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The Structure and Calcification of the Crustacean Cuticle1

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The Structure and Calcification of the Crustacean Cuticle1 Amer. Zool., 24:893-909 (1984) The Structure and Calcification of the Crustacean Cuticle1 Robert Roer and Richard Dillaman Institute of Marine Biomedical Research, Universityof North Carolina at Wilmington, Wilmington,North Carolina 28403 Synopsis. The integument of decapod crustaceans consists of an outer epicuticle, an exocuticle, an endocuticle and an inner membranous layer underlain by the hypodermis. The outer three layers of the cuticle are calcified. The mineral is in the form of calcite crystals and amorphous calcium carbonate. In the epicuticle, mineral is in the form of spherulitic calcite islands surrounded by the lipid-protein matrix. In the exo- and endo- cuticles the calcite crystal aggregates are interspersed with chitin-protein fibers which are organized in lamellae. In some species, the organization of the mineral mirrors that of the organic fibers, but such is not the case in certain cuticular regions in the xanthid crabs. Thus, control of crystal organization is a complex phenomenon unrelated to the gross morphology of the matrix. Since the cuticle is periodically molted to allow for growth, this necessitates a bidirec- tional movement of calcium into the cuticle during postmolt and out during premolt resorption of the cuticle. In two species of crabs studied to date, these movements are accomplished by active transport effected by a Ca-ATPase and Na/Ca exchange mech? anism. The epi- and exocuticular layers of the new cuticle are elaborated during premolt but do not calcify until the old cuticle is shed. This phenomenon also occurs in vitro in cuticle devoid of living tissue and implies an alteration of the nucleating sites of the cuticle in the course of the molt. Introduction within the matrix and mechanisms for con? While the crustacean cuticle has been trol or cessation of crystal growth. The crustacean cuticle has a rich the subject of study for over 250 years provided source of information with to each (Reaumur, 1712, in Drach, 1939), the focus respect of these central In addition, the of those investigations has generally been questions. Crustacea offer some for concerned with the process of molting. Our unique problems those interested in biomineralization. approach will be slightly different; we will deal with the exoskeleton of the Crustacea Since the mineralized exoskeleton ofthe Crustacea is to as a mineralized tissue that is made partic? subjected periodic molting, bidirectional net movement of mineral ularly interesting by the fact that its struc? different of the molt is ture is affected by a cyclic molting process. during stages cycle This situation is in con? When investigating any mineralized tis? necessary. sharp trast to other in which sue, one must address some basic problems: calcifying systems net or 1) the chemical nature and crystalline form accretionary growth patterns slightly are the rule. Further? of the mineral; 2) the nature and form of shifting equilibria more, crustaceans demonstrate drastic the organic matrix; 3) the relationship differences within the same tissue between the organic and inorganic com? temporal with to the extent of and ponents of the tissue and the influence of regard capacity for mineralization. Such differ? the matrix on crystal morphology; 4) the temporal ences, marked and discrete tran? sources of mineral for deposition; 5) the by rapid sitions, allow one to ask and pathways for mineral movement into or very specific answerable about the control of out from the mineralized structures; 6) questions nucleation and mineralization. rates of mineral deposition; and 7) the nature and location of nucleation sites The subject of crustacean cuticles is as diverse as is the taxon and, hence, an ency- clopedic overview is impossible. We will restrict our review, in to the 1 From the on Mechanisms large part, Symposium of Calcification crustaceans in Biological Systemspresented at the Annual Meeting decapod although examples from other orders will serve to remind us ofthe American Society of Zoologists, 27-30 Decem? ber 1983, at Philadelphia, Pennsylvania. ofthe hazards of sweeping generalizations. 893 894 R. Roer and R. Dillaman Structure of the Decapod im ] Ep 5, Integument Basic cuticular structure The integument of the decapod Crus? tacea is, in general, comprised of a rigid exoskeleton or cuticle underlain by the cel? Ex 65pm lular hypodermis (Richards, 1951). The cuticle is not homogeneous, but contains 2.2Hm/l four discrete layers. Despite the fact that this observation was made more than a cen? tury ago (Williamson, 1860) and has been the subject of numerous subsequent stud? ies, the nomenclature of the four layers of the cuticle varies from author to author. The terminology of Travis (1963), how? ever, has come to be widely accepted and will be used exclusively in the present work. These layers from the most external to the 'V-> most internal are: the epicuticle, the exo- cuticle, the endocuticle and the membra- nous layer (Fig. 1). The epicuticle is the outermost and thin- nest ofthe cuticle. It consists of tanned En 195pm layer lipoprotein impregnated with calcium salts It is bilaminar, with the 8.1 Hm/I (Travis, 1955a). basal layer pervaded by mineral-filled canals normal to the surface (Hegdahl et al, 1977c). The exocuticle immediately underlies the epicuticle. It is composed of chitin-protein fibers stacked in layers of continuously changing orientation (Travis, 1955a; Green and Neff, 1972). In Cancer pagurus 34% by weight of the organic component is chitin (Welinder, 19756). The exocuticle is hard- ened by quinone tanning and calcification (Travis, 1955a), with the mineral crystals situated between the fibers (Bouligand, 1970; Hegdahl etal, 19776). The endocuticle is the thickest and the most heavily calcified layer of the cuticle (Travis, 1955a, 1965). The endocuticle, like the is of hori? Fig. 1. Montage ofthe mineralized cuticular layers exocuticle, composed = of Carcinus maenas carapace (from Roer 1979). En zontal lamellae of chitin-protein fibers with Ex = = Num? endocuticle, exocuticle, Ep epicuticle. continuously changing orientation (Green bers the total thickness of the individual represent and Neff, 1972; etal, the and the thickness of endo- and exocuticular Hegdahl 1977a), layers material 73% chitin lamellae (1). organic being by weight in Cancer pagurus (Welinder, 19756). The endocuticle is apparently not tanned, but hardened solely by Ca salts (Travis, 1955?). Calcification in Crustacean Cuticle 895 The membranous layer is the innermost there are an estimated 150,000-220,000 layer of the cuticle and is in contact with pore canals per mm2 (Hegdahl et al, 1977a); the hypodermis. It consists of chitin and in Carcinus maenas there are about protein, the chitin representing 74% ofthe 950,000/mm2 (Roer, 1980); and Orconectes organic material in Cancer pagurus (Wel? virilis there are 50-90 pore canals ema- inder, 19756), but contains no mineral nating from each epithelial cell or about (Travis, 1955a). 4,000,000/mm2 (Travis, 1963). Thus, the The mineral in the outer three layers of cuticle is in close contact with the hypo? the cuticle is CaC03 in the form of calcite dermis at all levels and should be consid? or poorly crystalline, amorphous calcium ered living tissue. carbonate (Travis, 1963). The molt The hypodermis is heterogeneous, hav? cycle ing numerous cell types arranged in three Rather detailed accounts ofthe phenom? principal layers (Travis, 1955a, b, 1957, ena related to the molt cycle of the Crus? 1965). The layer in contact with the cuticle tacea come from the last century (Vitzou, and apparently responsible for its forma? 1882), but the first method for describing tion is the outer epithelial layer or the cuti? the molt cycle that could be applied to the cle secreting cells of Green and Neff (1972). Crustacea in general did not appear until The outer epithelial layer is one cell thick much later (Drach, 1939). According to and may range from squamous to colum? this method, the molt cycle is divided into nar as will be discussed below. Beneath the five stages (A-E), with further subdivisions outer epithelium is the sub-epithelial con? within each stage. Thus the postmolt period nective tissue layer (Travis, 1955a, 6) which corresponds to stages Al9 A2, Bb B2, Cl9 consists of oval reserve cells, blood sinuses C2, and C3; intermolt is stage C4; premolt with hemocytes, lipoprotein cells (Sewell, is comprised of stages D0, D/, D/', D/", 1955) and pigment cells (Green and Neff, D2, D3, and D4; and the act of ecdysis or 1972). Proximal to the connective tissue molting is stage E (Drach and Tchernigov- layer is the inner epithelium which is sim? tzeff, 1967). ilar to the outer epithelium but reduced in The intermolt size. The inner epithelium is bounded on integument its inner margin by a basement membrane Most adult decapods spend the majority with the exception of those regions cov? ofthe molt cycle in the intermolt condition ering the branchial chamber, where the (stage C4), molting only once or twice yearly inner epithelium elaborates a thin, non- (Passano, 1960). The cuticle has its four calcified cuticle resembling the outer epi? layers complete and is fully calcified (Fig. cuticle in other respects (Skinner, 1962). 2). The hypodermis is in its most reduced The cuticle is pervaded by vertically run? state at this time. The epithelial cells in ning pore canals first described by Valentin contact with the cuticle are extremely (1837, in Richards, 1951). Further exam? squamous (Green and Neff, 1972) having ination has revealed these to be cytoplas? a height of only 9 pm in Orconectes virilis mic extensions of the outer epithelial cells (Travis, 1965). The secretory activity of which emanate from the apical cell bor- the Golgi of the epithelial cells is at a min? ders, extend through the membranous imum (Chassard-Bouchaud and Hubert, layer, endocuticle and exocuticle, and ter? 1973; Hubert and Chassard-Bouchaud, minate at (Travis, 1963; Green and Neff, 1978) and the endoplasmic reticulum is 1972) or in (Hegdahl et al, 1977'c) the epi? reduced (Green and Neff, 1972).
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