Social integration of macroparasites in ant societies: ultimate and proximate mechanisms

Ant colonies are commonly parasitized simultaneously by several species. While some parasites are recognized and attacked by their ant hosts, others have apparently cracked the ants’ recognition code and interact mainly peacefully with their hosts. Although such apparent differences in social integration among ant parasites have been described, the underlying mechanisms resulting in differential integration remain mostly unknown. Using Leptogenys army ants and their parasites, I studied ultimate mechanisms that might be responsible for differing integration levels by comparing the strength of host defence with the negative impact of parasites. In addition, I investigated proximate mechanisms of differing integration levels by evaluating the role of chemical deception by mimicry. The interactions of several parasitic beetle species with their Leptogenys hosts revealed that particular species fed on host larvae, while others did not. The hosts’ aggressiveness was enhanced towards brood-killing species, while non-predatory species received almost no aggression, resulting in social integration. Accordingly, the fitness costs of parasites likely influence the evolution of host defences against them in a multi-parasite situation. The role of chemical mimicry has been investigated in detail for two kleptoparasites, namely the silverfish Malayatelura ponerophila and the spider Gamasomorpha maschwitzi. By analyzing the transfer of a chemical label from the host ants to the parasites, I empirically demonstrated for the first time that ant parasites are able to acquire mimetic compounds from their host. Additional biosynthesis of mimetic compounds seems unlikely in both parasites, since the concentration of each cuticular hydrocarbon decreased in individuals that were isolated from the host. In addition, a high accuracy in chemical host resemblance was shown to be beneficial for the social integration of both parasites. Reduced accuracy in chemical host resemblance resulted either in aggressive host responses towards the silverfish or elevated host inspection behaviour towards the spider. The degree of dependency on chemical mimicry to achieve social integration differed considerably between the two parasites, however. Accordingly, the parasites’ level of social integration is affected by ultimate mechanisms such as the negative impact on the host as well as by proximate mechanisms such as the degree of accuracy in chemical host resemblance

Acquisition of chemical recognition cues facilitates integration into ant societies

<p>Abstract</p> <p>Background</p> <p>Social insects maintain the integrity of their societies by discriminating between colony members and foreigners through cuticular hydrocarbon (CHC) signatures. Nevertheless, parasites frequently get access to social resources, for example through mimicry of host CHCs among other mechanisms. The origin of mimetic compounds, however, remains unknown in the majority of studies (biosynthesis vs. acquisition). Additionally, direct evidence is scarce that chemical mimicry is indeed beneficial to the parasites (e.g., by improving social acceptance).</p> <p>Results</p> <p>In the present study we demonstrated that the kleptoparasitic silverfish <it>Malayatelura ponerophila </it>most likely acquires CHCs directly from its host ant <it>Leptogenys distinguenda </it>by evaluating the transfer of a stable-isotope label from the cuticle of workers to the silverfish. In a second experiment, we prevented CHC pilfering by separating silverfish from their host for six or nine days. Chemical host resemblance as well as aggressive rejection behaviour by host ants was then quantified for unmanipulated and previously separated individuals. Separated individuals showed reduced chemical host resemblance and they received significantly more aggressive rejection behaviour than unmanipulated individuals.</p> <p>Conclusion</p> <p>Our study clarifies the mechanism of chemical mimicry in a social insect parasite in great detail. It shows empirically for the first time that social insect parasites are able to acquire CHCs from their host. Furthermore, it demonstrates that the accuracy of chemical mimicry can be crucial for social insect parasites by enhancing social acceptance and, thus, allowing successful exploitation. We discuss the results in the light of coevolutionary arms races between parasites and hosts.</p

On the Use of Adaptive Resemblance Terms in Chemical Ecology

Many organisms (mimics) show adaptive resemblance to an element of their environment (model) in order to dupe another organism (operator) for their own benefit. We noted that the terms for adaptive resemblance are used inconsistently within chemical ecology and with respect to the usage in general biology. Here we first describe how resemblance terms are used in general biology and then comparatively examine the use in chemical ecology. As a result we suggest the following consistent terminology: “chemical crypsis” occurs when the operator does not detect the mimic as a discrete entity (background matching). “Chemical masquerade” occurs when the operator detects the mimic but misidentifies it as an uninteresting entity, as opposed to “chemical mimicry” in which an organism is detected as an interesting entity by the operator. The additional terms “acquired” and “innate” may be used to specify the origins of mimetic cues

Comparative chemical analysis of army ant mandibular gland volatiles (Formicidae: Dorylinae)

