Characterization of darter (Etheostoma spp.) interspecific energetic responses to climate change induced temperature changes

Abstract

Shallow freshwater ecosystems are predicted to experience increases in temperature variability as the occurrence and severity of heat waves continues to rise. Ectothermic organisms like fish are especially vulnerable to these acute temperature increases as their physiological functioning is directly regulated by environmental conditions. Thus, understanding their capabilities of responding to thermal stress is critical to predict how these species will be affected by climate change. Here, we characterized the elevated temperature responses of three closely related darter species: Fantail (Etheostoma flabellare; FTD), Rainbow (Etheostoma caeruleum: RBD), and Johnny darter (Etheostoma nigrum; JD) native to the Grand River of Southern Ontario, via three experiments: Experiment #1: assessment of thermal tolerance limits and energetic enzymatic activity, Experiment #2: determination of thermal preference, and Experiment #3: characterization of metabolic responses to elevated temperatures. Specifically, Experiment #1 determined each darter’s CTmax and quantified activity and gene expression of enzymes involved in glycolysis, the Krebs cycle, and the electron transport chain in brain and heart tissue at 15C baseline and at thermal tolerance limits. Experiment #2 determined differences in thermal preference and mobility between species, and Experiment #3 compared darter aerobic scope (AS) during exposure to four different heat ramp exposures designed to mimic previously recorded heat waves. Significant differences were observed in the thermal tolerance limits of each species. For brain tissue, FTD had higher baseline enzymatic activity compared to JD and RBD, however at CTmax, this difference was lost, as both JD and FTD had similarly high enzyme activity relative to RBD. Intraspecifically, JD demonstrated a superior plastic ability, often having a significantly higher enzyme activity at CTmax compared to its baseline counterparts, while RBD activity declined at CTmax with respect to its baseline levels. Heart tissue exhibited no interspecific differences in activity levels at baseline. At CTmax, however, JD had greater activity than RBD for all heart enzymes, although neither JD or RBD were different from FTD. Similar intraspecific trends as brain were observed, with FTD and JD increasing activity at CTmax, and RBD decreasing. No differences were observed in thermal preference between species, although FTD demonstrated significantly higher mobility than JD. Metabolically, FTD AS was significantly greater than JD and RBD at both 25C and 30C, however no differences were observed at 15 or 20C. These results suggest that FTD may be the best equipped at responding to temperature-induced increased metabolic demands due to their higher baseline enzymatic activity and broader aerobic scope. This FTD advantage, and the interspecific differences observed throughout this study, may a be a result of prior adaptation and acclimatization to each species’ respective microhabitat conditions, as it is expected that FTD reside in warm, high flow, and thermally variable regions, JD in warm, moderately thermally variable, low flow environments, and RBD in cold, fast flow, and thermally stable habitats. Exposure to warm and fluctuating habitats, and high mobility levels, have been shown to broaden metabolic function, potentially explaining the high enzyme activity and aerobic scope seen in FTD, defining their superior CTmax. Collectively, these findings provide insight to predict how climate change will affect local species, and may have conservation applications for determining which species may be most at risk with increased occurrence of extreme heat events.