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Autotomy of the visceral mass in the feather star himeroinetra robustipinna (crinoidea, comatulida).

Introduction

Many animals are capable of autotomy, which is the nervously controlled separation of a body part. This phenomenon is not taxon specific and has developed independently in different groups of animals. Autotomy is an adaptation that helps animals avoid death when attacked by predators and reduces the negative effects on the body during such an attack. Currently, over 200 species from different taxa are known to practice autotomy (Fleming et al., 2007). Autotomy is characterized by three main features (Wilkie, 2001; Fleming et al., 2007). First, autotomy is a protective function of an organism, mainly designed for protection against predators and, accordingly, is triggered by external stimuli. Second, autotomy is performed by internal mechanisms. Third, autotomy is controlled by the nervous system. The loss of body parts is also usually followed by their complete regeneration.

Autotomy and the subsequent regeneration of various body parts have been identified in all classes of echinoderms (Emson and Wilkie, 1980). Crinoids can discard and then regenerate various appendages, such as arms, cirri, pinnules (Candia Carnevali, 2006), and the entire calyx and internal organs (Amemiya and Oji, 1992). Sea stars can separate arms (Emson and Wilkie, 1980). Ophiuroids can autotomize arms and the aboral portion of the disc (Litvinova and Zharkova, 1977; Dobson, 1985; Dobson and Turner, 1989; Charlina et al., 2009; Frolova and Dolmatov, 2010). Autotomy of tubercles and spines has been described for sea urchins (David and Neraudeau, 1989). In holothurians, this phenomenon occurs in two forms. Apodida can discard the posterior region of the body (Pearse, 1909; Domantay, 1931; Baugh, 1991), whereas autotomy in the Aspido-chirotida and Dendrochirotida takes the form of auto-evisceration, which is characterized by the extrusion of internal organs through a rupture in the body wall (Emson and Wilkie, 1980; Byrne, 1985, 1986; Dolmatov, 1996, 2009).

Autotomy mechanisms in echinoderms depend on the ability of the connective tissue to change its mechanical properties (Wilkie, 1979, 1984, 2001, 2005; Motokawa, 1982; Motokawa and Tsuchi, 2003; Motokawa et aL, 2012). In many echinoderm organs, the connective tissue is represented by mutable collagenous tissue, which can alter tensile strength under the control of the hyponeural division of the nervous system (Wilkie, 1979; Dobson and Turner, 1989; Wilkie et al., 1990, 1995, 1999; Heinzeller and Welsch, 1994). These properties of the mutable collagenous tissue are attributed to special types of cells in the extracellular matrix, which are known as juxtaligamental cells (Wilkie, 2001, 2005). Juxtaligamental cell cytoplasm contains numerous electron dense granules that are believed to release substances that affect the interaction between the extracellular matrix molecules and cause rapid changes in the mechanical properties of the connective tissue in response to stimuli from the nervous system (Wilkie and Emson, 1987; Wilkie. 1996; Koob et al., 1999; Szulgit and Shadwick, 2000; Trotter, 2000; Wilkie et aL, 2004). This may also involve specific enzymes (matrix metalloproteinases and their inhibitors) that participate in the transformation of connective tissue (Ribeiro et al., 2012).

In several crinoid species, the internal organ complex located in the calyx (visceral mass) can be easily removed mechanically. This phenomenon was initially described by Dendy (1886) as "evisceration." Furthermore, comatulid individuals with missing or regenerating visceral masses have frequently been identified in nature (Clark, 1915; Meyer, 1988). Meyer (1985) believes that the absence of a visceral mass in crinoids is related to predation pressure, which is mostly caused by fish. Nevertheless, the mechanisms of the removal of the internal organs remain unclear. Do crinoids lose their visceral mass because of the mechanical tearing by predators, or can they shed the internal organs without assistance under the effect of an external factor, as a lizard sheds its tail? In the latter case, separation of the visceral mass should be regarded as autotomy. According to Wilkie (2001), the easy removal of the visceral mass in several species of crinoids argues in favor of autotomy. Nevertheless, there are no available data to confirm the mechanisms for visceral mass autotomy in these animals.

The comatulid Himerometra robustipinna (Carpenter, 1881) is widely distributed in the Indian and Pacific Oceans (Clark and Rowe, 1971). The visceral mass of this species is easily separated from the calyx and can be rapidly regenerated (Meyer, 1985, 1988). In this study, we have demonstrated that the separation of the visceral mass in H. robustipinna is an example of natural autotomy, which is most likely controlled by the nervous and juxtaligamental systems.

