Within-group behavioral variation promotes biased task performance and the emergence of a defensive caste in a social spider

The social spider Anelosimus studiosus exhibits a behavioral polymorphism where colony members express either a passive, tolerant behavioral tendency (social) or an aggressive, intolerant behavioral tendency (asocial). Here we test whether asocial individuals act as colony defenders by deflecting the suite of foreign (i.e., heterospecific) spider species that commonly exploit multi-female colonies. We (1) determined whether the phenotypic composition of colonies is associated with foreign spider abundance, (2) tested whether heterospecific spider abundance and diversity affect colony survival in the field, and (3) performed staged encounters between groups of A. studiosus and their colony-level predator Agelenopsis emertoni (A. emertoni)to determine whether asocial females exhibit more defensive behavior. We found that larger colonies harbor more foreign spiders, and the number of asocial colony members was negatively associated with foreign spider abundance. Additionally, colony persistence was negatively associated with the abundance and diversity of foreign spiders within colonies. In encounters with a colony-level predator, asocial females were more likely to exhibit escalatory behavior, and this might explain the negative association between the frequency of asocial females and the presence of foreign spider associates. Together, our results indicate that foreign spiders are detrimental to colony survival, and that asocial females play a defensive role in multi-female colonies.     

Behavioral evolution in the major worker subcaste of twig-nesting <Emphasis Type="Italic">Pheidole</Emphasis> (Hymenoptera: Formicidae): does morphological specialization influence task plasticity?

Polymorphism frequently correlates with specialized labor in social insects, but extreme morphologies may compromise behavioral flexibility and thus limit caste evolution. The ant genus Pheidole has dimorphic worker subcastes in which major workers appear limited due to their morphology to performing defensive or trophic functions, thus providing an ideal model to investigate specialization and plasticity. We examined worker morphology, brood-care flexibility, and subcaste ratio in 17 species of tropical twig-nesting Pheidole by quantifying nursing by major workers in natural colonies and in subcolonies lacking minors, in which we also measured brood survival and growth. Across species, majors performed significantly less brood care than minors in intact colonies, but increased rates of brood care 20-fold in subcolonies lacking minors. Brood nursed by majors had lower survival than brood tended by minors, although rates of brood growth did not vary between subcastes. Significant interspecific variation in rates of brood care by major workers did not lead to significant differences in brood growth or survival. Additionally, we did not find a significant association between the degree of major worker morphometric specialization and rates of nursing, growth, or survival of brood among species. Therefore, major workers showed reduced efficacy of brood care, but the degree of morphological specialization among species did not directly compromise task plasticity. The compact nests and all-or-nothing consequences of predation or disturbance on colony fitness may have influenced the evolution of major worker brood-care competency in twig-nesting Pheidole. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users. Dedicated to Professor Edward O. Wilson on the occasion of his 80th birthday.     

Effects of colony size and stage of development on defense response by the swarm-founding wasp<Emphasis Type="Italic"> Polybia occidentalis</Emphasis>

In social insects the level of defensive effort generally increases with colony size, but the effects of the size of the defending adult population and the size of the brood population being defended have not been separated. We used pre-emergence-stage colonies of the swarm-founding wasp, Polybia occidentalis, to distinguish the effects of these two parameters on the intensity of colony defense. We elicited defensive behavior by using both mechanical (taps) and chemical (alarm-pheromone-containing venom) stimuli, and scored the responses as the number of attacks on a standard target. The intensity of defense increased linearly throughout the colony's first 25 days of development, despite the decrease in absolute numbers of adults during the same period. That is, the per capita attack rate increased strongly during this period, leading us to conclude that the intensity of defense is a function of the colony's investment in brood and not of the number of defending adults. We provide evidence that the increase is attributable neither to sensitization due to frequent disturbance, nor to the aging of the adult wasps. We further show that defensive effort on a per capita basis decreased with increasing size across colonies, whether colony size was measured as number of adults or as investment in brood. This pattern suggests that the cost-benefit relationship of defending the colony changes with colony size.Communicated by R.F.A. Moritz     

Nest defense and early production of the major workers in the dimorphic ant Colobopsis nipponicus (Wheeler) (Hymenoptera : Formicidae)

