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Tentacle Musculature in the Cubozoan Jellyfish Carybdea marsupialis.

The diploblastic cnidarian body plan comprising the epidermis and gastrodermis has remained largely unchanged since it evolved roughly 600 Ma. The origin of muscle from the mesoderm in triploblastic lineages is a central evolutionary question in higher animals. Triploblasts have three embryonic germ layers: the endoderm, mesoderm, and ectoderm, which develop into organs, muscle, and skin, respectively. Diploblasts lack the mesoderm, the layer thought to give rise to the skeletomuscular system. However, phyla such as Cnidaria and Ctenophora, which are typically classified as diploblasts, possess striated musculature. Within phylum Cnidaria, class Cubozoa includes carnivorous box jellyfish, which are capable of extending and contracting their tentacles for predation and defense mechanisms, thus suggesting a well-organized system of muscles. Here, the tentacle musculature of the cubomedusae Carybdea marsupialis is investigated using transmission electron microscopy in conjunction with light microscopy to further understand the arrangement of musculature in these primitive animals. Cross sections of tentacles confirmed that the gastrodermis is separated from the epidermis by a collagenous mesogleal layer containing numerous longitudinal muscle cells arranged in fascicles. Longitudinal muscles permit the tentacle to retract toward the bell during fast tentacle shortening and crumpling behavioral responses. Circular muscle cells were found in the gastrodermis and epidermis, encircling the layer of longitudinal muscle. These circular muscles likely enable the elongation process that allows the tentacles to return to a resting state after contraction. The presence of a definitive muscle cell layer within the mesoglea suggests that C. marsupialis has an advanced muscle morphology that is similar to triploblastic animals.

Introduction

The cnidarian body plan has remained relatively unchanged since its development about 600 Ma (Cartwright et al., 2007). The evolution of muscle cells in triploblastic organisms is a defining feature in the early phylogeny of the bilaterian lineage. Bilaterians, often referred to as triploblasts, display bilateral symmetry and advanced body plans throughout a broad spectra of species (Burton, 2008). The triploblastic body plan derives from three embryonic germ layers: the endoderm, mesoderm, and ectoderm. During development, the endoderm forms the gastrodermis, and the ectoderm produces the epidermis. The mesoderm plays a crucial role by creating specific anatomical structures such as the skeletomuscular system, connective tissues, and organs, including the heart and the liver (Wolpert et al., 1998). Diploblasts such as Cnidaria and Ctenophora lack the mesodermal layer but possess a layer of mesoglea, an acellular gel-like matrix of connective tissue, that separates the gastrodermis and the epidermis (Burton, 2008). The lack of the mesoderm is puzzling in cnidarians and ctenophores because representatives of both phyla possess striated musculature, a mesodermal derivative in most triploblasts (Werner et al., 1976; Chapman, 1978; Seipel and Schmid, 2005, 2006; Steinmetz et al., 2012). Early observations of the cubomedusae Carybdea marsupialis suggest that muscle cells are organized in longitudinal tubes contained within the mesoglea of the tentacles (Claus, 1878). Other cnidarian species, such as the scyphozoan Pelagia, have similar muscular organization (Seipel and Schmid, 2005, 2006). These traits, along with molecular data (Martindale et al., 2004). fuel the debate about whether either phylum is truly diploblastic; and they may be the key to understanding the triploblastic lineage and evolution of the Bilateria.

Cubomedusae are unique cnidarians that display strong swimming and tentacle contraction behaviors regulated by separate neuronal networks (Eichinger and Satterlie, 2014). The striated swim musculature of the subumbrella has previously been described (Satterlie et al., 2005) and is responsible for the strong, efficient swimming contractions characteristic of this group (Stewart, 1996). Longitudinal muscle contraction in the tentacles is responsible for two separate behaviors: tentacular shortening for feeding and tentacular crumpling for protection (Satterlie, 2014). The feeding response is regulated by longitudinal contraction of a single tentacle, with an inward bending of the pedalium that transfers captured prey from a tentacle to the manubrium (Larson, 1976). A coordinated inward bending of all four tentacles into the bell produces a crumpling response that curls the marginal structures into the bell for protection (Berger and Conant, 1900; Yatsu, 1917; Hyman, 1940). Understanding the anatomical organization of the tentacle musculature is essential to interpreting the functions that enable these characteristic cubozoan behaviors. In addition, the unique arrangement of longitudinal muscle within the mesoglea may provide morphological support for the hypothesis that Cnidaria represent an evolutionary link to the bilaterian lineage (Seipel and Schmid, 2005,2006; Burton, 2008; Steinmetz et al., 2012).

