Gill-cleaning Mechanisms of Paratya Curvirostris (Caridea: Atyidae) and Comparisons With Seven Species of Japanese Atyid Shrimps

Abstract

Fresh-water atyid shrimps are an ancient group of carideans that uses passive cleaning mechanisms to protect their gills from fouling. We studied gill cleaning in Paratya curvirostris from New Zealand, and P. compressa, Caridina japonica, C. typus, C. leucosticta, C. serratirostris, Neocaridina denticulata, and Atyopsis spinipes from Japan. Gill cleaning in atyids involves epipod-setobranch complexes, associated with their pereiopods, and multidenticulate setae on the posterior end of the scaphognathite. Multidenticulate scaphognathite setae are particularly well developed in atyids and show a negative correlation with the number of setobranch setae in different species. At one extreme is A. spinipes, lacking setobranch setae but having the largest number of multidenticulate scaphognathite setae, which are relatively longer and have the maximum number of digitate scale setules. At the other extreme are P. curvirostris and P. compressa, with the largest number of setobranch setae but the smallest number of multidenticulate scaphognathite setae, which are relatively shorter and have a smaller number of digitate scale setules. In atyids, there is a compromise between these two gill-cleaning mechanisms. Mapping gill types and gill-cleaning mechanisms on a decapod cladogram suggests that phyllobranchiate gills represent a convergent derived state that evolved independently from trichobranchiate ancestors, in carideans, thalassinids, anomalans, and brachyurans. There are no particular associations between the type of gills and the mechanism used to clean them. Active gill cleaning, using pereiopods, has evolved independently in several lines. If the primitive gill-cleaning mechanism is setiferous epipods, then epipod-setobranch complexes must have been independently derived in carideans and the astacid-thalassinid group. Multidenticulate scaphognathite setae occur with both setiferous epipods and epipod-setobranch complexes. The multidenticulate scaphognathite setae may be the ancestral state for the Pleocyemata, or a synapomorphy of the Caridea, and the Homarida-Astacida-Thalassinida-Brachyura group, having been lost in the Anomala which have active gill cleaning. Atyids are an ancient group of fresh-water shrimps widespread throughout the tropics, with a few species penetrating cooler regions (Ortmann, 1894; Fryer, 1977; Hung et al., 1993). Their diverse habitats include estuaries, ponds, lakes, swift mountain streams, and caves. In all these habitats atyid shrimps are exposed to harmful debris and the attacks of fouling organisms. It is, therefore, necessary for them to clean their body surface and especially the antennae, gills, and embryos. Though cleaning mechanisms are diverse among different species, crustacean decapods generally clean their antenna using the endopodite of the third maxillipeds, the thoracic body and gills using the first, second, and fifth pereiopods or epipodite of the third maxillipeds, and the abdomen and telson using the fifth pereiopods (Bauer, 1975, 1977, 1978, 1979, 1981, 1989; Felgenhauer and Schram, 1978, 1979; Pohle, 1989b; Read et al., 1991). In all decapods, the gills are flushed regularly by the pumping action of the scaphognathite of the second maxilla. Water enters the gill chamber near the posterior thoracopods and exits through the oral region. This respiratory current brings harmful debris and fouling organisms to the gill chamber. The branchiostegite not only protects the gills, but also provides a sheltered habitat for other organisms. A number of gill-cleaning mechanisms have evolved to prevent settlement of fouling organisms (Bauer, 1979; Ritchie and H0eg, 1981; Fleischer et al., 1992). Decapod gills are cleaned by up to four major kinds of appendages: the thoracic epipods with compound setae are mainly used in penaeids, nephropids, palinurids, and brachyurans; the pereiopods in carideans, stenopodids, thalassinids, and anomurans; the epipod-setobranch complex in carideans or setobranchs only in axiids and astacids; and scaphognathite setae (reviewed in Bauer, 1981, 1989). Reversal of the respiratory current also cleans