Summary Production of the major subcaste and its contribution to nest survival in the dimorphic ant Colobopsis nipponicus was examined in the field. In this species, the first major workers were reared in the second brood, very early in the colony life cycle. A field experiment demonstrated that artificial colonies without major workers could not survive, whereas colonies with at least one major worker per nest entrance could. Because major workers of C. nipponicus defend the nest entrance by head plugging, the lack of nest defenders in the experimental colonies seemed to be a major cause of nest failure. The defensive value of major workers was much higher than that of minor workers. Many artificial colonies without major workers were displaced by competitors for nest sites, especially by those of other conspecific colonies. In addition, more than 90% of field colonies nested with other conspecific colonies on the same tree. The early production of major workers in C. nipponicus seemed to be very important for the survival of incipient colonies.     

Caste allocation in litter Pheidole: lessons from plant defense theory

The allocation to growth, defense and reproduction varies in social insects within a species' life cycle and between species. A life cycle model (Oster and Wilson 1978) generally failed to predict caste allocation in small litter-nesting colonies of Neotropical Pheidole. Two of its assumptions were often invalid: food was unlikely to be limiting in four of five populations, and sexual biomass production accelerated, not decelerated, with colony size in three of five populations. One of five Pheidole populations studied had higher caste ratios (soldiers /workers) in reproductive colonies as predicted, and in no species did caste functions conform to predictions. We also adapted three models from plant defense theory to study between-species patterns of caste allocation. Among 12 litter Pheidole the amount of sterile biomass devoted to soldiers varied from 18 to 62%. Queen size, growth rate, and soldier investment positively covaried. Only one model, the cost of replacement hypothesis (McKey 1979), correctly predicted that species with costly female alates invest more in defense. The two hypotheses linking apparency to defense may also be valid if fast-growing colonies are more likely to attract the attention of predators.     

Relatedness,recognition errors,and colony fusion in the termite <Emphasis Type="Italic">Nasutitermes corniger</Emphasis>

Loss of aggression between social groups can have far-reaching effects on the structure of societies and populations. We tested whether variation in the genetic structure of colonies of the termite Nasutitermes corniger affects the probability of aggression toward non-nestmates and the ability of unrelated colonies to fuse. We determined the genotypes of workers and soldiers from 120 colonies at seven polymorphic microsatellite loci. Twenty-seven colonies contained offspring of multiple founding queens or kings, yielding an average within-colony relatedness of 0.33. Genotypes in the remaining 93 colonies were consistent with reproduction by a single queen and king or their progeny, with an average within-colony relatedness of 0.51. In standardized assays, the probability of aggression between workers and soldiers from different colonies was an increasing function of within-colony relatedness. The probability of aggression was not affected significantly by the degree of relatedness between colonies, which was near zero in all cases, or by whether the colonies were neighbors. To test whether these assays of aggression predict the potential for colony fusion in the field, we transplanted selected nests to new locations. Workers and soldiers from colonies that were mutually tolerant in laboratory assays joined their nests without fighting, but workers and soldiers that were mutually aggressive in the assays initiated massive battles. These results suggest that the presence of multiple unrelated queens or kings promotes recognition errors, which can lead to the formation of more complex colony structures.     

Chemical basis of nestmate recognition in a defense context in a one-piece nesting termite

Nestmate recognition is a necessary capacity for the occurrence of discrimination between nestmate and non-nestmate individuals. In one-piece nesting termites, which nest and forage in a single piece of wood, nestmate recognition is poorly studied mainly because the probability of encountering exogenous individuals is low in comparison with separate-piece nesting termites. Previous work described that production of soldiers of Neotermes chilensis, a one-piece nesting termite, increased when the risk of invasion of their colony increased, for example when neighboring colonies were present in the same nesting substrate and members of different colonies met when digging galleries. If soldiers are to fulfill their defensive role under these circumstances, they should show nestmate recognition ability; moreover, based on work on other social insects, such nestmate recognition should be based on cuticular compounds (CC). Bioassays were performed in which a soldier of N. chilensis was confronted with a nestmate or non-nestmate primary reproductive, pseudergate or another soldier, and in which a soldier was confronted with untreated and with CC-deprived dead primary reproductives. The results showed that soldiers were indeed more aggressive toward non-nestmates than nestmates for all castes, and that this discrimination was mediated mainly by qualitative (simple matching coefficient) and quantitative (Renkonen index) differences in CC.     

