The Antarctic fish Harpagifer antarcticus under current temperatures and salinities and future scenarios of climate change

Highlights

• H. antarcticus is able to cope with a moderate temperature increase in the Antarctic.

• A drastic increment in mortality was observed with seawater warming.

• The stenothermal nature of H. antarcticus was confirmed.

Abstract

Antarctic coasts are highly vulnerable environments where temperature have remained very constant along millions of years. These unique environmental conditions have generated a large number of stenoic species that could be highly sensitive to future scenarios of climate change. We investigated the separate and interactive effects of increasing seawater temperature and decreasing salinity on the physiological performance of the notothenioid fish, Harpagifer antarcticus. Adult individuals were exposed to an orthogonal combination of five temperatures (2, 5, 8, 11, 14 °C) and three salinities (23, 28, 33 psu) for a 10-day period. A drastic increment in mortality was observed with seawater warming; the pattern in response to lower salinity was less clear. No fish died at the two lowest temperatures (2 and 5 °C); however, mortality increased significantly at the two highest temperatures across the salinity treatments (33.3% at 11 °C; 93.3% at 14 °C). No data were obtained at 14 °C that could be included in the physiological analyses. Ingestion and absorption rates were significantly affected by temperature and salinity, but not by the interaction of the two. Finally, we observed a negative effect of temperature but not of salinity or the interaction of both on the scope for growth of H. antarcticus. These results suggest that this species could cope with a moderate temperature increase (5 °C) in the Antarctic. However, the higher metabolic rates observed at 8 and 11 °C are associated with conditions beyond the natural thermal window of this species, representing a disadvantage in the face of climate change. Therefore, and even in the hypothetical case that H. antarcticus were able to disperse to sub-Antarctic areas such as the Magellan Region, current and projected scenarios of seawater temperatures might be unsuitable for the development of effective populations of this species. The results confirm the stenothermal nature of H. antarcticus, considering its high vulnerability to environmental changes and its limited ability to cope with the more severe global warming models projected for the Antarctic and Magellan regions for the end of the century (mainly temperature).

Introduction

Antarctic coasts are highly vulnerable environments and sensitive to climate changes and the environmental conditions (e.g., seawater temperature, dissolved oxygen) there have remained very constant along millions of years. Ectotherms living in these unique environmental conditions have generated a large number of stenoic species that could be highly sensitive to environmental changes such as those expected by the end of the century (Ficke et al., 2007, IPCC, 2014). It should be noted that coastal Antarctic communities are characterized by high endemism (Hogg et al., 2011, Griffiths and Waller, 2016) and that the limited ability to move to colder latitudes as the ocean warms, makes them potentially vulnerable to warming scenarios.

The Antarctic Peninsula has been described as one of the environments most affected by climate change in the world, which can disrupt local interactions and, thus, ecosystem functioning and stability (Duffy et al., 2017). Changes in temperature and salinity in the Southern Ocean have been described as a prominent signal of climate change. On average, surface seawater of the Western Antarctic Peninsula has warmed nearly 1 °C in the last half century, and salinity has experienced strong changes, especially in coastal surface waters, due to melting Antarctic sea ice (Szafranski and Lipski, 1982, Meredith and King, 2005, Turner et al., 2005, Haumann et al., 2016). Currently, temperatures up to 3 °C have already been reported for shallow benthic environments in the Antarctic Peninsula (Cárdenas et al., 2018). Despite these rapid abiotic changes, the responses of Antarctic organisms and consumer-resource interactions to ocean warming and reduced salinity remain unclear.

The ability of an organism to face changes in temperature and salinity is related to its level of tolerance. Stenoic organisms have low tolerance and can only survive in a narrow thermal range. Therein, their aerobic performance is maximal and covers all physiological costs. When the organism is exposed to either extreme of the temperature range, its capacity for aerobic performance is reduced (Pejus temperatures; Pörtner, 2002). Beyond those critical temperatures, the mitochondrial demand for oxygen cannot be met.

Stenohaline organisms also have a rather narrow range of tolerance for salinity, and survival decreases above and below the optimal range (Kinne, 1964). In terms of the relationship between temperature and salinity, a reduction in salinity can heighten the sensitivity of an organism, reducing its thermal tolerance range as well as its capacity to respond to certain levels of environmental change (Kinne, 1970).

Temperature is one of the most important environmental variables for ectotherms as it controls all biochemical reactions within the body tissues (Hochachka and Somero, 2002). Because many marine organisms live close to their thermal compensatory capacity (Somero, 2002), they are highly affected (i.e., behavioral and physiological responses) by environmental temperatures that fluctuate beyond their species-specific optimum, with effects extending to survival and ecological interactions (Pörtner, 2006, Godbold and Solan, 2013, Sandblom et al., 2014). Thus, physiological plasticity has been described as one of the main factors influencing survival in ectothermic organisms, and the capacity to acclimate has been recognized as a key process for coping (or not) with climate change drivers (Calosi et al., 2008, Peck et al., 2010).

The coastal ichthyofauna of Antarctica is highly endemic and dominated by fish belonging to the suborder Notothenioids (Andriashev, 1987). The physiological characteristics of this group of fish are related to its isolation as well as the physical characteristics of the environment (Clarke, 1983): stable low temperatures, high salinity, and seasonal changes in the ice sheet. The model species for the present study was the Antarctic notothenioid fish, Harpagifer antarcticus. This stenothermic species (Brodeur et al., 2003) inhabits shallow waters (0–20 m) from the Antarctic Peninsula to the South Sandwich Islands (White and Burren, 1992). Harpagifer antarcticus consumes mobile preys, principally gammarid amphipods, of which Gondogeneia antarctica is the most abundant species (Duarte and Moreno, 1981, Daniels, 1982). Because amphipods can form dense assemblages of up to 300,000 ind m⁻² (Amsler et al., 2014), they constitute an important trophic resource for Antarctic coastal fish. Thus, in order to improve our understanding of the consequences of climate change for Antarctic coastal ecosystems, we must determine whether and how climate change factors (e.g., seawater warming, salinity changes) affect the capacity of Antarctic notothenioid fish to prey on gammarid amphipods.

Here, we test the hypothesis that warmer seawater and lower salinity induced by climate change will affect predator-prey interactions in this Antarctic coastal ecosystem. This hypothesis led to the prediction that significant drops in salinity will reduce the thermal tolerance range of the notothenioid fish, H. antarcticus, leading to a reduction in its aerobic performance capacity and a concomitant decline of predation rates on the gammarid amphipod, G. antarctica. To test this prediction, we investigate the effects of a suite of temperature-salinity combinations (current and projected conditions in the Antarctic and Sub-Antarctic Magellan Region) on the physiological performance of H. antarcticus and its predation rate on G. antarctica. This study will help to prove why there are separate species of Harpagifer in the Magellan and Antarctic regions and why there could be no gene flow from south to north, even if oceanographic conditions allowed it – that is, the role of local environmental filtering in the structuring of local Antarctic and Sub-Antarctic communities.