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Vespula wasps show consistent differences in colony-level aggression over time and across contexts

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Abstract

Social wasps are well-known for aggressively defending their nests when these are approached, threatened, or directly attacked. However, the variability, consistency, and the determinants of such defensive and aggressive responses of wasp colonies are largely unknown. Here, we quantify the aggressiveness of Vespula vulgaris and V. germanica wasp colonies to determine if colonies exhibit consistent differences in aggression across different spans of time and disturbance contexts, and if colony-level aggression is linked to intrinsic and/or extrinsic parameters that seem to predict the aggressive response of other social insects. We conducted three experiments in locations throughout the South Island of New Zealand, where we quantified foraging activity, as well as unprovoked, and provoked (post-disturbance) colony aggression across short (one day), moderate (one week), and long (one month) spans of time. We also estimated the colony investment into nest size and pupae, as well as the temperature near the nest entrance, to determine if these intrinsic and extrinsic parameters could predict colony-level defensive response to a simulated predator attack. We found that, across all three durations of time, some wasp colonies are consistently aggressive, while other colonies exhibit little to no aggressive response to disturbance. We show that colony aggression levels are consistent across contexts over moderate and long spans of time, and that the intensity of colony response is consistent under different types of nest disturbance. The aggressive response of wasp colonies could not be predicted by activity level, temperature, or investment into nest or pupae. The existence of consistent differences in wasp colony aggression suggests that both aggressive and non-aggressive behavioral types can have fitness benefits in a population. Aggressive colonies might defend their nests more effectively, deterring potential predators better than docile colonies. On the other end, less aggressive colonies could go unnoticed by humans and develop undisturbed. Our study further suggests that different mechanisms could underlie the evolution of a wide spectrum of aggressive colony phenotypes in the eusocial Hymenoptera.

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... The intensity and duration of collective defense by some species suggests a strong selection pressure exerted by nest predators, though we have yet to understand the links between predation frequency and type and the interspecific variation in defensive behaviors exhibited by social wasps. Colonies within a species can also vary greatly in the magnitude of the collective defensive response, which can be, but is not always, associated with colony size and developmental stage (Brito et al., 2018;Jandt et al., 2020;London and Jeanne, 2003). ...
... obs.), or mount a relatively weak defense (Vespula consobrina; Akre et al., 1982;Gaul, 1952). However, their close relatives produce impressive defensive responses (e.g., Vespula germanica; Jandt et al., 2020;Synoeca;de Castro e Silva et al., 2016). The Vespa colonies, with their large workers, strong venom, and terrifying aggressiveness may be the ultimate evolutionary response to attacks on vespine colonies. ...
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Social insects are well known for their aggressive (stinging) responses to a nest disturbance. Still, colonies are attacked due to the high-protein brood cached in their nests. Social wasps have evolved a variety of defense mechanisms to exclude predators, including nest construction and coordinated stinging response. Which predatory pressures have shaped the defensive strategies displayed by social wasps to protect their colonies? We reviewed the literature and explored social media to compare direct and indirect (claims and inferences) evidence of predators attacking individuals and colonies of wasps. Individual foraging wasps are predominantly preyed upon by birds and other arthropods, whereas predators on wasp brood vary across subfamilies of Vespidae. Polistinae wasps are predominantly preyed upon by ants and Passeriformes birds, whereas Vespinae are predominantly preyed upon by badgers, bears, and hawks. Ants and hornets are the primary predators of Stenogastrinae colonies. The probability of predation by these five main Orders of predators varies across continents. However, biogeographical variation in prey–predator trends was best predicted by climate (temperate vs. tropical). In social wasps’ evolutionary history, when colonies were small, predation pressure likely came from small mammals, lizards, or birds. As colonies evolved larger size and larger rewards for predators, the increased predation pressure likely selected for more effective defensive responses. Today, primary predators of large wasp colonies seem to be highly adapted to resist or avoid aggressive nest defense, such as large birds and mammals (which were not yet present when eusociality evolved in wasps), and ants.
... Moreover, aggressiveness may be different between the populations in their native environment versus in the invaded areas. Aggressiveness has been found to vary between individuals of V. vulgaris (Santoro et al. 2015) and among V. germanica and V. vulgaris colonies in New Zealand (Jandt et al. 2020). Jandt et al. (2020) observed a consistent difference wasp colony aggression and suggested that both aggressive and nonaggressive behavioral types can have fitness benefits in a population. ...
