Behavioral Interactions Between <Emphasis Type="Italic">Aphaenogaster rudis</Emphasis> (Hymenoptera: Formicidae) and <Emphasis Type="Italic">Reticulitermes flavipes</Emphasis> (Isoptera: Rhinotermitidae): The Importance of Physical Barriers

Predation pressure from ants is a major driving force in the adaptive evolution of termite defense strategies and termites have evolved elaborate chemical and physical defenses to protect themselves against ants. We examined predator–prey interactions between the woodland ant, Aphaenogaster rudis (Emery) and the eastern subterranean termite, Reticulitermes flavipes (Kollar), two sympatric species widely distributed throughout deciduous forests in eastern North America. To examine the behavioral interactions between A. rudis and R. flavipes we used a series of laboratory behavioral assays and predation experiments where A. rudis and R. flavipes could interact individually or in groups. One-on-one aggression tests revealed that R. flavipes are vulnerable to predation by A. rudis when individual termite workers or soldiers are exposed to ant attacks in open dishes and 100% of termite workers and soldiers died, even though the soldiers were significantly more aggressive towards the ants. The results of predation experiments where larger ant and termite colony fragments interacted provide experimental evidence for the importance of physical barriers for termite colony defense. In experiments where the termites nested within artificial nests (sand-filled containers), A. rudis was aggressive at invading termite nests and inflicted 100% mortality on the termites. In contrast, termite mortality was comparable to controls when termite colonies nested in natural nests comprised of wood blocks. Our results highlight the importance of physical barriers in termite colony defense and suggest that under natural field conditions termites may be less susceptible to attacks by ants when they nest in solid wood, which may offer more structural protection than sand alone.     

Aggression,cooperation, and relatedness among colonies of the invasive ant, <Emphasis Type="Italic">Monomorium pharaonis</Emphasis>, originating from different areas of the world

The cooperation and aggression between five laboratory colonies of Monomorium pharaonis were compared using an aggressiveness test and pupa-carrying test in laboratory arenas. The colonies were derived from field collections in different parts of Europe and USA. Generally, inter-colony aggressiveness was low and acceptance of pupae from other colonies was high. Workers from one colony (Lužiny, CZ), however, frequently displayed aggressive behavior when paired with workers from other colonies, and the Lužiny pupae were avoided by workers of other colonies in pupa-carrying tests. Behavioral tests were only partly consistent with the phylogenetic relatedness of ants because the Wisconsin colony (USA) grouped with the Lužiny colony (and not with the other three colonies) in the phylogenetic analysis but grouped with the other three colonies in the behavioral tests.     

Bioassay design and length of time in the laboratory affect intercolonial interactions of the Formosan subterranean termite (Isoptera, Rhinotermitidae)

This study examined the effect of diet, experimental design, and length of time in the laboratory on intercolonial agonism among Formosan subterranean termite, Coptotermes formosanus Shiraki, colonies. In pairings of 12 C. formosanus Shiraki colonies collected in an urban forest, there was no significant reduction in survival of termites in 30 out of 59 colony pairs compared to colony controls, but there was <50% survival in 18 colony pairs and <10% survival in six colony pairs. There was no correlation between the level of aggressive behavior and the laboratory diet of the termites. Effect of bioassay design and length of time in the laboratory was evaluated in three colony pairs where tests were first conducted on the day of field collection, then colony pairs were retested every 7 days. Aggressive behavior decreased over time in both bioassays, but it tended to decrease more rapidly in the Petri dish tests. The rapid loss of agonism in groups of termites kept in the laboratory demonstrates that changes in environmental factors affect intercolonial agonism. This article presents the results of research only. Mention of a commercial or proprietary product does not constitute endorsement or recommendation by the USDA.     

Variation in ant aggression and kin discrimination ability within and between colonies

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.     

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.     

Symbiotic flagellate protists as cryptic drivers of adaptation and invasiveness of the subterranean termite Reticulitermes grassei Clément

