Fear is the mother of invention: anuran embryos exposed to predator cues alter life-history traits, post-hatching behaviour, and neuronal activity patterns

Abstract

Neurophysiological modifications associated to phenotypic plasticity in response to predators are largely unexplored, and there is a gap of knowledge on how the information encoded in predator cues is processed by prey sensory systems. To explore these issues, we exposed Rana dalmatina embryos to dragonfly chemical cues (kairomones) up to hatching. At different times after hatching (up to 40 days), we recorded morphology and anti-predator behaviour of tadpoles from control and kairomone-treated embryo groups as well as their neural olfactory responses, by recording the activity of their mitral neurons before and after exposure to a kairomone solution. Treated embryos hatched later and hatchlings were smaller than control siblings. In addition, the tadpoles from the treated group showed a stronger anti-predator response than controls at 10 days (but not at 30 days) post-hatching, though the intensity of the contextual response to the kairomone stimulus did not differ between the two groups. Baseline neuronal activity at 30 days post-hatching, as assessed by the frequency of spontaneous excitatory postsynaptic events and by the firing rate of mitral cells, was higher among tadpoles from the treated versus the control embryo groups. At the same time, neuronal activity showed a stronger increase among tadpoles from the treated versus the control group after a local kairomone perfusion. Hence, a different contextual plasticity between treatments at the neuronal level was not mirrored by the anti-predator behavioural response. In conclusion, our experiments demonstrate ontogenetic plasticity in tadpole neuronal activity after embryonic exposure to predator cues, corroborating the evidence that early-life experience contributes to shaping the phenotype at later life stages.

Mechanisms underlying the control of responses to predator odours in aquatic prey

“…Chemical information is then passed from the olfactory bulb via mitral cells to the forebrain, where higher-order processing of the olfactory information occurs. The role of the olfactory pathway in processing predator odours is further supported by the fact that prolonged exposure to predator odours alters the activity of mitral cells and their sensitivity to predator odours in Rana dalmatina tadpoles (Gazzola et al, 2015). The different types of ORNs are sensitive to different odour classes, meaning food odours, pheromones and alarm cues are processed along predominantly separate pathways (Derby and Sorensen, 2008;Døving and Lastein, 2009;Hamdani and Døving, 2003).…”

“…Prey display a range of responses to predator odours and diet cues, which include alterations in behaviour, morphology, physiology and life histories (Bronmark and Miner, 1992;Chivers and Mirza, 2001;Dawidowicz and Loose, 1992;Fonner and Woodley, 2015;Gazzola et al, 2015;Hazlett, 1999). The expression of these various responses is sensitive to the time scales over which they might be beneficial in relation to the costs of induction and maintenance (Ferrari et al, 2009;Relyea, 2002;Steiner and Van Buskirk, 2009).…”

“…The expression of these various responses is sensitive to the time scales over which they might be beneficial in relation to the costs of induction and maintenance (Ferrari et al, 2009;Relyea, 2002;Steiner and Van Buskirk, 2009). Acute exposure to predator odours results in prey displaying a range of short-term antipredator behaviours, such as reduced activity (Gazzola et al, 2015), reduced feeding rate (Foam et al, 2005), increased hiding (Briones-Fourzán et al, 2008) and altered habitat use (Dawidowicz and Loose, 1992). The magnitude and duration of these behavioural defences reflect a trade-off against other fitnessenhancing activities, such as feeding, mating or guarding territories (Lima and Dill, 1990).…”

“…Unfortunately, neither study explored whether these changes directly modified cognition or behaviour. Gazzola et al (2015), working on R. dalmatina tadpoles, found that baseline activity of mitral neurons and their sensitivity to predator odours increased following prenatal exposure to predator odours. In addition to these changes in neuronal activity, tadpoles changed their baseline activity and overall activity levels following exposure to predator odours.…”

Chemically-induced plasticity in early life history ofPalaemon argentinus: are chemical alarm cues conserved within palaemonid shrimps?

“…Phenotypic plasticity, i.e. the ability of many organisms to produce different phenotypes with a given genome in response to environmental stimuli (Pigliucci et al, 2006;West-Eberhard, 2003), can be described as a chain process where sensory systems are the first step by which environmental information is acquired by the organism, and the phenotypic modification is the final product (DeWitt and Scheiner, 2004;Gazzola et al, 2015). Predatorinduced phenotypic modification of prey is a classic example of phenotypic plasticity, including the so-called inducible defenses that are thought to improve the fitness of organisms despite its inherent tradeoffs (e.g.…”