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Behavior is a complex phenotype that is plastic and evolutionarily labile. The advent of genomics has revolutionized the field of behavioral genetics by providing tools to quantify the dynamic nature of brain gene expression in relation to behavioral output. The honey bee Apis mellifera provides an excellent platform for investigating the relationship between brain gene expression and behavior given both the remarkable behavioral repertoire expressed by members of its intricate society and the degree to which behavior is influenced by heredity and the social environment. Here, we review a linked series of studies that assayed changes in honey bee brain transcriptomes associated with natural and experimentally induced changes in behavioral state. These experiments demonstrate that brain gene expression is closely linked with behavior, that changes in brain gene expression mediate changes in behavior, and that the association between specific genes and behavior exists over multiple timescales, from physiological to evolutionary. Expected final online publication date for the Annual Review of Genetics Volume 46 is November 02, 2012. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.
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Understanding the ecological relevance of variation within and between colonies has been an important and recurring theme in social insect research. Recent research addresses the genomic and physiological factors and fitness effects associated with behavioral variation, within and among colonies, in regulation of activity, cognitive abilities, and aggression. Behavioral variation among colonies has consequences for survival and reproductive success that are the basis for evolutionary change.
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Using a laboratory test, newly emerged worker honeybees (Apis mellifera) were evaluated for their response to four alarm pheromones (isobutyl acetate, isopentyl acetate, 2 heptanone, 1 pentanol), under five temperature/humidity regimens (30°C, 30 6°C, 26°7°C, at 45% RH; 35°C at 30% and 85% RH). With a higher temperature, there was increased probability of a response, and the speed, intensity and duration of that response were also greater. Relative humidity seemed to affect only the intensity, higher humidities increasing it. Occurrence of Nasonov fanning as a part of the response by some bees depended largely on the pheromone being tested; the effects of temperature and humidity were less clear-cut.
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Social insect colonies and the workers comprising them, each exhibit consistent individual differences in behavior, also known as 'personalities'. Because the behavior of social insect colonies emerges from the actions of their workers, individual variation among workers' personality may be important in determining the variation we observe among colonies. The reproductive unit of social insects, on which natural selection acts, is the colony, not individual workers. Therefore, it is important to understand what mechanisms govern the observed variation among colonies. Here I propose three hypotheses that address how consistent individual differences in the behavior of workers may lead to consistent individual differences in the behavior of colonies: 1. Colonies differ consistently in their average of worker personality; 2. The distribution but not the average of worker personalities varies consistently among colonies; and 3. Colony personality does not emerge from its worker personality composition but from consistent external constraints. I review evidence supporting each of these hypotheses and suggest methods to further investigate them. The study of how colony personality emerges from the personalities of the workers comprising them may shed light on the mechanisms underlying consistent individual differences in the behavior of other animals [Current Zoology 58 (4): , 2012].
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Social insect societies are characterized not only by a reproductive division of labor between the queen and workers but also by a specialization of workers on different tasks. However, how this variation in behavior or morphology among workers influences colony fitness is largely unknown. We investigated in the ant Temnothorax longispinosus whether aggressive and exploratory behavior and/or variation among nest mates in these behavioral traits are associated with an important fitness measure, that is, per worker offspring production. In addition, we studied how body size and variation in size among workers affect this colony fitness correlate. First, we found strong differences in worker body size, aggression, and exploration behavior among colonies. Most notably, intracolonial variance in aggression was positively correlated with per worker productivity, suggesting a selective advantage of colonies with a higher variability in worker aggression. Because ant colonies in dense patches were both more aggressive and more productive, we cannot exclude the possibility that higher productivity and greater variability in aggression could both be results of good habitat quality and not causal influences on one another. This study suggests that social insect societies with stronger behavioral variation among nest members, and possibly a more efficient task allocation, are more productive in the field.
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-1 , averaged over the year = 1097 g ha -1 ) is as great as, or greater than combined biomasses of birds (best estimate = 206 g ha -1 ), rodents (up to 914 g ha -1 in some years, but usually much lower) and stoats (up to 30 g ha -1 ). Relative V. vulgaris biomass is also estimated to be two orders of magnitude greater than native wasp biomass during the peak V. vulgaris season in one beech forest. Mean density of Vespula workers at the peak of the season was estimated to be 10,000 workers ha -1 , a greater density than the densities attained by other large wasp species when they have been used (with some success) at 'enhanced densities' as biological control agents overseas. The biological impacts of Vespula, and particularly V. vulgaris, in honeydew beech forest are likely to be great, but most of these impacts have not been documented.
