Non-associative versus associative learning by foraging predatory mites

Abstract

BackgroundLearning processes can be broadly categorized into associative and non-associative. Associative learning occurs through the pairing of two previously unrelated stimuli, whereas non-associative learning occurs in response to a single stimulus. How these two principal processes compare in the same learning task and how they contribute to the overall behavioural changes brought about by experience is poorly understood. We tackled this issue by scrutinizing associative and non-associative learning of prey, Western flower thrips Frankliniella occidentalis, by the predatory mite, Neoseiulus californicus. We compared the behaviour of thrips-experienced and -naïve predators, which, early in life, were exposed to either thrips with feeding (associative learning), thrips without feeding (non-associative learning), thrips traces on the surface (non-associative learning), spider mites with feeding (thrips-naïve) or spider mite traces on the surface (thrips-naïve).ResultsThrips experience in early life, no matter whether associative or not, resulted in higher predation rates on thrips by adult females. In the no-choice experiment, associative thrips experience increased the predation rate on the first day, but shortened the longevity of food-stressed predators, a cost of learning. In the choice experiment, thrips experience, no matter whether associative or not, increased egg production, an adaptive benefit of learning.ConclusionsOur study shows that both non-associative and associative learning forms operate in foraging predatory mites, N. californicus. The non-rewarded thrips prey experience produced a slightly weaker, but less costly, learning effect than the rewarded experience. We argue that in foraging predatory mites non-associative learning is an inevitable component of associative learning, rather than a separate process.Electronic supplementary materialThe online version of this article (doi:10.1186/s12898-016-0112-x) contains supplementary material, which is available to authorized users.

Interference in early dual-task learning by predatory mites

“…This is probably because of the facultative feeding habit of N. californicus larvae, which feed extremely rarely (Schausberger & Croft, 1999). Mere exposure of N. californicus larvae to thrips cues, without feeding, is sufficient for learning to occur (Schausberger et al, 2010; Schausberger & Peneder, 2017). Like N. californicus , an ability to recognize kin in cannibalism contexts is known from the specialized spider mite predator P. persimilis (Schausberger 2001, 2007) and the omnivorous generalist predator I. degenerans (Faraji et al, 2000).…”

“…For the learning phase of both experiments, first-instar thrips were killed by deep-freezing at −18 °C for at least 2 h and, after thawing, immediately used in the experiments. Dead thrips were offered to facilitate feeding by the juvenile predators and allow reinforcement (Schausberger & Peneder, 2017; Schausberger et al, 2010).…”

“…Experiment 2 aimed at determining whether a multistimulus environment, that is, the simultaneous presence of kin, interferes with the ability of N. californicus to learn the cues of thrips early in life. Socially isolated N. californicus , that is, in the absence of conspecific stimuli, have repeatedly been shown to learn the cues of thrips (Schausberger & Peneder, 2017; Schausberger et al, 2010). Each experiment consisted of an early learning phase and a behavioural assay (Table 1).…”

“…Depending on the treatment, the larvae could contact and possibly become familiar with siblings and/or contact and feed on thrips. When the first protonymphs appeared, they were transferred to a new acrylic cage and fed with mixed stages of spider mites, which do not interfere with the consolidation of memory of early thrips experience (Schausberger & Peneder, 2017; Schausberger et al, 2010), until they reached adulthood. Once the predators were adult, their sex was determined, based on body size (females are approximately twice as large as males), and males were removed from the experiment.…”

“…Commonly, juvenile predators become familiar with each other early in life, by direct contact, and later remember and recognize familiar individuals (Schausberger, 2007). Neoseiulus californicus has not yet been tested for kin recognition but, like other predatory mites, has a highly sensitive phase early in life, in the facultative-feeding larval stage (Schausberger & Croft, 1999), allowing imprinting on prey: exposure to thrips, which are difficult to grasp, early in life improves foraging on this prey later in life, by shortening attack latencies and increasing predation rates (Schausberger & Peneder, 2017; Schausberger et al, 2010). Depending on food availability, ovipositing N. californicus females aggregate or disperse their eggs, with the emerging juvenile mites growing up in the same or different sites (McMurtry & Croft, 1997; Schausberger, 2003; Walzer & Schausberger, 2011).…”