Behavioral Interactions of Two Solitary,Halictine Bees with Comparisons among Solitary,Communal and Eusocial Species

Laboratory behavioral experiments were conducted with two solitary, halictine bee species, in the genus Lasioglossum, to examine the nature of behavioral interactions between non-nestmate females. The experimental design of this study was identical to previous work on both a communal (Kukuk 1992) and a eusocial Lasioglossum species (Breed et al. 1978), thereby providing data for comparison of female-female interactions in species within a single, very large genus that exhibit different sociality. Both solitary species exhibited low levels of aggressive behavior yet nearly all females were reproductively active, as determined by subsequent dissections. Neither ovarian width nor size was associated with aggression in either species. Interspecific comparisons reveal large differences in cooperation and aggression among the four congeneric species. The communal species exhibits significantly more cooperative and less aggressive behavior than all other species suggesting that communal social behavior in Lasioglossum is not phenetically intermediate between the behavior of solitary and eusocial species.     

Socially peaceful: foragers of the eusocial bee Lasioglossum malachurum are not aggressive against non-nestmates in circle-tube arenas

Due to the universally found nestmate recognition in eusocial insects, it is predictable that non-nestmates interact aggressively. In sweat bees (Hymenoptera: Halictidae), this trend was largely shown for queen–queen interactions, but data on worker–worker interactions are still scarce and somehow controversial. We studied behavioural interactions between foragers of the eusocial and ground-nesting bee Lasioglossum malachurum within circle-tubes. Independently of colony membership, bees exhibited high frequencies of cooperative behaviours, together with lack of aggression and moderate avoidance of social interactions. The cooperative mutual passing was the most frequently recorded behaviour. Size difference between the opponents had no effects on cooperation or avoidance. In a heterospecific experiment, bee foragers were observed to react more aggressively and to pass very rarely towards cuckoo bees, suggesting that our results were not biased by the circle-tube methodology. Our results and comparisons with other bee species suggest that studying worker interactions may be not enough to predict the social organisation in bees. Whatever the evolutionary meaning of this generalised tolerance towards conspecifics, the present findings are somehow in agreement with recent studies showing that L. malachurum colonies may have imperfect nestmate recognition and often include a mixture of related and unrelated workers.     

Reproductivity and relatedness in a communal halictine beeLasioglossum (Chilalictus) hemichalceum

Summary The biology of communal species is not well known. Here we report the reproductivity (number of offspring per female) and genetic relatedness forLasioglossum (Chilalictus) hemichalceum, a communal halictine bee. There is a positive Model II regression, with a slope indistinguishable from one, between natural logarithms of the number of offspring and the number of adult females in a colony; indicating that as colony size increases the reproductivity per female does not decrease. This pattern is like that found in one other communal species and unlike that found in a wide variety of eusocial species. Relatedness among adult nestmates, based on two variable loci, is low. For 52 colonies it is about 0.13, and for a subset of 25 reproductively active colonies it was not distinguishable from zero. This indicates that the role of kin selection is minor at best in this highly cooperative, communal species. A review of the relatedness data available for communal groups, both foundress associations and species that are communal throughout their colony cycle, indicates that communal sociality is often but not always associated with low intra colony relatedness.     

Social wasp parasites affect the nestmate recognition abilities of their hosts (<Emphasis Type="Italic">Polistes atrimandibularis</Emphasis> and <Emphasis Type="Italic">P. biglumis</Emphasis>, Hymenoptera,Vespidae)

Summary. Queens of the parasitic social wasp, Polistes atrimandibularis, temporarily mimic the odor of their host species, Polistes biglumis, but their offspring have parasite-specific odors. As a consequence, in parasitized colonies individuals with different odors co-inhabit the colony and host workers, who are responsible for colony defense, accept wasps with different odors. In order to verify whether this particular condition causes a change in recognition abilities of hosts, we tested nestmate/non-nestmate discrimination in field colonies invaded by social parasites (and in non-parasitized colonies as controls). Results show that parasitized colonies distinguish between nestmates and non-nestmates, distinguish their parasite queen from those that usurped alien colonies, and accept their parasite's non-mimetic offspring but make more recognition errors than non-parasitized colonies. The optimal acceptance threshold model predicts that when the frequency of encountering non-kin increases, residents become less permissive towards intruders. However, my data show that parasitized colonies are more permissive towards non-nestmates with respect to non-parasitized colonies but they are also more aggressive towards nestmates, suggesting that host workers' learning abilities are impaired.     

