Behavioral phase change in the Australian plague locust, Chortoicetes terminifera, is triggered by tactile stimulation of the antennae

School of Biological Sciences, The University of Sydney, Sydney, New South Wales 2006, Australia.
Journal of insect physiology (Impact Factor: 2.47). 05/2010; 56(8):937-42. DOI: 10.1016/j.jinsphys.2010.04.023
Source: PubMed


Density-dependent phase polyphenism is a defining characteristic of the paraphyletic group of acridid grasshoppers known as locusts. The cues and mechanisms associated with crowding that induce behavioural gregarization are best understood in the desert locust, Schistocerca gregaria, and involve a combination of sensory inputs from the head (visual and olfactory) and mechanostimulation of the hind legs, acting via a transient increase in serotonin in the thoracic ganglia. Since behavioural gregarization has apparently arisen independently multiple times within the Acrididae, the important question arises as to whether the same mechanisms have been recruited each time. Here we explored the roles of visual, olfactory and tactile stimulation in the induction of behavioural gregarization in the Australian plague locust, Chortoicetes terminifera. We show that the primary gregarizing input is tactile stimulation of the antennae, with no evidence for an effect of visual and olfactory stimulation or tactile stimulation of the hind legs. Our results show that convergent behavioural responses to crowding have evolved employing different sites of sensory input in the Australian plague locust and the desert locust.

