Visual Ecology and Functional Morphology of Cubozoa (Cnidaria)1 (2023)

Melissa M. Coates

Abstract

INTRODUCTION

The class Cubozoa (Werner, 1975) is the smallest class within the phylum Cnidaria with only: one order (Cubomedusae), two families (Carybdeidae and Chiropdropidae), seven genera, and roughly two dozen species. In spite of this small size there is a lack of consensus on the naming and description of species. As a result the reader will notice different spellings of genera, for example Charybdea xaymacana (Conant, 1898) vs.Carybdea sivickisi (Hoverd, 1985) depending on the choice of the author who described that species. For this review I have chosen to hold to the spellings of the original authors.

Originally grouped as an order within the class Scyphozoa, the Cubozoa were elevated to class status once research revealed the magnitude of the differences between this and other cnidarian groups (Werner, 1973; Werner et al., 1976). Berger (1900) first noticed the physiological intermediacy of the cubomedusae between the scyphomedusae and hydromedusae. Although they share traits with the scyphozoans (rhopalia that come in multiples of four) and hydrozoans (possession of a nerve-ring), cubozoans also possess traits found in neither of the two other medusoid classes. These include complete metamorphosis from polyp to medusa (Werner, 1971, 1973; Arneson and Cutress, 1976; Laska-Mehnert, 1985), box-shaped exumbrella (in most species, Tripedalia cystophora being a notable exception), and, complex lensed camera-type eyes (Berger, 1898).

The eyes are located on the rhopalia, marginal sense organs which hang from the bell on stalks and are weighted down by a statolith. The function of the statolith is not known and it has been proposed as both a gravity-sensing organ and as a weight to keep the eyes oriented in the same direction regardless of body orientation (Berger, 1900). On each rhopalium there are two lensed eyes (large complex eye and small complex eye), an identical pair of pit-shaped ocelli (pit eyes), and an identical pair of slit-shaped ocelli (slit eyes) (Fig. 1A). There is one rhopalium on each side of the box-shaped bell, four in all. These alternate with a single tentacle, or a group of tentacles, at each corner of the bell (Fig. 1B). This makes four rhopalia per medusa, six eyes per rhopalium, a total of twenty-four eyes. What are the cubomedusae doing with all this visual hardware?

Nilsson and Pelger (1994) predict that eye evolution responds rapidly to lifestyle changes (see also Darwin, 1872). This implies that visual needs shape eye design much more than phylogenetic position. Therefore, it is useful to look at lifestyle differences between the cubozoans and other cnidarians and to ask: what is the need for complex eyes? Is this need driven by ecological imperatives unique to cubomedusae (among Cnidaria)?

VISUAL ECOLOGY: INTERACTIONS BETWEEN AN ORGANISM AND ITS ENVIRONMENT MEDIATED BY VISUAL INFORMATION

Ecology is the study of interactions of animals with their environment. While this is often the study of energy or nutrients moving through a system, information is an equally important component of the environment. Information is collected, dispersed, processed, created, and hidden by organisms in countless ways. The question becomes: with what sensory information do cubomedusae interact with their environment? How could that information enable the cubomedusae to succeed by encoding cues about location, habitat, obstacles, foods, mates, and so forth? Compared with the open ocean, kelp forests, mangroves, and coral reefs are similar near-shore environments in terms of obstacles in the water column. These obstacles all present low frequency visual information. These near-shore environments are the prefered habitat of cubozoan species (Table 1).

Cubomedusae exhibit many light mediated behaviors (Conant, 1898; Berger, 1900; Barnes, 1966; Hartwick, 1991; Hamner et al., 1995; Matsumoto, 1996; Stewart, 1996; Coates and Thompson, 2000). For example, Chironex fleckeri avoids dark obstacles in a tank and in the wild (Hamner et al., 1995) and can also orient to the light of a match (Barnes, 1966). Tripedalia cystophora rapidly swims away from dark objects and is attracted to light shafts in the water (personal observation; Coates and Thompson, 2000). Presumably the eyes of the sensory clubs mediate these behaviors based on the visual information they extract from the environment.