The Problems of a Priori Categorisation of Agonism and Cooperation: Circle‐Tube Interactions in Two Allodapine Bees

Circle‐tube experiments have been widely used to both examine nestmate recognition in social and solitary insects, as well as to characterise interactions in terms of agonism, cooperation, and avoidance. Despite their use in studies of halictid bees, carpenter bees, adrenid bees, and wasps, they have never been used to explore social interactions in the bee tribe Allodapini, where sociality varies widely in terms of complexity. Here, we investigate behaviours displayed within the highly eusocial allodapine Exoneurella tridentata and the facultatively social Exoneura robusta, using a standardised circle‐tube apparatus. We present two broad and important results: (i) Discrimination between nestmates and non‐nestmates is much more strongly expressed in the facultatively social species and (ii) principal components analyses do not indicate suites of behaviours that permit clear interpretations as being agonistic, cooperative, or avoidance. Our first set of results suggests that nestmate recognition is not an essential ability for social species. Our second set of results raise important questions about a priori functional categorisations of behaviours and whether these can be used to reliably classify observed behaviours as either avoidance, cooperation, or aggression. Our analyses highlight the risks of interpreting social insect interactions and call for a more cautious approach.     

Social Interactions and Familiarity in a Communal Halictine Bee Lasioglossum (Chilalictus) hemichalceum

Social organization in Hymenoptera is quite variable, but most group-living species have a reproductive division of labor. Communal species, by definition, do not; all individuals work and all are reproductive. In order to understand the evolution and maintenance of such cooperative societies the essential first step is characterization of the behavioral interactions between individuals. In particular, it is important to investigate the influence of common group membership (familiarity) on these interactions. Circle-tube arenas were used to observe the interactions between 42 pairs of field-collected Lasioglossum (Chilalictus) hemichalceum females either from the same nest, from different nests but the same nest aggregation, or from different aggregations. Identical procedures were applied to 24 pairs of females from laboratory colonies. There was a striking lack of agonistic behavior with Lunging occurring in only 0.03% of all bouts, and C-Postures (threat behavior) in only 19% of bouts using field bees and 27 % of bouts using females held in the laboratory. Passing was virtually ubiquitous, occurring in 98 % of all bouts. None of these behavior patterns is significantly associated with the level of familiarity between females. The lack of agonistic behavior and the indiscriminate cooperative behavior (Passing) suggest that all conspecifics are accepted and are treated similarly. This is in contrast to previous studies of L. (Dialictus) zephyrum that demonstrated both kin recognition and nepotism. While Avoidance behavior was rare, significantly more was seen between bees taken from different nest aggregations. Trophallaxis Solicitation occurred in 13 bouts between field bees. While the proportion of bouts in which this occurred is not associated with familiarity, the number of solicitations per bout is greater between females from different nest aggregations. These minor but statistically significant differences suggest that L. hemichalceum females can discriminate between familiar and unfamiliar individuals. Therefore the proximate mechanism underlying universal acceptance of all conspecifics cannot be a lack of recognition cue expression or recognition cue perception. Rather, it is due to a lack of clearly preferential treatment toward familiar individuals. This suggests that some component of fitness is positively associated with group membership per se, or group size. The high levels of mutual tolerance suggest, as do other lines of evidence (Kukuk & Schwarz 1987), that communal societies are not intermediate between solitary and eusocial species.     