Materials and Methods

Adult specimens of Himerometra robustipinna (Crinoidea, Comatulida) were collected in the Nha Trang Bay in the South China Sea. To study the normal anatomy of the internal organs, the cirri and most of each arm was removed from the specimens with scissors, and the remaining calyx with the visceral mass was placed into a fixative. The separation of the internal organs in intact animals was induced by mechanical action, specifically by holding the visceral mass with forceps. Immediately after visceral mass autotomy, the cirri and arms were removed, and the visceral mass and calyx were placed into a fixative.

The material for light microscopy was fixed in Bouin's fixative (Humason, 1962). The animals were stored in the fixative for 1-2 mon at 4 [degrees]C prior to processing. The material was washed with 96% ethanol, dehydrated in a mixture of ethanol and chloroform (1:1) and in chloroform, and embedded in paraffin. Sections (5-6 pm thick) were prepared with a MicroTec CUT 4050 microtome and stained with hematoxylin and eosin (Humason, 1962).

For electron microscopy, the material was fixed in 2.5% glutaraldehyde in 0.05 mol [l.sup.-1] cacodylate buffer (pH 7.6) for 1-7 days at 4 [degrees]C, then rinsed in the identical buffer and post fixed in 1% Os[O.sub.4] for 1 h. Decalcification was performed for 25 days in an ascorbic acid solution (Dietrich and Fontaine, 1975). The material was dehydrated in a graded series of ethanol and acetone and then embedded in a mixture of araldite M and Epon 812 (Fluka) according to the standard procedure (Glauert and Lewis, 1998). The sections were prepared using a Reichert Ultracut E microtome. Semithin sections (0.7 p.m thick) were stained with 1% methylene blue. The semithin sections were analyzed and photographed using a Leica DM-4500 microscope. Ultrathin (60 nm thick) sections were stained with 1% uranyl acetate in 10% ethanol and Reynolds' lead citrate and then analyzed using a Libra 120 transmission electron microscope.

Results

The gross anatomy of Himerometra robustipinna

The body of H. robustipinna consists of the calyx, five branching arms, and aboral appendages (cirri) that are used by the animal to attach to a substrate (Fig. 1A). The visceral mass is located in the concavity of the calyx. Ambulacral grooves descend from the arms, run along the surface of the visceral mass, and unite at the centrally located mouth (Fig. 1B). The oral side of the visceral mass is covered by a tegmen, which consists of an epidermis and underlying layer of connective tissue (Fig. 1C).

Numerous modified proximal pinnules occur at the base of the arms (Fig. IA). These pinnules are longer and more heavily calcified than those located more distally. The proximal pinnules most likely play an important role in protecting the internal organs. When an animal is stimulated (e.g., when the visceral mass is touched), the proximal pinnules descend to cover the oral side of the calyx. Therefore, the visceral mass is completely covered with a dense layer of calcified pinnules (Fig. ID).

The visceral mass consists of a helically twisted endocyclic type digestive tube and a centrally located axial organ. The slit like mouth opening is located in the center of the visceral mass (Fig. 1B). Within the radii, the digestive tube yields five lateral outgrowths that extend to the base of the arms, thus giving the visceral mass a five bladed shape. The digestive system ends with an anal cone. The tip of the anal cone contains an eccentrically located anal orifice (Fig. 1 B).

The intestine is surrounded by a narrow subintestinal coelom and is held in place by mesenteries (Fig. IC). The subintestinal coelom and other body cavities are clearly visible in animals fixed in Bouin's fixative because carbon dioxide produced during fixation accumulates in the body cavities and causes significant expansion (Fig. 1C). The aboral coelom, which is divided into numerous cavities by septa, is located under the aboral wall of the subintestinal coelom. The aboral coelom separates the visceral mass from the skeletal elements of the calyx.

The ultrastructure of the intact attachment sites of the visceral mass to the calyx

The visceral mass is attached to the calyx by septa of the aboral coelom and attached by the tegmen on the periphery. Septa are thin connective tissue partitions covered by coelomic epithelium (Fig. 2A), and their oral components attach to the aboral wall of the subintestinal coelom (Fig. 2B). Toward the calyx, the septa form an intricate system of cavities (Fig. IC). The coelomic epithelium of the middle region of the septa consists of mainly flat peritoneal cells (Fig. 2A, C). The apical surfaces of the cells bear a cilium and rare microvilli. There are exocytotic vesicles in the apical portion of the cytoplasm (Fig. 2C. E). The rough endoplasmic reticulum (RER) and moderately developed Golgi apparatus (GA) can be observed in the cytoplasm. Occasionally, groups of myoepithelial cells and spicules occur, which are embedded in septal connective tissue (Fig. 2D).

