Thomas Parmentier

Context-dependent specialization in colony defence in the red wood ant Formica rufa

In many species, specialized defence traits and strategies are crucial for surviving enemy attacks or securing resources. In numerous social insect lineages, a morphologically and behaviourally distinct soldier caste specializes in colony defence, with larger foragers typically engaging most in the aggressive defence of the colony against external threats. We hypothesized, however, that specialization in aggression could show vastly different patterns in the context of the defence against small intranidal parasites that prey on brood. This is because we expected that small, intranidal nurse workers could be better suited to defend against these parasitic myrmecophiles (=ant associates) due to their better matching size, high encounter rate and the high task switching costs that would occur if foragers had to carry out this task. Here, we present data that support this hypothesis from a study on specialization in defence against two parasites in the red wood ant Formica rufa. In particular, we show that small workers displayed the strongest aggressive behaviour towards the parasitic rove beetle Thiasophila angulata and the spider Thyreosthenius biovatus, and present evidence that small workers were better at preventing brood predation than larger workers. In addition, there was worker task specialization in defensive behaviour, with nurses and workers at nest entrances being more aggressive towards T.xa0angulata than extranidal foragers. We argue that this context-dependent specialization in aggression and nest defence was likely to be important in favouring the pronounced worker polymorphism observed in both this and other ant species and discuss our findings in relation to models for the evolution of division of labour and caste polymorphism in insect societies.

Do well-integrated species of an inquiline community have a lower brood predation tendency? A test using red wood ant myrmecophiles.

BackgroundA host infected with multiple parasitic species provides a unique system to test evolutionary and ecological hypotheses. Different parasitic species associated with a single host are expected to occupy different niches. This niche specialization can evolve from intraguild competition among parasites. However, niche specialization can also be structured directly by the host when its defence strategy depends on the parasite’s potential impact. Then it can be expected that species with low or no tendency to prey on host brood will elicit less aggression than severe brood parasitic species and will be able to integrate better in the host system.We examined this hypothesis in a large community of symbionts associated with European red wood ants (Formica rufa group) by testing the association between 1) level of symbiont integration (i.e. presence in dense brood chambers vs. less populated chambers without brood) 2) level of ant aggression towards the symbiont 3) brood predation tendency of the symbiont.ResultsSymbionts differed vastly in integration level and we demonstrated for the first time that relatively unspecialized ant symbionts or myrmecophiles occur preferentially in brood chambers. Based on their integration level, we categorize the tested myrmecophiles into three categories: 1) species attracted to the dense brood chambers 2) species rarely or never present in the brood chambers 3) species randomly distributed throughout the nest. The associates varied greatly in brood predation tendency and in aggression elicited. However, we did not find a correlation for the whole myrmecophile community between a) brood predation tendency and host’s aggression b) integration level and host’s aggression c) integration level and brood predation tendency.ConclusionsOur results indicate that red wood ants did not act more hostile towards species that have a high tendency to prey on brood compared to species that are less likely or do not prey on brood. We show that potentially harmful parasites can penetrate into the deepest parts of a social insect fortress. We discuss these seemingly paradoxical findings in relation to models on coevolution and evolutionary arms races and list factors which can make the presence of potentially harmful parasites within the brood chambers evolutionary stable.

Arthropods Associate with their Red Wood ant Host without Matching Nestmate Recognition Cues

Social insect colonies provide a valuable resource that attracts and offers shelter to a large community of arthropods. Previous research has suggested that many specialist parasites of social insects chemically mimic their host in order to evade aggression. In the present study, we carry out a systematic study to test how common such chemical deception is across a group of 22 arthropods that are associated with red wood ants (Formica rufa group). In contrast to the examples of chemical mimicry documented in some highly specialized parasites in previous studies, we find that most of the rather unspecialized red wood ant associates surveyed did not use mimicry of the cuticular hydrocarbon recognition cues to evade host detection. Instead, we found that myrmecophiles with lower cuticular hydrocarbon concentrations provoked less host aggression. Therefore, some myrmecophiles with low hydrocarbon concentrations appear to evade host detection via a strategy known as chemical insignificance. Others showed no chemical disguise at all and, instead, relied on behavioral adaptations such as particular defense or evasion tactics, in order to evade host aggression. Overall, this study indicates that unspecialized myrmecophiles do not require the matching of host recognition cues and advanced strategies of chemical mimicry, but can integrate in a hostile ant nest via either chemical insignificance or specific behavioral adaptations.