Changes in flagellate protist communities of subterranean termite Reticulitermes grassei across different locations were evaluated following four predictions: (i) Rural endemic (Portugal mainland) termite populations will exhibit high diversity of symbionts; (ii) invasive urban populations (Horta city, Faial island, Azores), on the contrary, will exhibit lower diversity of symbionts, showing high similarity of symbiont assemblages through environmental filtering; (iii) recent historical colonization of isolated regions—as the case of islands—will imply a loss of symbiont diversity; and (iv) island isolation will trigger a change in colony breeding structure toward a less aggressive behavior. Symbiont flagellate protist communities were morphologically identified, and species richness and relative abundances, as well as biodiversity indices, were used to compare symbiotic communities in colonies from urban and rural environments and between island invasive and mainland endemic populations. To evaluate prediction on the impact of isolation (iv), aggression tests were performed among termites comprising island invasive and mainland endemic populations. A core group of flagellates and secondary facultative symbionts was identified. Termites from rural environments showed, in the majority of observed colonies, more diverse and abundant protist communities, probably confirming prediction (i). Corroborating prediction (ii), the two least diverse communities belong to termites captured inside urban areas. The Azorean invasive termite colonies had more diverse protist communities than expected and prediction (iii) which was not verified within this study. Termites from mainland populations showed a high level of aggressiveness between neighboring colonies, in contrast to the invasive colonies from Horta city, which were not aggressive to neighbors according to prediction (iv). The symbiotic flagellate community of R. grassei showed the ability to change in a way that might be consistent with adaptation to available conditions, possibly contributing to optimization of the colonization of new habitats and spreading of its distribution area, highlighting R. grassei potential as an invasive species.     

Protein marking reveals predation on termites by the woodland ant, <Emphasis Type="Italic">Aphaenogaster rudis</Emphasis>

Subterranean termites provide a major potential food source for forest-dwelling ants, yet the interactions between ants and termites are seldom investigated largely due to the cryptic nature of both the predator and the prey. We used protein marking (rabbit immunoglobin protein, IgG) and double antibody sandwich enzyme-linked immunosorbent assay (DAS-ELISA) to examine the trophic interactions between the woodland ant, Aphaenogaster rudis (Emery) and the eastern subterranean termite, Reticulitermes flavipes (Kollar). We marked the prey by feeding the termites paper treated with a solution of rabbit immunoglobin protein (IgG). Subsequently, we offered live, IgG-fed termites to ant colonies and monitored the intracolony distribution of IgG-marked prey. Laboratory experiments on the distribution of protein-marked termite prey in colonies of A. rudis revealed that all castes and developmental stages receive termite prey within 24 h. In field experiments, live, protein-marked termites were offered to foraging ants. Following predation, the marker was recovered from the ants, demonstrating that A. rudis preys on R. flavipes under field conditions. Our results provide a unique picture of the trophic-level interactions between predatory ants and subterranean termites. Furthermore, we show that protein markers are highly suitable to track trophic interactions between predators and prey, especially when observing elusive animals with cryptic food-web ecology. Received 19 January 2007; revised 23 March 2007; accepted 26 March 2007.     

Agonistic behavior correlated with hydrocarbon phenotypes in dampwood termites,Zootermopsis (Isoptera: Termopsidae)

The dampwood termite genus ZootermopsisEmerson contains three recognized species with four distinct and consistent hydrocarbon phenotypes. Agonistic behaviors among nonreproductive insects from colonies of the same and different hydrocarbon phenotypes were observed in the laboratory. Various combinations of soldier versus nymphs, pseudergate versus pseudergate, and soldier versus soldier encounters were used in experimental trials. Soldiers or pseudergates seldom attack individuals of the same hydrocarbon phenotype. Z. angusticollis(Hagen) (phenotype II) is typically aggressive toward phenotype III of Z. nevadensis(Hagen) but not always aggressive against phenotype I of Z. nevadensis.The variation in response is dependent on which castes are placed in the bioassay arena: soldier versus soldier bouts result in consistent aggression, while pseudergate versus pseudergate or soldier versus nymphs contacts do not. Both pseudergates and soldiers of Z. laticeps(Banks) (phenotype IV) respond agonistically toward the other three phenotypes: Z. angusticollis (II) and Z. nevadensis(I and III). Although hydrocarbon phenotypes I and III, both Z. nevadensis,are morphologically indistinguishable, agonistic behavioral responses between phenotype I and phenotype III are not equivalent to I versus I or III versus III behavioral responses. The I versus III engagements, regardless of the castes involved, display a greater proportion of avoidance and aggressive responses than I or III intraphenotype encounters. We interpret the lack of avoidance or aggressive behavior within each of the two phenotypes of Z. nevadensisand the significant avoidance and aggressive behavior between phenotypes as definite evidence of discrimination between disparate hydrocarbon phenotypes. These agonistic bioassays along with data on distinct hydrocarbon patterns and geographic distributions serve as the basis for creating two subspecies of Z. nevadensis: Z. n. nevadensis(Hagen) and Z. n. nuttingiHaverty and Thorne, ssp. nov.     

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.