The coelomic epithelial cells are cuboidal at the connection between the septa and aboral wall of the subintestinal coelom (Fig. 2B). The number of myoepithelial cells increases at this site. In the aboral portions of septa, particularly where they form a system of cavities, cuboidal peritoneocytes also constitute the coelomic epithelium with processes of myoepithelial cells among them (Fig. 2E).

The septum connective tissue is composed of bundles of striated collagen fibrils, an amorphous component, and spicules (Figs. 2, 3). The collagen bundles differ in thickness and orientation. Moreover, septum connective tissue contains various types of cells. One cell type is most likely secretory and has cytoplasm containing large vacuoles with electronlucent contents (Fig. 2A). These cells are often situated closer to the coelomic epithelium. Also present are juxtaligamental cells (Figs. 2A, 3A) with cytoplasm containing two types of granules. One granule type is rounded or oval with contents of moderate electron density. These granules range from 0.6 to 1[micro]m long and from 0.3 to 0.8 [micro]m wide. The second granule type is characterized by a higher electron density. These granules are typical for juxtaligamental cells, and their diameter varies from 0.2 to 0.5 Juxtaligamental cells have oval euchromic nuclei with nucleoli. The cytoplasm contains numerous RER cisternae and mitochondria (Fig. 3B). Amoebocytes are also present in the septum connective tissue; they are irregularly shaped and contain large, oval electron dense granules from 0.3 to 2 [micro].m (Fig. 2A, 3C). The amoebocyte nucleus has an irregular shape, and the cytoplasm has a well developed GA and numerous small transparent vacuoles (Fig. 3C).

In addition to these types of cells, the connective tissue of the septa contains individual sclerocytes or sclerocyte clusters, which surround the forming spicules (Fig. 3D). Moreover, nerve cells and bundles of axons are observed in the extracellular matrix (Fig. 3E, F). Nerve cells and axons contain electron dense vesicles that are 0.2-0.3 .[micro]m in diameter. Axons are often located close to the processes and bodies of juxtaligamental cells (Fig. 3E).

The tegmen is covered by an epidermis, which consists of epithelial cells partly embedded in connective tissue. Wide apical parts of the epithelial cells form a thin layer constituting the surface of the animal (Fig. 4A, B). The apical surface bears cilia and numerous microvilli. The bodies of the cells, which contain the nucleus and organelles, are embedded in connective tissue (Fig. 4C). In addition to epitheliocytes, two types of secretory cells occur in the epidermis (Fig. 4A). The first type has large granules with reti form contents of medium electron density. The granules in the semithin sections stained pink with methylene blue, and therefore contain an acidic substance. In the second type of secretory cell, the granules are smaller and include an electron dense material.

The structure of the tegmen connective tissue is similar to that of the septa of the aboral coelom. The connective tissue includes bundles of collagen fibrils of various thicknesses and orientations, amorphous components, spicules, and cell types such as cells with large electronlucent vacuoles, juxtaligamental cells, amoebocytes, neurons, and sclerocytes (Fig. 4C-E).

The process of visceral mass separation

The separation of the internal organs of H. robustipinna as a result of mechanical action occurs relatively rapidly. Immediately after the visceral mass is gripped with forceps, the proximal pinnules are lowered and form a dense cluster covering the calyx (Fig. 1 D). If the visceral mass is held for 20-30 s, the proximal pinnules are raised (Fig. 5A). At this time, the visceral mass has separated from the calyx and can be easily removed.

When the visceral mass is separated, the tegmen is ruptured at the interradii along the periphery of the calyx and at the base of the arms, where the lateral processes of the digestive system end (Fig. 5A-C). Internally, the separation of the visceral mass occurs under the aboral wall of the subintestinal coelom along the aboral coelom septa (Fig. 1C; 5D, E). Only the ruptured septa of the aboral coelom remain on the surface of the calyx after visceral mass autotomy (Fig. 5E-G).

Ultrastructure of the ruptured attachment sites of the visceral mass to the calyx

The coelomic epithelia at the damaged site retain their normal structures (Fig. 6A-D). Cilia and microvilli are observed on the surfaces of the cells. At the rupture site, the cells and basal lamina may become separated from the underlying extracellular matrix (Fig. 6A, B). However, the appearance of the torn connective tissue in the septa differs from that of the intact connective tissue. The extracellular matrix becomes less dense and contains fewer collagen fibrils. The morphology of the juxtaligamental cells changes, and the granules swell and develop an electron transparent halo (Fig. 6E, F). This may indicate that the granule contents are beginning to disperse. Some granules are released into the extracellular matrix (Fig. 6G). More over, areas of structureless matrix with no collagen fibrils are observed in the torn connective tissue ends of the septa (Fig. 6G). These may be regions of connective tissue lysis.

