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Biogeography, diversity, and evolution through vicariance of the hydrothermal vent aplacophoran genus Helicoradomenia (Aplacophora, Mollusca).

ABSTRACT Species of the neomenioid aplacophoran genus Helicoradomenia Scheltema & Kuzirian are found only in areas of hydrothermal vents, oceanic ridges, and back-arc basins and have been collected widely in the East Pacific, Southwest Pacific, and the Triple Junction in the Indian Ocean, but not in the Atlantic. As with other vent taxa, species diversity of Helicoradomenia in the East Pacific is greatest south of the subduction zone of the Pacific Plate under the North American Plate, which divided the ridge system into two sectors during the Eocene: the northern Juan de Fuca system and southern East Pacific Rise. Diversity of Helicoradomenia species reflects, in smaller numbers, the diversity of the vent limpets in the two sectors. Two Helicoradomenia sister species are illustrated with the characters that separate them, H. juani Scheltema and Kuzirian (1991) from the northern sector and H. acredema Scheltema (2000) from the southern. They apparently speciated when the vicariant event of subduction of a once continuous ridge occurred.

KEY WORDS: Helicoradomenia juani, Helicoradomenia acredema, taxonomy, symbionts, dispersal, Juan de Fuca ridge, East Pacific Rise

INTRODUCTION

Aplacophoran molluscs are a small taxon with fewer than 400 described species including both neomenioids (Neomeniomorpha or Solenogastres) and the chaetoderms (Chaetodermomorpha or Caudofoveata). They are found throughout the world's oceans in an amazing assortment of habitats: level-bottom muds subtidally on the continental shelf to hadal depths >7,000 m in deep-sea trenches, interstitially in sands, upon isolated seamounts rising from the seafloor at 4,000-m depths, upon octocorals, and from the tropics to polar regions. Included among the habitats where aplacophorans occur are the chemosynthetic, sulfur-based communities of the hydrothermal vents in oceanic spreading ridges and back-arc basins. Species of the genus Helicoradomenia have been collected, sometimes in surprisingly large numbers, in the East Pacific, Southwest Pacific back-arc basins, and Indian Ocean (Tables 1, 2), but not in the Atlantic. They live upon hard substrates (e.g., rocks, pebbles, worm tubes, clam beds) away from the hot venting fluids.

EAST PACIFIC RIDGE SYSTEM

Since the first discovery in 1977 of a remarkable community living chemosynthetically in regions of hydrothermal vents (Lonsdale 1977, Woods Hole Oceanographic Inst. 2007), the most studied ridge system over the longest period of time is the north-south oceanic ridge in the East Pacific. The ridge is divided into two sectors where the Pacific-Farallon Plate was subducted under the North American Plate in the Eocene, a zone marked beneath continental California by the San Andreas Fault (Tunnicliffe et al. 1996). The ridge sector north of 35[degrees]N is the Juan de Fuca Ridge (itself made up of a subset of segments) and the segment from 21[degrees]N and southward, the East Pacific Rise (EPR). At 0[degrees] latitude, the Galapagos Rift runs eastward perpendicular to the East Pacific Rise.

Species of Helicoradomenia, the genus to which most aplacophoran vent species belong, occur on northern and southern segments and at the Galapagos Rift. They apparently are endemic to the sulfide-based, chemosynthetic fauna of the hydrothermal vents. Two genera, one perhaps being Helicoradomenia, are also found on whalefalls (unpublished). However, Helicoradomenia has not been found with the other important sulfide-based fauna in seeps. The Helicoradomenia species awaiting description are tallied here unnamed.

THE NEOMENIOID GENUS HELICORADOMENIA

Helicoradomenia belongs to the neomenioid aplacophorans, which are narrow or wide cylinder-shaped molluscs ("wormshaped" in the literature) covered by aragonite sclerites held by body mantle cuticle--the scleritome. There is a narrow ventral groove within which is a ciliated foot-fold that glides upon a mucous track. Helicoradomenia is defined by its radula, type of ventrolateral salivary glands, body shape, types of sclerites, and presence of paired copulatory spicules.

Description

Helicoradomenia species are usually 5 mm or less in length when contracted. The radula (Fig. 1B, 1C; 2C, 2D) has two mirror-image teeth per row (=distichous). It is carried on a radula membrane in a long radular sac before emerging into the pharynx, where the two sides of the radula separate and spiral into paired anteroventral pockets that usually unite distally. These radula-filled, anteroventral pockets seem to serve as struts to hold open and expand the proboscis (personal observation), which is usually withdrawn. Each tooth has a number of denticles, added during growth, affixed to a bar, with the longest denticle lateral. The denticles overlap indentations on the next adjacent tooth (Fig. 1B, 2C).