The cost of ant attendance and melezitose secretion in the black bean aphid Aphis fabae

1. The aphid Aphis fabae (Scopoli) is facultatively tended by Lasius niger (Linnaeus) ants. Previously, we found that A. fabae colonies can be made up of several clones, and that clones display significant differences in the composition of their honeydew sugars, especially in the amount of the ant attractant sugar melezitose that they produce.

An apparent mutualism between Afrotropical ant species sharing the same nest

Social insects have a highly developed nestmate and species recognition system that is quite effective at keeping out unwanted intruders. Rare cases of “parabiosis,” however, are known in some ants where two species apparently live peacefully alongside each other within the same nest. Here, we report on such an association between the tiny Afrotropical ant Strumigenys maynei and the large ant Platythyrea conradti. We demonstrated that both ants peacefully share the same arboreal nests in spite of the presence of clearly distinct nestmate recognition cues. Because of the large size differences, we hypothesized that each of the two species would benefit from specializing in carrying out particular tasks, in analogy to the size-related division of labor observed in species with size-polymorphic workers. In line with this theory, we found that the tiny ant S. maynei was highly efficient at nest defense against intranidal arthropods and alien ant intruders, whereas the large ant P. conradti was highly skilled in nest engineering. We argue that the described association is likely mutualistic, as P. conradti clearly benefited from the supreme defense capabilities of S. maynei, and that, conversely, S. maynei took advantage of small prey thriving in the organic nest material collected by P. conradti.Significance statementAssociations between social insects are typically parasitic in nature. A few cases, however, are known of beneficial associations between social insects. Here, we report such a rare association between two Afrotropical species that share the same nest even though they lack matching colony odors. The large ant Platythyrea conradti benefited from the presence of Strumigenys maynei as this tiny, but highly aggressive, ant was much more efficient in attacking intranidal and extranidal enemies. S. maynei in turn took advantage of P. conradti as this ant constructs a unique nest which attracts suitable prey.

Contrasting indirect effects of an ant host on prey–predator interactions of symbiotic arthropods

Indirect interactions occur when a species affects another species by altering the density (density-mediated interactions) or influencing traits (trait-mediated interactions) of a third species. We studied variation in these two types of indirect interactions in a network of red wood ants and symbiotic arthropods living in their nests. We tested whether the ant workers indirectly affected survival of a symbiotic prey species (Cyphoderus albinus) by changing the density and/or traits of three symbiotic predators, i.e., Mastigusa arietina, Thyreosthenius biovatus and Stenus aterrimus, provoking, respectively, low, medium and high ant aggression. An ant nest is highly heterogeneous in ant worker density and the number of aggressive interactions towards symbionts increases with worker density. We, therefore, hypothesized that varying ant density could indirectly impact prey–predator interactions of the associated symbiont community. Ants caused trait-mediated indirect effects in all three prey–predator interactions, by affecting the prey capture rate of the symbiotic predators at different worker densities. Prey capture rate of the highly and moderately aggressed spider predators M. arietina and T. biovatus decreased with ant density, whereas the prey capture rate of the weakly aggressed beetle predator S. aterrimus increased. Ants also induced density-mediated indirect interactions as high worker densities decreased the survival rate of the two predatory spider species. These results demonstrate for the first time that a host can indirectly mediate the trophic interactions between associated symbionts. In addition, we show that a single host can induce opposing indirect effects depending on its degree of aggression towards the symbionts.

Prudent behavior rather than chemical deception enables a parasite to exploit its ant host

Many parasites display complex strategies to evade host detection. The principal view is that the parasites of social insects deceive their host by means of advanced chemical adaptations such as mimicking the cuticular host recognition cues, being chemically odorless, or emitting manipulative volatiles. Apart from these chemical adaptations, parasites of social insects may also use simpler behavioral strategies to evade host detection. As yet, such a behavior has rarely been studied. Here we tested which chemical and behavioral strategies the unspecialized parasitic rove beetle Thiasophila angulata uses to avoid detection by its aggressive Formica rufa red wood ant host. Chemical comparisons of the beetles and the host ants cuticular hydrocarbons showed that the beetle carried an idiosyncratic cuticular profile that was clearly different from that of its host. Beetles that were isolated from their host or were placed in the nests of another Formica species perfectly retained their original cuticular profiles and provoked equal levels of aggression. These results suggest that the beetles do not avoid host detection through chemical deception. In contrast, the beetle adapted its behavior to avoid aggression by the ants. In the presence of ants, the beetle behaved much more prudently by hiding more frequently and engaging in less risky runs. Overall, these results highlight that for relatively unspecialized parasites, general strategies such as prudent behavior can be equally effective as more specialized deception strategies to evade host detection.