CUBOMEDUSAE POSSESS THREE DISTINCT TYPES OF EYES

Cubomedusae have six eyes located on each of the four rhopalia. The eyes can be separated into three distinct types: camera-type eyes, slit shaped ocelli, and pit shaped ocelli (Fig. 1A). All three eye types possess ciliated photoreceptors (Yamasu and Yoshida, 1976; Laska and Hündgen, 1982). Although the earliest reports of cubomedusae all mention these three eye types, often the number of ocelli present ranged from one to several (Haeckel, 1879; Agassiz and Mayer, 1902). Haake (1887, as reported by Berger [1900]) claimed that the simple lateral ocelli (pit and slit eyes) were present in young Charybdea rastonii, but absent in the adults. We know this to be incorrect from more recent descriptions of this species; the ocelli are present in both the young and the adults (Matsumoto, 1996). In fact all species on which current research has focused (Carybdea sp.—Satterlie, 1979; Mackie, 1999; Tripedalia cystophor—Laska and Hündgen, 1982; Stewart, 1996; Coates and Thompson, 2000; Chironex fleckeri—Hamner et al., 1995; Carybdea rastonii—Matsumoto, 1996) have the six eyes (two of each type) described here.

The ocelli

The ocelli come in two shapes, pits and slits, and are paired symmetrical to the medial line of the rhopalium (Fig. 1A). The ocelli are formed by invagination of the surface epithelium (Conant, 1898). The distal portions of the epithelial cells lining the invaginations are heavily pigmented (Berger, 1900; Ng, 1974). Berger (1900) and Conant (1898) found only one type of cell in these invaginations (as did Laska and Hündgen, 1982) while they mention that earlier authors (Schewiakoff, 1889; Claus, 1878) found two. The invaginated cells are photoreceptors (Yamasu and Yoshida, 1976). There is a refracting secretion in the space of this invagination presumably protecting the photoreceptor cells (Conant, 1898; Berger, 1900; Yamasu and Yoshida, 1976).

The camera-type eyes are similar in morphology to those of vertebrates and cephalopods

The complex eyes are made up of a cornea, cellular lens, possibly a vitreous space (see below) and a retina with pigmented cells (Conant, 1898; Berger, 1898). The similar morphology to that of other camera-type eyes, vertebrates and cephalopods, suggests a similar function (Pearse and Pearse, 1978). Apart from size differences, the large and small complex eyes are similar in morphology. In Carybdea marsupialis the large eye is 350–400 μm in diameter while the small eye has a diameter of 250–300 μm. The lens diameter is 150 μm in both eyes (Martin, 2002). Although there is some variation in eye size between cubozan species, the complex eyes are always roughly on this same order of magnitude.

The cornea is made up of flattened cells continuous with the epithelium of the rhopalium (Berger, 1898). All authors seem to be in agreement with this interpretation. The lens is cellular but the ‘interior lacks nuclei, cell walls, and protoplasmic structure’ (Berger, 1900). Berger also noted that the degree of cellularization of the interior of the lens varied with lens size, smaller lenses being more cellular. This difference holds between small and large eyes within a specimen, and between eyes of smaller and larger (younger and older) specimens. The lens is ectodermal in origin (Berger, 1900) and biconvex and heterogeneous. Mackie (1999) assumes this is a graded index of refraction lens. The crystallin proteins are novel (Piatigorsky et al., 1989, 1993). The lens is surrounded closely by a capsule which may be a secretion from the lens cells (Berger, 1900). Ng (1974) refers to this capsule as a vitreous humor, believing its position and function synonymous to that of the vertebrate eye.

Earlier authors report the presence of a large vitreous body beteween the lens and the retina (Schewiakoff, 1889; Conant, 1898). Conant (1898) reported what he termed ‘prism cells' in this body which possess a central fiber and concluded that they were extensions of the retinal cells. Berger (1900) clarifies this by proposing that the retina and the vitreous body are histologically different parts of the same structure (see also Laska and Hündgen, 1982). The term retina is thus used for both taken together, while vitreous body refers only to the vitreous portion of the retina. It is important to note that this implies there is no space between the lens and the retina, with the receptive segments of the photoreceptors extending all the way to the lens, as suggested by more recent authors (Laska and Hündgen, 1982; Pearse and Pearse, 1978; Satterlie, 2002). In this way Berger divided the retinal cells into three topographical regions or zones: the vitreous zone (vitreous body of other authors), the pigmented zone, and the nuclear zone. Martin (2002) still claims the presence of a vitreous space, although a much smaller one than earlier authors.