Mating structure and nestmate relatedness in a communal bee, Andrena jacobi (Hymenoptera, Andrenidae), using microsatellites

Complex eusocial insect societies are generally matrifilial, suggesting kin selection has been of importance in their development. For simpler social systems, factors favouring their existence, in particular kin selection, have rarely been studied. Communal nesting is one of these simple social organizations, and is found in a diversity of insect species. To examine whether kin selection may play a role in the evolution and maintenance of communality, we estimated genetic relatedness of nestmate females of the facultatively communal bee, Andrena jacobi . Microsatellite loci were developed for this species and used to analyse individuals from two populations. Loci were variable, they were in heterozygote deficit and showed positive inbreeding coefficients. This may arise from nonrandom mating; previous observations (Paxton & Tengö 1996) indicate that a large proportion of females mate intranidally with nestmate males in their natal nests before first emerging. Nestmate relatedness was low, no different from zero for all loci in one population and for three of four loci in the other population. The large number of nestmates sharing a common nest (up to 594) may explain the low relatedness estimates, although relatedness was also independent of the number of females sharing a nest. Lack of inclusive fitness payoffs could constrain social evolution in this communal species.     

Threat,Signal or Waste? Meaning of Corpses in two Dulotic Ant Species

Ant corpses, besides representing threat of infection by pathogens and parasites, can also be used during interspecific conflicts to inhibit the activity of the attacked colony, or they can be consumed as food. In the view of the former, the signal properties of corpses can be manifold. Besides discriminating nestmates and foes, the corpses of different ant species may act as cues for foragers, signaling the presence of other rival species, and triggering appropriate responses (e.g., alarm, retreat or foraging). In our study, we examined the responses of the facultative slave-maker Formica sanguinea and those of the obligate Polyergus rufescens towards corpses of nestmates, non-nestmate conspecifics, heterospecific slave-makers and their slaves, and corpses of non-enslaved host species under laboratory conditions. Both dulotic species responded differently to corpses of different origin. In F. sanguinea, the most intensive response was elicited by the corpses of P. rufescens and its slave, but also the corpses of non-nestmate conspecifics and their slaves elicited many adverse responses. In P. rufescens, the corpses of non-nestmate conspecifics and their slaves elicited the most adverse response. Both dulotic species distinguished corpses of their slaves from corpses of non-enslaved hosts. Based on our results, ant corpses are not meaningless objects scattered in the field, but cues carrying information that trigger different behavioral responses, and in F. sanguinea they can even represent an important food source.     

Worker size variation and the evolution of an ant-plant mutualism: Comparative morphometrics of workers of two closely related plant-ants, Petalomyrmex phylax and Aphomomyrmex afer (Formicinae)

Summary: We compared intranidal variation in worker size in the two closely related plant-ants Aphomomyrmex afer and Petalomyrmex phylax. Each of these genera is monotypic, and the two appear to be sister species among extant ants. Workers of A. afer are larger on average and exhibit much greater intranidal size variation. Workers of P. phylax are smaller and much less variable in size. Both species show weak allometry for some pairs of characters. Head shape is also different in workers of the two species. We discuss these differences in relation to the ecology of A. afer and P. phylax, and propose a scenario for the evolutionary divergence of worker morphology in these two species. Based on comparisons of these two monotypic genera with related ants, we suggest that reduced intranidal variation in worker size is a derived trait in Petalomyrmex.     

Social Network Analysis of Male Dominance in the Paper Wasp Mischocyttarus mastigophorus (Hymenoptera: Vespidae)

Social aggression is a pervasive feature of insect societies. In eusocial Hymenoptera, aggression among females can affect task performance and competition over direct reproduction (egg laying); in most species males participate in social interactions relatively rarely. Males of the independent-founding paper wasp Mischocyttarus mastigophorus are exceptional: they are aggressive toward female nestmates, leading us to explore the function of this unusual behavior. We applied social network analyses to data on M. mastigophorus social aggression to quantify sex differences in giving and receiving social aggression. The network analyses supported the pattern of biased male aggression toward female nestmates; females are relatively rarely aggressive to males. We then asked whether male aggression toward females was biased by females’ relative ovary development. Males were more aggressive toward females with better-developed ovaries, opposite to patterns of aggression among females. Because food brought to the colonies is often monopolized by dominant females, we suggest that males direct aggression toward socially dominant females with better-developed ovaries to obtain food. The implications of biased male aggression for female task performance and physiology are unknown.

