If/^Hrf /^Us<^^^ ^^^/^J the Amphibian Cutaneous Glands^: C/^ Some

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If/^Hrf /^Us<^^^ ^^^/^J the Amphibian Cutaneous Glands^: C/^ Some /i/^h\r^i/ if/^hrf /^us<^^^ //^Cn^4^ jf/Z'^ ^^^/^j The amphibian cutaneous glands^: C/^ ^2^e<r some aspects of their structure and adaptive role R. Brizzi', G. Delfino', S. Jantra', B.B. Alvarez^ D.M. Sever^ 1. Dip. di Biologia Animale e Genetica, Universita di Firenze, Via Romana 17, 50125 Firenze Italia 2. Dep. de Biologia, Facultad de Ciencias Exactas y Naturales y Agrimensura, Universidad Nacional del Nordeste, 9 de Julio 1449, 3400 Corrientes, Argentina 3. Dep. of Biology, Saint Mary's College, Notre Dame, IN 46556, USA Abstract This paper reviews the main characteristics of the cutaneous glands in two amphibian orders, Anura and Urodela, and provides indications on the most significative morphological and func• tional patterns. On the basis of structural and ultrastructural data, the skin glands can be distin• guished in four types: serous, mucous, mixed and lipid in nature. In addition, a prevalently top• ographical criterion, related to their diffuse or localized distribution on the body skin, permits to recognize ordinary and specialized cutaneous glands. These latter are essentially involved in defensive strategies or in fiinctions related to social communication and/or reproduction. Introduction The cutaneous apparatus plays a crucial role in the homeostasis of the Amphibia. Basically it exchanges substances as water, respiratory gas and salts, acting as interface between the organism and the external environment. In addition, a lot of specific func• tional roles may be referred to the different skin components, each exhibiting unicel• lular, multicellular or extracellular organization (see Duellman & Trueb, 1986; Fox, 1994). Among the cutaneous multicellular structures, noteworthy is the rich supply of exocrine glands, characterized by very different morphology and functions. In this paper are summarized the main morphological traits of the integumental glands and their ordinary or specialized roles. For the study we used skin strips of Anura and Urodela, and observed gland morphology, cytology and histochemistry using light (LM) and transmission (TEM) electron microscopes. In the lack of personal observa• tions, data on the third major group of amphibians, the caecilians, are not included in this repertory. Results and Discussion Ordinary cutaneous glands and their function With the term "ordinary" glands we define multicellular secretory structures widely scattered in the integument of the various body regions. On the basis of their structure, the amphibian glands are usually distinguished in four types: granular glands (also defined "serous" or "poison glands") (figs A-B), mucous glands (figs B, F), mixed 43 Herpetologia Candiana glands (fig. C) and lipid (or wax) glands (fig. D). Although the gland structural planes are homogeneous throughout the class, some differences exist between different taxa. In the anuran skin the secretory units of serous and lipid glands are syncytial, whereas discrete secretory cells form the mucous glands. In this order mixed glands are rare. An epithelial organization characterizes, on the contrary, the three gland types of the > urodeles (serous, mucous and mixed). In these amphibia lipid glands have not been, at the moment, specifically described. Usually the serous glands release a product in form of granules, that appear strongly eosinophilic at LM but very different in their structural and ultrastructural caracteris- tics according to the species. In this gland type, the term "serous" defines the nature of its fluid product, including bioactive peptides and amynes. The term "poison" glands indicates their possible antipredatory role. The toxic nature of serous secretions in many salamanders and frogs has led to assume that they are "poison glands" in all the amphibians, although this function seems to lack in some lineages (Neuwirth et al, 1979). According to other authors (Bachmayer et al., 1967; Barberio et al, 1987; Zasloff et al, 1988), the granular glands are involved in the production of substances aging as antimicrobical film over the body surface. However, the ancestral function of granular glands, probably involved in some forms of defense, regulative functions, storage, or all, is still an open question. The product of mucous glands is basophilic and usually PAS positive. The secretory cells (mucocytes) are orderly arranged around an obvious lumen (figs B, F). The mucous glands are involved in general functions as saline and gas exchange, as well as in regulation of water loss during terrestrial phases or in friction reduction during swimming. Mixed glands consist of a large granular portion and a smaller mucigenous acinus (fig. C). These are well distinguishable also on the basis of their