Division of labor during honey bee colony defense

Summary Some worker honey bees respond to major disturbances of the colony by flying around the assailant and possibly stinging; they are a subset of the bees involved in colony defense. These defenders have an open-ended age distribution similar to that of foragers, but defensive behavior is initiated at a younger age than foraging is. Behavioral and genetic evidence shows that defenders and foragers are distinct groups of older workers. Behaviorally, defenders have less worn wings than foragers, suggesting less flight activity. Genetically, defenders differ in allozyme frequencies, demonstrating different subfamily composition from foragers in the same colony. They also differ in allozyme frequencies from guards in the same colony, providing further evidence for division of labor associated with colony defense. We use this information to develop a model for honey bee colony defense involving at least two distinct groups of workers and we propose that the non-guard defenders be called soldiers, due to their important role in colony defense.Offprint requests to: M.D. Breed     

Assured fitness returns favor sociality in a mass-provisioning sweat bee,Megalopta genalis (Hymenoptera: Halictidae)

Assured fitness returns models for the evolution of sociality emphasize the selective value of ensuring that offspring receive adequate parental care to reach maturity. If a member of a social group dies, it can accrue returns on investment in offspring through the efforts of surviving social partners. We provide evidence that in the mass-provisioning, facultatively social sweat bee Megalopta genalis, adult presence in the nest throughout brood development provides protection from ant predation. Nests with adults present were well protected, and brood in nests with adults removed suffered higher predation. Females in observation nests showed effective defensive behavior against experimentally introduced ants, and bees in natural nests repulsed naturally occurring ant raids. Megalopta nest architecture and behavior are such that the brood of several cooperating females can be defended with little additional cost relative to solitary nesting. The benefits of cooperative defense may favor group living in mass provisioning bees. Our observations and experiments suggest that parental care throughout brood development can be adaptive in mass provisioning species, supporting the predictions of assured fitness returns models.     

Trading-off risks from predators and from aggressive hosts

Some birds exploit the aggressiveness of others that are more capable of defending their nests against predators. Usually this behaviour is selected for through improved breeding success for the timid (associate) species. The risk of predation from the more aggressive (host) species is generally rare but may select against the behaviour. The breeding success of red-breasted geese (Branta ruficollis) nesting in association with peregrine falcons (Falco peregrinus) in arctic Siberia was investigated from 1995 to 1999. Nest-predation risk for geese within colonies was positively correlated with distance from the falcons' eyries and negatively correlated with colony size. Though predation risk from the hosts was low, the risk of being attacked by the falcons was high, which we suggest explains why the likelihood of geese deserting their nests was negatively correlated with distance from the eyries. The optimal distance geese nested from eyries was 46 m, though only 37% of pairs managed to nest within 20 m of this. In years with low predation pressure, some geese within colonies nested farther from the falcons. This may be the first evidence to suggest a trade-off between costs and benefits in a nesting association, both of which are directly mediated by the host's nest defence behaviour.     

Experimental evidence for effective and altruistic colony defence against natural predators by soldiers of the gall-forming aphid Pemphigus spyrothecae (Hemiptera : Pemphigidae)

Summary The thick-legged first instar soldiers of the gall-forming aphid Pemphigus spyrothecae Pass. are able to protect the aphids in the gall from being eaten by a range of insect predators. In artificial galls, the soldier aphids were able to kill first instar ladybirds Adalia bipunctata (L.) (Coleoptera: Coccinellidae), early third instar hoverfly larvae Eupeodes (Metasyrphus) corollae (Fab.) (Diptera: Syrphidae), and first-third instar Anthocoris nemoralis (Fab.) (Hemiptera: Cimicidae). Almost all the aphids that attacked the predators were themselves killed. The soldiers were also able to kill predators introduced into natural galls. Experiments were devised in which individuals of Anthocoris minki, which is the most important insect predator of the gall generations of Pemphigus at the study site, were free to enter and leave the gall: the soldiers were effective both in preventing the predator's access to the gall and in killing those predators that did manage to get in. In galls with experimentally manipulated numbers of soldiers and non-soldiers, it was clearly shown that it is the soldiers alone that kill the predators (Anthocoris minki and 1st instar Adalia bipunctata) (see Table 3). Even though many soldiers may die during these encounters, the selective advantage of killing the predators is high, since observations show that individual A. minki can pass through more than one instar inside a gall and kill all the aphids therein. The aphids were not observed to attack conspecific aphids from other galls or the cohabiting aphid Chaitophorus leucomelas Koch. The primary role of the soldier caste is therefore the defence of the aphid colony against predators.     