The tegmental structure of the calyx at the rupture site is similar to that of the torn septa of the aboral coelom. Some epidermal cells are destroyed at visceral mass autotomy, but the undamaged cells retain their organization (Fig. 7A). The connective tissue at the rupture site appears looser compared with its normal appearance (Fig. 7B). The processes of juxtaligamental cells contain granules with halo (Fig. 7B). Moreover, isolated granules and areas of structureless matrix are observed in the connective tissue (Fig. 7B. C). Some of the calyx surface is covered with a thin layer of amorphous material, which is presumably coagulated coelomic fluid (Fig. 7D).

Discussion

Our study has demonstrated that the structure of the calyx and visceral mass in Himerometra robustipinna is similar to that of other comatulids (Heinzeller and Welsch, 1994). The intestine is located in the subintestinal coelom and is attached to the tegmen and calyx by mesenteries. However, unlike that of previously described species, the aboral coelom in H. robustipinna, which is divided into numerous cavities by septa, is located under the visceral mass. The aboral coelom is most likely homologous to the axial sinus of other comatulids in terms of location (Heinzeller and Welsch, 1994). Because the septa of the aboral coelom are thin, such structures may facilitate the separation of the visceral mass from the calyx during autotomy.

The structure of the tegmen and septa of the aboral coelom is typical for comatulids (Holland, 1984; Heinzeller and Welsch, 1994). The composition of the epidermis ineludes two types of secretory cells in addition to epithelial cells. The septa are covered by coelomic epithelium, consisting of peritoneocytes and myoepithelial cells, which is typical for echinoderms (Heinzeller and Welsch, 1994; Garcia Arraras and Dolmatov, 2010). A distinguishing feature of the connective tissue in H. robustipinna is a large quantity of secretory cells with electronlucent vacuoles. These cells were observed in the extracellular matrix of both the tegmen and septa.

Although visceral mass separation in Crinoidea was described over 100 years ago (Dendy, 1886), its causes and functions remain unknown. Meyer (1985) showed that the absence of a gut in crinoids might result from predation. Meyer's data included direct observations of crinoids being attacked by fish. Moreover, the number of individuals with damaged or missing organs was higher among exposed than cryptic (nocturnal) species. These results suggest that visceral mass separation in crinoids is an adaptation to predation effects and is induced by external stimuli (Meyer, 1985).

In H. robustipinna, the separation of the visceral mass occurs at a distinct location: under the aboral wall of the subintestinal coelom. Calyx lesions are minimal as a result of autotomy; a relatively smooth wound surface is formed after the visceral mass has separated. These conditions supposedly facilitate the rapid regeneration of lost structures. For instance, the crinoid Antedon mediterranea appears unable to autotomize internal organs. Nevertheless, the visceral mass in this species can regenerate after it is removed manually. The gut is restored after approximately 7 days, and the main structures of the visceral mass develop within 14 days (Mozzi et al., 2006). In H. robustipinna, the gut forms on the 4th day after visceral mass autotomy, and regeneration is complete after 7-10 days (Meyer, 1985).

We found that it is sufficient to hold the visceral mass for 20-30 s with forceps to provoke autotomy. Therefore, there are internal mechanisms promoting the separation of the visceral mass in H. robustipinna. In all echinoderms. the separation of body parts during autotomy occurs with the participation of juxtaligamental cells. These cells have a characteristic morphology and have electron dense granules (0.2- 0.7 [micro]m in diameter) in the cytoplasm (Holland and Grimmer, 1981; Byrne, 1994; Wilkie, 2001. 2005; Mashanov et al., 2007; Charlina et al., 2009). It is hypothesized that the contents of the granules induce changes in the mechanical properties of the connective tissue, which leads to rupture of the structure (Wilkie and Emson, 1987; Wilkie, 1996, 2005; Koob et al., 1999; Szulgit and Shadwick, 2000; Trotter, 2000; Wilkie et al., 2004). In H robustipinna, we observed juxtaligamental cells with a typical morphology in the septa of the aboral coelom and in the tegmen. These cells were present in the connective tissue individually or in small clusters, and their processes, which contain granules, were widespread in the extracellular matrix. In echinoderms, clusters of juxtaligamental cells directly contact neurons or their processes, which most likely indicates a nervous regulation of the juxtaligamental system (Wilkie, 2001, 2005; Mashanov et al., 2007; Charlina et al., 2009). We could not observe the synapses between axons and juxtaligamental cells in H. robustipinna: however, nerve processes are often located close to the processes or bodies of juxtaligamental cells.