different histochemical stain, typical of the two gland types. Mixed glands are a stable type in urodeles (Delfino et al., 1986), where they possibly represent an adaptation for the synergic pro• duction of both mucous and serous products. In anurans, on the contrary, these glands seem to correspond to a transitory stage in granular gland development (Duellman & Trueb, 1986) or restorafion (Delfino, 1980). Currently, lipid glands (fig. D) have been reported only in some hilids (Blaylock et al, 1976; Cei, 1980, Delfino et al, 1998), but we sfill consider them "ordinary glands" since in this family they are widely distributed over the skin. At LM wax glands show a relatively large lumen containing discrete secretory bodies which exhibit positive response in trials for lipids. Observed under TEM the wax glands reveal their syncy• tial nature and secretory aggregates consisting of heterogeneous material. Their secre• tion serves as a cutaneous lubrificant in the water, or reduces dehydration during the terrestrial life phases. ^ 44 Brizzi et al. Fig.A: Physalaemus biligonigerous. Ordinary serous gland observed under TEM. Bar = 5 |im; Fig.B: Triturus carnifex. Ordinary serous and mucous glands observed under LM. Bar = 200nm; Fig.C: Hydromantes genei. Note, in the mixed gland, the small mucous acinus inside the large serous portion (LM). Bar = 50 |im; Fig.D: Phyllomedusa hypocondrialis. Patterns of lipids glands (LM). Bar = 50 ^m; Fig.E: Bufo bufo. As a rule, the antipredatory parotoid glands are very large serous glands inserted in the dermis. (LM).(compare with Fig.F). 500 )xm; Fig.F: Salamandra lanzai. Also in this species the parotoid glands exhibit serous characteristics and large dimensions (LM) (compare with Fig.E). Bar = 200 nm; Fig.G: Plethodon glutinosus. Male mental glands are elongated, mucous glands specialized in production of courtship chemosignals.(LM) (compare with Fig.H). Bar = 200)im; Fig.H: Hydromantes italicus. Cloacal vent glands are male glands specialized in pheromone production. Note their mucous structure and compare with Fig.G (LM). Bar = 50 urn. Labels: dd = dense dermis, e = epidermis, gn = gland neck, Ig = lipid gland, ma = mucous acinus, mec = myoepithelial cell, meg = mental gland, mg = mucous gland, pg = parotoid gland, sd = spongy dermis, sg = serous gland, vg = vent gland. Herpetologia Candiana Main gland portions All the gland types are simple alveolar and intradermal. Independently of their nature, they exhibit the same structural pattern based upon integration of four parts. Proceeding according to the functional way of secretory release, a gland consists of: 1) myoepithelial sheath; surrounding the gland acinus and involved in gland discharge, 2) secretory unit; the most characteristic portion of a gland providing to its typical func• tion, 3) intercalary tract, or neck; a trunco-conical, subepidermal region between gland body and duct. It consists of imbricated adenoblasts and myoblasts which serve as a regenerative matrix after gland holocrine discharge, 4) duct; an intradermal channel for the secretory product, bordered by epidermal cells. The myoephitelial sheath of serous and lipid glands possesses direct innervation, whereas, as a rule, this lacks in mucous glands. In this case the release of the neurotransmitter from nerve terminals occurs, very likely, in the stromal environment and diffuses more slowly towards the gland. Specialized cutaneous glands With the term "specialized" glands we define secretory organs localized in limited skin regions and involved in peculiar roles related to the species biology. In this connection, although several different gland specializations have been reported in both Anura (see Barthalmus, 1994) and Urodela (see Houck & Sever, 1994), all of which are referable to two main strategies: antipredatory defence or social communication and reproduc• tion. When specialized glands occur, the most prominent differences with the ordinary ones concern the secretory units. As a rule these are large and/or elongated and close• ly packed together, forming, in some cases, obvious outgrovv1:hs (plicae, swellings, patchs, a.s.o). On the basis of cytological traits and/or secretory products, most specialized glands of the amphibians pertain to the serous type. This is the rule for the antipredatory units of both anurans and urodeles. Serous are also the parotoid glands producing defensive toxins and occurring in some anurans (pelobatids and bufonids; fig.E) as well as in sev• eral families of salamanders, including ambystomatids, plethodontids and salaman- drids (fig. F). Other anurans and salamanders possess localized patches of granular glands that per• form the same defensive function as the parotoid ones. Among anurans, these are, for example, the leg glands occurring in the skin of the zeugopodium of Bombina varie-
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