Abstract
Crustaceans have successfully adapted to a variety of environments including fresh- and saltwater as well as land. Transition from an aquatic to a terrestrial lifestyle required adaptations of the sensory equipment of an animal, particularly in olfaction, where the stimulus itself changes from hydrophilic to mainly hydrophobic, air-borne molecules. Hermit crabs Coenobita spp. (Anomura, Coenobitidae) have adapted to a fully terrestrial lifestyle as adults and have been shown to rely on olfaction in order to detect distant food items. We observed that the specialized olfactory sensilla in Coenobita, named aesthetascs, are immersed in a layer of mucous-like substance. We hypothesized that the mucous is produced by antennal glands and affects functioning of the aesthetascs.Using various microscopic and histochemical techniques we proved that the mucous is produced by aesthetasc-associated epidermal glands, which we consider to be modified rosette-type aesthetasc tegumental glands known from aquatic decapods. These epidermal glands in Coenobita are multicellular exocrine organs of the recto-canal type with tubulo-acinar arrangement of the secretory cells. Two distinct populations of secretory cells were clearly distinguishable with light and electron microscopy. At least part of the secretory cells contains specific enzymes, CUB-serine proteases, which are likely to be secreted on the surface of the aesthetasc pad and take part in antimicrobial defense. Proteomic analysis of the glandular tissue corroborates the idea that the secretions of the aesthetasc-associated epidermal glands are involved in immune responses.We propose that the mucous covering the aesthetascs in Coenobita takes part in antimicrobial defense and at the same time provides the moisture essential for odor perception in terrestrial hermit crabs. We conclude that the morphological modifications of the aesthetasc-associated epidermal glands as well as the functional characteristics of their secretions are important adaptations to a terrestrial lifestyle.
Highlights
Among hermit crabs (Decapoda, Anomura), Coenobitidae represents a perfect model to study the impact of terrestrialization on the structure and function of the olfactory system in invertebrates
In Coenobita, we identified CUB-immunoreactivity in the enlargements formed by the sheath cells surrounding the dendrites of the olfactory sensory neurons
The innate immune system is usually represented by its humoral and cellular components, so we find the need of a specialized structure, such as antennular epidermal glands producing a particular type of serine proteases in several crustacean species, is very remarkable
Summary
Among hermit crabs (Decapoda, Anomura), Coenobitidae represents a perfect model to study the impact of terrestrialization on the structure and function of the olfactory system in invertebrates. From their earliest appearance in coastal habitats, which was 20 Mya according to the fossil record [1,2], coenobitids have adapted to a fully terrestrial lifestyle as adults [3]. Numerous openings in the cuticle closely associated with the aesthetascs have been found in marine decapods [13] These pores were identified as openings of epidermal exocrine glands, referred to as aesthetasc tegumental glands in Panulirus argus (Latreille, 1804), here abbreviated as ATGs [13]. CUB possesses four conserved cysteine residues, which form two disulfide bridges [15,16]
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