Schewiakoff (1889, as reported by Conant, 1898) held that there are two types of cells in the retina of both the large and small complex eyes, called pigment and visual cells. Conant (1898) himself could not distinguish two types of cells in the retina. Berger (1900) found three distinct cell types in the large complex eye, which he termed: prism cells and pyramid cells (both presumed sensory), and long pigment cells (presumed structural). Here, he draws an analogy between the prism and pyramid cells and the rods and cones of vertebrates. However, he found only one type of cell, the prism cell, in the small complex eye (Berger, 1900). Ng (1974) reports four types of cells in the retina of the large complex eyes: long and short pigmented cells, and type A and B receptor cells. Laska and Hündgen (1982) report three types of cells in the large, and two in the small, complex eyes. The number and type of cells reported in the retina differ largely from author to author and it is not useful to go into the details of each of the cell types beyond this. Rather I will say this is an area where careful revisitaiton will lead to much clarification. Obviously there is conflicting information here and not all these descriptions can be accurate. This variation likely comes from collection, fixation, or microscopy techniques all of which have improved greatly since these earliest descriptions.

The Photoreceptors

The photoreceptors of cubozoans, and all cnidarians, are ciliary with the 9+2 arrangement of microtubules (Yamasu and Yoshida, 1976). They are made up of a receptive outer segment, a pigmented layer, and a nuclear layer. Many microvilli extend from the central cilium (Yamasu and Yoshida, 1976) and these are thought to be involved in primary photoreception (Laska and Hündgen, 1982; Takasu and Yoshida, 1984). The photoreceptors themselves contain the screening pigment (Laska and Hündgen, 1982). Martin (2002) reports that the outer segments possess stacks of parallel membranes which form discs similar to vertebrate rod cells. These cells contain many mitorchondria and vesicles (Martin, 2002). An axon leaves from the nuclear side. Connections from these photoreceptors lead to the rest of the nervous system through interneurons (Laska and Hündgen, 1982).

NERVOUS SYSTEM ORGANIZATION

In 1898, Conant recognized the presence of the nerve ring as distinguishing cubomedusae from scyphomedusae. The nerve ring connects between the rhopalia and the pedalia (points of attachment of the tentacles) (Conant, 1898; Laska and Hündgen, 1984). The nervous system can be divided into three functional parts: the sensory clubs or rhopalia, the conducting nerve ring, and the motor nerve net underlying the subumbrellar epithelium (Conant, 1898; Passano, 1982). In the course of the nerve ring there are several sets of ganglia: four radial ganglia situated where the nerve ring branches to connect to the rhopalia and four pedal ganglia situated where the nerve ring sends off nerves to the tentacles (Conant, 1898; Laska and Hündgen, 1984).

The rhopalia are filled with nerve fibers and cell bodies, referred to as a rhopalial ganglion. This ganglion fills most of the space between the sensory organs and the extension of the gut which enters the rhopalium (Conant, 1898; Ng, 1974; Laska and Hündgen, 1984). There are two groups of large multipolar ganglion cells, one above each pit ocelli. The area between and behind the small complex eye is filled with a large group of network cells (Berger, 1900). The tissue directly below the retina is composed of ganglion cells and nerve fibers (Conant, 1898; Berger, 1900). These form synaptic connections (Laska and Hündgen, 1982) via interneurons to the rhopalial ganglion cells (Yamasu and Yoshida, 1976).

Removing the rhopalia completely leads to a cessation of swimming (Berger, 1900). Satterlie (1979, 2002) has shown that the swim pacemaker cells reside in the rhopalial ganglia. Unfortunately, due to the location of these pacemaker cells, and the close association of the rhopalial ganglia with the eyes, it is impossible to do the desired experiment of removing the rhopalial ganglion and leaving the eyes and swimming behavior intact. If this experiment were possible I would predict that removing the rhopalial ganglion cells would eliminate a behavioral response to light even if the eyes and the swim system remained unharmed. It is my opinion that the location of the rhopalial ganglion cells leaves them poised to sort information encoded by the eyes and to dictate appropriate behavioral responses.

Cephalization may not be appropriate for a radially symmetrical animal

It is easy to be biased by bilateral symmetry and assume that a centralized nervous system is necessary for any integrative nervous system function. However, this may not only be unnecessary but actually detrimental in a radially symmetrical animal, where sensory input comes from several directions. Spencer and Arkett (1984) have suggested, based on work in the hydromedusae Polyorchis, that: 1) “the nerve-rings constitute the central nervous system of hydrozoan jellyfish and that the condensation of neuronal networks into ring structures is the maximum degree of localization that can be tolerated, bearing in mind the integrative mechanisms used,” 2) “networks of identical neurones are the radiates' equivalent of identifiable, paired neurones in the CNS of bilateral protostomes” and 3) “rather than cephalic condensation …the hydromedusae have distributed their ganglia throughout the outer nerve-ring so as to match the distributed arrangement of mulitcellular sense organs such as the ocelli.” These ideas are supported by other authors for a host of cnidarian groups (Passano, 1976; Satterlie, 2002; Mackie, 2002). These arguments hold for the cubomedusan nervous system as well.

