The epithelial cells of crustacean gills
In addition to non-epithelial cells like fibroblasts, neurons,endothelial cells, glandular cells and ‘nephrocytes’, five
different cell types can be distinguished in the gill epithelium(Taylor and Taylor, 1992): thin cells, thick cells, flange cells,
attenuated cells and pilaster cells. This classification, however,is not exclusive, owing to intergradations and transitions between certain cell types.Thin cells are laterally expanded cells of 1 to 5 μm in height that form a squamous epithelium. They occur in all the gills of marine osmoconforming crabs, in the anterior gills of hyperosmoregulators like Carcinus maenas, Eriocheir sinensis and Callinectes sapidus, and in amphibious and terrestrial crabs(Copeland, 1968; Copeland and Fitzjarrell, 1968; Barra et al.,1983; Compère et al., 1989; Goodman and Cavey, 1990). In certain hyperosmoregulating species, thin cells also appear in the posterior gills near patches of thick cells (see below). Thin
cells appear to constitute a respiratory epithelium. However,they may also participate in other functions like ammonium
excretion (see below). In Holthusiana transversa, thin cells exhibiting apical and basolateral foldings associated with an
increased number of mitochondria line the surface of all gill lamellae (Taylor and Greenaway, 1979). Since H. transversa is a hyperosmoregulator, thin cells may play a role in both respiration and ion absorption.Thick cells are 10 to 20 μm in height. Their apical and basal surfaces are characterized by extensive membrane foldings associated with a large number of mitochondria (Copeland,1968; Copeland and Fitzjarrell, 1968; Compère et al., 1989; cf.Péqueux et al., 1989). Because extensive membrane infoldings in the form of leaflets or microvilli constitute a characteristic of ion transporting cells, thick cells are also termed ionocytes or osmoregulatory cells in crabs. In E. sinensis, thick cells dominate the posterior gills, and in such gills of other hyperregulators like C. maenas and C. sapidus, they form patches surrounded by thin cells (Goodman and Cavey, 1990). In some species,thick cells protrude into the hemolymph space and abut on thick cells projecting from the epithelium on the opposing side of the lamella, forming the so-called “thick pilaster cells” (Compère et al., 1989). Flange cells occur in the gills of lobsters, palaemonid and penaeid shrimps, and freshwater crayfish, where they have beentermed “pear cells” (Morse et al., 1970). Flange cells consist of a large, central perikaryon that protrudes into the hemolymph space making contact with the intralamellar septum, and thin,radial, apical extensions after which the cells are named. In crayfish gill filaments, the large perikarya of flange cells exhibit numerous, basolateral infoldings associated with mitochondria,while the apical membrane shows moderate surface amplification.Respiratory and transporting filaments have been distinguished in crayfish based on the different thickness of the epithelial cells (see below). In freshwater shrimps, like Macrobrachium olfersi and M. amazonicum, the apical membrane of the flange cells immediately below the thin cuticle (Fig. 12C)forms microvilli and leaflets (Figs. 12E and 13A) that become reduced or even disappear on acclimation to saline media(McNamara and Lima, 1997). Flange cells thus incorporate structural features of both the thin and thick cells of crabs, and thus may be considered as an interface undertaking both gas exchange and ion transport. Attenuated cells are flange cells with extremely thin flanges. In crabs and freshwater shrimps,they line the peripheral, marginal hemolymph canals of the gill lamellae.Pilaster cells, also called pillar cells, are found in crab gill lamellae and in the crayfish lamina, their most characteristic feature being an abundance of microtubules and desmosomallike tonofilaments at the basal cell surface. Two or more pilaster cells may span the entire hemolymph space across the lamella/lamina. They sustain the intralamellar septum in crab gill lamellae and limit deformation of the hemolymph space during changes in hydrostatic pressure. While the most simple pilaster cells may exert these structural functions exclusively, other pilaster cells show similarities with thick cells and flange cells and appear to be involved in ion transport. In E. sinensis, the V(H+)-ATPase, an important driving force for active NaCl absorption from freshwater, is located exclusively in the pilastercells (Putzenlechner et al., 1992; Putzenlechner, 1994; see also Fig. 11).
Fig. 1. Schematic representation of morphology and fine structure in a transporting, posterior crab gill. 1, Cuticle; 2, thick cell; 3, pilaster cell; 4, hemolymph space; 5,
intralamellar septum. The drawing (from Onken and Riestenpatt, 1998) is based on microscopic studies in Uca spp. In an anterior, respiratory gill the cuticle would be
lined with thin cells and thin pilaster cells. See text for further details.