The role of per-capita productivity in the evolution of small colony sizes in ants

The evolution of colony size in social insects is influenced by both extrinsic and colony-intrinsic factors. An important intrinsic trait, per-capita productivity, often declines in larger colonies. This pattern, known as Michener’s paradox, can limit the growth of insect societies. In this study, we first describe this problem, survey its occurrence across different ant species, and present a case study of eight cavity-dwelling ants with very small colony sizes. In these species, colonies might never reach sizes at which per-capita productivity decreases. However, in six out of the eight focal species, per-capita productivity did decline with increasing size, in accordance with other studies on per-capita productivity in ants. Several mechanisms, such as resource availability or nest-site limitation, may explain the decrease in per-capita productivity with increases in colony size in our focal species. In these central-place foragers, the individual foraging mode is expected to lead to an increase in travel time as colonies grow. We suggest that polydomy, the concomitant occupation of several nest sites, could serve as a potential strategy to overcome this limitation. Indeed, for one species, we show that polydomy can help to circumvent the reduction in productivity with increasing colony size, suggesting that limited resource availability causes the observed decrease in per-capita productivity. Finally, we discuss the influence of other factors, such as the nesting ecology and colony homeostasis, on the evolution of colony size in these cavity-dwelling ants.     

How identity of the homopteran trophobiont affects sex allocation in a symbiotic plant-ant: the proximate role of food

We provide evidence for the proximate role of food in sex allocation by an ant species, and demonstrate how identity of the homopteran partner affects benefits to colonies of a plant-symbiotic ant. The system studied includes a plant-ant that nests in swollen hollowed internodes of a myrmecophyte, and two species of homopteran trophobionts (a coccid and a pseudococcid) tended inside domatia by these ants, for which they are an essential source of food. Total investment in pupae was greater for ant colonies that tended solely or primarily coccids than for those that tended pseudococcids. In particular, biomass invested in sexuals increased more rapidly with size of the colony in trees where ants tended coccids. This greater investment in sexuals was not made at the expense of investment in workers, but reflected increased resources available to coccid-tending colonies. Higher reproductive output indicates that ant fitness may be greater when they tend coccids. These additional resources led to a greater increase in production of alate females than in that of males. Consequently, the sex investment ratio of coccid-tending colonies was more female biased than in those that tended pseudococcids. Differences in resource supply affected numbers of individuals produced but not per-individual investment, with one partial exception: in very small colonies, pseudococcid-tending colonies produced small workers while coccid-tending colonies did not, further underlining the higher resource supply to coccid-tending colonies. This study provides evidence for the proximate role played by food in sex allocation at the colony level. We discuss our results in the context of hypotheses aimed at explaining sex ratio at the colony and population levels.     

A genetic component to size in queens of the ant,<Emphasis Type="Italic"> Formica truncorum</Emphasis>

The genetic basis of morphological traits in social insects remains largely unexplored. This is even true for individual body size, a key life-history trait. In the social insects, the size of reproductive individuals affects dispersal decisions, so that small size in queens is often associated with reduced dispersal, and large size with long-range dispersal and independent colony founding. Worker size is connected to division of labour when workers specialize in certain tasks according to their size. In many species, variation in worker size has been shown to increase colony performance. In this study, we present the first evidence of an additive genetic component to queen size in ants, using maternal half sib analysis. We also compared intra-colony size variation in colonies with high (queen doubly mated) versus low (queen singly mated) genetic variability. We found a high and significant heritability (h²=0.51) for queen size in one of the two study years, but not in the other. Size variation among queens was greater in colonies headed by a doubly mated queen in one of the study years, but not in the other. This indicates that genetic factors can influence queen size, but that environmental factors may override these under some circumstances. The heritability for worker size was low (h²=0.09) and non-significant. Increased genetic diversity did not increase worker size variation in the colonies. Worker size appeared largely environmentally determined, potentially allowing colonies to adjust worker size ratios to current conditions.Communicated by J. Heinze     

