Differential responses to environmental challenge by common carp Cyprinus carpio highlight the importance of coping style in integrative physiology

Abstract

Common carp Cyprinus carpio displaying proactive or reactive stress coping styles were acclimated to two environmental regimes (low oxygen and low temperature), and selected groups were tested for response to an inflammatory challenge (Escherichia coli lipopolysaccharide, LPS). Plasma glucose and lactate levels were measured, as were selected C. carpio-specific messenger (m)RNA transcript abundance, including cortisol receptor (CR), enolase (ENO), glyceraldehyde 3-phosphate dehydrogenase (GAPDH) and interleukin-1-beta (IL1β) was measured in individual whole brain samples. Basal levels (in sham injected fish held in normoxic conditions at 25° C) of plasma lactate and glucose differed between coping styles, being significantly lower in proactive individuals. Both variables increased in response to LPS challenge, with the exception of plasma glucose in reactive fish held in hypoxia. Baseline levels of gene expression under control conditions were significantly different for GAPDH between behavioural phenotypes. The responses to experimental challenge were sometimes diametrically opposed between stress-coping styles in a transcript-specific manner. For CR and GAPDH, for example, the response to LPS injection in hypoxia were opposite between proactive and reactive animals. Proactive fish showed decreased CR and increased GAPDH, whereas reactive showed the opposite response. These results further highlight that screening for stress-coping styles prior to experiments in adaptive physiology can significantly affect the interpretation of data obtained. Further, this leads to a more finely tuned analytical output providing an improved understanding of variation in individual responses to both environmental and inflammatory challenge.