Materials and Methods

Specimens of Carybdea marsupialis (Linnaeus, 1758) were obtained by divers at the University of California, Santa Barbara. Medusae were relaxed in a 1 : 2 mixture of Mg[Cl.sub.2 ](0.33 mol [L.sup.-1]) and seawater (Pantin, 1960). Tentacles were dissected and fixed in 2.5% glutaraldehyde in 0.2 mol [L.sup.-1 ]Millonig's phosphate buffer, pH 7.6 (Millonig, 1961). Samples were postfixed with 1 % osmium tetroxide in sodium bicarbonate buffer, pH 7.2. Tissue was washed with phosphate buffer and dehydrated through an ascending, graded ethanol series before embedding in Spurr's epoxy resin (Spurr, 1969). Thick (500-nm) tissue sections were prepared for light microscopy and stained with 2% toluidine blue. Thin (90-nm) tissue sections were arranged for electron microscopy and stained with 2% uranyl acetate in 50% ethanol and Reynolds' lead citrate (Reynolds, 1963).

Samples were examined and images were acquired using the Olympus BX60 compound light microscope (Waltham, MA) and the Tecnai G2 Spirit BT transmission electron microscope (FEI, Hillsboro, OR). Photomicrographs were adjusted for brightness, contrast, and gamma levels using Adobe Photoshop CS6 (Adobe Systems, San Jose, CA).

Results

General tentacle anatomy

Carybdea marsupialis has a cube-shaped bell with muscular pedalia that branch off of each corner of the bell. Each pedalium gives rise to a single tentacle (Fig. 1 A). Pedalia contain longitudinal muscle found in thick bands running toward the tentacles. The longest muscle fibers are located on the oral side, while fibers on the aboral side are relatively short (Satterlie et al., 2005). Each cylindrical tentacle extends from a blade-like pedalium. Tentacles have intermittent ridges of nematocyst batteries within the epidermis. These batteries appear as bands around the tentacle circumference, alternating with rings of tissue lacking nematocysts (Fig. 1B).

The tentacle core is composed of three layers: the epidermis, mesoglea, and gastrodermis (Figs. 1, 2). The complete tentacle structure appears to be compact, lacking a prominent central cavity (Fig. 1). Each layer has its own distinct cellular composition and structure. The epidermis is the outermost tissue layer and contains numerous nematocysts and cilia along the apical surface (Figs. 1, 3). Circular muscle cells, spumous cells, and large, vacuolated cells lie within the outer region of the epidermis (Fig. 3). Spumous cells, described by Chapman (1978), contain wide, electron-dense mucous granules that appear as large, dark ovals within the cell membrane (Fig. 3). Cells in close proximity to the mesogleal layer typically become more compact and contain abundant vesicles along with other dense granules (Fig. 3).

The mesogleal layer is defined with a distinct inner and outer border and contains multiple muscle cells arranged in fascicles (Figs. 2, 4, 5). Strands of collagen fibers run throughout the extensible, jelly-like mesoglea with no directed arrangement (Fig. 4) and likely provide support for muscle contraction. The inner mesogleal border, which abuts the gastrodermal tissue, is not as clearly delineated as the outer mesogleal border. The gastrodermis contains densely stained cells packed with organelles, granules, and other cellular deposits (Fig. 6). Macrogranular cells are frequently observed in the gastrodermis. These cells have characteristically large, dark deposits that dominate the intracellular space between the nucleus and other organelles (Fig. 6).

Muscular composition

Carybdea marsupialis tentacles contain two types of muscle: longitudinal retractor muscles and circular muscles. Each type has its own distinct muscular composition, location, and function that aid the animal in feeding and protective behavioral responses.