Multiple reproductive strategies in a tropical hover wasp

Reproductive skew theory has been an important component of efforts to design a unifying theory of social evolution, as it aims to explain patterns of reproductive partitioning in animal societies as a function of relatedness, group productivity, fighting ability and ecological constraints on independent reproduction. However, empirical tests of the theory have often provided ambiguous or non-conclusive results, assumptions behind alternative models have rarely been tested, and theoretical elaborations have shown the limitations of the reproductive skew approach. Here we analyse a relatively large sample of colonies of the Stenogastrine wasp Parischnogaster mellyi with a powerful set of DNA microsatellite markers. We show that various apparently stable forms of social organisation co-exist in a single population, and that sharing of reproduction between related and unrelated egg-laying females occurs in some of the nests. Present reproductive skew theory appears to be at best partly sufficient to account for the observed complexity of social organisation. The observed patterns of colony composition and reproductive sharing are weakly consistent with the hypothesis of reproductive transactions, while they can more parsimoniously be explained by the life-history characteristics of the species.Communicated by R.F.A. Moritz     

Genetic influence on caste in the ant Camponotus consobrinus

Genetic influences on polyethism within social insect colonies are well known, suggesting that the determination of caste (soldiers and minor workers) may also be genetically mediated. The Australian sugar ant Camponotus consobrinus is suitable for such a study, having soldiers and minor workers that follow a complex allometry. Further, although most C. consobrinus colonies are monogynous, 13 of 42 surveyed using microsatellites were found to be polygynous. Thus, although a minority of colonies were polygynous, the great majority of queens live in polygynous colonies. From the 29 monogynous colonies studied, we inferred that the queens are monandrous. Ants from four polygynous colonies were assigned to families on the basis of microsatellite genotypes, after measurements had been taken of head width and scape length. These measurements reflect a complex allometry interpretable as soldier and minor worker growth curves with a large changeover zone. Genetic influence on caste determination was examined by testing for differences between families within colonies in the distribution of scape lengths, residuals from the overall colony allometric curve, and proportions of soldiers and minor workers (as determined by head width falling above or below the inflection point of the overall colony allometric curve). Families in all four colonies differed significantly in caste proportions and in head-width distributions, and three of the four colonies showed significant differences between families in residuals from the overall colony growth curve. Nested ANOVAs using head widths and scape-length residuals showed that when the effect of family is removed, intercolony differences in allometry are negligible. This evidence indicates genetic rather than environmental causes for the observed differences between families. We speculate that this variation may reflect some selective advantage to within-colony heterogeneity between families or that selective differences are few between a wide array of family growth patterns. Received: 16 June 1999 / Received after revision: 13 September 1999 / Accepted: 25 September 1999     

Frequent colony fusions provide opportunities for helpers to become reproductives in the termite Zootermopsis nevadensis

In many termite taxa, colonies occupying the same nesting resource can meet, interact, and merge with unrelated conspecific neighbors. Because proto-termite ancestors likely also co-inhabited resources and experienced interactions with neighboring conspecific families, extant species that form fused colony units may offer fundamental clues to explaining the origins of eusociality in Isoptera, particularly if both original families retain the potential for reproduction. We allowed entire colonies of Zootermopsis nevadensis (Archotermopsidae) to interact, merge, and develop in the lab, then used genetic markers to determine the family of origin of reproductives, soldiers, and helpers. Persisting and new members of all castes arose from both original colonies and in some cases were hybrids of the two original lineages. We also measured the frequency of mixed-family colonies in natural settings. Ten out of 30 field sampled colonies contained mixed families, demonstrating that interactions and fusions are common in nature. We discuss the implications of our findings as a model system for understanding the evolution of eusociality in termites, highlighting the importance of ecological circumstances impacting direct, indirect, and colony-level fitness.     