The function of the nervous system is to sense the environment and respond appropriately (Satterlie and Nolen, 2001). Cubomedusae have their sensory systems located around the margin of the bell where they can receive information from all directions. They have their integrative centers (rhopalial ganglia) concentrated near these sensory inputs (Satterlie, 1979; Satterlie and Spencer, 1979; Laska and Hündgen, 1984). It is known that the swim pacemakers located in the rhopalial ganglia communicate with eachother via the nerve ring (Sattelie and Nolen, 2001). These rhopalial ganglia presumably sort this information and then distribute it to the appropriate effectors, the swim musculature, via the distributed nerve net of the subumbrella. Distributed sense organs make the most sense in a radially symmetric organism (Satterlie and Spencer, 1987; Satterlie, 2002).

Satterlie and Nolen (2001) have shown that the reduction to only four swim pacemakers in cubomedusae, compared to the higher multiples of four seen in scyphomedusae, represents a partial of centralization of the cubozoan nervous system. These swim pacemakers are located in the rhopalia and allow for rapid responses to asymetrical stimuli (Satterlie and Nolen, 2001). This accounts for the agile swimming ability and rapid directional changes seen in cubomedusae (Satterlie and Nolen, 2001). Could this be in response to visual information?

PREVIOUS IDEAS FOR THE ROLE OF THE COMPLEX EYES IN A BOX JELLYFISH

Lenses not only focus light but they also increase light capture. Some authors have suggested that this may be the sole purpose of the complex eyes (Laska and Hündgen, 1982; Stewart, 1996). However, there are no known examples of animals that employ this strategy (Nilsson, personal communication). Another idea that has been put forth is that the complex eyes allow for orientation to luminescent prey at night (Pearse and Pearse, 1978). Matsumoto (1996) suggests that vision is primarily involved in feeding and reproduction (see also Pearse and Pearse, 1978; Martin, 2002). These two tasks can also be carried out with chemoreception. Several authors have suggested some sort of near-sighted view of small objects inside the bell (Berger, 1898; Conant, 1898; Pearse and Pearse, 1978; Laska and Hündgen, 1984; Stewart, 1996; Matsumoto, 1996) because of the inward orientation of the eyes. However, viewing small objects inside the bell is also unlikely. The optics of the lenses of both the large and small complex eyes show long focal lengths (Coates et al., 2001). This means the lens acts as a low pass filter. A low pass filter removes high spatial frequency image information (such as small objects) before that information reaches the retina. This leaves only low frequency image information (larger objects such as mangrove roots) for the retina to detect. This will be the ideal use for the complex eyes. A low pass filter will give enough information to avoid obstacles in the water. Also, transparency of the bell allows for possibly unencumbered view of the outside world (Stewart, 1996). Meaning that the inward pointing orientation of the complex eyes will not restrict the field of view to objects within the bell.

THE LIFE HISTORY AND ECOLOGY OF THE CUBOMEDUSAE DIFFERS FROM OTHER MEDUSAE

Most medusae are open ocean drifters

Most medusae are found far from shore and are planktonic, at the mercy of the currents and not capable of swimming against them (Graham et al., 2001). In many areas it is uncommon to see medusae near shore unless they have been swept in by changing currents and tides. Often in these cases, medusae are washed up on shore and die.

Noteably, all epipelagic, midwater, and deepsea medusae have very simple, reduced, or absent ocelli. For example, all species in the order Narcomedusae lack ocelli (Mayer, 1910). Species of narcomedusae are found from the surface down to depths greater than 1,000 m (Raskoff, 2001). While we think of jellyfish as predators, their method of food capture more closely resembles fishing than hunting. Beyond predator and prey locations, or conspecific interactions, the open ocean offers little environmental visual information. Still, with simple ocelli, openwater medusae perform phototactic behaviors. For example, Aurelia aurita (Scyphozoa) navigates by sun-compass (Hamner et al., 1994). Many hydrozoan species perform large vertical diel migrations, which may bring individuals together in spawning aggregations (Mills, 1983). Even with large migrations, open ocean jellyfish rarely encounter obstacles in their environments.