     

Intranidal mating,emergence, and sex ratio in a communal beeAndrena jacobi Perkins 1921 (Hymenoptera: Andrenidae)

The extent of preemergence intranidal mating, schedules of emergence, and sex ratio at emergence were documented forAndrena jacobi, a communal, univoltine bee, by collecting and dissecting adults as they emerged from their fossorial nests in 1994. Over 70% of females had mated intranidally with nestmate males, thus potentially incestuously, before emerging. Preemergence intranidal mating did not vary during a day or between nests within a day, though it was less frequent at the start and end of the period of emergence. It was independent of a female's size.A. jacobi was protandrous, though some males emerged after all females. The sex ratio at emergence was remarkably female biased, possibly a consequence of local mate competition. Intranidal mating may represent a characteristic trait of communal bees where a high density of receptive females are predictably aggregated within a nest.     

Species and Colony Components in the Recognition Odor of Young Social Wasps: Their Expression and Learning (Polistes biglumis and P. atrimandibularis; Hymenoptera: Vespidae)

In Polistes, nestmate recognition relies on the learning of recognition cues from the nest. When wasps recognize nestmates, they match the template learned with the odor of the encountered wasp. The social wasp Polistes biglumis use the homogeneous odor of their colony to recognize nestmates. When these colonies become host colonies of the social parasite P. atrimandibularis, colony odor is no longer homogeneous, as the parasite offspring have an odor that differs from that of their hosts. In trying to understand how the mechanism of nestmate recognition works in parasitized colonies and why parasite offspring are accepted by hosts, we tested the responses of resident Polistes biglumis wasps from parasitized and unparasitized colonies to newly emerged parasites and to nestmate and non-nestmate conspecifics. The experiments indicate that immediately upon eclosion both young parasites and young hosts lack a colony odor and that colony odor can be soon acquired from the accepting colony. In addition, while residents of nonparasitized colonies recognize only the odor of their species, resident hosts of parasitized colonies have learned a template that fits the odors of two species.     

Collective exploration and area marking in the ant Lasius niger

Summary: The aphid tending ant species, Lasius niger collectively explore new areas. Scouts are mobilised within the first five minutes of exploration with activity thereafter decreasing and stabilising after 40 minutes. Collective path choices of colonies underline the existence of chemical recruitment and area marking during exploration. To identify the territorial or home-range role of exploratory marking, we examined its influence on agonistic behaviour during intraspecific encounters. Ten nestmates and ten alien conspecifics were confronted: (i) on a paper marked by their own colony, (ii) on a paper marked by the alien colony or (iii) on a paper not chemically marked by ants. Residents and intruders showed a weak level of aggression and behaved similarly whatever the type of area marking. As no colony-specificity was observed in the odds of eliciting aggression, exploratory area marking in Lasius niger seems to be rather a home-range than a true territorial marking. We discuss the role of collective exploration, home-range marking and intraspecific interactions in the structuring and use of foraging space by neighbour Lasius niger colonies.     

