Evidence of a thoracic crop in workers, soldiers, and queens of Carebara perpusilla ants (Formicidae: Myrmicinae).

The ability to share and store food is paramount in group-living animals, allowing a finely tuned distribution of resources over time and individuals and an enhanced survival over periods of food scarcity. Ants have several ways to store food: one of them is their gastral crop, also known as a "social stomach." Nutrients in the crop can be regurgitated to nestmates through oral trophallaxis (mouth-to-mouth) or proceed to the midgut by opening the proventriculus, a valve connecting the crop to the midgut. However, some ants are also known to have a so-called "thoracic crop," an extension of the esophagus that allows for additional storage space. In this study, we provide the first evidence of a thoracic crop in the genus Carebara, in reproductive (queen) and sterile (soldier and worker) castes. We discuss how the ant body plan allowed for the evolution of a novel food storage structure in the mesothorax.

The loss of flight in ant workers enabled an evolutionary redesign of the thorax for ground labour.

BACKGROUND: Explanations for the ecological dominance of ants generally focus on the benefits of division of labour and cooperation during foraging. However, the principal innovation of ants relative to their wasp ancestors was the evolution of a new phenotype: a wingless worker caste optimized for ground labour. Ant workers are famous for their ability to lift and carry heavy loads, but we know surprisingly little about the morphological basis of their strength. Here we examine the consequences of the universal loss of flight in ant workers on skeletomuscular adaptations in the thorax for enhanced foraging on six legs. RESULTS: Using X-ray microcomputed tomography and 3D segmentation, we compared winged queens and wingless workers in Euponera sikorae (subfamily Ponerinae) and Cataglyphis savignyi (subfamily Formicinae). Workers are characterized by five major changes to their thorax: i) fusion of the articulated flight thorax (queens) into a rigid box optimized to support the muscles that operate the head, legs and abdomen, ii) redesign of internal cuticular structures for better bracing and muscle attachment, iii) substantial enlargement of the neck muscles for suspending and moving the head, iv) lengthening of the external trochanter muscles, predominant for the leg actions that lift the body off the ground, v) modified angle of the petiole muscles that are key for flexion of the abdomen. We measured volumes and pennation angles for a few key muscles to assess their increased efficacy. Our comparisons of additional workers across five genera in subfamilies Dorylinae and Myrmicinae show these modifications in the wingless thorax to be consistent. In contrast, a mutillid wasp showed a different pattern of muscle adaptations resulting from the lack of wing muscles. CONCLUSIONS: Rather than simply a subtraction of costly flight muscles, we propose the ant worker thorax evolved into a power core underlying stronger mandibles, legs, and sting. This contrasts with solitary flightless insects where the lack of central place foraging generated distinct selective pressures for rearranging the thorax. Stronger emphasis is needed on morphological innovations of social insects to further our understanding of the evolution of social behaviours.

Skeletomuscular adaptations of head and legs of Melissotarsus ants for tunnelling through living wood.

BACKGROUND: While thousands of ant species are arboreal, very few are able to chew and tunnel through living wood. Ants of the genus Melissotarsus (subfamily Myrmicinae) inhabit tunnel systems excavated under the bark of living trees, where they keep large numbers of symbiotic armoured scale insects (family Diaspididae). Construction of these tunnels by chewing through healthy wood requires tremendous power, but the adaptations that give Melissotarsus these abilities are unclear. Here, we investigate the morphology of the musculoskeletal system of Melissotarsus using histology, scanning electron microscopy, X-ray spectrometry, X-ray microcomputed tomography (micro-CT), and 3D modelling. RESULTS: Both the head and legs of Melissotarsus workers contain novel skeletomuscular adaptations to increase their ability to tunnel through living wood. The head is greatly enlarged dorsoventrally, with large mandibular closer muscles occupying most of the dorsal half of the head cavity, while ventrally-located opener muscles are also exceptionally large. This differs from the strong closing: opening asymmetry typical of most mandibulated animals, where closing the mandibles requires more force than opening. Furthermore, the mandibles are short and cone-shaped with a wide articulatory base that concentrates the force generated by the muscles towards the tips. The increased distance between the axis of mandibular rotation and the points of muscle insertion provides a mechanical advantage that amplifies the force from the closer and opener muscles. We suggest that the uncommonly strong opening action is required to move away crushed plant tissues during tunnelling and allow a steady forward motion. X-ray spectrometry showed that the tip of the mandibles is reinforced with zinc. Workers in this genus have aberrant legs, including mid- and hindlegs with hypertrophied coxae and stout basitarsi equipped with peg-like setae, and midleg femura pointed upward and close to the body. This unusual design famously prevents them from standing and walking on a normal two-dimensional surface. We reinterpret these unique traits as modifications to brace the body during tunnelling rather than locomotion per se. CONCLUSIONS: Melissotarsus represents an extraordinary case study of how the adaptation to - and indeed engineering of - a novel ecological niche can lead to the evolutionary redesign of core biomechanical systems.

