Insect-like olfactory adaptations in the terrestrial giant robber crab.

The robber crab (Birgus latro), also known as the coconut crab, is the world's largest land-living arthropod, with a weight reaching 4 kg and a length of over half a meter. Apart from the marine larval stage, this crab is fully terrestrial, and will actually drown if submerged in water. A transition from sea to land raises dramatically new demands on the sensory equipment of an animal. In olfaction, the stimulus changes from hydrophilic molecules in aqueous solution to mainly hydrophobic in the gaseous phase. The olfactory system of land crabs thus represents an excellent opportunity for investigating the effects of the transition from sea to land. Have land crabs come to the same solutions as other terrestrial animals, or is their olfactory sense characterized by unique innovations? Here, we show that the robber crab has evolved an olfactory sense with a high degree of resemblance to the insect system. The similarities extend to physiological, behavioral, and morphological characters. The insect nose of the robber crab is a striking example of convergent evolution and nicely illustrates how similar selection pressures result in similar adaptation.

A review of feeding and nutrition of herbivorous land crabs: adaptations to low quality plant diets.

This paper reviews the nutritional ecology, the digestive physiology, and biochemistry of herbivorous land crabs and the adaptations that they possess towards a diet of plant material. Land crab species that breathe air and forage out of water can be divided into three feeding specialisations: primarily carnivorous, deposit feeders feeding on micro-organisms and organic matter in the sediment, and herbivores consuming mainly plant material and its detritus. The last forms the focus of this review. The diets of the herbivores are low in nitrogen and high in carbon, are difficult to digest since they contain cellulose and hemicellulose, and may disrupt digestion due to the presence of tannins. Herbivorous crustaceans are able to efficiently utilise plant material as their primary nutrient source and are indeed able to meet their nitrogen requirements from it. Herbivorous land crabs display a range of adaptations towards a low nitrogen intake and these are discussed in this review. They also appear to endogenously produce cellulase and hemicellulase enzymes for the digestion of cellulose and hemicellulose. Generalised and specific adaptations allow them to inhibit the potentially negative digestive effects of tannins. To digest plant material, they possess a plastic digestive strategy of high food intake, short retention time, high assimilation of cell contents, and substantial digestion of cellulose and hemicellulose.

Endogenous production of endo-beta-1,4-glucanase by decapod crustaceans.

The potential ability to produce cellulase enzymes endogenously was examined in decapods crustaceans including the herbivorous gecarcinid land crabs Gecarcoidea natalis and Discoplax hirtipes, the amphibious freshwater crab Austrothelphusa transversa, the terrestrial hermit crab, Coenobita variabilis the parastacid crayfish Euastacus, and the crayfish Cherax destructor. The midgut gland of both G. natalis and D. hirtipes contained substantial total cellulase activities and activities of the cellulase enzymes endo-beta-1,4-glucanase and beta-glucosidase. With the exception of total cellulase and beta-glucosidase from D. hirtipes, the enzyme activities within the midgut gland were higher than those within the digestive juice. Hence, the enzyme activities appear to reside predominantly within midgut gland, providing indirect evidence for endogenous synthesis of cellulase enzymes by this tissue. A 900 bp cDNA fragment encoding a portion of the endo-beta-1,4-glucanase amino acid sequence was amplified by RT-PCR using RNA isolated from the midgut gland of C. destructor, Euastacus, A. transversa and C. variabilis. This provided direct evidence for the endogenous production of endo-beta-1,4-glucanase. The 900 bp fragment was also amplified from genomic DNA isolated from the skeletal muscle of G. natalis and D. hirtipes, clearly indicating that the gene encoding endo-beta-1,4-glucanase is also present in these two species. As this group of evolutionary diverse crustacean species possesses and expresses the endo-beta-1,4-glucanase gene it is likely that decapod crustaceans generally produce cellulases endogenously and are able to digest cellulose.

The morphology and vasculature of the lungs and gills of the soldier crab, Mictyris longicarpus.

