Thermal tolerance, safety margins and vulnerability of coastal species: Projected impact of climate change induced cold water variability in a temperate African region

Highlights

• Marine ectotherms physiology is a key research focus under climate change effects.

• Dynamic method determined marine ectotherms upper and lower thermal limits.

• Individual thermal limits differed based on taxonomy, biogeography and habitat.

• Macro-invertebrates are more thermally tolerant than fish species in this region.

• Tropical and temperate fish species may be susceptible to rising upwelling events.

Abstract

Anthropogenic induced climate change is predicted to increase the thermal variability in coastal waters, which can have strong physiological effects on individuals and populations of marine ectotherms. The magnitude and direction of these thermal effects varies depending on species, life stage, biogeography, habitat and season. This study aimed to compare the thermal tolerance of a range of juvenile fish and adult macro-invertebrates from intertidal and estuarine habitats in a warm-temperate, thermally variable region on the south-east coast of South Africa. Seasonal variability in thermal tolerance was compared between species, taxonomic groups, biogeographical distribution and habitat affinity and related to existing and projected water temperature data to gauge the local vulnerability of each species. Critical thermal maximum (CT_max), critical thermal minimum (CT_min), thermal breadths and scopes, and the thermal safety margins of each species were quantified. The greatest differences in thermal tolerance patterns were based on taxonomy, with macro-invertebrates having broader thermal tolerance compared to fish, with the exception of the Cape sea urchin, in both summer and winter. Relatively narrow lower breadths in tolerance and safety margin values for transient juvenile sub-tropical and temperate fish species from the intertidal rocky low-shore habitat were observed in both summer and winter. This indicates that these fish species and the Cape sea urchin may be more vulnerable to projected increases in cold temperature (upwelling in summer) than warm temperature variability in this warm-temperate region if they are unable to seek thermal habitat refuge.

Introduction

Anthropogenic induced changes in temperature patterns are evident in many of the world's marine ecosystems causing shifts in organism phenologies, traits, distributions, productivity and species interactions (e.g. Hoegh-Guldberg and Bruno, 2010; Somero, 2010; Doney et al., 2012). Compared to terrestrial endotherms, marine ectotherms are unable to regulate their body temperature physiologically (Pörtner, 2002) and occupy habitats within their thermal limits (Pörtner and Peck, 2010). As such, they are more exposed to the threat of thermal climatic changes (especially warming, Pinsky et al., 2019). Predicting the impacts of continued increasing mean ocean temperatures (predicted increase of 2.0–4.0 °C by the end of the century, IPCC, 2014) and extreme weather events on marine ectotherms at ecological, physiological and evolutionary levels is therefore a key research focus (Somero, 2010).

A first step towards understanding the vulnerability of marine ectotherms to temperature change is to determine which taxa currently live near their upper and lower thermal limits (thermal tolerance) and whether they can adjust such limits under increasing climatic stress (Stillman, 2003; Somero, 2010, 2012). The dynamic method, characterised by the critical thermal maximum (CT_max) and the critical thermal minimum (CT_min), can quantify thermal tolerance of marine ectotherms to a constant temperature change (Cowles and Bogert, 1944; Lowe and Vance, 1955; Cox, 1974). This approach can be used to infer resilience and vulnerability to warming and cooling according to biogeography, habitat and taxonomy (Somero, 2010; Madeira et al., 2012a; Vinagre et al., 2016).

For instance, eurythermal temperate species with broad thermal scopes (CT_max – CT_min), possess a great capacity to tolerate temperature variability (at both the warm and cold end of the temperature spectrum) unlike stenothermic tropical species who possess narrow thermal scopes (Pörtner and Gutt, 2016). Nearshore habitats are dynamic due to rapid, spatio-temporal changes of environmental variables, making intertidal and supratidal species better adapted than subtidal species to thermal heat shocks (i.e., higher CT_max; Madeira et al., 2012a, 2012b; Madeira et al., 2014a, 2014b; Vinagre et al., 2013, 2015). The resilience of different marine ectotherms to temperature change may also be broadly categorised according to locomotory properties (Peck et al., 2009; Somero, 2010; Tittensor et al., 2010), with mobile species (e.g. fish) having lower thermal tolerance than sessile/sedentary species (e.g. macro-invertebrates) (Somero, 2010). This is because vagile organisms can avoid unfavourable thermal conditions, while sessile organisms are forced to experience and hence withstand harsh environments (e.g. Hiddink & ter Hofstede, 2008; Huang et al., 2015; Messmer et al., 2017).

Thermal tolerance studies using CT_max and CT_min limits to assess the local vulnerability of marine ectotherms to climate change often focus on long-term mean ocean temperature increases and fail to address the potential impacts of increases in the severity and occurrence of extreme weather events (i.e. marine heatwaves – MHWs and upwelling induced cold events) (as discussed in Bates et al., 2018; Vinagre et al., 2018). Evaluating the potential effects of these predicted increases in extreme events in relation to the CT_max and CT_min limits of coastal marine ectotherms, especially in temperate regions where seasonal variability is highest, is essential in order to obtain a more realistic assessment of their local vulnerability or resilience to the impacts of climate change.

In South Africa, the warm-temperate coast is a region of increasing thermal variability, characterised by a large annual thermal range when compared with the cool-temperate and sub-tropical coasts. This variability is due to the strengthening and warming of the Agulhas Current's water on the Agulhas Bank, the presence of current and wind-driven upwelling cells (e.g. Port Alfred) along the shoreward side of the Agulhas Current in this coastal section (Maree et al., 2000; Roberts, 2005; Lutjeharms, 2007) and the effects of embayments and capes throughout the region (Schlegel et al., 2017). Marine heatwaves and cold spells will most likely have the greatest biological impact along this coastline (Duncan et al., 2019). Analysis of inshore (in situ) and offshore (optimally interpolated SST – OISST; Reynolds et al., 2007) temperature data spanning a 21-year time series (in situ – 40 years; OISST – 33 years) indicates that MHW and MCS events along the warm-temperate region are more intense and longer in duration than those along the cool-temperate and sub-tropical regions (Schlegel et al., 2017). In addition, recent climate modelling consensus predicts an increase in the intensity and frequency of El Niño-Southern Oscillation (ENSO) events (Cai et al., 2014, 2015; Wang et al., 2017), which will intensify upwelling and occurrence of seasonal extremes along the South African coast (Rouault et al., 2010). For example, recently recorded declines in SST of ~12 °C in less than 12 h have been recorded in the Tsitsikamma region, on the south-east coast, as a result of wind-driven upwelling during summer (Duncan et al., 2019). These sharp temperature decreases may be particularly detrimental because they occur in summer, when organisms are warm acclimated and may lose tolerance to cold temperatures (Pörtner and Gutt, 2016).

A comparative understanding of the effects of rapid warming and cooling in relation to seasonally adjusted CT_max and CT_min, on a broad taxonomic selection of coastal marine ectotherms with different thermal niches (biogeographic and habitat) is still lacking (Vinagre et al., 2015). Within this framework, this research aimed to: 1) determine the thermal limits (CT_max and CT_min) of fish and macro-invertebrate species from rocky shores and estuarine habitats in a temperate variable coastal system to establish seasonal differences in thermal tolerance based on taxonomy, habitat and biogeographic affinity; 2) relate these limits to current seasonal in situ water temperature data to assess the species vulnerability to existing and projected increases in extreme and seasonal weather events associated with climate change.