     

Male–male aggression peaks at intermediate relatedness in a social spider mite

Theory predicts that when individuals live in groups or colonies, male–male aggression peaks at intermediate levels of local average relatedness. Assuming that aggression is costly and directed toward nonrelatives and that competition for reproduction acts within the colony, benefits of aggressive behavior are maximized in colonies with a mix of related and unrelated competitors because aggression hurts nonkin often, thereby favoring reproduction of kin. This leads to a dome‐shaped relation between male–male aggression and average relatedness. This prediction has been tested with bacteria in the laboratory, but not with organisms in the field. We study how male–male aggression varies with relatedness in the social spider mite Stigmaeopsis miscanthi. We sampled 25 populations across a wide geographic range between Taiwan and Japan, representing a gradient of high to low within‐population relatedness. For each population the weaponry of males was measured as the length of the first pair of legs, and male–male aggression was tested by placing pairs of nonsibling males together and scoring the frequency of male death over a given period. As these two morphological and behavioral variables correlate strongly, they both reflect the intensity of male–male conflict. Our data on the social spider mite show that male–male aggression as well as weapon size strongly peak at intermediate, average relatedness, thereby confirming theoretical predictions.     

Chill out: cooling promotes aggressive behavior in the ant Formica xerophila

Studies of insect behavior often involve cooling individuals prior to performing experiments or making observations. For such studies, it is important to know how cooling might affect subsequent behavior. Here I investigate how anesthetization by cooling (relative to anesthetization by carbon dioxide or control individuals) affects the aggressive behaviors of two closely related ant species, Formica xerophila and F. integroides. These species regularly compete for resources, and individuals of both species regularly experience nighttime temperatures similar to those of cold-induced anesthetization. I show that cooling increases aggression (toward both interspecific competitors as well as nestmates) for F. xerophila, but has no effect on F. integroides behavior. Although previously cooled F. xerophila are more aggressive during both intraspecific and interspecific interactions, intraspecific fights are much shorter in length than interspecific fights. Furthermore, aggression by F. xerophila decreases as time since being cooled increases. These data suggest that cooling produces a short-term reduction in the ants’ discriminatory abilities, which leads to mistaken identities during encounters. The difference in species’ behaviors after cooling can be attributed to their differences in strategies when encountering potential competitors. Results here confirm that cold anesthesia can affect subsequent behavior, and needs to be tested in behavioral studies with insects. Received 6 September 2008; revised 29 October 2008; accepted 4 November 2008.     

Does lack of intraspecific aggression or absence of nymphs determine acceptance of foreign reproductives in <Emphasis Type="Italic">Macrotermes</Emphasis>?

The rejection or acceptance of a foreign reproductive by an alien colony may not always be as straightforward as cue recognition between worker termites. This paper aims to determine whether adoption of foreign reproductives is caused simply by lack of intraspecific aggression or is contingent on the reproductive status of the host colony. In the fungus-culturing termites, Macrotermes gilvus (Hagen) and Macrotermes carbonarius (Hagen), major workers showed low intraspecific aggression towards non-nestmates irrespective of geographic distance between source colonies. Our results indicated that workers were hardly aggressive towards non-nestmates. In royal cell-swapping experiments, both species responded in a similar way: (1) in host colonies with nymphs present, the foreign reproductives were rejected; while (2) in host colonies without nymphs the foreign reproductives were either accepted and breeding resumed or the host colonies died eventually. Workers from the host colonies preferentially maintained offspring nymphs from which adultoid replacement reproductives develop rather than accepting foreign reproductives. There is no fitness gain for the queenless workers in accepting foreign reproductives; however, there is overall benefit to the newly born population.     

Agonistic behavior among colonies of the Formosan subterranean termite,Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae), from Florida and Hawaii: Lack of correlation with cuticular hydrocarbon composition

Cuticular hydrocarbon patterns of the Formosan subterranean termite, Coptotermes formosanus Shiraki, were similar among colonies from the same geographical location. Hydrocarbon patterns of Florida colonies were easily distinguished from those of Hawaii colonies by using canonical discriminant analysis. Groups of termites from the same colony did not fight one another when placed in an arena. Intercolonial aggression was not recorded among C. formosanuspopulations from Florida but three colonies from Hawaii fought with the other Hawaiian and three Florida colonies. Of the 12 colonies (six each from Florida and Hawaii) tested, 3 Florida colonies did not direct or receive aggression from any other colony. Cuticular hydrocarbon patterns were not correlated with agonistic behavior.     