Army ants are keystone species in many tropical ecosystems. Yet, little is known about the chemical compounds involved in army ant communication. In the present study, we analyzed the volatile mandibular gland secretions—triggers of ant alarm responses—of six Neotropical army ant species of the genus Eciton (outgroup: Nomamyrmex esenbeckii). Using solid-phase microextraction, we identified 12 chemical compounds, primarily ketones with associated alcohols, one ester and skatole. Most compounds were shared among species, but their relative composition was significantly different. By comparing chemical distances of mandibular gland secretions to species divergence times, we showed that the secretions’ compositions are not strictly determined by phylogeny. By identifying chemical bouquets of seven army ant species, our study provides a valuable comparative resource for future studies aiming to unveil the chemicals’ precise role in army ant alarm communication

Comparative chemical analysis of army ant mandibular gland volatiles (Formicidae: Dorylinae)

Army ants are keystone species in many tropical ecosystems. Yet, little is known about the chemical compounds involved in army ant communication. In the present study, we analyzed the volatile mandibular gland secretions—triggers of ant alarm responses—of six Neotropical army ant species of the genus Eciton (outgroup: Nomamyrmex esenbeckii). Using solid-phase microextraction, we identified 12 chemical compounds, primarily ketones with associated alcohols, one ester and skatole. Most compounds were shared among species, but their relative composition was significantly different. By comparing chemical distances of mandibular gland secretions to species divergence times, we showed that the secretions’ compositions are not strictly determined by phylogeny. By identifying chemical bouquets of seven army ant species, our study provides a valuable comparative resource for future studies aiming to unveil the chemicals’ precise role in army ant alarm communication

Hunting habits die hard: Conserved prey preferences in army ants across two distant neotropical rainforests

Army ants are widely recognized as keystone species in neotropical rainforests due to their role as important arthropod predators. Their large‐scale raids involve thousands of workers scouring the forest floor in pursuit of prey, primarily capturing other invertebrates. Up to 20 species of army ants coexist in a rainforest, and dietary niche differentiation has been proposed as a mechanism to alleviate competition among them. Based on only a handful of study sites, however, our understanding of the precise dietary preferences and the extent of niche differentiation remains notably limited. In this study, we aimed to expand our knowledge of army ant communities by resolving an Ecuadorian predation network consisting of 244 prey species and 13 army ant species representing the five known neotropical army ant genera: Cheliomyrmex, Eciton, Labidus, Neivamyrmex, and Nomamyrmex. We collected 2156 prey items from 180 army ant raids/emigrations, and of these, we identified 1945 prey items to the family level, 1313 to the genus level, and 664 to the species level based on morphological identifications and DNA barcodes. Prey consisted primarily of other ants (1843 prey items; 153 ant species), to the largest part ant brood (N = 1726). Hence, most army ant species chiefly plundered the nests of other ants, while the three swarm raiding species, that is, Lab. praedator, Lab. spininodis, and Ec. burchellii, exhibited a relatively high proportion of non‐ant invertebrate prey in their diet. The predation network showed a high degree of specialization (H2′ = 0.65), characterized by little dietary niche overlap among sympatric species. We compared the Ecuadorian network with one previously studied in Costa Rica and found that, despite the large geographic distance, prey preferences remained remarkably similar. We discovered species‐specific preferences for captured ant genera and species, despite some species turnover in both army ants and prey. Additionally, army ants also exhibited consistent spatiotemporal raiding preferences across study sites. In conclusion, predation preferences within army ant communities exhibited consistency in multiple niche dimensions across two distant neotropical rainforests, suggesting a notable level of predictability within army ant predation networks

Rapid ant community reassembly in a Neotropical forest: Recovery dynamics and land‐use legacy

Regrowing secondary forests dominate tropical regions today, and a mechanistic understanding of their recovery dynamics provides important insights for conservation. In particular, land‐use legacy effects on the fauna have rarely been investigated. One of the most ecologically dominant and functionally important animal groups in tropical forests are the ants. Here, we investigated the recovery of ant communities in a forest–agricultural habitat mosaic in the Ecuadorian Chocó region. We used a replicated chronosequence of previously used cacao plantations and pastures with 1–34 years of regeneration time to study the recovery dynamics of species communities and functional diversity across the two land‐use legacies. We compared two independent components of responses on these community properties: resistance, which is measured as the proportion of an initial property that remains following the disturbance; and resilience, which is the rate of recovery relative to its loss. We found that compositional and trait structure similarity to old‐growth forest communities increased with regeneration age, whereas ant species richness remained always at a high level along the chronosequence. Land‐use legacies influenced species composition, with former cacao plantations showing higher resemblance to old‐growth forests than former pastures along the chronosequence. While resistance was low for species composition and high for species richness and traits, all community properties had similarly high resilience. In essence, our results show that ant communities of the Chocó recovery rapidly, with former cacao reaching predicted old‐growth forest community levels after 21 years and pastures after 29 years. Recovery in this community was faster than reported from other ecosystems and was likely facilitated by the low‐intensity farming in agricultural sites and their proximity to old‐growth forest remnants. Our study indicates the great recovery potential for this otherwise highly threatened biodiversity hotspot