Abstract
BackgroundPrenatal or embryonic learning, behavioral change following experience made prior to birth, may have significant consequences for postnatal foraging behavior in a wide variety of animals, including mammals, birds, fish, amphibians, and molluscs. However, prenatal learning has not been previously shown in arthropods such as insects, spiders and mites.Methodology/Principal FindingsWe examined prenatal chemosensory learning in the plant-inhabiting predatory mite Neoseiulus californicus. We exposed these predators in the embryonic stage to two flavors (vanillin or anisaldehyde) or no flavor (neutral) by feeding their mothers on spider mite prey enriched with these flavors or not enriched with any flavor (neutral). After the predators reached the protonymphal stage, we assessed their prey choice through residence and feeding preferences in experiments, in which they were offered spider mites matching the maternal diet (neutral, vanillin or anisaldehyde spider mites) and non-matching spider mites. Predator protonymphs preferentially resided in the vicinity of spider mites matching the maternal diet irrespective of the type of maternal diet and choice situation. Across treatments, the protonymphs preferentially fed on spider mites matching the maternal diet. Prey and predator sizes did not differ among neutral, vanillin and anisaldehyde treatments, excluding the hypothesis that size-assortative predation influenced the outcome of the experiments.Conclusions/SignificanceOur study reports the first example of prenatal learning in arthropods.
Highlights
Prenatal or embryonic learning, defined as behavioral change following experiences before birth, i.e. in ovo or in utero, (e.g. [1]), is a widespread type of maternal effect
Choice experiment Wilcoxon signed rank tests revealed that predator protonymphs chose the chamber containing the spider mites matching the maternal diet significantly more often, irrespective of their origin and the type of non-matching spider mites offered (Z,22.037, n = 24, and p,0.05 for each of the six choice situations; figure 1)
In 17 of the remaining 24 cases the protonymphs first fed on spider mites matching the maternal diet, which was significantly higher than random expectation
Summary
Prenatal or embryonic learning, defined as behavioral change following experiences before birth, i.e. in ovo or in utero, (e.g. [1]), is a widespread type of maternal effect. Prenatal or embryonic learning, defined as behavioral change following experiences before birth, i.e. in ovo or in utero, Most research on prenatal learning to date has been carried out with mammals, humans, rats and dogs One of the first terms employed to describe prenatal learning in humans was fetal conditioning [7,8]. This study [15] reports pre-imaginal, i.e. larval (postnatal), rather than embryonic learning by insects. Behavioral change following experience made prior to birth, may have significant consequences for postnatal foraging behavior in a wide variety of animals, including mammals, birds, fish, amphibians, and molluscs. Prenatal learning has not been previously shown in arthropods such as insects, spiders and mites
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