Minute workers and large soldiers in the subterranean ant Carebara perpusilla: Musculoskeletal consequences of Haller's rule in the thorax.

Many organismal traits vary with body size, often reflecting trade-offs in the face of size-dependent constraints. For example, Haller's rule, the allometric pattern whereby smaller organisms have proportionally larger brains, can have carry-on effects on head design as the brain competes for space with other structures. Ant species with polymorphic worker castes are interesting cases for helping us understand these allometric effects. Here, we examine the effects of miniaturization on the ant power core, the mesosoma (thorax), with particular attention to how the scaling of nervous system structures affects the skeletomuscular elements involved with load bearing and locomotion. Using X-ray computed microtomography (microCT), we studied the thorax of Carebara perpusilla, an African ant species that has minute workers (1.5 mm-long) and larger soldiers (3.0 mm-long), allowing strong intraspecific comparisons. We find that the thoracic nervous system is relatively larger in minute workers, similar to Haller's rule, with consequences on the skeletomuscular organisation. Minute workers have relatively smaller petiole muscles and indirect head muscles, but relatively larger external trochanter muscles and direct head muscles. We link these allometric trade-offs to miniaturization and division of labor, and discuss how thorax design underlies the success of minute ants.

The basitarsal sulcus gland, a novel exocrine structure in ants.

The basitarsus of the mid- and/or hindlegs of several Amblyoponinae ants shows a deep longitudinal groove or sulcus on its anterior face in workers and queens. Histological examination reveals this sulcus is associated with a conspicuous novel epithelial gland, which brings the number of exocrine glands in the legs of ants to 25. The ultrastructural characteristics of the gland show the presence of a well-developed smooth endoplasmic reticulum. This is indicative for the elaboration of a non-proteinaceous and thus possibly pheromonal secretion. Behavioural observations show that this secretion is collected by the tarsomeres and spread onto the brood and nest, suggesting a role in nestmate recognition. A similar basitarsal sulcus gland was also found in Nothomyrmecia, Paraponera and Tetraponera, which represents both a wide phylogenetic and ecological distribution, as it includes arboreal, ground-dwelling as well as subterranean taxa.

Boat noise prevents soundscape-based habitat selection by coral planulae.

Understanding the relationship between coral reef condition and recruitment potential is vital for the development of effective management strategies that maintain coral cover and biodiversity. Coral larvae (planulae) have been shown to use certain sensory cues to orient towards settlement habitats (e.g. the odour of live crustose coralline algae - CCA). However, the influence of auditory cues on coral recruitment, and any effect of anthropogenic noise on this process, remain largely unknown. Here, we determined the effect of protected reef (MPA), exploited reef (non-MPA) soundscapes, and a source of anthropogenic noise (boat) on the habitat preference for live CCA over dead CCA in the planula of two common Indo-Pacific coral species (Pocillopora damicornis and Acropora cytherea). Soundscapes from protected reefs significantly increased the phonotaxis of planulae of both species towards live CCA, especially when compared to boat noise. Boat noise playback prevented this preferential selection of live CCA as a settlement substrate. These results suggest that sources of anthropogenic noise such as motor boat can disrupt the settlement behaviours of coral planulae. Acoustic cues should be accounted for when developing management strategies aimed at maximizing larval recruitment to coral reefs.