Longitudinal retractor muscles run the length of the tentacle and are arranged in fascicles within the mesogleal layer (Figs. 1, 2, 5, 7). Each fascicle varies in shape and contains two or more muscle cells, depending on the development of the individual jellyfish. Retractor muscle cells display characteristic organelles, including nuclei, mitochondria, Golgi bodies, and sarcoplasmic reticulum (Figs. 5, 7, 8). Most preparations show the longitudinal muscles to be smooth muscle with no striations present. However, some micrographs reveal a semi-repetitive striation pattern reminiscent of skeletal muscle (Fig. 8). These striations do not display the typical sarcomere structure because of their lack of Z-disks, but they might display an intermediate stage between smooth muscle and striated muscle.

Circular muscles run perpendicular to the longitudinal retractor muscles and form a ring throughout the tentacle (Fig. 9). These circular muscles appear to be larger in diameter and more cylindrical in shape compared to the longitudinal muscle cells, which can sometimes appear wedge shaped or oval shaped. Circular muscles are present individually (Fig. 9), rather than in a fascicle arrangement, as seen in the mesogleal layer (Figs. 2,4,5). Circular muscle is present in both the ectoderm and the gastroderm. Cilia, displaying the characteristic 9 + 2 arrangement, were occasionally found adjacent to the epidermal circular muscles. Gastrodermal circular muscles were accompanied by multiple dense granular cells (Fig. 9).

Carybdea marsupialis tentacles attach to the medusa bell via the pedalium, a muscular structure that enables inward bending of the tentacle. However, for each muscle cell, no definitive point of attachment has been observed. Presumably, the mesoglea provides a tensile support for the contractile force of each tentacle. Muscle cells appear to be innervated by neurites that run parallel to the longitudinal retractor muscles and are bundled in the center of the fascicle (Fig. 10).

Discussion

Transmission electron microscopy of Carybdea marsupialis tentacles, in conjunction with light microscopy, provides an organizational understanding of the muscular system of the highly contractile tentacles. The presence or absence of true musculature has traditionally established the level of organismal complexity that distinguishes animals as either diploblastic or triploblastic (Burton. 2008). The literature refers to Cnidaria and Ctenophora as diploblastic, sister phyla to the Bilateria (Martindale et al., 2002, 2004; Seipel and Schmid, 2005, 2006; Burton, 2008), but also commonly recognizes the presence of both striated and smooth muscle within these organisms (Chapman, 1978; Hernandez-Nicaise et al., 1980, 1984; Satterlie et al., 2005). More recent analyses support the placement of Ctenophora as the sister phylum to all other animals, with a possible independent evolution of mesoderm-derived muscles (Ryan et al., 2013; Borowiec et al., 2015; Moroz et al., 2015; Whelan et al., 2015). Our data on C. marsupialis show definitive muscle cells located entirely within the mesogleal layer, thus providing support that cubomedusae may have similarities to triploblastic animals.

The histological comparison of the tentacle musculature of both Tripedalia and Carybdea cubopolyps shows variability in muscle location (Werner et al., 1976). Tripedalia species contain epitheliomuscular cells that bulge into the mesoglea, while Carybdea species have muscle cells located completely within the mesoglea (Werner et al., 1976). Tripedalia medsuae are typically smaller organisms with shorter tentacles compared to Caiybdea species, which can have tentacles extending roughly a meter from the bell. Tripedalia species also have three tentacles that branch off of each pedalium, whereas Carybdea species have a single tentacle attached to each pedalium. Carybdea marsupialis may rely on the mesogleal support required to contract longitudinal muscles bringing extended tentacles toward the manubrium during feeding or protective behaviors.

Chapman (1978) described the tentacle musculature of the Tripedalia cystophora cubopolyp as smooth longitudinal epitheliomuscular cells but noted the presence of striated myofibrils near the distal tip of the tentacles. Carybdea marsupialis tentacles have predominantly smooth muscle cells, but some cells displayed an intermediate striation pattern similar to those described by Chapman (1978). Carybdea marsupialis tentacle muscles lack Z-disks characteristic of a typical sarcomere structure but do possess light and dark myofilament bands. This semi-repetitive arrangement suggests that these tentacular muscle cells could be a transitional form between smooth musculature and striated musculature. The swim musculature of cubomedusae has a more conventional striated appearance (Satterlie, 1979; Laska and Hundgen, 1984).

