Calymne, THOMSON, 1877

Saucede, Thomas, Mironov, Alexander N., Mooi, Rich & David, Bruno, 2009, The morphology, ontogeny, and inferred behaviour of the deep-sea echinoid Calymne relicta (Holasteroida), Zoological Journal of the Linnean Society 155 (3), pp. 630-648 : 644-646

IS CALYMNE EPIFAUNAL OR INFAUNAL?

Recent holasteroids are all deep-sea forms and consequently little is known about their behaviour (but see Southward et al., 1976; Rice et al., 1979; David & Sibuet, 1985; Lauermann & Kaufmann, 1998; David et al., 2003b). Nevertheless, functional and ecological interpretations have been reliably deduced from studies of functional anatomy ( Mironov, 1975, 2008). There are, of course, problems with this approach for some groups. These are exemplified by the case of soft-bodied ‘regular’ echinoids, the echinothurioids, which have fleshy aboral spines. Few could have speculated accurately about the functions of these spines without direct observations ( Emson & Young, 1998).

Morphology-based interpretations of the mode of life of atypical irregular echinoids such as Calymne are necessarily hypothetical, and require confirmation by vehicle-based direct observation ( Southward et al., 1976; David & Sibuet, 1985; Lauermann & Kaufmann, 1998). Fortunately, in irregular sea urchins, many characteristics of the test permit inferences concerning their behaviour and Calymne is no exception. When morphological characters are considered, comparisons with analogous (and sometimes even homologous) structures found in spatangoids – the closest relatives of holasteroids ( Mintz, 1968; Smith, 1984) – take functional analysis from the realm of speculation to that of testable hypotheses. Correlations between actual behaviour of spatangoids and their functional morphology have been studied in detail and continue to provide reliable results supported by ecological observations ( Nichols, 1959a; Kier & Grant, 1965; Chesher, 1968; Smith, 1980a, b; Kanazawa, 1992).

We feel that observations such as the ones provided above concerning the test and appendages permit robust, testable hypotheses regarding the mode of life of echinoids, because so many of their vital functions, such as locomotion, burial, respiration, and excretion are directly related to skeletal characteristics ( Smith, 1984). The most significant morphological features of Calymne that might inform these hypotheses are: the high arch of the test when viewed in profile, the anterior placement of the mouth, the relatively high placement of the periproct on the posterior face of the test, the occurrence of a marginal fasciole, plastronal spines with an apparent reverse power stroke, a subanal tuft, and posterior spine frills on either side of an aboral, posterior bulge in the test.

The first step in interpreting Calymne ’s behaviour is to determine its living position relative to the sea floor. The only robust data we have concern one young specimen found within the first 5 cm of the upper sediment layer in station 2462, cruise 23 of the R/V ‘Akademik Mstislav Keldysh’. Unfortunately, this is not sufficient to determine with precision Calymne ’s living position. The problem is confounded by the fact that juveniles of some echinoids can exploit levels in the sediment different from those of their corresponding adults. In addition, interpretations of the position in life for Calymne in particular are made more difficult because seemingly incompatible characters occur together: specialized spines evocative of burrowing forms co-occur with general features unsuited for a permanent infaunal position. From that, it is necessary to consider several hypotheses regarding Calymne ’s mode of life and ability to burrow.

Calymne is characterized by a high test profile ( Fig. 2C–E ). Such a high, inflated test camber is found in other extant deep-sea holasteroids such as the pourtalesiid genera Echinocrepis and Cystocrepis , and in fossils such as Echinocorys , all of which have been observed or inferred to be epifaunal, or at most, shallow burrowers ( Stephenson, 1963; Mironov, 1975, 2008; Southward et al., 1976; Lauermann & Kaufmann, 1998; David et al., 2003b). Moreover, the epifaunal lifestyle is a common behaviour among holasteroids, although the fossil genus Infulaster , with its exceptional morphology, has been interpreted to be infaunal ( Gale & Smith, 1982). Among spatangoids, most species are burrowers, with the exception of certain epifaunal deep-sea species (e.g. Linopneustes murrayi , Genicopatagus affinis ) which evolved high test profiles and ambulacra with less welldeveloped petaloids ( Mortensen, 1950; Fischer, 1966; Smith, 1980b; Kanazawa, 1992; David et al., 2003a). These morphological features have been interpreted to be correlated with an evolutionary return from an infaunal habit to life at the surface of the sea floor ( Fischer, 1966; Kanazawa, 1992).