Cubomedusae are neritic, often living in complex near-shore habitats such as mangrove swamps

A note on taxonomy: the number and descriptions of species has changed many times over the years (Haeckel, 1879; Mayer, 1910; Bigelow, 1918, 1938; Stiasny, 1930; Kramp, 1961; Uchida, 1970) and there is a great need to revisit this issue to form some consensus. For the discussion below, however, I am interested in conveying the typical habitat of the cubomedusae. To this end I will use the species names and spellings used by the authors who collected and remarked on the habitat of a certain cubozoan.

Cubomedusae are near-shore species, usually tropical or sub-tropical (Werner, 1973). Agassiz and Mayer (1902) found one individual, Carybdea grandis in a trawl that came from a depth of 300 fathoms during the expedition of the ‘Albatross,’ 1899–1900. This may have contributed to the early misconception that cubomedusae were deepsea animals. However, the very next day they found a swarm of mature adults very near the surface off Anaa Island.

Reports of cubomedusae date back more than 200 years (Linne, 1758). While the exact habitats are not always recorded, we are beginning to get a sense of their natural history, and they appear to prefer near-shore habitats, such as mangroves, kelp forests, coral reefs, and sandy beaches (Table 1).

The cubozoan Tripedalia cystophora actively swims near the surface during the day (Conant, 1898; Stewart, 1996), maintaining position among the mangrove roots without damaging its delicate body. Cubozoans are agile swimmers (Stewart, 1996) and voracious feeders (Larson, 1976).

DISCUSSION

By bringing together all the work of previous authors, whether it be on life history or nervous system function, a picture emerges that details the interactions of cubozoans with their environments. From this picture it is now possible to make predictions about vision in the Cubozoa.

SUPPOSITION: SPATIAL VISION ALLOWS FOR EXPLOITATION OF PRODUCTIVE NEAR-SHORE HABITATS BY CUBOZOANS

As seen in Table 1, all known species of cubomedusae are found in near-shore habitats. Have the eyes of the cubomedusae allowed them to expand into this ecological niche?

Presupposition: medusae are soft, delicate, and easily damaged by obstacles in the water column

For many years these beautiful creatures were incompletely described because what came up in plankton nets was often severely damaged. Improved collecting techniques increased knowledge over the past century, but still laboratory observations of behavior were often short-term before the invention of the planktonkriesel (Greve, 1968; Hamner, 1990; Raskoff et al., 2003). This specialized tank creates a waterflow that keeps medusae and other delicate animals in constant suspension assuring that their tissues are not destroyed by abrasive contact with aquarium walls. Can an animal with such a delicate body survive a near-shore habitat, where obstacles form effective walls? Cubomedusae live in such environments but they must have some way to keep from colliding with such obstacles.

Presupposition: vision is a useful way to detect objects at a distance

Chemoreception lacks the resolution needed to avoid obstacles. Mechanoreception will not give information on a time scale which leaves the medusae able to respond; once contact is made the damage has been done. Given the right resolution, spatial vision will allow for detection and avoidance of obstacles.

Counter-supposition: cubozoan eyes represent evolution gone wild, form without function

Gerhart and Kirschner (1997) propose that the cubozoan eyes shows how far form can go without function; citing the lack of a brain as evidence against the usefulness of these eyes. In fact, most skepticism about the image forming capabilities of the box jellyfish eye comes in this form: what good is an image without the nervous ability to interepret it (Nilsson and Pelger, 1994; Darwin, 1872)? Mackie (1999) is quick to point out the under appreciation of, and in fact often misinformation concerning, the cnidarian nervous system (see also Passano, 1976; Mackie, 2002; Satterlie, 2002). Everyone agrees that cnidarians can respond to mechanical and chemical stimulation, should visual information be fundamentally different?

Although cubomedusae are a somewhat neglected group more is being learned about them all the time. When compared to other meduseae we see sophisticated eye design, complex nervous systems, and a unique ecological niche. Bringing together the knowledge of previous researchers we are poised to explore the role of vision in the Cubozoa.

1

From the Symposium Comparative and Integrative Vision Research presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2003, at Toronto, Canada.

2

Present address: Melissa Coates c/o Department of Cell and Organism Biology, Lund University, Helgonavägen 3, Lund, Sweden, 223 62; E-mail: honu@stanford.edu

I would like to thank Jamie Theobald for support, advice, and useful discussion, as well as Stuart Thompson and Dan-Eric Nilsson. I thank Caren Braby and Christian Reilly for careful reading of this manuscript as well as the two anonymous reviewers. Thanks to Mason Posner for inviting me to participate in the symposium. Thanks to Mason Posner, Todd Oakley, and Sonke Johnson for organizing the symposium.

References

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