The five gill pairs of Mictyris longicarpus have the lowest weight specific area reported for any crab. The cuticle of the gill lamellae is lined with epithelial cells which have structural features characteristic of iontransporting cells. Pillar cells are regularly distributed in the epithelium and serve to maintain separation of the two faces of the lamellae. The central hemolymph space is divided into two sheets by a fenestrated septum of connective tissue cells. The dorsal portion of the marginal canal of each lamella receives hemolymph from the afferent branchial vessel and distributes it to the lamella while the ventral portion of the canal collects hemolymph and returns it to the efferent branchial vessel. The lung is formed from the inner lining of the branchiostegite and an outgrowth of this, the epibranchial membrane. Surface area is increased by invagination of the lining which forms branching, blind-ending pores, giving the lung a spongy appearance. The cuticle lining the lung is thin and the underlyng epithelial cells are extremely attenuated, giving a total hemolymph/gas distance of 90-475 nm. Venous hemolymph is directed close to the gas exchange surface by specialised connective tissue cells and by thin strands of connective tissue which run parallel to the cuticle. Air sacs are anchored in position by paired pillar cells filled with microtubules. Afferent hemolymph is supplied from the eye sinus, dorsal sinus, and ventral sinus. Afferent vessels interdigitate closely with efferent vessels just beneath the respiratory membrane. The two systems are connected by a "perpendicular system" which ramifies between the airways and emerges to form a sinus beneath the carapace and then flows back between the air sacs to the efferent vessels. The afferent side of the perpendicular system is the major site of gas exchange. Efferent vessels return via large pulmonary veins to the pericardial cavity. Pa O2 levels were high (95.5 Torr), indicating highly efficient gas exchange.

Intracellular purine deposits in the gecarcinid land crab Gecarcoidea natalis.

The terrestrial crab Gecarcoidea natalis stores large amounts of purine in the body. The major component of the purine deposits is urate (85% of the total purines). The other 15% is comprised of hypoxanthine, guanine, and xanthine. Microscopy studies reveal that these urate deposits are located intracellularly in spongy connective tissue cells throughout the body. Urate exists as numerous membrane-bound crystals 1 µm in diameter. Vesicles thought to represent urate vesicles at various stages of development are also present in the cytoplasm of the cell. Few organelles are visible in the urate storage cells, and it is unlikely that the urate is synthesized on site. Crabs (N = 2) fed a high-nitrogen diet have greater numbers of urate storage cells at more connective tissue sites, and the cells are larger (36.3 ± 1.8 µm (mean ± SE) and 44.0 ± 1.4 µm (mean ± SE)) and contain more urate than urate storage cells in animals collected from the field (N = 3) or maintained in the laboratory on a low-nitrogen diet (N = 1). The mean diameter of urate storage cells in animals fed a diet low in nitrogen and field-collected animals ranges from (13.5 ± 0.5 µm (SE) - 22.3 ± 1.0 µm (SE)). This histological study supports a strong correlation between purine accumulation and the nitrogen content of the diet. J. Morphol. 231:101-110, 1997. © 1997 Wiley-Liss, Inc.

The venous system of the terrestrial crab Ocypode cordimanus (Desmarest 1825) with particular reference to the vasculature of the lungs.

The respiratory system of Ocypode cordimanus consists of seven pairs of gills, modified for aerial gas exchange, and a single pair of lungs. Each lung is formed from the inner surface of the branchiostegite and the thoracic wall of the branchial chamber. The branchiostegal surface is increased by a fleshy infolding, the branchiostegal shelf, whilst the surface area of the thoracic lung wall is enhanced by a large flaplike fold. The anatomy of the major sinus systems and the vascular supply to the lungs were investigated. Venous hemolymph is supplied to the lungs potentially from all the major body sinuses. The dorsal, ventral, hepatic, and infrabranchial sinuses are all connected anteriorly to the two eye sinuses which distribute hemolymph to the lungs. Each eye sinus gives off five branches to the branchiostegal lung surface and one to the thoracic lung wall. These afferent vessels are highly branched and interdigitate closely with efferent vessels. The two systems are connected by flat lacunae lying just beneath the respiratory epithelium and these are believed to be the site of gas exchange. The efferent vessels empty into two pulmonary veins on each side, one serving the branchiostegal lung wall and the other the thoracic wall. The two vessels on each side fuse before joining the pericardial cavity as a single trunk on each side.

Presence and properties of cellulase and hemicellulase enzymes of the gecarcinid land crabs Gecarcoidea natalis and Discoplax hirtipes.

