Physiological Ecology of the Mud-Burrowing Shrimp, Calocaris macandreae Bell

Several species of thalassinid shrimp are found in the U.K., all of which construct burrows in muddy sediments of the intertidal or sublittoral. The most abundant species in Scottish west coast waters is the axiid Calocaris macandreae Bell, which burrows in soft mud from 10 to several hundred metres water depth. Previous studies have indicated that oxygen availability within the burrows of other burrowing decapods is limited. A study was made of Calocaris macandreae, in particular of the respiratory environment of the burrows, the behaviour associated with burrowing and of the respiratory physiology and metabolism of this species. In addition, literature information concerning other Thalassinidea was reviewed. The structure and distribution of Calocaris burrows was investigated in the field using diving-based methods. Burrows were mapped and polyester resin-casts were made. Burrows constructed by Calocaris in sediment columns in laboratory aquaria were also examined. Oxygen tensions in burrows constructed by animals kept in laboratory aquaria were determined, and showed that respiratory conditions in burrows may be permanently and severely hypoxic, with oxygen tensions as low as 15 Torr recorded in the deeper levels of a burrow. The range of burrow forms constructed by thalassinid species was reviewed with regard to possible functions of a burrow. The behaviour patterns shown by Calocaris macandreae in laboratory burrows were analysed using video recordings. In general, Calocaris has a behavioural regime characterised by low levels of activity. Burrow irrigation by pleopod beating was infrequent and of short duration in 'normal' conditions, but increased during experimental depletion of oxygen tension in the overlying water column. The branchial morphology of seven thalassinid species (from the U.K. ) were compared using scanning electron microscopy. A range of gill formulae and gill anatomy was observed, with a trend towards simplification of the gill formula and a phyllobranchiate gill structure in Upogebia and Callianassa. In addition, the surface area of the gills of Calocaris macandreae was determined to be relatively small compared to other, more active decapods. In view of the hypoxic conditions encountered by Calocaris macandreae, an investigation of respiratory physiology in this species was made. Open and closed respirometry techniques showed that the rate of oxygen consumption by Calocaris is low compared to that of most other decapods (but similar to those recorded for other thalassinids). However, oxygen consumption is maintained at a constant rate even at very low oxygen tensions (the 'Pc' varied between 10 and 20 Torr). Measurement of heart and scaphognathite rates using an impedance technique showed that hyperventilation is a consistent response to environmental hypoxia, although there was no response of heart rate. Comparative data from the literature suggest that adaptive responses of the haemolymph oxygen transport system may be a major component of adaptation to hypoxia in Crustacea. The respiratory pigment of Calocaris macandreae (and other thalassinids reported in the literature) has a larger molecular weight haemocyanin than those of other Crustacea (as determined by gel filtration), although the subunit molecular weight is similar. The concentration of haemocyanin in the haemolymph is comparatively low, resulting in a low oxygen carrying capacity (thought to be related to low activity levels). The oxygen affinity of the haemocyanin was studied using a diffusion chamber system. The haemocyanin oxygen affinity is exceptionally high in Calocaris macandreae (P50 as low as 1.8 Torr under in vivo conditions), probably resulting in efficient oxygen transport to the tissues even in severe hypoxia. However, there is little evidence for modulation of oxygen affinity. The functional significance of modulation of haemocyanin oxygen affinity in Calocaris and other decapods is discussed. In conclusion, both comparative and functional approaches were used to interpret the ecological physiology of Calocaris macandreae. An integrated suite of behavioural, physiological and metabolic characteristics represent adaptation to low activity levels and to the hypoxic burrow environment.