Fight‐flight or freeze‐hide? Personality and metabolic phenotype mediate physiological defence responses in flatfish

Abstract

Survival depends on appropriate behavioural and physiological responses to danger. In addition to active 'fight-flight' defence responses, a passive 'freeze-hide' response is adaptive in some contexts. However, the physiological mechanisms determining which individuals choose a given defence response remain poorly understood. We examined the relationships among personality, metabolic performance and physiological stress responses across an environmental gradient in the olive flounder, Paralichthys olivaceus. We employed four behavioural assays to document the existence of two distinct behavioural types ('bold' and 'shy') in this species. We found consistent metabolic differences between individuals of a given behavioural type across an environmental gradient: shy individuals had overall lower aerobic scope, maximum metabolic rate and standard metabolic rate than bold individuals in both high (25 ppt) and low (3 ppt) salinity. These behavioural and metabolic differences translated into divergent physiological responses during acute stress: shy individuals adopted a passive 'freeze-hide' response by reducing their oxygen consumption rates (akin to shallow breathing) whereas bold individuals adopted an active 'fight-flight' response by increasing their rates of respiration. These distinct defence strategies were repeatable within individuals between salinity treatments. Although it has been suggested theoretically, this is the first empirical evidence that the metabolic response to stressful situations differs between bold and shy individuals. Our results emphasize the importance of incorporating physiological measures to understand the mechanisms driving persistent inter-individual differences in animals.

Polymorphism and multiple correlated characters: Do flatfish asymmetry morphs also differ in swimming performance and metabolic rate?

“…Sinistral P. stellatus had greater RMR than dextrals, and although the difference was subtle, it did not differ significantly among three sampled localities ( Figure 5). Increased RMR is associated with improved swimming performance, faster recovery after exertion, behavioral boldness, and more active predator escape responses in other fishes (Killen, Mitchell et al, 2014;Marras et al, 2010;Metcalfe et al, 2016;Rupia et al, 2016;Yan, He, Cao, & Fu, 2013). Therefore, subtle RMR increases in sinistral P. stellatus could influence their swimming performance and trophic interactions and might be one factor leading to trophic segregation between morphs (Bergstrom & Reimchen, 2018).…”

“…Impacts on fish swimming performance also exist, and although studies testing this effect among individuals within species are rare, findings suggest swimming performance (Metcalfe, Van Leeuwen, & Killen, ) and recovery after exercise (Killen, Mitchell et al, ; Marras, Claireaux, McKenzie, & Nelson, ) are positively associated with greater metabolic rates. Olive flounder ( Paralichthys olivaceus ) exhibit variation in personality, with bold flounder have greater metabolic rates and a more active swimming escape response to threats than shy flounder (Rupia, Binning, Roche, & Lu, ). However, to our knowledge the association between metabolic rate and swimming performance has not been demonstrated for P. stellatus , nor have metabolic differences between morphs been assessed in other polymorphic flatfishes.…”

Thermal preference predicts animal personality in Nile tilapia Oreochromis niloticus

“…The existence of "intermediate" individuals is common when working with domestic species due to low environmental challenge (Boersma 2011). Despite the extensive range of behavioural methodologies used, different suites of personality traits have been observed in many animal species (Réale et al 2007, Briffa et al 2013, Montiglio et al, 2014 and multiple fish species including the olive flounder, Paralichthys olivaceus (Rupia et al, 2016), Mulloway Argyrossomus japonicas (Raoult et al 2012), Gilthead…”

Demystifying animal ‘personality’ (or not): why individual variation matters to experimental biologists

“…For example, MacKenzie et al (2009) found that 'proactive' and 'reactive' carp (Cyprinus carpio) exhibit distinct and sometimes opposite patterns of gene expression under control conditions and in response to an immune challenge. Similarly, Rupia et al (2016) characterized the behavioural and physiological stress responses of olive flounder, Paralichthys olivaceus. They found that flounder with 'bold' behavioural types responded to acute stress by increasing their metabolic rates, whereas 'shy' types decreased their metabolic rates relative to routine.…”