How Do Predators Learn to Recognize a Mimetic Complex: Experiments with Naive Great Tits and Aposematic Heteroptera

Abstract

We tested the importance of innate wariness, avoidance learning, memory and generalization for the formation of predatory behaviour in naive great tits (Parus major) towards mimetic complex of four aposematic species of true bugs (Insecta: Hemiptera: Heteroptera): Lygaeus equestris, Spilostethus saxatilis, Pyrrhocoris apterus and Graphosoma lineatum. The birds showed almost no innate wariness against the aposematically coloured bugs, although a hidden wariness elicited by defensive chemicals of some of the bug species is not excluded. Naive birds learned to avoid different species at different rates, which resulted in different prey mortalities. The avoidance learning was faster when the defensive chemicals produced an immediate irritating effect (particularly when squirted into distance – G. lineatum) than when they caused sickness several minutes after the consumption (P. apterus). The experience of birds from learning to avoid a particular species of bug affected their subsequent behaviour to other species – experience with better‐defended species resulted in longer attack latencies, more cautious attacks, broader generalization and lower prey mortality. The least defended species, P. apterus, benefited from the experience of birds with better‐defended species, whereas the birds' experience with P. apterus did not reduce mortality risk of the other species comparably. Judging from the inexperienced young birds, the mimetic relationships are likely to be quasi‐Batesian. However, as wild‐caught great tits avoid all the four species to the same extent, the relationships may become more mutualistic (quasi‐Müllerian) in later phases of learning under natural conditions. The relationships among species in the mimetic complex thus seem to depend on the amount of experience of the bird predators.

Comparative Analysis of Volatile Defensive Secretions of Three Species of Pyrrhocoridae (Insecta: Heteroptera) by Gas Chromatography-Mass Spectrometric Method

“…Moreover, P . apterus is characterized by a moderate chemical defense with a delayed effect on predator and only releases its defense secretion when it is strongly irritated [15, 19]. This species was used for optimization experiments focused on finding the most efficient approach for extracting and analyzing defensive secretion in Pyrrhocoridae.…”

“…The identity of the antipredatory chemicals and the composition of secretion may be taxon-specific and sex-dependent [1]. The antipredatory infochemicals of true bugs are mostly volatile and strongly odorous, often repellent for vertebrate predators [15], and may be toxic for predatory arthropods and even for the secreting bug itself [16]. Short-chain alcohols, aldehydes, oxo-aldehydes, ketones, esters, alkanes, organic acids, monoterpenes and aromatic alcohol/aldehydes are typical compounds, and the composition of the secretion may depend on the physiological, nutritional and developmental state of the individual and on the season [17].…”

“…the firebugs, family Pyrrhocoridae) are reluctant to release their secretion because of behavioral constraints, reduced metathoracic glands (MTGs) or anatomical architecture of their secretion releasing MTGs system [18]. Even when not released, the secretion may still be effective by making a predator sick after consuming the bug, and this experience may induce learned aversion [15, 19]. …”

Diversity of warning signal and social interaction influences the evolution of imperfect mimicry

“…However, if several sympatric, defended models vary in phenotype, predators in this area may be conservative in the avoidance of harmless species with similar warning signals, even if mimicry of the defended models is inexact (Edmunds, 2000). Experimental evidence demonstrates that predators indeed generalize a bad experience with one prey species to others (Hotová Svádová, Exnerová, Kopečková, & Štys, 2013). …”

A Desire for Parsimony

“…Certain arthropods might gain a defensive mechanism by simply and incrementally turning their setae into barbed urticating setae that easily detach from the integument when disturbed [33]. While predators that can learn to resist toxic prey based on the simple rule ‘avoid red-colored prey’ may survive longer than another that must experience the distaste of every toxic red species encountered [34,35]. Indeed, Batesian mimicry by non-toxic species relies on predators learning such parsimonious rules [36].…”