During visceral mass autotomy in H. robustipinna, the juxtaligamental cells and connective tissues were altered in the septa of the aboral coelom and tegmen. After separation, the granules of the juxtaligamental cells appeared swollen and had an electronlucent halo. This suggests that the granule contents were being depleted. Some granules were released into the connective tissue. At the breakage site, the extracellular matrix became loose. These results imply that the juxtaligamental system participates in the separation of the visceral mass in this species. Similar morphological patterns were observed for autotomy in the feather star Florometra serratissima (Holland and Grimmer, 1981) and ophiuroids (Wilkie and Emson, 1987; Dobson and Turner, 1989). On the other hand, juxtaligamental cells did not appear to change in holothurians and separation of the autotomy structures was facilitated by muscle contraction (Byrne, 2001).

The alterations of connective tissue are provided by specific proteases, such as matrix metalloproteinases (Woessner, 1991) and aminopeptidases (Nakajima and Chop, 1991). These enzymes are able to degrade all known types of extracellular matrix proteins and, hence, play an important role in many morphogenetic processes in both vertebrate and invertebrate animals (Massova et al., 1998; JourdanLeSaux et al., 2010). Recent studies show that matrix metalloproteinases and their inhibitors may participate in the alteration of the mechanical properties of mutable collagenous tissue by controlling the density of linkages between the collagen fibrils (Ribeiro et al., 2012). Our observation of areas of structureless matrix in the connective tissue at sites of torn tegmen and septa in H. robustipinna suggest that matrix metalloproteinases or other proteases might directly degrade collagen fibrils at autotomy.

We have not attempted to evaluate the effect of the nervous system on the process of visceral mass separation. However, we believe that the nervous system plays an important role in this process. Crinoids exhibit distinct behavioral responses to stimulation. Immediately after the visceral mass is gripped with forceps, the proximal pinnules are lowered and form a dense layer over the soft tissues of the calyx, thus protecting them from the external stressor. In some cases, this behavior may protect the crinoid's visceral mass. According to Meyer (1985), individuals have been observed with intact internal organs and fresh scars on the proximal pinnules, which were most likely caused by a predator's failed attack.

When the visceral mass is subjected to an external force (for instance, when gripped by a predator or forceps), we hypothesize that the juxtaligamental cells are activated, and the septa of the aboral coelom and the tegmen tear. The visceral mass then separates from the calyx. The proximal pinnules rise to uncover the calyx and enable the removal of the damaged visceral mass. These complex behavioral responses are not feasible without the participation of the nervous system. In addition, the site where the visceral mass is attached is well innervated. Nerve cells and their processes are observed in the connective tissues of the tegmen and septa of the aboral coelom.

Thus, we have shown for the first time that the separation of the visceral mass in H. robustipinna is characterized by all the main features of autotomy. First, autotomy is a defense response whose role is to reduce the degree of damage to the organism as a result of external factors. Second, the removal of the visceral mass occurs with the assistance of the animal's internal mechanisms. H. robust ipinna has a juxtaligamental system typical of echinoderms, which may induce changes in the extracellular matrix resulting in the rupture of the structures. Third, this process is controlled by the nervous system. Complex behavioral responses and nerve processes in the connective tissue and near juxtaligamental cells support this assumption.

Acknowledgments

The authors express their gratitude to Dr. Bui Hong Long (Director of I0 VAST), Department of Marine Living Resources, and the Marine Aquaculture Laboratory for the opportunity to work at I0 VAST, and to Dr. T.N. Dautova and Dr. S.Sh. Dautov for their help in the collection of the animals. Our special thanks are extended to two anonymous reviewers, whose valuable critical comments enabled us to improve the quality of the manuscript. The study was partly supported by the Russian Foundation for Basic Research (Grant No. 14-04-00239), Far Eastern Branch of the Russian Academy of Sciences (Grant No.12-I-P28-04), and the Government of the Russian Federation (Grant No. 11.G34.31.0010).

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NADEZHDA V. BOBROVSKAYA (1) AND IGOR YU. DOLMATOV(1) ,(2).*

(1) A. V. Zhirmunsky Institute of Marine Biology, FEB RAS, Palchevsky 17, Vladivostok, 690041, Russia; and (2) Far Eastern Federal University, Suhanova 8, Vladivostok, 690950, Russia

Received 28 May 2013; accepted 14 February 2014.

* To whom correspondence should be addressed. E-mail: idolmatov@mail.ru
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Author:Bobrovskaya, Nadezhda V.; Dolmatov, Igor Yu.
Publication:The Biological Bulletin
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Geographic Code:4EUNE
Date:Apr 1, 2014
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