Retention of learned predator recognition in embryonic and juvenile rainbow trout

Abstract

Minimizing predation risk, especially for young or naïve individuals, can be achieved by learning to recognize predators. Embryonic learning may optimize survival by allowing for the earliest possible response to predation threats posthatch. However, predatory threats often change over an individual’s lifetime, and using old information can be detrimental if it becomes outdated. Adaptive forgetting allows an individual to discount obsolete information in decision-making and instead emphasize newer, more relevant information when responding to predation threats. Little is known about the extent to which young individuals can learn and forget information about predation threats. Here we demonstrate that rainbow trout 1) are capable of learning from both conspecific and heterospecific alarm cues as embryos, newly hatched larvae, and free-swimming larvae, 2) exhibit adaptive forgetting of predator information at all stages, and 3) display dynamic adaptive forgetting based on the ontogeny of learning. Specifically, fish that learned information as embryos retained the information for longer periods than those that learned the same information as newly hatched alevins.

An evolutionary model of sensitive periods when the reliability of cues varies across ontogeny

“…A large body of research on reversal learning shows that organisms are capable to infer the reliability of cues in nature ( Izquierdo et al 2017 ). Trout, for example, learn to recognize the sight or smell of potential predators ( Behrens et al 2007 ; Horn et al 2019 ). When studying phenotypic plasticity in cases where the optimal response is known to the organism, we study so-called “switch-like” plasticity ( Snell-Rood 2012 ; Frankenhuis et al 2019 ).…”

Do predator odours and warmer winters affect growth of salmonid embryos?

“…To conclude, while previous studies on the effects of environmental conditions on fish embryogenesis have mainly focused on abiotic factors such as temperature (Johnston, 2006; Lavery & Cunjak, 2019), we included both temperature and a predator threat. Temperature and predator‐induced effects during embryogenesis may result in adaptive preconditioning, improving the chances for fish to reduce predation risk as juveniles (Horn et al, 2019; Nelson et al, 2013). However, our results showed that there seems to be no straightforward picture of how temperature and predator threat affect growth during the embryonic stage.…”

“…Predators both consume prey and induce nonlethal effects on prey physiology and behaviour (McCauley et al, 2011; Stoks et al, 2006). Learned predator recognition during embryogenesis has been reported in teleosts (Horn et al, 2019; Nelson et al, 2013), amphibians (Ferrari & Chivers, 2010; Garcia et al, 2017) and gastropods (Dalesman et al, 2015). For example, rainbow trout ( Oncorhynchus mykiss ) conditioned both to northern pike ( Esox lucius ) odours and conspecific alarm cues during embryogenesis exhibit anti‐predator behaviours as juveniles in the presence of pike (Horn et al, 2019).…”

“…Learned predator recognition during embryogenesis has been reported in teleosts (Horn et al, 2019; Nelson et al, 2013), amphibians (Ferrari & Chivers, 2010; Garcia et al, 2017) and gastropods (Dalesman et al, 2015). For example, rainbow trout ( Oncorhynchus mykiss ) conditioned both to northern pike ( Esox lucius ) odours and conspecific alarm cues during embryogenesis exhibit anti‐predator behaviours as juveniles in the presence of pike (Horn et al, 2019). At emergence, salmonids are susceptible to predation from a variety of fishes, including salmonids (Brännäs, 1995; Taylor & McPhail, 1985).…”

“…Given ongoing climate warming (IPCC, 2013), thermal impacts on embryogenesis will likely become more evident in the near future (Jonsson & Jonsson, 2009), with effects on fish life‐history traits later in ontogeny (Jonsson & Jonsson, 2014, 2019). In addition, not only abiotic factors such as temperature but also biological factors, for example, predator presence during embryogenesis, can have nonlethal effects on fish embryos (Atherton & McCormick, 2015; Oulton et al, 2013), fry (Jones et al, 2003) and juveniles (Horn et al, 2019; Nelson et al, 2013).…”