A high test profile and a sparse aboral spine canopy seem incompatible with complete burrowing. Moreover, the anterior ambulacrum of mud-burrowers is distinguished by the presence of specialized organs and structures involved in nutrition and burrowing: penicillate tube feet and/or an oral groove with specialized spines ( De Ridder, Jangoux & De Vos, 1987). In Calymne , the absence of such specialized structures in the anterior ambulacrum is congruent with an epifaunal hypothesis. The presence of a marginal fasciole suggests that Calymne is partly buried, at least up to the ambitus just above the fasciole. Concomitantly, the low marginal position of Calymne’s fasciole does not support a completely infaunal mode of life either. Generally, spatangoid burrowers that lack an aboral fasciole can live buried only in gravels or coarse sands, whereas all mud-burrowers possess an aboral fasciole ( Smith, 1980a). Therefore, while the functional significance of marginal fasciole remains poorly understood, the absence of an aboral fasciole in Calymne prevents us from suggesting that this echinoid is a deep burrower. The presence of a subanal tuft as well as of spatulate spines on both sides of the fasciole (on the posterior side) reinforces the hypothesis of partial burrowing. Taking into account the upper frills of large spatulate spines at the posterior of the test, the direction of stroke, and the considerably enlarged S1 spines, we suggest a function related to sediment or particle (deep-sea marine snow) transfer over the posterior part of the test or more likely, to a pushing action against the sediment.

INFERRED BEHAVIOUR

Most benthic deep-sea animals cannot, energetically speaking, ‘afford’ a sessile lifestyle. In fact, most of the adaptations to the abyssal benthic lifestyle seem directed towards enhanced mobility in order to exploit opportunistically the occasional rich marine snowfall or patchy distributions of otherwise sparse nutrients. This principle is manifested in several diverse echinoderms: swimming elasipodid holothuroids ‘leaping’ from place to place ( Ohta, 1985); swimming aspidochirote holothuroids undulating above the bottom ( Rice et al., 1979); other holothuroids that can walk on enlarged podia (pers. observ.); crawling crinoids ( Fujita, Ohta & Oji, 1987); and fast-moving, lightly constructed echinothurioid sea urchins with hooves on their spines ( Emson & Young, 1998).

These observations reinforce the likelihood that Calymne is epifaunal. However, any such hypothesis of an epifaunal lifestyle must also accommodate the unorthodox position of the fasciole and two groups of spines. First, the occurrence of a marginal fasciole and of a subanal tuft implies that Calymne might live partly buried, the flat oral surface shallowly ploughing the sea floor, mouth-first. In this interpretation, the subanal tuft may be used to stabilize the test on the unstable deep-sea mud. Second, the function of the upper-posterior frills of large spines is difficult to envisage in the context of well-known echinoid behaviours. A superficial examination might lead to a first hypothesis involving cleaning of the test or a covering reaction, but this would depart significantly from all direct observations made on other deep-sea holasteroids ( Rice et al., 1979; David et al., 2003b). A second hypothesis would suggest that the frills help overturned specimens to right themselves. Although it might seem unusual to evolve a specialized spination for this purpose alone, this hypothesis is supported by the shape of the test. It is very high, and therefore likely to be unstable in nearly any current regime, and lacks robust lateral spines that would otherwise perform this righting function. This hypothesis could also explain the spatulate shape of the spines, which is ideally suited for pushing against sediment.

The forward motion of Calymne almost undoubtedly results from the coordinated strokes of L2 and L3 spines located on the oral surface. In these spines, curvature is orientated forward, allowing efficient contact and thrust upon the substrate. During locomotion, plastronal S2 spines can rest perpendicular to the test without producing any forward stroke, but would participate in stabilizing the test. The shallow burial could be accomplished by the combined strokes of plastronal (S2) spines, frontal spines (S3), and ventro-lateral L2 and L3 spines. In this scenario, while ventro-lateral spines excavate that part of the sediment located beneath the test, their action is assisted by a slight rocking movement of the test. This movement, facilitated by the thixotropy of the substrate, would be achieved by the antagonistic and coordinated actions of plastronal and frontal spines. These spines would tilt the test alternatively frontward through action of the frontward stroke of plastronal spines, and then backward by the downward stroke of frontal spines. Rocking movements have already been observed in Brissopsis lyrifera and wedge-shaped spatangoids that rock while burrowing in muddy substrates ( Kanazawa, 1992; Hollertz & Duchêne, 2001). If we accept that Calymne is partially infaunal, we might envisage that it uses the phyllopodia to gather and transfer food from the relatively rich upper marine snow layers to the anteriorly placed mouth. One might even suggest that as Calymne does so, it is tilted upward to bring the mouth closer to the upper layers. This rocking behaviour could in fact help to orientate the animal to initiate this ‘tilted ploughing’.

In Calymne , the combination of atypical morphological characters is a challenge to the functional morphological approach, particularly given the lack of detailed knowledge of deep-sea environments. Nevertheless, such morphological inference for function should not be the domain of palaeontology alone. For extant organisms that inhabit environments that remain relatively unexplored, it is necessary to develop hypotheses and even predictions concerning behaviour in order to develop a context for the unusual morphologies these animals represent. With further data from direct deep-sea observation, the soundness of such analyses can only be improved.

Figures

Figure 2. Specimen from R/V ‘Akademik Kurchatov’ cruise 37, station 3787. A, aboral surface. B, oral surface. C, anterior surface. D, posterior surface. E, right side.