High background risk induces risk allocation rather than generalized neophobia in the fathead minnow

Abstract

To cope with the heterogeneous nature of predation and the trade-off between predator avoidance and foraging, prey animals have evolved several cognitive rules. One of these is the risk allocation hypothesis, which predicts that in environments with long periods of sustained high risk, individuals should decrease their antipredator effort to satisfy their metabolic requirements. The neophobia hypothesis, in turn, predicts increased avoidance of novel cues in high-risk habitats. Despite the recent interest in predator-induced neophobia across different sensory channels, tests of such generalized neophobia are restricted to a single fish taxon, the Cichlidae. Hence, we retested the generalized neophobia hypothesis in fathead minnows Pimephales promelas, a small schooling North American cyprinid fish. From hatching onward, minnows were exposed to conspecific alarm cues, which indicate predation risk, or distilled water in a split-clutch design. After 1 month, shoaling behavior was examined prior and subsequent to a mechanical predator disturbance. Fish previously exposed to elevated background risk formed compact shoals for a shorter time interval after the stimulus compared with controls. These results contrast previous studies of generalized neophobia but match the risk allocation hypothesis. Consequently, risk allocation and generalized neophobia are not ubiquitous cognitive rules but instead evolved adaptations of different taxa to their respective environments.

Predation risk induces age- and sex-specific morphological plastic responses in the fathead minnow Pimephales promelas

“…30 , we suspect that the plastic modifications regress outside of the breeding period in P. promelas as well. This may be possible because under perceived predation risk fathead minnows adjust their behaviour (ranging from different shoaling behaviour to altered activity patterns) independent of sex and developmental stage 34,37–44,49,60 , which may be sufficient to compensate for the lower levels of predation risk experienced by both males outside of the breeding period and females while the higher maintenance and production costs of morphological defences 5 pay off only under high predation pressure. Moreover, that the perceived level of predation pressure was high at the onset of sexual maturity in our experimental fish (i.e.…”

“…Indeed, recent research suggests that inducible defences are not uniformly expressed but instead display variation among developmental stages and sexes 30 . However, patterns of predator-induced morphological variation may differ between species similar to predator-induced behavioural traits 34 . Thus, using previous studies on inducible defences as a reference without further verification across taxa is likely to misinterpret the degree of plasticity present in nature, which distorts our view of the ability of organisms to cope with fluctuating levels of predation risk 2 .…”

Anticipatory plastic response of the cellular immune system in the face of future injury: chronic high perceived predation risk induces lymphocytosis in a cichlid fish

“…Long-term exposure to high perceived predation risk as communicated through these cues during development plastically induces generalized neophobia (Meuthen et al 2016). In adult fish, high perceived risk during development induces male-specific morphological modifications (Meuthen et al 2018a), alters loser strategies during intrasexual competition (Meuthen et al 2019a), and plastically adjusts mate preferences by lowering investment into mate choice (Meuthen et al 2019b). Our aim here was to study the impact of the same developmental environment on the cellular immune system in the P. taeniatus individuals from the studies by Meuthen et al (2016), Meuthen et al (2018a), Meuthen et al (2019b), and Meuthen et al (2019a).…”

“…In adult fish, high perceived risk during development induces male-specific morphological modifications (Meuthen et al 2018a), alters loser strategies during intrasexual competition (Meuthen et al 2019a), and plastically adjusts mate preferences by lowering investment into mate choice (Meuthen et al 2019b). Our aim here was to study the impact of the same developmental environment on the cellular immune system in the P. taeniatus individuals from the studies by Meuthen et al (2016), Meuthen et al (2018a), Meuthen et al (2019b), and Meuthen et al (2019a). To ensure that we studied antipredator plasticity in the differential leukocyte profiles of P. taeniatus rather than a short-term response to environmental modification, we investigated the immune response of P. taeniatus after individuals had completed more than half of their lifetime under high perceived predation risk.…”

“…Second, we exposed the other half of each clutch to conspecific alarm cues derived from ground whole conspecifics (a combination of four male and four female donor fish in every instance) in a concentration of 7.2 mg/l as a proxy for high perceived predation risk; alarm cue preparation has been described in more detail in Meuthen et al (2019b). The applied alarm cue concentration has previously been shown to induce behavioral (Meuthen et al 2016(Meuthen et al , 2019a and morphological (Meuthen et al 2018a) antipredator phenotypic plasticity in P. taeniatus and in other fish species (Chivers and Smith 1994). The benefits of using conspecific alarm cues to generate high perceived predation risk are that fish do not habituate to them even after chronic exposure, while they do in response to predator odors (Imre et al 2016).…”