Fig. 2. A summary and location diagram showing the general anatomy of the sixth, right posterior gill (A) and of a constituent gill lamella (B) in the freshwater shrimp
Macrobrachium olfersi. Hemolymph flows from the lateral efferent vessels (ev), through the outer marginal canals (mc), across the hemilamella (hl) by way of the gill
capillaries (gc) to the inner marginal canals, and back through the central afferent vessel (av). C, A cross-section of the hemilamella (between arrows in B) reveals the
lattice-like organization of the gill tissue, resulting from the semi-regular arrangement of opposing pillar cells (pc). The perikarya of the pillar cells are surrounded by
hemolymph spaces (hs) and abut the lateral regions of the median, intralamellar, septal cells (SC). The fine pillar cell flanges (pcf), in contact with the thin cuticle(c),
form the primary epithelial interface between the hemolymph and the external medium. Drawing from McNamara and Lima (1997).
2.1.2. Organization of phyllobranchiate crab gills In the phyllobranchiate gills of crabs (Fig. 1), the gill shaft is flattened and contains one afferent and one efferent vessel,respectively located at the dorsal and ventral margins. On the anterior and posterior sides of the gill shaft, the gill lamellae interconnect the two vessels. The lamellae are larger at the gill
base, becoming progressively smaller towards the tip that points upwards to the median part of the animal. Each lamella is formed by a single-layered epithelium covered by cuticle. The hemolymph space between the two epithelial cell layers
contains an intralamellar, cellular septum mechanically sustained by the pilaster cells. In the gills of osmoconforming
crabs, the epithelium is dominated by thin cells and by regularly spaced pilaster cells. In the posterior gills of hyperosmoregulating crabs, patches of thick cells and thick pilaster cells (Fig. 1)dominate the microanatomy
2.1.3. Organization of phyllobranchiate shrimp gills In the phyllobranchiate, pleurobranch gills of palaemonid shrimps (Fig. 2), one or more axes of symmetry may be present.In addition to bilateral symmetry along the dorso-ventral,longitudinal axis (Fig. 2A), also seen in crab gills, palaemonid shrimp gills are roughly symmetrical on both sides of the median anterior–posterior plane (Fig. 2A), where the hemolymph vessels insert. The gill shaft is flattened and contains one afferent and two efferent vessels connected via two rows of hemilamellae (Fig. 2B). The epithelium within the lamellae consists exclusively of pilaster cells with extensive apical flanges (Fig. 12A, B). The pillar cell bases frequently adjoin the
cells of the intralamellar septum that horizontally divides the lamella into two symmetrical compartments (Fig. 12A, B),
forming a system of lacunae (Fig. 12D) through which the
hemolymph courses during its passage across the lamella from
the afferent to the efferent marginal canal (Fig. 2C).
2.1.4. Organization of crayfish gills
Trichobranchiate crayfish gills consist of a cylindrical stem
that contains the afferent and efferent vessels, and bears numerous,
tubular filaments. The podobranch gills fuse with their
respective epipodites, forming wing-like laminae (Fig. 3) whose
epithelial structure resembles the organization of crab gills, with
pilaster cells sustaining the hemolymph space, although a
septum is absent. The tubular filaments contain the afferent and
efferent vessels, separated by a fine septum (Fig. 3), joining at
the tip of the filament. However, hemolymph may also flow
laterally via lacunae from the afferent to the efferent vessel.
Interesting specializations related to ion transport have arisen in
the gills of freshwater crayfish (Fig. 3 and below).
2.2. Gill functions associated with osmotic and ionic regulation
Crustacean gills are multifunctional organs. In addition to
their role in gas exchange (McMahon and Wilkens, 1983), gills
are essential for osmotic and ionic homeostasis (for comprehensive
reviews see Potts and Parry, 1964; Mantel and Farmer,
1983). In Crustacea that inhabit dilute seawater or freshwater,
active, transbranchial NaCl absorption constitutes one element
of the hyperosmoregulatory process while water excretion
comprises the other; both processes have been intensively
studied in many species (for reviews see Mantel and Farmer,
1983; Péqueux et al., 1989; Péqueux, 1995; Onken and
Riestenpatt, 1998; Kirschner, 2004). Although seldom investigated
and poorly understood, active NaCl secretion in
hyporegulating Crustacea from marine, estuarine or hypersaline
media also appears to be generated by the gills. Land crabs have