Although less prominent than longitudinal muscle, circular muscle forms a basal ring bordering the mesoglea in both the epidermis and the gastrodermis of C. marsupialis tentacles. The circular muscles presumably aid in elongation of the tentacles after longitudinal contraction. The presence of cilia associated with circular muscle in the epidermis is perplexing but may represent a form of proprioception. The anthozoan Ceriantheopsis americanus possesses mechanoreceptive cilia in conjunction with its epidermal musculature (Peteya, 1973). Peteya (1973) suggested that the cilia are proprioceptors that assist the organism by sensing body tilt relative to gravity and that they are activated through associated muscle movement. The presence of cilia in close proximity to the ectodermal circular muscles may provide a similar function within C. marsupialis tentacles.

Clusters of neurites were observed, typically in the center of muscle cell fascicles and running parallel to the long axis of the tentacles. Neither interneuronal synapses nor neuromuscular synapses were observed in our investigation of cubozoan C. marsupialis tentacles. The parallel arrangement of the muscle cells and neurites would make the occurrence of synapses rare in random thin sections.

Medusozoans include scyphozoans, hydrozoans, and cubozoans, all of which contain muscle cells generally described as elongated cells with contractile myofilaments of either smooth or striated organization (Calgren, 1949). The scyphozoan Pelagia noctiluca displays smooth muscle cells in its medusoid tentacles. These mesogleal muscle cells form bundles with neurons that are separate from other tissue layers (Krasinska, 1914). Hydrozoans have a specific layer called the entocodon, from which striated muscle is produced independently of both the endoderm and the ectoderm (Boelsterli, 1977); it should therefore be considered mesodermal (Seipel and Schmid, 2005, 2006). Our tentacle data also include the bundled arrangement of muscle cells located completely within the mesogleal region. This supports the early observations of Krasinska (1914) and Claus (1878) and provides further evidence that cnidarians possess some triploblastic properties.

The arrangement of the longitudinal muscle in flattened tubes within the mesoglea is interesting in terms of the comparative organization of muscle in cnidarians. The common form of muscle cells that make up epidermal or gastrodermal muscle sheets is the epitheliomuscular cell (Chapman, 1974). Muscle cells within epitheliomuscular sheets can have striated or smooth myofibrils. Muscle cells with reduced epithelial components, or "pure myocytes" (without an epithelial component), are best seen in the swim musculature of scyphozoan, cubozoan, and some hydrozoan meduase (Chapman, 1974; Satterlie and Spencer, 1983: Satterlie, 2011, 2015). In both epitheliomuscular cells and myocytes, the myofibrils typically abut the mesoglea. This association is modified in areas where fast or extensive contractions are utilized. This includes the septal retractor muscles of anthozoan polyps, where rows of longitudinal myocytes project into the mesoglea (e.g., in gorgonian and stoloniferan octocoral polyps; Satterlie and Case, 1978, 1980). The projections are similar to the mesoglea] tubes of cubomedusan tentacles but are still attached to the gastrodermis. Within the pennatulids (sea pens), some species are capable of strong longitudinal contractions of the colonial tissue, so that the colony can be withdrawn rapidly into the substrate. These contractions are extensive in these pen-shaped organisms. Interestingly, the colonial musculature (longitudinal) that controls these retractions is composed of longitudinal tubules that are totally contained within the mesoglea, similar to those seen in cubomedusan tentacles (Satterlie et al., 1976). Of the two types of organization, the mesogleal tubules are found in structures where the overall contraction is very extensive, such as in pulling the pen-like colonies into the substrate or shortening the long trailing tentacles of cubomedusae.

Molecular evidence suggests that striated muscle of cnidarians evolved independently of that of bilaterians. One muscle-specific protein, myhc-st, is predominantly expressed in fast-contracting cnidarian muscle, including striated swim musculature of medusae and smooth retractor muscles in Nematostella (Steinmetz et al., 2012). The latter location suggests that the protein is not specific to striated muscle. Yet, the retractor muscles of anthozoan polyps can be considered relatively fast-contracting muscles. From this, we can assume that selective pressure for contractile speed was important for cnidarian muscle evolution.