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The author reviews work done on the social organization of the harvester ant Pogonomyrmex barbatus in the grasslands of SE Arizona. Early ideas on the collective behaviour of social insects revolved around the idea of a rigid caste system. More recently the idea of a distributed process has gained ground, ie an individual can perform many tasks. The experiments described were designed to discover if different tasks were interdependent. Results suggest that interaction rates play an important role in the behaviour of an ant colony. However, interaction rate is only one of many possible cues, and a direct link between interaction rate and task allocation has yet to be proven. -S.R.Harris
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Measurements of carbohydrate foraging behavior of Vespula germanica yellowjackets show that the distribution of the number of foragers over the number of trips is highly skewed with a few foragers making a disproportionate number of trips. We tested several empirical models based on different biological assumptions to see which model best described the distribution. For all periods of observation, the data are well fitted by a straight line on a log-log plot. This fit indicates that the distribution of labor is non-increasing monotonic; i.e. continually decreasing, and follows a power law. Stochasticity and self-organization are two possible explanations for the power law distribution. As an alternative approach, cluster analysis of various foraging characteristics of individual foragers clearly separated foragers into two groups and is consistent with a bimodal model for the division of foraging labor. Based on these cluster results, we operationally defined workers as either 'elite' or 'non-elite'. We found that elite foragers are not more likely than non-elites to be task specialists. The data show that workers develop into elites but do not support the hypothesis of self-reinforcement as the mechanism.
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During 1979, cocoons of the ichneumonid Sphecophaga vesparum hurra (Cresson), a parasitoid of some Vespinae, were imported from Washington State, USA to New Zealand. Two adults and four cocoons raised in quarantine on Vespula germanica (F.), the German wasp, were field released, but there was no evidence of establishment. Subsequent imports of S. vesparum vesparum (Curtis) from Europe were propagated mainly on the recently immigrant V. vulgaris (L.), the Common wasp. Thirteen generations of S. v. vesparum were raised by July 1985, and all stages of the parasitoid were released into wasp nests in Canterbury. Six of seven V. vulgaris nests and three of six V. germanica nests were parasitised. Although releases occurred late in the growth cycle of nests, at least one generation of parasitoids emerged in four V vulgaris nests and one V. germanica nest. One of the V. vulgaris nests probably developed two generations of parasitoids. Parasitoid numbers in this nest increased approximately eight-fold.
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In search for factors which could drive the spectacular spring migrations of pre-reproductive queens of bumblebees and social wasps, we made a literature search of potential mortality factors of individuals and colonies. Although the role of parasitism cannot be ruled out, we highlight the potential of vole cyclicity in explaining the migrations. Because the spatial scale of vole-cycle asynchrony is located at the same level (γ scale) as the range of migratory movements, spring flights could rid bumblebees and wasps of strong nest-site competition among colony-founding queens, and of severe predation by voles in high vole-density regions, to take advantage of abundant, empty vole burrows as nest sites in low-predation, relatively vole-free areas. As a corollary of the migratory movements, relaxed parasite pressure is expected.
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Inter- and intraspecific competition was investigated in ants of the myrmicine genus leptothorax in a deciduous woodland near Würzburg, Germany. The most common species, A. (Myrafant) nylanderi, lives in rotting pine, oak, and elder sticks and may locally reach densities of 10 nests per m2. In the studied sites, only a small fraction of colonies were polydomous, i.e. single colonies typically did not inhabit several nest sites. The home ranges of nylanderi colonies overlap the ranges of other conspecific colonies and colonies of other species, especially L. (s.str.) gredleri. Foragers from different colonies encountering one another in the field back off without exhibiting strong aggression, suggesting that colonies do not defend absolute foraging territories. In laboratory experiments, the frequency and severity of agonistic interactions among workers from different colonies, all living in pine sticks, increased significantly with the distance between their nests. Workers from colonies nesting in different types of wood exhibited significantly more aggression. Experiments in which we transferred colonies from pine sticks into artificial pine or oak nests corroborate the hypothesis that nesting material strongly influences colony odour in L. nylanderi. The evolutionary significance of this apparent dear-enemy phenomenon is discussed.