Kleptoparasites: a twofold cost of group living for the colonial spider, Metepeira incrassata (Araneae, Araneidae)

Several species of kleptoparasitic and araneophagic spiders (Araneae: Family Theridiidae, Subfamily Argyrodinae) are found in colonial webs of the orb-weaving spider Metepeira incrassata (Araneae, Araneidae) from Mexico, where they steal food and/or prey upon their spider hosts. Census data from natural M. incrassata colonies reveal that the incidence of these species increases with colony size. This pattern may reflect the presence of several other orb-weaving spiders, each with their own kleptoparasitic species, invading larger M. incrassata colonies. As the number of these associated spiders increases, so does the density and number of Argyrodinae species in M. incrassata colonies, suggesting that associated spiders might reduce their own kleptoparasite load by building their webs within M. incrassata colonies. This represents a twofold cost to M. incrassata, as a field enclosure experiment revealed that a primarily kleptoparasitic species (Argyrodes elevatus) may reduce prey available to their hosts, but a kleptoparasitic/araneophagic species (Neospintharus concisus) inflicts high mortality upon M. incrassata. However, the cost of kleptoparasitism and predation by these species may be offset in part for M. incrassata individuals in large colonies by certain defensive mechanisms inherent in groups, i.e., “attack-abatement” and “selfish herd” effects. We conclude that increased occurrence of kleptoparasitic and/or predatory Argyrodinae spiders is a consequence of colonial web building and is an important potential cost of group living for colonial web-building spiders.     

Living close, doing differently: small-scale asynchrony in demography of two species of seabirds

Studies on spatiotemporal pattern of population abundance predict that close populations should exhibit a high level of synchrony, reflected in a parallel time variation of at least one demographic parameter. We tested this prediction for two threatened species of Procellariiformes sharing similar life history traits: the European Storm Petrel (Hydrobates pelagicus) and the Balearic Shearwater (Puffinus mauretanicus). Within each species, we compared adult survival, proportion of transients (breeders that do not settle), and average productivity at two neighboring colonies. Physical and environmental features (e.g., food availability) of the breeding sites were similar. However, while Balearic Shearwater colonies were free of predators, aerial predators occurred especially in one colony of the European Storm Petrel. Despite this difference, we found similar results for the two species. A high proportion of transient birds was detected in only one colony of each species, ranging between 0.00-0.38 and 0.10-0.63 for the petrels and shearwaters, respectively. This seems to be an emergent feature of spatially structured populations of seabirds, unrelated to colony size or predator pressure, that can have important demographic consequences for local population dynamics and their synchrony. Local survival of resident birds was different at each colony, an unexpected result, especially for predator-free colonies of Balearic Shearwater. Productivity varied between the two colonies of European Storm Petrels, but not between the two colonies of Balearic Shearwaters. We demonstrated that within each species, several demographic parameters were colony specific and sufficiently different to generate short-term asynchronous dynamics. Our findings suggest that, in spatially structured populations, local factors, such as predation or small-scale habitat features, or population factors, such as individual quality or age structure, can generate unexpected asynchrony between neighboring populations.     

Costs, benefits, and plasticity of construction of nest defensive structures in paper wasps

Various animals build nests with defensive structures to deter predation on offspring. Construction of nest defensive structures can reduce the probability of predation but will involve various costs. Here, we examined both the costs and benefits of the construction of a nest defensive structure in a paper wasp, Polistes chinensis antennalis, and clarify whether the paper wasp changes the level of defensive structures of nests depending on predation risk. A foundress (queen) of the paper wasp starts a colony in spring and maintains her nest alone until the emergence of workers. At this stage, pupae in the nests are sometimes preyed on by conspecifics of other nests. The intruder needs to break the cocoon, which seals the entrance of the cell, to extract the pupa from the cell. Foundresses often apply nest material (pulp) to the surface of cocoons in their nests. We found that pulp on a cocoon increased the time an intruder required to break the cocoon. This result shows that the pulp structure on cocoons helps to prevent predation on pupae. On the other hand, pulp on cocoons involved costs, including time required to collect pulp and being a potential obstacle to the emergence of workers from the cocoon. Additionally, we found that the amount of pulp on cocoons was greater in nests under higher predation risk than nests under lower predation risk. These results suggest that pulp on cocoons is a nest defensive structure, and foundresses adjusted the construction of the defensive structure depending on predation risk.