Based on our work on cubomedusan tentacle musculature, we would like to consider two additional factors that may have shaped the organization and position of retractor musculature in cnidarians. Retractor muscles, represented by the longitudinal muscle of the cubomedusan tentacle and the septal retractor muscle of polyps, must be capable of an unusually high degree of contractility. Carybdea tentacles can extend 1 meter from the bell, and they must contract to pull the tentacle into the bell opening to transfer prey. Similarly, but to a lesser degree, the retractor muscle of polyps must show a greater degree of contractility than the general musculature of the body wall or oral disk. This degree of contractility likely would create problems with wrinkling if the musculature were composed of epitheliomuscular cells, because compression of the epithelial component would resist the shortening of the muscular component. The structure of Carybdea tentacles is interesting in this respect. The alternation of nematocyst-bearing epidermal ridges with rings of thin epidermis creates an "accordion effect" that should aid in the mechanics of extreme shortening.

Another potential selective pressure operating on these retractor muscles is contractile force. When fully expanded, the Carybdea tentacles have an extremely small cross-sectional area. Yet, with their powerful toxins, they are able to catch and subdue relatively large prey. The retractor muscle of the tentacle would require a significant degree of contractile strength, relative to cross-sectional area, to bring large prey items to the bell. A solution in the organization of the longitudinal muscle of the tentacle involves a dense packing of myocytes into fascicles that circle the tentacle within the mesoglea. A similar strategy is found in the septal retractors or pennatulid anthozoans (Satterlie and Case, 1978, 1980). Here, the gastrodermal myocytes are packed into multiple parallel bundles that invaginate into the mesoglea. The solution is the same in both cases--muscle power is increased by increasing myocyte number and density.

The association of the muscle processes with mesoglea is consistent for most cnidarian muscle types, including epitheliomuscular cells and myocytes with reduced or absent epithelial components. Without hard skeletal elements, cnidarians make use of hydrostatic skeletons when possible. However, in areas that lack hydrostatic resistance and at the level of individual muscle cells, the myofibrils must act against the connective fibers of the mesoglea. In the two situations in which muscular force is increased by increased density of myocytes, their effectiveness still requires a close association with the mesoglea. It is likely that the highly invaginated nature of the polyp retractor muscles and the fascicular arrangement of the tentacle retractors are designed for maximal surface area of contact with the mesoglea. In the case of the tentacle retractors, this involves total enclosure of the muscle tubes within the mesoglea.

The morphology of C. marsupialis tentacles suggests that they possess features of triploblasty, with an epidermis, a gastrodermis, and a distinct middle layer of muscle cells embedded in the mesoglea. consistent with the mesoderm in advanced animals. Most myofilaments are smooth in organization, but some reveal a simple striated pattern. Based on these observations, the tentacles of C. marsupialis display a muscular organization that is suggestive of a triploblastic form that could represent an intermediate evolutionary stage between diploblasty and triploblasty. In addition, selective pressures for contractile speed, contractile strength, and degree of contractility likely influenced the organization and position of retractor musculature in cnidarians.

Acknowledgments

Carybdea specimens were collected by Shane Anderson, University of California, Santa Barbara. Drs. Alison R. Taylor and Robert H. Condon provided comments and suggestions for improvement of the manuscript. Mark Gay provided technical assistance in the microscopy lab. This work was supported by National Science Foundation grant IOS-920825 and the Frank Hawkins Kenan Endowment.

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STEPHANIE L. SIMMONS AND RICHARD A. SATTERLIE (*)

Department of Biology and Marine Biology and Center for Marine Science, University of North Carolina, Wilmington, 5600 Marvin K. Moss Lane, Wilmington, North Carolina 28409

Received 9 April 2018; Accepted 18 June 2018; Published online 24 August 2018.

(*) To whom correspondence should be addressed. E-mail: satterlier@uncw.edu.
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Author:Simmons, Stephanie L.; Satterlie, Richard A.
Publication:The Biological Bulletin
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Date:Oct 1, 2018
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