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Significant variation in aggressiveness and kin discrimination ability occurs between different laboratory colonies of the ant Rhytidoponera confusa.Different colonies show consistently high (or low) levels of aggression toward nonnestmates over 4–19 weeks. Earlier studies excluded colony size and the natural presence or absence of the queen in colonies and differences in hunger as possible sources of variation. The present study excluded the number of larvae in colonies and the time of the light period of the light cycle when recognition tests were carried out. Highly significant variation occurs between the kin discrimination ability of individual workers in any particular colony. Approximately 28% of the workers in colonies of R. confusashowed very poor kin discrimination. Much of the colony's kin discrimination is carried out by a small number of highly aggressive workers.
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The Argentine ant, Linepithema humile, is a widespread invasive species characterized by reduced intraspecific aggression within introduced populations. To illuminate the mechanisms underlying nestmate recognition in Argentine ants, we studied the spatial and temporal fidelity of intraspecific aggression in an introduced population of Argentine ants within which intraspecific aggression does occur. We quantified variation in the presence or absence of intraspecific aggression among nests over time both in the field and under controlled laboratory conditions to gain insight into the role of environmental factors as determinants of nestmate discriminatory ability. In addition, we compared levels of intraspecific aggression between nest pairs to the similarity of their cuticular hydrocarbons to determine the potential role of these compounds as labels for nestmate discrimination. In both field and laboratory comparisons, nest pairs behaved in a consistent manner throughout the course of the experiment: pairs that fought did so for an entire year, and pairs that did not fight remained nonaggressive. Moreover, we found a negative relationship between cuticular hydrocarbon similarity and the degree of aggression between nests, suggesting that these hydrocarbons play a role in nestmate discriminatory ability. In contrast to the prevailing pattern, ants from one site showed a marked change in behaviour during the course of this study. A concomitant change was also seen in the cuticular hydrocarbon profiles of ants from this site. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.
Article
Social insects use a complex of recognition cues when discriminating nestmates from non-nestmate conspecifics. In the Argentine ant, Linepithema humile, recognition cues can be derived from exogenous sources, and L. humile acquires prey-derived hydrocarbons that are used in nestmate discrimination. We studied Argentine ant population-level distinctions in response to external recognition cues. Ants belonging to a California population were strongly affected by the imposition of prey-derived hydrocarbons, with spatially isolated colony fragments that had been fed different cockroach prey (Blattella germanica or Supella longipalpa) showing high and injurious intracolony aggression when reunited. In contrast, colonies of Argentine ants from the southeastern U.S. showed only moderate and noninjurious aggression when subjected to the same treatment. Field-collected colonies of L. humile had hydrocarbons in the range of those provided by S. longipalpa, and colonies from the southeastern U.S. had significantly higher initial levels of Supella-shared hydrocarbons. When fed cockroaches, Argentine ants from both regions acquired additional amounts of Supella- and Blattella-specific hydrocarbons, with a significant increase in levels of Blattella-specific hydrocarbons. Therefore, diet partitioning produced a greater change in the proportion of prey hydrocarbons in the California than in the southeastern U.S. populations, which may be responsible for the altered behaviour observed in the California population. Identifying factors underlying geographical variation in cue expression and/or perception may bring us closer to elucidating the selective forces driving nestmate recognition systems.
Article
Ecology Letters (2012) Interspecific trait variation has long served as a conceptual foundation for our understanding of ecological patterns and dynamics. In particular, ecologists recognise the important role that animal behaviour plays in shaping ecological processes. An emerging area of interest in animal behaviour, the study of behavioural syndromes (animal personalities) considers how limited behavioural plasticity, as well as behavioural correlations affects an individual’s fitness in diverse ecological contexts. In this article we explore how insights from the concept and study of behavioural syndromes provide fresh understanding of major issues in population ecology. We identify several general mechanisms for how population ecology phenomena can be influenced by a species or population’s average behavioural type, by within-species variation in behavioural type, or by behavioural correlations across time or across ecological contexts. We note, in particular, the importance of behavioural type-dependent dispersal in spatial ecology. We then review recent literature and provide new syntheses for how these general mechanisms produce novel insights on five major issues in population ecology: (1) limits to species’ distribution and abundance; (2) species interactions; (3) population dynamics; (4) relative responses to human-induced rapid environmental change; and (5) ecological invasions.