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    • "Some aphids, for example, show density-dependent change from asexual to sexual reproduction depending on population size (Srinivasa and Brisson, 2012). Several species of grasshoppers , the swarm forming locusts, show some of the most striking examples of phenotypic plasticity (Pener and Yerushalmi, 1998; Cullen et al., 2010). The economically important pest species the desert locust, Schistocerca gregaria, expresses an extreme form of density-dependent polyphenism, or phase change (Opstad et al., 2004; Pener and Simpson, 2009). "
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    ABSTRACT: Phenotypic plasticity allows animals to modify their behavior, physiology, and morphology to adapt to environmental change. The global pest, the desert locust, shows two extreme phenotypes; a solitarious phase that is relatively harmless and a gregarious phase that forms swarms and causes extensive agricultural and economic damage. In the field, environmental conditions can drive isolated animals into crowded populations and previous studies have identified the biogenic amine serotonin as a key determinant of this transition. Here we take an integrated approach to investigate the neurochemical, physiological, and behavioral correlates defined by a laboratory based paradigm that mimics facets of swarm break down as gregarious locusts become isolated. Following isolation there was an increased propensity of locusts to avoid conspecifics, and show a reduced locomotion. Changes in choice behavior occurred within 1 h of isolation although isolation-related changes progressed with increased isolation time. Isolation was accompanied by changes in the levels of the biogenic amines dopamine, octopamine, and serotonin within the CNS within 1 h. Dopamine levels were higher in isolated animals and we focused on the role played by this transmitter in synaptic changes that may underpin solitarization. Dopamine reduced synaptic efficacy at a key central synapse between campaniform sensilla (CS) and a fast extensor tibiae motor neuron that is involved in limb movement. We also show that dopamine injection into the haemocoel was sufficient to induce solitarious-like behavior in otherwise gregarious locusts. Further, injection of a dopamine antagonist, fluphenazine, into isolated locusts induced gregarious-like behavior. This highlights that dopaminergic modulation plays an important role in the plasticity underpinning phase transition and sets a context to deepen the understanding of the complementary role that distinct neuromodulators play in polyphenism in locusts.
    Full-text · Article · Nov 2014
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    • "Since this behavioural transformation encompasses several discrete behavioural changes, binary logistic regression analysis has been used for many years as a means to characterise the solitarious and gregarious behavioural states in several species of locust (Roessingh et al., 1993, Roessingh and Simpson 1994, Roessingh et al., 1998; Bouaichi et al., 1995, 1996; Islam et al., 1994; Simpson et al., 1999, 2001; Hagele and Simpson, 2000; Rogers et al., 2003; Sword, 2003; Lester et al., 2005; Anstey et al., 2009; Gray et al., 2009; Cullen et al., 2010, 2012; Ma et al., 2011; Ott et al., 2012). Logistic regression is a useful method of classifying locust behaviour as it encapsulates several distinct activities and condenses them into a single metric of phase state. "
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    ABSTRACT: Desert locusts can change reversibly between solitarious and gregarious phases, which differ considerably in behaviour, morphology and physiology. The two phases show many behavioural differences including both overall levels of activity and the degree to which they are attracted or repulsed by conspecifics. Solitarious locusts perform infrequent bouts of locomotion characterised by a slow walking pace, groom infrequently and actively avoid other locusts. Gregarious locusts are highly active with a rapid walking pace, groom frequently and are attracted to conspecifics forming cohesive migratory bands as nymphs and/or flying swarms as adults. The sole factor driving the onset of gregarization is the presence of conspecifics. In several previous studies concerned with the mechanism underlying this transformation we have used an aggregate measure of behavioural phase state, Pgreg, derived from logistic regression analysis, which combines and weights several behavioural variables to characterise solitarious and gregarious behaviour. Using this approach we have analysed the time course of behavioural change, the stimuli that induce gregarization and the key role of serotonin in mediating the transformation. Following a recent critique that suggested that using Pgreg may confound changes in general activity with genuine gregarization we have performed a meta-analysis examining the time course of change in the individual behaviours that we use to generate Pgreg. We show that the forced crowding of solitarious locusts, tactile stimulation of the hind femora, and the short-term application of serotonin each induce concerted changes in not only locomotion-related variables but also grooming frequency and attraction to other locusts towards those characteristic of long-term gregarious locusts. This extensive meta-analysis supports and extends our previous conclusions that solitarious locusts undergo a rapid behavioural gregarization upon receiving appropriate stimulation for a few hours that is mediated by serotonin, at the end of which their behaviour is largely indistinguishable from locusts that have been in the gregarious phase their entire lives.
    Full-text · Article · Apr 2014 · Journal of insect physiology
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    • "Furthermore, in the fruit fly Drosophila, evidence suggests that olfactory signalling alone could mediate the reduction of aggression in socially grouped males [53,54]. Similarly in locusts, a few short hours of olfactory and visual, or alone mechanosensory contact via the legs in Schistocerca gregaria [55], or antennae in Chortoicetesterminifera [56], is sufficient and necessary to change the social behaviour of solitarious individuals to that characteristic of the gregarious, swarm phase [4,57]. As in Drosophila [53,54,58] the pheromone signature perceived by the antennae in crickets is essential for species and sex recognition, and for inducing courtship and aggressive behaviours [50,59,60]), but not it seems for the subduing effect of grouping on aggression. "
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    ABSTRACT: Population density has profound influences on the physiology and behaviour of many animal species. Social isolation is generally reported to lead to increased aggressiveness, while grouping lowers it. We evaluated the effects of varying degrees of isolation and grouping on aggression in a territorial insect, the Mediterranean field cricket, Gryllusbimaculatus. Substantiating early observations, we show that dyadic contests between weight-matched, adult male crickets taken from groups rarely escalate beyond threat displays, whereas interactions between pairs of previously isolated crickets typically escalate to physical fights lasting several seconds. No significant differences were found between 1, 2 and 6-day isolates, or between individuals grouped for a few hours or lifelong. Unexpectedly, crickets grouped in immediate proximity within individual mesh cages that precluded fighting while permitting visual, olfactory and mechanical, antennal contact, were as aggressive as free isolates. This suggests that reduced aggression of grouped animals may be an acquired result of fighting. Supporting this notion, isolated crickets initially engage in vigorous fights when first grouped, but fighting intensity and duration rapidly decline to the level of life-long grouped crickets within only 10 min. Furthermore, grouped crickets become as aggressive as life-long isolates after only 3 hours of isolation, and on the same time course required for crickets to regain their aggressiveness after social defeat. We conclude that the reduced aggressiveness of grouped crickets is a manifestation of the loser effect resulting from social subjugation, while isolation allows recovery to a state of heightened aggressiveness, which in crickets can be considered as the default condition. Given the widespread occurrence of the loser effect in the Animal Kingdom, many effects generally attributed to social isolation are likely to be a consequence of recovery from social subjugation.
    Full-text · Article · Sep 2013 · PLoS ONE
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