Contact between supercolonies elevates aggression in Argentine ants

Complex recognition systems underlie the social organization of many organisms. In social insects the acceptance of other individuals as nestmates can involve a variety of different cues, but the relative importance of these cues can change in relation to the fitness costs of accepting or rejecting other individuals. In this study we investigate the mechanisms that underlie recognition behaviour in Argentine ants (Linepithema humile). Introduced populations of Argentine ants are characterized by a social structure known as unicoloniality where intraspecific aggression is absent over large distances resulting in the formation of expansive supercolonies. Recent research has identified sites where multiple, mutually aggressive supercolonies co-occur allowing an examination of Argentine ant behaviour at territorial boundaries. We found that workers from different supercolonies always interact aggressively with one another, but that neighbours from different colonies (i.e., workers from nests located in the immediate vicinity of territory borders) consistently exhibited higher levels of aggression compared to those displayed by non-neighbours from different colonies (i.e., workers from nests located far enough away from a territory border so that interactions are unlikely). This difference in the level of aggression displayed between neighbours and between non-neighbours from different supercolonies cannot be explained by differences in relatedness or genetic similarity. Instead our findings suggest that direct contact between mutually antagonistic colonies is sufficient to elevate aggression. A laboratory experiment in which we manipulated the extent to which colonies with no prior history of contact could interact with one another, revealed that aggression increased after colonies were permitted to interact, but dropped after connections between colonies were severed. Moreover, the mere presence of an aggressive supercolony was sufficient to elicit elevated aggression. Overall these patterns are opposite to the “dear enemy” phenomenon and could be the result of the intense territorial aggression exhibited by established supercolonies of this species. Received 8 January 2007; revised 27 March 2007; accepted 28 March 2007.     

Intra- and Inter-colonial Agonistic Behavior in the Termite, Microcerotermes fuscotibialis Sjostedt (Isoptera: Termitidae: Termitinae)

Pairing termite workers from cultures obtained from same colony of Microcerotermes fuscotibialis Sjostedt did not result in agonistic behavior or mortality of the paired individuals. Termite pairings from different colonies located at different distances resulted in serious encounters and aggressive behavior leading to significant mortality of the individuals. Subtle agonistic behavior was observed when colony mates were reunited after months of separation, but this did not result in any significant mortality. These results confirmed observations of non-overlap of foraging trails of these termites in the field which averts possible encounters and conflict. Therefore these termites are able to recognize their colony mates irrespective of period of separation, a factor for colony affiliation, kinship and recognition.     

Colonial and geographic variations in agonistic behaviour,cuticular hydrocarbons and mtDNA of Italian populations of <Emphasis Type="Italic">Reticulitermes lucifugus</Emphasis> (Isoptera,Rhinotermitidae)

Summary The subterranean termite, Reticulitermes lucifugus (Rossi), is found throughout Italy. The purpose of this study was to assess variations among colonies collected from the north to south of Italy. A multidisciplinary approach was used including behavioral tests, cuticular hydrocarbon analysis and partial sequencing of mitochondrial DNA. Results showed that Italian R. lucifugus populations were moderately aggressive and that aggressive behavior was unrelated to intercolonial geographic distance. Analysis of cuticular hydrocarbons demonstrated no qualitative variations between colonies, but quantitative differences were found according to caste and colony. Alkene content tended to decrease from north to south. Sequencing of mtDNA indicated kinship between two Tuscan populations and R. l. corsicus. This finding is suggestive of transtyrrenian distribution of the Corsican subspecies. Moreover, distance between haplotypes appears to be associated with intercolonial geographic distance.Received 25 March 2003; revised 3 October 2003; accepted 10 November 2003.     

Intraspecific interactions in a community of arboreal nesting termites (Isoptera: Termitidae)

In coconut plantations of northern New Guinea, the arboreal nesting termite community comprises three species:Nasutitermes princeps, N. novarumhebridarum, andMicrocerotermes biroi. In orde to assess the importance of intraspecific interactions in this community, we conducted pairwise encounters between batches of individuals in the laboratory and between entire nest populations in seminantural conditions. Three levels of agonism were defined in laboratory bioassays: anagonism, moderate agonism, and strong agonism. Anagonism was observed during all control tests with homocolonical groups and in some tests with allocolonial groups of all species. Moderate agonism included initial aggressiveness that subsequently faded out, and initially passive encounters where aggression progressively built up and led to fighting. Strong agonism corresponded to initial aggressiveness and fighting. Results obtained in alboratory bioassays were consistent with bioassays in seminatural conditions. WhenNasutitermes colonies were anagonists in laboratory bioassays, their foraging trails merged without aggression in field tests.N. princeps nests that were moderately agonistic in laboratory tests fought and either continued to avoid each other or finally joined after elimination of the most aggressive individuals. The most aggressiveM. biroi andN. princeps colonies fought and their foraging trails diverged afterward. Direct attacks on alien nests were winnessed inM. biroi. In all species, anagonism occurred in 21–34% of the combinations tested, between either geographically close or distantcolonies. An exeption was a group of 112 anagonist nests ofN. princeps, which most probably constituted a supercolony. The level of agonism betweenNasutitermes colonies was constant during the wet and dry season. Termite colonies excluded each other, both intra- and interspecifically, from the coconut trees, and their territories seem distributed in a mosaic pattern. Agonism between colonies may result in the elimination of the weakest colonies or in trail divergence, maintaining this mosaic. In cotrast, lack of agonism between some colonies suggests the possibility of colony fusion and gene exchanges without nuptial flights.     

