Categorizing experience-based foraging plasticity in mites: age dependency, primacy effects and memory persistence

Abstract

Behavioural plasticity can be categorized into activational (also termed contextual) and developmental plasticity. Activational plasticity allows immediate contextual behavioural changes, whereas developmental plasticity is characterized by time-lagged changes based on memory of previous experiences (learning). Behavioural plasticity tends to decline with age but whether this holds true for both plasticity categories and the effects of first-in-life experiences is poorly understood. We tackled this issue by assessing the foraging plasticity of plant-inhabiting predatory mites, Amblyseius swirskii, on thrips and spider mites following age-dependent prey experience, i.e. after hatching or after reaching maturity. Juvenile and young adult predator females were alternately presented thrips and spider mites, for establishing 1st and 2nd prey-in-life experiences, and tested, as gravid females, for their foraging plasticity when offered both prey species. Prey experience by juvenile predators resulted in clear learning effects, which were evident in likelier and earlier attacks on familiar prey, and higher proportional inclusion of familiar prey in total diet. First prey-in-life experience by juvenile but not adult predators resulted in primacy effects regarding attack latency. Prey experience by adult predators resulted mainly in prey-unspecific physiological changes, with easy-to-grasp spider mites providing higher net energy gains than difficult-to-grasp thrips. Prey experience by juvenile, but not adult, predators was adaptive, which was evident in a negative correlation between attack latencies and egg production. Overall, our study provides key evidence that similar experiences by juvenile and adult predators, including first-in-life experiences, may be associated with different types of behavioural plasticity, i.e. developmental and activational plasticity.

Learned predators enhance biological control via organizational upward and trophic top‐down cascades

“…Lack of research scrutinizing organizational up-scaling and trophic down-cascading of learning is possibly due to the widespread assumption that experience-based behavioural changes attenuate with accumulating experiences over time and cancel out in the next generation, because of the released individuals' offspring making their own experiences. However, early life experiences may lead to pervasive and persistent, sometimes lifetime, changes that cannot be compensated for by experiences made later in life (Immelmann, 1975;Monaghan, 2008;Schausberger et al, 2010Schausberger et al, , 2018Schausberger & Peneder, 2017;Stamps & Krishnan, 2017).…”

“…Lack of research scrutinizing organizational up‐scaling and trophic down‐cascading of learning is possibly due to the widespread assumption that experience‐based behavioural changes attenuate with accumulating experiences over time and cancel out in the next generation, because of the released individuals' offspring making their own experiences. However, early life experiences may lead to pervasive and persistent, sometimes lifetime, changes that cannot be compensated for by experiences made later in life (Immelmann, 1975; Monaghan, 2008; Schausberger et al., 2010, 2018; Schausberger & Peneder, 2017; Stamps & Krishnan, 2017). Importantly, individual learning may decisively influence population and community dynamics if, for example, released learned individuals have an improved prey/host finding and predation/parasitization capacity and especially if such improved predation/parasitization performance translates into enhanced reproduction (Christiansen et al., 2016).…”

“…Both non‐associative (unrewarded; only exposed to prey or their cues but no feeding on prey) and associative (rewarded; exposed to prey and feeding on prey) prey experiences during early life of the predators result in profound and persistent enhancement of predation of familiar prey later in life. Enhanced predation is evident in shortened attack latencies, which increase prey profitability (Stephens & Dunlap, 2017), and higher predation rates, which, in turn, increase the reproductive output (Christiansen & Schausberger, 2017; Christiansen et al., 2016; Reichert et al., 2017; Schausberger et al., 2018, 2020; Seiter & Schausberger, 2016). We hypothesized that the behavioural changes brought about by the predators' early life experience of thrips as prey cascade up to the population and community levels and enhance the predators' efficacy in biological control of thrips, relative to thrips‐naïve predators.…”

“…The effect size of experience and learning intensity are commonly age‐, life‐stage‐ and phase‐specific (Little et al., 2019; Stamps & Krishnan, 2017). In many animals, it is especially experiences made in the early phases of life, when the neural system is more plastic than later on, that produce profound and persistent changes in behavioural trajectories (Rohlfs Dominguez, 2014; Schausberger et al., 2018; Stamps, 2016). Learning is an individual‐level trait yet the effects of individual‐based learning may have important consequences at higher organizational levels such as populations and communities (e.g.…”

“…Enhanced predation is evident in shortened attack latencies, which increase prey profitability (Stephens & Dunlap, 2017), and higher predation rates, which, in turn, increase the reproductive output Christiansen et al, 2016;Reichert et al, 2017;Schausberger et al, 2018Seiter & Schausberger, 2016). We hypothesized that the behavioural changes brought about by the predators' early life experience of thrips as prey cascade up to the population and community levels and enhance the predators' efficacy in biological control of thrips, relative to thripsnaïve predators.…”