Aphids Playing Possum – Defensive or Mutualistic Response?

Journal of Insect Behavior, Jan 2018

Paper presents the phenomenon of thanatosis or death-feigning in selected aphids species. This specific reaction was predominantly analysed on the example of aphid subfamily Lachninae. Individuals of this group were used in experiments, during which a thanatotic response was induced with various results. The response differed from prolonged thanatosis, lasting for several minutes (Eulachnus rileyi), through shrinking behaviour (e. g. in Stomaphis graffii) to non-responsive species such as Cinara (Schizolachnus) pineti. The large interspecies variation of observed responses can be linked to other defensive mechanisms existing in the studied species, as well as to their mutualistic relationship with ants. The behaviour of shrinking is hypothesized to be the mutualistic response, developed from thanatosis, and being adapted to transportation by ant workers.

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Aphids Playing Possum – Defensive or Mutualistic Response?

J Insect Behav Aphids Playing Possum - Defensive or Mutualistic Response? Aleksandra Bilska 0 1 2 Jacek Francikowski 0 1 2 Aleksandra Wyglenda 0 1 2 Adrian Masłowski 0 1 2 Natalia Kaszyca 0 1 2 Łukasz Depa 0 1 2 0 Department of Animal Physiology and Ecotoxicology, Faculty of Biology and Environmental Protection, University of Silesia , Bankowa 9, 40-007 Katowice , Poland 1 Students' Scientific Association of Zoologists BFauantycy 2 Department of Zoology, Faculty of Biology and Environmental Protection, University of Silesia , Bankowa 9, 40-007 Katowice , Poland 3 , Faculty of Biology and Environmental Protection, University of Silesia , Bankowa 9, 40-007 Katowice , Poland Paper presents the phenomenon of thanatosis or death-feigning in selected aphids species. This specific reaction was predominantly analysed on the example of aphid subfamily Lachninae. Individuals of this group were used in experiments, during which a thanatotic response was induced with various results. The response differed from prolonged thanatosis, lasting for several minutes (Eulachnus rileyi), through shrinking behaviour (e. g. in Stomaphis graffii) to non-responsive species such as Cinara (Schizolachnus) pineti. The large interspecies variation of observed responses can be linked to other defensive mechanisms existing in the studied species, as well as to their mutualistic relationship with ants. The behaviour of shrinking is hypothesized to be the mutualistic response, developed from thanatosis, and being adapted to transportation by ant workers. Thanatosis; immobility; adaptation; fitness; predation Introduction Thanatosis, or the so called Bdeath feigning^ or Bplaying possum^ is a wellrecognized phenomenon in many animal taxa (Honma et al. 2006) . It is considered as a basic mechanism of the Blast chance^ defence behaviour, where endangered individual exhibits immobility and catatonic muscle tension. In this state the animal does not lose its conscience and is aware of the phenomena taking place in the environment (Rogers and Simpson 2014) . This behaviour, sometimes accompanied by excreting various body fluids, is known both, in vertebrates as well as invertebrates (Miyatake et al. 2004) . In case of insects, it is well known in stick-insects or some groups of beetles, where immobility is very common defensive behaviour (Godden 1972, 1974; Prohammer and Wade 1981; Gaiger and Vanin 2006; Miyatake et al. 2008; Farkas 2016) . Apart from various defensive adaptations, aphids are known to exhibit thanatosis, as a form of defence behaviour. It was observed as often exhibited behaviour after fall off the host plant (Losey and Denno 1998; Gish and Inbar 2006; Hodge et al. 2011) by non myrmecophilous aphids. In case of Acyrthosiphon pisum the aphids are known to maintain in thanatosis after the drop off for various periods of time, dependent on the nature of the stimulus (Wohlers 1981) and after that they undertake movement of various characters (Niku 1976) . The time spent in thanatosis also depends on the height of fall (Niku 1975) . This behaviour was also observed in other species such as: Aualcorthum circumflexum, Lipaphis erysimi, Macrosiphum euphorbiae and Megoura viciae (Robert 1987) , all these species being non myrmecophilous species feeding predominantly on herbaceous plants. However, little is known about the aphid’s thanatosis itself. More important seemed to be the behaviours of waving of abdomens and/or legs, escape and searching of new host plant after drop off as adaptive mechanisms against predators and other environmental factors (Roitberg et al. 1979; Mann et al. 1995; Hodge et al. 2011) . It may be suspected, that in case of apterous morphs of aphids (and contrary to alate morphs), thanatosis could be promoted defensive behaviour in terms of natural selection (Ohno and Miyatake 2007) . However, the adaptive nature of this phenomenon is not well understood. Aphids due to their sedentary life mode exhibit a very wide range of defensive mechanisms: waxy excreta, covering the body; alarm pheromones inducing escape behaviour in the colony; mutualistic relationship with ants – which serve as guards protecting aphid colony and even soldier morphs (Dixon 1998). In this view, it seemed interesting to check, whether thanatotic behaviour is somehow correlated with existing defensive mechanisms of aphids. For this purpose several representatives of the aphid subfamily Lachninae were assigned. This is a relatively homogenous group of aphids in respect of morphology, connected with woody gymnosperms and angiosperms, showing a high variety of ecological adaptations (Jousselin et al. 2013; Chen et al. 2016) . We chose this group due to a single field observation of individual of obligate myrmecophilous, tree-trunk feeding species Stomaphis graffii, which exhibited remarkable behaviour: after being turned on back and touched with tweezers, it stopped moving and curled appendages towards the body for a (...truncated)


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Aleksandra Bilska, Jacek Francikowski, Aleksandra Wyglenda, Adrian Masłowski, Natalia Kaszyca, Łukasz Depa. Aphids Playing Possum – Defensive or Mutualistic Response?, Journal of Insect Behavior, 2018, pp. 42-53, Volume 31, Issue 1, DOI: 10.1007/s10905-018-9662-4