The paired ventrolateral glands, presumably salivary, are a type particular to Helicoradomenia (Handl & Todt 2005, Todt & Salvini-Plawen 2005). Each of the pair is a group of extraepithelial glandular cells bundled together by a thin muscle sheath and emptying individually through long necks into the junction of the pharynx and anteroventral pocket (Fig. 1A). The body is short to somewhat elongate and broad, widest posteriorly (Fig. 1D, 1E, 2A, 2B). The sclerites are solid and upright (i.e., not hollow or adpressed against the body), and are short to elongate; there can be few types or many (Fig. 1F, 2H). The appearance of the scleritome ranges from slightly fuzzy to somewhat to very spiny (Fig. 1D, 1E). For individual sclerites, they are best viewed under cross-polarized light, as different thicknesses produce bands of color, or isochromes (e.g., Fig. 1F, 2H sclerites 4a). For line drawings, the bands are indicated by dotted lines (cf. Fig. 1F, 2H). The copulatory spicules are species specific, although sister species may be morphologically similar (Fig. 2E to 2G), and are sometimes elaborate and numerous; they grow in length with the growth of an individual.

Because the body shape, appearance of the scleritome, and hard parts together are so characteristic, species are relatively easy to differentiate without recourse to histological sectioning. Helicoradomenia species tend to be similar both at the level of cellular studies and in general internal anatomy (H. acredema and Helicoradomenia sp., Todt & Salvini-Plawen 2005; H.juani, Scheltema & Kuzirian 1991). Such studies may give other diagnostic characters in addition to the hard parts. Genetic studies would also be useful, particularly in cases of sister species or for a species from many vent populations along a ridge, such as H. acredema from 21[degrees]N to 17[degrees]S.

Differentiating Morphologies in H. juani and H. acredema, Sister Species

Hard parts and body shape distinguish these very similar species as follows, H. juani listed first (j), H. acredema second

(a). The differences are based on adults of large populations of both species (Scheltema & Kuzirian 1991, Scheltema 2000).

Body: length >5 mm (j), <5 mm (a); appearance of scleritome: fuzzy (j), spiny (a) (Fig. 1D, 1E; 2A, 2B).

Radula: length of denticle number: 2 <1/2 length of denticle number 1 (j), >1/2 length of denticle no.1 (a); number of denticles: usually 5, sometimes 6 (j); usually 6, sometimes 7 (a) (Fig. 2C, 2D).

Copulatory spicules: 2 in each of paired sacs, morphologically very similar but up to 1 mm (j), up to 0.7 mm (a) (Fig. 2E, 2F); accessory copulatory spicules: curve relatively shallow (j), relatively deep (a), "bumps" 3-4 in both (Fig. 2G).

Sclerites: indicated by numbers 1-4, species by "j" or "a" in Figure 2H. Differences in sclerite size between the two species within a particular type as illustrated here are not significant, e.g., type 4 from the posterior end of the body can be up to ~130 lam in both species. The differentiating sclerites are type 1 from beside the pedal groove: convex on one side, straight on the other (j), curved on both sides (a); and type 4 over entire body: tips without swelling (j), tips often swollen, as seen under cross-polarized light (a) (Fig. 1F). (The species name acredema refers to this distinguishing character.)

Feeding

Most aplacophorans are carnivorous, but a few feed on detritus. Most neomenioids are predators on octocorals or hydroids, whose nematocysts are seen in their midguts. Helicoradomenia species, however, do not feed on cnidarians, as telltale nematocysts are lacking in their guts. The remains of food in two species, H. acredema and Helicoradomenia sp., were examined by transmission electron microscopy and found to be of a triploblastic metazoan, most probably a polychaete (Todt & Salvini-Plawen 2005).

