Chemical disguise of myrmecophilous cockroaches and its implications for understanding nestmate recognition mechanisms in leaf-cutting ants

Abstract

BackgroundCockroaches of the genus Attaphila regularly occur in leaf-cutting ant colonies. The ants farm a fungus that the cockroaches also appear to feed on. Cockroaches disperse between colonies horizontally (via foraging trails) and vertically (attached to queens on their mating flights). We analysed the chemical strategies used by the cockroaches to integrate into colonies of Atta colombica and Acromyrmex octospinosus. Analysing cockroaches from nests of two host species further allowed us to test the hypothesis that nestmate recognition is based on an asymmetric mechanism. Specifically, we test the U-present nestmate recognition model, which assumes that detection of undesirable cues (non-nestmate specific substances) leads to strong rejection of the cue-bearers, while absence of desirable cues (nestmate-specific substances) does not necessarily trigger aggression.ResultsWe found that nests of Atta and Acromyrmex contained cockroaches of two different and not yet described Attaphila species. The cockroaches share the cuticular chemical substances of their specific host species and copy their host nest’s colony-specific cuticular profile. Indeed, the cockroaches are accepted by nestmate but attacked by non-nestmate ant workers. Cockroaches from Acromyrmex colonies bear a lower concentration of cuticular substances and are less likely to be attacked by non-nestmate ants than cockroaches from Atta colonies.ConclusionsNest-specific recognition of Attaphila cockroaches by host workers in combination with nest-specific cuticular chemical profiles suggest that the cockroaches mimic their host’s recognition labels, either by synthesizing nest-specific substances or by substance transfer from ants. Our finding that the cockroach species with lower concentration of cuticular substances receives less aggression by both host species fully supports the U-present nestmate recognition model. Leaf-cutting ant nestmate recognition is thus asymmetric, responding more strongly to differences than to similarities.Electronic supplementary materialThe online version of this article (doi:10.1186/s12898-016-0089-5) contains supplementary material, which is available to authorized users.

Strategies of the beetle Oochrotus unicolor (Tenebrionidae) thriving in the waste dumps of seed‐harvesting Messor ants (Formicidae)

“…There was only a weak difference in the beetle's cuticular profile across the host nests. Specialised myrmecophiles copy colony‐specific hydrocarbon profiles (Nash et al ., ; Nehring et al ., ) and individuals transferred from other colonies of the host species experience higher levels of aggression (Elmes et al ., ; Nehring et al ., ). The lack of colony‐specific similarity was reflected in similar behaviour of the ants towards associated beetles and those found in an alien M. barbarus colony.…”

“…The body niche may be even compartmentalised in multiple ‘subniches’ when the ectoparasites have adapted to different body parts (Rettenmeyer et al ., ). Nest chambers with food storage are also colonised by inquilines, as exemplified by the arthropods living in fungus gardens of termites and leaf‐cutter ants (Kistner, ; Nehring et al ., ). Another major niche that is occupied by many symbionts is found in the waste dumps or refuse piles in and around the nest entrances.…”

The relationship between epicuticular long-chained hydrocarbons and surface area - volume ratios in insects (Diptera, Hymenoptera, Lepidoptera)

“…The surface of the cuticle is functionally important for interactions of animals with their environment and may therefore be crucial for the animal’s ecophysiological responses [25, 36, 37]. Some studies [8, 38] thus used geometric approximations of the insects’ surfaces. Here we used direct surface measurements of the flower visitors (Fig 1B) using a modified structured light 3D scanner [25] and were therefore able to calculate the CHC density per surface area [ng/mm 2 ].…”

“…A standardization by body mass (dry weight) may be appropriate to describe the relative resource allocation of an insect to its chemical substances on the cuticle, but it may not be ideal to allow conclusions about the importance of surface area. Thus, we suggest that the CHC density per surface area could be included as functional trait in future studies, particularly for environmental responses such as thermal resilience, but maybe also to study the degree of social integration in mimicry-systems such as acquired chemical mimicry in myrmecophiles and their host ants [8, 38]. …”

Interspecific Eavesdropping on Ant Chemical Communication

“…3.5 mm) and wingless with reduced sensory and glandular systems (Box 1D) (Brossut, 1976;Wheeler, 1900). They live in the ants' fungus garden, where they graze (Wheeler, 1900;Phillips et al, 2017) and acquire nestspecific cuticular hydrocarbon signatures (Nehring et al, 2016) while behaving as cleptoparasites ( Table 1). Attaphila climb onto virgin Atta queens just before they leave the nest, and remain attached until they are brought into the new host nest.…”