Manipulation of colony environment modulates honey bee aggression and brain gene expression

The social environment plays an essential role in shaping behavior for most animals. Social effects on behavior are often linked to changes in brain gene expression. In the honey bee (Apis mellifera L.), social modulation of individual aggression allows colonies to adjust the intensity with which they defend their hive in response to predation threat. Previous research has showed social effects on both aggression and aggression‐related brain gene expression in honey bees, caused by alarm pheromone and unknown factors related to colony genotype. For example, some bees from less aggressive genetic stock reared in colonies with genetic predispositions toward increased aggression show both increased aggression and more aggressive‐like brain gene expression profiles. We tested the hypothesis that exposure to a colony environment influenced by high levels of predation threat results in increased aggression and aggressive‐like gene expression patterns in individual bees. We assessed gene expression using four marker genes. Experimentally induced predation threats modified behavior, but the effect was opposite of our predictions: disturbed colonies showed decreased aggression. Disturbed colonies also decreased foraging activity, suggesting that they did not habituate to threats; other explanations for this finding are discussed. Bees in disturbed colonies also showed changes in brain gene expression, some of which paralleled behavioral findings. These results show that bee aggression and associated molecular processes are subject to complex social influences .     

Sex differences in intrasexual aggression among sex-role-reversed,cooperatively breeding cichlid fish <Emphasis Type="Italic">Julidochromis regani</Emphasis>

In sex-role-reversed species, females compete for resources (e.g., mates) more intensively than do males. However, it remains unclear whether these species exhibit sex differences in the intensity of aggressive behavior in the context of within-sex contests. Cichlid fish in the genus Julidochromis exhibit intraspecific variation in mating systems, ranging from monogamy to cooperative polyandry with sex-role reversal. In the study reported here, we observed aggressive interactions among three same-sex individuals in Julidochromis regani in the laboratory and tested whether inter-female aggression was more intense than inter-male aggression. Although difference in body size strongly determined the direction of aggression in fish, aggression by a smaller-sized individuals toward larger ones was occasionally observed. This type of aggression was common between individuals of a similar body size (≤5 mm) and occurred more frequently among females than males. In contrast, differences in body size and sex did not affect the frequency of aggression by larger-sized individuals against smaller ones. Bidirectional aggression (i.e., mouth fighting) occurred frequently when two individuals had similar body size, and there was no difference in its frequency between sexes. However, temporal analysis showed that females performed bidirectional aggression more persistently than males. These sex differences in the intensity of intrasexual aggression could be the behavioral mechanisms underpinning cooperative polyandry.     

Intercontinental union of Argentine ants: behavioral relationships among introduced populations in Europe, North America, and Asia

Many invasive ants, including the Argentine ant Linepithema humile, form expansive supercolonies, within which intraspecific aggression is absent. The behavioral relationships among introduced Argentine ant populations at within-country or within-continent scales have been studied previously, but the behavioral relationships among intercontinental populations have not been examined. The present study investigated the levels of aggression among intercontinental Argentine ant populations by transporting live ants from Europe and California to Japan and conducting aggression tests against Japanese populations. Workers from the dominant supercolonies of Europe and California did not show aggressive behavior toward workers from the dominant supercolony of Japan, whereas they fought vigorously against workers from minor supercolonies. The three massive supercolonies, together with Argentine ants from Macaronesia, may be the largest non-aggressive unit formed by a social insect species in which intraspecific aggression exists. Absence or low levels of aggression at transcontinental scale, which may have derived from low genetic variation, may help introduced Argentine ants maintain expansive supercolonies. The lack of aggression implies possible frequent exchanges of individuals among the intercontinental populations mediated by human activities.