Digestive juice from the herbivorous gecarcinid land crabs Gecarcoidea natalis and Discoplax hirtipes exhibited total cellulase activity and activities of two cellulase enzymes; endo-beta-1,4-glucanase and beta-1,4-glucosidase. These enzymes hydrolysed native cellulose to glucose. The digestive juice of both species also contained laminarinase, licheninase and xylanase, which hydrolysed laminarin, lichenin and xylan, respectively, to component sugars. The pH optima of beta-1,4-glucosidase, endo-beta-1,4-glucanase and total cellulase from G. natalis were 4-5.5, 5.5 and 5.5-7, respectively. In the digestive juice from D. hirtipes, the corresponding values were 4-7, 5.5-7 and 4-9, respectively. The pH of the digestive juice was 6.69+/-0.03 for G. natalis and 6.03+/-0.04 for D. hirtipes and it is likely that the cellulases operate near maximally in vivo. In G. natalis, total cellulase activity and endo-beta-1,4-glucanase activity were higher than in D. hirtipes, and the former species can thus hydrolyse cellulose more rapidly. beta-1,4-glucosidase from G. natalis was inhibited less by glucono-d-lactone (K(i)=11.12 mmol l(-1)) than was the beta-1,4-glucosidase from D. hirtipes (K(i)=4.53 mmol l(-1)). The greater resistance to inhibition by the beta-1,4-glucosidase from G. natalis may contribute to the efficiency of the cellulase system in vivo by counteracting the effects of product inhibition and possibly dietary tannins. The activity of beta-1,4-glucosidase in the digestive juice of D. hirtipes was higher than that of G. natalis.

Land crabs with smooth lungs: Grapsidae, Gecarcinidae, and Sundathelphusidae ultrastructure and vasculature.

The highly terrestrial grapsids and gecarcinids and the amphibious sundathelphusids all have large, expanded branchial chambers. The lining of the branchial chambers is smooth and well vascularized, and it functions as a lung. The respiratory membrane and the cuticle lining the lung are extremely thin (200-350 nm). The blood vessels within the lung are formed from connective tissue cells supported by collagen fibres and lined by a basal lamina. The major vessels in the lung are embedded deep in the branchiostegite and lie just beneath the thick outer carapace. These vessels branch towards the respiratory membrane, where they eventually lose their connective tissue coverings to form thin, flattened lacunae directly below the respiratory epithelium. The lacunae (exchange sites) are bordered by specialized connective tissue cells, which either bear microvilli on their apical surface (fimbriated cells) or are very smooth. The respiratory circulation in the lung is very complex, with two portal systems present between the afferent and efferent systems, producing a total of three lacunal exchange beds. Portal systems increase the surface area available for gas exchange. The major distributing vessel in the lung is the branchiostegal vein, which runs along the inner margin of the branchiostegite. The main venous supplies come anteriorly from the infraorbital and ventral sinuses and posteriorly from the procardial sinus. The main collecting vessel is the pulmonary vein, which arises anteriorly and which runs around the ventral perimeter of the branchiostegite before emptying into the pericardial sinus. © 1993 Wiley-Liss, Inc.

Dietary assimilation and the digestive strategy of the omnivorous anomuran land crab Birgus latro (Coenobitidae).

On Christmas Island, Indian Ocean, the diet of robber crabs, Birgus latro (Linnaeus) was generally high in fat, storage polysaccharides or protein and largely comprised fruits, seeds, nuts and animal material. The plant items also contained significant amounts of hemicellulose and cellulose. In laboratory feeding trials, crabs had similar intakes of dry matter when fed artificial diets high in either fat or storage polysaccharide, but intake was lower on a high protein diet. Assimilation coefficients of dry matter (69-74%), carbon (72-81%), nitrogen (76-100%), lipid (71-96%) and storage polysaccharide (89-99%) were high on all three diets. B. latro also assimilated significant amounts of the chitin ingested in the high protein diet ( 93%) and hemicellulose (49.6-65%) and cellulose (16-53%) from the high carbohydrate and high fat diets. This is consistent with the presence of chitinase, hemicellulase and cellulase enzymes in the digestive tract of B. latro. The mean retention time (27.2 h) for a dietary particle marker ((57)Co-labelled microspheres) was longer than measured in leaf-eating land crabs. The feeding strategy of B. latro involves the selection of highly digestible and nutrient-rich plant and animal material and retention of the digesta for a period long enough to allow extensive exploitation of storage carbohydrates, lipids, protein and significant amounts of structural carbohydrates (hemicellulose, cellulose and chitin).