Presence of Symbiotic Bacteria

Four types of epibiotic and endocuticular bacteria on sclerites and in body mantle cuticle have been demonstrated as symbionts in H. cf. aeredema and Helicoradomenia sp. (Katz et al. 2006). Unlike the nutritional necessity of symbiotic bacteria for many vent invertebrates, in Helicoradomenia the bacteria appear to have all the benefits of the association. Individual aplacophoran sclerites are covered by a cuticle as they are extruded from the forming epidermal cell (Haas 1981), a cuticle not related to the formation of the cuticular body mantle. The presence of two different cuticles might afford an explanation for why the symbionts are unusually both epibiotic and endocuticular in these species of Helicoradomenia.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

Reproduction

All aplacophorans, except for some brooders, seem to have planktonic lecithotrophic larvae (some perhaps demersal), determined from (1) egg size in the gonads (e.g., Scheltema 1987; and personal observations); (2) the occurrence of swimming larvae (Pruvot 1890, Baba 1938, Okusu 2002, Nielsen et al. 2007); or (3) settlement of larvae into experimental, in situ settlement boxes (Scheltema 1987) or onto panels (L. Mullineaux, pers. comm.). Active vent sites are ephemeral in that they die and new ones form with noticeable regularity. Recruitment into new areas is thus necessary if the associated fauna is to survive. Ongoing recruitment experiments at vent sites using substrates placed in situ demonstrate the ability of Helicoradomenia species to disperse.

DIVERSITY AND AGE OF HELICORADOMENIA SPECIES IN THE EAST PACIFIC

Diversity

The diversity of organisms in the East Pacific Rise, in genera and species, is many times greater than that in the Juan de Fuca system (Tunnicliffe 1988). The abundant limpet gastropods afford a good example of a mollusc fauna for comparing the two sectors; their diversity is tabulated from Desbruyeres et al. (2006) in Table 3.

Helicoradomenia species have the same dispersal capabilities as the limpets, with lecithotrophic planktonic larvae (for limpets, Desbruyeres et al. 2006; for Aplacophora, see earlier). Thus a direct comparison may be made between the limpets and Helicoradomenia (Table 3). Helicoradomenia has 6-fold greater number of species in the southern versus the northern sector (one species, Juan de Fuca; 6 species, East Pacific Rise). Similarly, limpets have five times more species in the southern sector (8 species, Juan de Fuca; 39 species, East Pacific Rise).

Vicariant Evolution in Helicoradomenia

Helicoradomenia juani and H. acredema are so similar morphologically to each other (Figs. 1, 2) and different from other species (examined but not yet described) that they presumably arose from a single species that inhabited hydrothermal vents when the East Pacific ridge was continuous before the Eocene subduction event. The two sectors, Juan de Fuca and East Pacific Rise, separated about 35 million years ago. Helicoradomenia juani is common and abundant in the San Juan sector, where there are no H. acredema. H. acredema is likewise common and abundant in the East Pacific Rise, where there are no H. juani. A single mitochondrial gene, CO1 has been sequenced only for H. juani (C. Schander, pers. comm.), and differentiation of the two species relies on their morphology (see earlier).

CONCLUSION

(1) The single most important genus of hydrothermal aplacophorans in number of species is the endemic neomenioid Helicoradomenia. It is known to occur in the East Pacific, Southwest Pacific, and Indian Ocean.

(2) The difference in diversity of Helicoradomenia species between the northern and southern sectors of the East Pacific is similar to that of limpets, both dispersing by lecithotrophic, planktonic larvae.

(3) Subduction of the Pacific plate under the North American plate caused a vicariant evolutionary event resulting in two very similar sister species, H. juani and H. acredema, that can, nevertheless, be identified from external and hard-part morphology.

(4) Symbiotic bacteria on sclerites and within the mantle cuticle of two Helicoradomenia species seem not to benefit the aplacophorans. Nutritionally, H. acredema and another Helicoradomenia species probably feed on polychaetes.

(5) Sectioned Helieoradomenia species indicate great similarity among them in internal anatomy and substantiate the adequacy of external and hard-part morphology including body shape and size, appearance of scleritome, sclerites, radula, and copulatory spicules for distinguishing species.

ACKNOWLEDGMENTS

All collections making this paper a possibility are from efforts of others, who have generously shared their collections. In particular the author recognizes, with thanks, the late Howard Sanders, Fred Grassle, Bob Hessler, Lisa Levin, Cindy Van Dover, Verena Tunnicliffe, Janet Voigt, Lauren Mullineaux, Susan Mills, Tim Shank, Amy Baco, Daniel Desbruyeres, and M. Segonzac, and all the sorters in the laboratories that they represent. The author also thanks Dmitry Ivanov for the fine photographs in Figure 1 from the Soviet collections made by the Akademik Keldysh. Not least of all those who have influenced the author's efforts in taxonomy has been Mel Carriker, whom the author first came to know at the University of North Carolina when Rudi Scheltema was a graduate student there. The author's friendship continued in Woods Hole when Mel directed the Systematics and Ecology program at the MBL. The author remembers the great excitement when Mel's wonderful SEM of a gastropod radula was published, when the blessing of that marvelous microscope first became available. Surely Mel revolutionized how the gastropod radula was seen and how it functioned. The author thanks Rich Lutz for inviting her to participate in this issue of the Journal of Shellfish Research as a memorial to Mel Carriker.