Use of artificial arenas to predict the social organisation of halictine bees: Data for fourteen species from Chile

I studied the behavioural profiles of fourteen species of Chilean halictine bee using the circle tube apparatus. Interactions were classified as aggressive, avoidance or cooperative. One species, Corynura chloris, is believed to be semisocial and its behaviour was largely aggressive, Ruizantheda mutabilis is known to be communal and its behaviour was predominantly cooperative whereas Penapis toroi is a member of a subfamily from which only solitary behaviour is known and it primarily exhibited avoidance behaviours. As a result, I suggest that the relative frequency of these different behaviours may be useful in establishing the social organisation of species. Based upon comparisons of behavioural profiles, I predict the social organizations of the remaining species and suggest that at least some of the bees in the populations of Ruizantheda proxima, Caenohalictus dolator, Ca. species A and Pseudagapostemon pississi investigated exhibit communal behaviour; those of Co. patagonica and Co. herbsti likely have a reproductive division of labour, probably within semisocial societies, and that the populations of Co. corinogaster, Co. melanocladius, Ca. pygosinuatum, Ca. cuprellus and Lasioglossum aricense studied are probably solitary. Phylogenies suggest that solitary behaviour in Ca. pygosinuatum and Ca. cuprellus is reversed from communal behaviour and solitary behaviour in L. aricense may be a reversal from eusociality. The response “back and follow” is not indicative of dominance or cooperation as it correlated only with the frequency of avoidance interactions among the taxa studied. I discuss the utility of the circle tube apparatus in the identification of populations worthy of more detailed sociobiological investigation. Received 10 August 2005; revised 8 March 2006; accepted 21 March 2006.     

Effect of group size and caste ratio on individual survivorship and social immunity in a subterranean termite

Individuals living within social groups may benefit from the efficiencies of division of labour, but on the other hand render themselves vulnerable to socially transmitted disease. This cost to social living should promote cooperative barriers to disease transmission, especially in eusocial taxa where spatial and genetic proximity to nestmates are characteristically pronounced. Termites are eusocial yet little is known about how their sociality is deployed to resist contagion. In this study, we manipulate two variables that are expected to affect the number and nature of social interactions and measure the ability of individuals within groups to resist fungal infection. From laboratory experiments on field-collected colonies, we report that both group size and caste composition directly affect the survivorship of individuals within groups, but only caste composition moderates survivorship upon immune challenge. Our study therefore provides no statistical evidence that individual Eastern subterranean termites (Reticulitermes flavipes) have increased resistance to disease in crowded groups—that is, there is no evidence for a density-dependent social immune response. Our results do suggest, however, that the caste-specific nature of interactions may be important for controlling disease in a social context.     

Ecological generalism facilitates the evolution of sociality in snapping shrimps

Evidence from insects and vertebrates suggests that cooperation may have enabled species to expand their niches, becoming ecological generalists and dominating the ecosystems in which they occur. Consistent with this idea, eusocial species of sponge‐dwelling Synalpheus shrimps from Belize are ecological generalists with a broader host breadth and higher abundance than non‐eusocial species. We evaluate whether sociality promotes ecological generalism (social conquest hypothesis) or whether ecological generalism facilitates the transition to sociality (social transition hypothesis) in 38 Synalpheus shrimp species. We find that sociality evolves primarily from host generalists, and almost exclusively so for transitions to eusociality. Additionally, sponge volume is more important for explaining social transitions towards communal breeding than to eusociality, suggesting that different ecological factors may influence the independent evolutionary origins of sociality in Synalpheus shrimps. Ultimately, our results are consistent with the social transition hypothesis and the idea that ecological generalism facilitates the transition to sociality.     

Kin recognition in the ant Rhytidoponera confusa II. Gestalt odour

Two models have been proposed for the transfer of genetically determined colony odour pheromones in social insects. The ‘Gestalt’ model suggests a complete transfer of pheromones amongst all nestmates whereas the ‘Individualistic’ model suggests no significant odour transfer with nestmates bearing individually distinct odours. In experiments with the ant Rhytidoponera confusa, colonies showed significantly more aggression (12% aggression) towards nestmates that had been kept in cages with non-nestmates than they did to nestmate controls (0% aggression). Colonies also showed significantly less aggression against non-nestmates that had been kept with nestmates in a separate cage (84% aggression) than they did to non-nestmate controls (100% aggression). A second experiment indicated that workers can absorb colony-specific odours from the nest materials of other colonies. However, whilst both experiments indicated a partial Gestalt component to the colony odour (ca. 28%), the Individualistic component seemed to be more important (ca. 72%).     

