Social harassment induces anxiety-like behaviour in crayfish

Abstract

Social interactions leading to dominance hierarchies often elicit psychological disorders in mammals including harassment and anxiety. Here, we demonstrate that this sequence also occurs in an invertebrate, the crayfish Procambarus clarkii. When placed in the restricted space of an aquarium, crayfish dyads generally fight until one of the opponents suddenly escapes, thereafter clearly expressing a submissive behaviour. Nevertheless, the winner frequently keeps on displaying excessive aggressive acts, having deleterious consequences in losers and interpreted as harassment behaviour. We indeed observed that, contrary to winners, losers expressed anxiety-like behaviour (ALB) in correlation with the stress intensity they suffered during the harassment period mainly. Injections of an anxiolytic abolished ALB, confirming its homology with anxiety. A serotonin (5-HT) antagonist had the same effect, suggesting a role for 5-HT, whose brain concentrations increased much more in losers than in winners. Our findings suggest that the bases of harassment and of its anxiogenic consequences have emerged very early during evolution, and emphasize crayfish as an unexpected but potentially fruitful model for the study of these social disorders.

Serotonin in Animal Cognition and Behavior

“…Physical or social stress imposed to crayfish lead to avoidance responses to light exposure. This type of responses of crayfish shares similarities with rodent behavior in some behavioral tests including the plus maze [32,170]. The avoidance response in crayfish was associated with an increase of 5-HT concentrations in the brain.…”

Emotional behavior in aquatic organisms? Lessons from crayfish and zebrafish

“…Stress‐related behavior has been studied in the red swamp crayfish ( P. clarkii) (Hobbs, ), a native to Mexico and South‐Central USA. Since crayfish naturally explore new environments and (like rodents) prefer the dark (Yamane & Takahata, ), their anxiety/avoidance‐like behavior can be assessed in the light‐dark plus maze consisting of two shaded “dark” and two open “light” arms (Figure ; Bacqué‐Cazenave, Cattaert, Delbecque, & Fossat, ; Fossat et al, , ). Stressing crayfish by an electric shock (Fossat et al, , ) or descending their social status (Bacqué‐Cazenave et al, ) increases preference for the dark arms (Table ).…”

“…In crayfish, stress‐related behavior has been linked to altered serotonin signaling (Fossat et al, ). For example, stressing crayfish via electric shocks (Fossat et al, , ) or by lowering their social status (Bacqué‐Cazenave et al, ), seems to increase anxiety‐like behaviors, an effect that is mimicked by injecting serotonin into crayfish hemolymph (Fossat et al, ; Table ). Serotonin also triggers crayfish aggression (Tierney et al, ), possibly by reducing the likelihood of retreating and by increasing fight duration (Huber & Delago, ), thus, evoking a pro‐aggressive and anxiogenic profile.…”

“…Since crayfish naturally explore new environments and (like rodents) prefer the dark (Yamane & Takahata, 2002), their anxiety/avoidancelike behavior can be assessed in the light-dark plus maze consisting of two shaded "dark" and two open "light" arms ( Figure 1; Bacqué-Cazenave, Cattaert, Delbecque, & Fossat, 2017;Fossat et al, 2014Fossat et al, , 2015. Stressing crayfish by an electric shock (Fossat et al, 2014(Fossat et al, , 2015 or descending their social status (Bacqué-Cazenave et al, 2017) increases preference for the dark arms (Table 1). Their sensitivity to benzodiazepines (Bacqué-Cazenave et al, 2017;Fossat et al, 2014) suggests some predictive validity of the model (e.g., similarity of drug effects with clinical treatment in humans) despite major neuroanatomical differences from mammals.…”

“…Stressing crayfish by an electric shock (Fossat et al, 2014(Fossat et al, , 2015 or descending their social status (Bacqué-Cazenave et al, 2017) increases preference for the dark arms (Table 1). Their sensitivity to benzodiazepines (Bacqué-Cazenave et al, 2017;Fossat et al, 2014) suggests some predictive validity of the model (e.g., similarity of drug effects with clinical treatment in humans) despite major neuroanatomical differences from mammals.…”