate that resilience to climate warming follows a geographical cline and that the 6Nelson Mandela University, Port Elizabeth, South Africa more sensitive western species and regions are conservation priorities. Correspondence Jody-Lee Reizenberg, Department of KEYWORDS Biological Sciences, University of Cape Town, Anabantidae, Austroglanidae, Cape Fold Ecoregion, Cyprinidae, Galaxiidae, thermal limits Rondebosch 7701, South Africa. Email: [email protected] Funding information The authors gratefully acknowledge the Water Research Commission (WRC) of South Africa (Project K5/2337) for funding this research, which was awarded to the Freshwater Research Centre. The National Research Foundation (NRF) South Africa and the University of Cape Town are acknowledged for student funding. 1 | INTRODUCTION annual average precipitation and the most observable hydrological alterations (Filipe et al., 2013). Non-native species introductions and Globally, the rise in atmospheric CO2 and temperature has been anthropogenic disturbance amplify the effects of these changes on recognized as one of the greatest threats to biodiversity Med-region freshwater ecosystems (Filipe et al., 2013). Consequently, (Intergovernmental Panel on Climate Change (IPCC), 2014), threaten- freshwater biodiversity has undergone acute bottlenecks resulting in ing the functioning of ecosystems at all levels of organization community structure changes and shifts in the distribution of many (Woodward et al., 2010). While climate warming is a universal phe- species (Carpenter et al., 1992; Dudgeon et al., 2006; Sunday et al., nomenon, the effects are disproportionately manifest across climatic 2012). Given their sensitivity to thermal alteration under projected regions (Woodward et al., 2010). Within the past decade, Mediterra- climate scenarios, the adaptability, vulnerability and distribution of nean climate regions (Med-regions) have experienced the most con- freshwater fauna has emerged as a primary research focus in Med- siderable increases in annual average air temperature, decreases in regions the world over. J Fish Biol. 2019;94:103–112. wileyonlinelibrary.com/journal/jfb © 2018 The Fisheries Society of the British Isles 103 104 FISH REIZENBERG ET AL. The Cape Fold Ecoregion (CFE) spans 87,900 km2 across the temperature at which physiological signs of heat stress are observed in south-eastern and south-western coasts of South Africa. It is a global ectothermic vertebrates and invertebrates (Becker & Genoway, 1979). biodiversity hotspot (Myers et al., 2000) and a priority biogeographic Physiologically, TCmax is the point at which behavioural thermoregula- unit for freshwater conservation (Abell et al., 2008; Nel et al., 2011). tion is impeded and the tissues of the organism begin to respond nega- The CFE is rich in headwater streams that provide the last remaining tively (Paladino et al., 1980). The behavioural manifestations of refuges for many small-bodied endemic fishes (Ellender & Weyl, physiological heat stress are generally consistent amongst fishes. Visible 2014). Since the formation of the Cape Fold Belt about 290 million symptoms (or biomarkers) of heat stress include the loss of righting years ago, freshwater fishes in the CFE have remained largely isolated, response (LRR) followed by the onset of muscular spasms (OS; Beitin- resulting in the high regional diversity and endemism of the freshwa- ger, 1990; Lutterschmidt & Hutchison, 1997). ter fish fauna. This fauna comprises 42 recognised taxa belonging to The widely-used protocol for determining TCmax is the critical the families Anabantidae, Austroglanidae, Cyprinidae and Galaxiidae thermal method (CTM). In the laboratory, the CTM is conducted over (Ellender et al., 2017). The majority of these endemic fishes (60%) are relatively short periods of time (1–2 h) and the thermal stress is short- on the IUCN Red List as either Endangered or Critically Endangered lived (given that the animal is removed from the experiment as soon (Ellender et al., 2017). With reference to climate change and freshwa- as visible symptoms of heat stress are observed); prolonged exposure ter ecosystem vulnerability, Dallas and Rivers-Moore (2014) recog- to TCmax in the wild however is lethal (Coutant & Brook, 1970; Eliason nised the CFE not only as a biodiversity hotspot, but a ‘hotspot for et al., 2011). Since TCmax is an indication of sensitivity to warming, it is concern’. Habitat degradation and invasion by alien fishes are the cur- useful for identifying thermally sensitive species under predicted cli- rent greatest threat to native fishes in the region (Ellender et al., mate change scenarios (Dallas & Ross-Gillespie, 2015; Somero, 2010). 2017), but the threat of climate warming may further affect these In the past, the CTM has been criticised for its ability to induce fishes adversely in the future (Shelton et al., 2018). stress in the test subjects, but the method produces data that are criti- The climate of the south-western CFE is classified as Mediterra- cal to understanding biological limits of organisms (Lutterschmidt & nean, with hot dry summers and cool wet winters (driven primarily by Hutchison, 1997). The CTM is appropriate for use with endangered winter frontal systems; Chase & Meadows, 2007; Gasith & Resh, species as alternative methods, such as the incipient lethal tempera- 1999; Reason & Rouault, 2005). Towards the south-east of the region, ture (ILT), requires death of the test individual (Becker & Genoway, rainfall is less predictable (following a year-round stochastic pattern; 1979; Beitinger et al., 2000; Dallas & Ketley, 2011) and are thus not Ellender & Weyl, 2015; Fauchereau et al., 2003). Global climate recommended for endangered species (Beitinger et al., 2000). Further- change models predict a summer maximum air temperature increase more, CTM allows for in situ experimental design, allowing for test of 2–4C and 4–6C in the eastern and western portions of the CFE organisms to be returned to the site of collection post-experiment, respectively, with an expected decrease and greater variability in rain- which is beneficial when working with endangered species. Alterna- fall respectively (Dallas & Rivers-Moore, 2014; Schulze, 2011). In tive methods, such as utilising stream temperature data to infer ther- mal limits of fish, have been used in the past, but field-based methods response to elevated air temperatures and decreased flows, stream do not account for individual responses and the ability of fish to miti- water temperatures are expected to increase throughout the CFE. In gate stressful conditions (Eaton et al., 1995). Furthermore, field data the eastern CFE where freshwater fishes, are and historically have are confounded by biotic interactions, whereas laboratory experi- been, exposed to greater variability in thermal habitat (Ellender & ments facilitate controlled exposure and the assessment of biological Weyl, 2015), this may translate into greater resilience with respect to responses that are more accurate (Todd et al., 2008). climate warming (when compared with the western conspecifics). At present, the lack of physiological information on native fishes in Temperature has been described as a master abiotic variable in the CFE is considered a major bottleneck in understanding their biol- aquatic ecosystems in that it has a particularly strong influence on fit- ogy, ecology, distributions and behaviour (Ellender et al., 2017), and ness, behaviour and life-histories of aquatic biota (Caissie, 2006; Dal- constrains the understanding of the potential consequences of climate las, 2008). Fitness,
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