The Effect of a Wasp's Age on Its Cuticular Hydrocarbon Profile and Its Tolerance by Nestmate and Non-Nestmate Conspecifics (Polistes fuscatus, Hymenoptera: Vespidae)

The effect of a wasp's age on its cuticular hydrocarbon profile and its tolerance by nestmate and non-nestmate conspecifics was investigated in a laboratory study of newly eclosed wasps ( Polistes fuscatus ) that were isolated from their comb at eclosion. In blind observations, mature females did not discriminate between young nestmates and non-nestmates that were ≤ 48 h-old. However, mature females did discriminate between young nestmates and non-nestmates that were 72 h old. Specifically, mature females were significantly more tolerant of (and significantly more likely to accept) 72 h-old nestmates than 72 h old non-nestmates. The abundance, relative abundance, and colony specificity of cuticular hydrocarbons changed significantly between 24 h-old and 72 h-old wasps. Our behavioral and chemical evidence indicates that wasps begin to develop a colony signature between 2 and 3 d of age.     

Cooperative Blood-feeding and the Function and Implications of Feeding Aggregations in the Sand Fly,Lutzomyia longipalpis (Diptera: Psychodidae)

Given the importance that the evolution of cooperation bears in evolutionary biology and the social sciences, extensive theoretical work has focused on identifying conditions that promote cooperation among individuals. In insects, cooperative or altruistic interactions typically occur amongst social insects and are thus explained by kin selection. Here we provide evidence that in Lutzomia longipalpis, a small biting fly and an important vector of leishmaniasis in the New World, cooperative blood-feeding in groups of non-kin individuals results in a strong decrease in saliva expenditure. Feeding in groups also strongly affected the time taken to initiate a bloodmeal and its duration and ultimately resulted in greater fecundity. The benefits of feeding aggregations were particularly strong when flies fed on older hosts pre-exposed to sand fly bites, suggesting that flies feeding in groups may be better able to overcome their stronger immune response. These results demonstrate that, in L. longipalpis, feeding cooperatively maximizes the effects of salivary components injected into hosts to facilitate blood intake and to counteract the host immune defences. As a result, cooperating sand flies enjoy enormous fitness gains. This constitutes, to our knowledge, the first functional explanation for feeding aggregations in this species and potentially in other hematophagous insects and a rare example of cooperation amongst individuals of a non-social insects species. The evolution of cooperative group feeding in sand flies may have important implications for the epidemiology of leishmaniasis.     

Aliens among us: nestmate recognition in the social huntsman spider, Delena cancerides

Unlike all other social spiders, the social huntsman spider, Delena cancerides, has been reported to rapidly respond to non-nestmates with lethal aggression, similar to the behavior of some eusocial insects. We tested for the presence of nestmate recognition in D. cancerides under laboratory conditions by introducing 105 unrelated alien conspecifics into foreign colonies and comparing their behavior to 60 control spiders removed and returned to their natal colony. Spiders demonstrated nestmate recognition by investigating alien spiders far more than nestmates and by resting closer to nestmates than to aliens. Serious attacks or deaths occurred in 23% of all trials; however, aggression was not directed significantly more toward aliens than to nestmates. Most notably, aggression was largely mediated by the adult females (resident or alien), who were most likely to attack or kill other subadult or mature individuals. Young individuals (resident or alien) were largely immune from serious aggression. Spiders recently collected from the field tended to be more aggressive than spiders born and raised in the laboratory, possibly due to blurring of recognition cues related to laboratory husbandry. Our findings support the prediction that nestmate recognition should evolve when there is a benefit to discriminating against non-kin, as in this social spider system where foraging individuals may enter a foreign colony and the colony retreat is a limited resource.