LITERATURE CITED

Baba, K. 1938. The later development of a solenogastre, Epimenia verrucosa (Nierstrasz). J. Dept. Agric. Kyusu Imperial Univ. 6:21-40.

Desbruydres, D., M. Segonzac & M. Bright. 2006. Handbook of Deep-Sea Hydrothermal Vent Fauna. 2nd ed. Denisia 18. Linz, Austria. 544 pp.

Haas, W. 1981. Evolution of calcareous hardparts in primitive molluscs. Malacologia 21:403-418.

Handl, C. H. & C. Todt. 2005. Foregut glands of Solenogastres (Mollusca): anatomy and revised terminology. J. Morphol. 265:28-42.

Katz, S., C. M. Cavanaugh & M. Bright. 2006. Symbiosis of epi- and endocuticular bacteria with Helicoradomenia spp. (Mollusca, Aplacophora, Solenogastres) from deep-sea hydrothermal vents. Mar. Ecol. Prog. Ser. 320:89-99.

Lonsdale, P. 1977. Clustering of suspension-feeding macrobenthos near abyssal hydrothermal vents at oceanic spreading centers. Deep-sea Res. 24:857-863.

Nielsen, C., G. Haszprunar, B. Ruthensteiner & A. Wanninger. 2007. Early development of the aplacophoran mollusca Chaetoderma. Acta Zool. 88:231-247.

Okusu, A. 2002. Embryogenesis and development of Epimenia babai (Mollusca Neomeniomorpha). Biol. Bull. 203:87-103.

Pruvot, G. 1890. Sur le developpement d'un Solenogastre. C. R. hebd. Seances l'Acad. Sci. Paris. 111:689-692.

Scheltema, A. H. 1987. Reproduction and rapid growth in a deep-sea aplacophoran mollusc, Prochaetoderma yongei. Mar. Ecol. Prog. Ser. 37:171-180.

Scheltema, A. H. 2000. Two new hydrothermal vent species, Helicoradomenia bisquama and Helicoradomenia acredema from the eastern Pacific Ocean (Mollusca, Aplacophora). Argonauta 14:15-25.

Scheltema, A. H. & D. L. Ivanov. 2004. Use of birefringence to characterize Aplacophora sclerites. Veliger 47:153-160.

Scheltema, A. H. & A. M. Kuzirian. 1991. Helicoradorneniajuani gen. et sp. nov., a Pacific hydrothermal vent Aplacophora (Mollusca: Neomeniomorpha). Veliger 34:195-203.

Todt, C. & L. V. Salvini-Plawen. 2005. The digestive tract of Helicoradomenia (Solenogastres, Mollusca), aplacophoran molluscs from the hydrothermal vents of the East Pacific Rise. Invert. Biol. 124:230-253.

Tunnicliffe, V. M. 1988. Biogeography and evolution of hydrothermal vent fauna in the eastern Pacific Ocean. Proc. R. Soc. Lond. B. Biol. Sci. 233:347-366.

Tunnicliffe, V. M., M. R. Fowler & A. G. McArthur. 1996. Plate tectonic history and hot vent biogeography. In: C. J. McLeod, P. A. Tyler & C. L. Walker, editors. Tectonic, magmatic, hydrothermal, and biological segmentation of Mid-Ocean Ridges. Spec. Publ. (Geol. Soc.). pp. 225-238.

Woods Hole Oceanographic Inst. 2007. The Discovery of hydrothermal ventswww.divediscover.whoi.edu/ventcd/index.html

AMELIE H. SCHELTEMA *

Biology Department MS #34, Woods Hole Oceanographic Institution, Woods Hole, MA 02543

* Corresponding author. E-mail: ascheltema@whoi.edu
TABLE 1.
Distribution of Helicoradomenia species in the East Pacific based on
author's examinations and unnamed, figured species in Desbruyeres et
al. (2006). Specimens provided by Woods Hole Oceanographic Institution,
IFREMER, and Field Museum (Chicago).

 Juan de Fuca

 Latitude

 49[deg- 48[deg- 41[deg- 21[deg-
Species rees]N rees]N rees]N rees]N

H.juani + + +
H. acredema +
H. bisquama +
Helico. sp. 1 +
Helico. sp. 2
Helico. sp. 3
Helico. sp. 4

 East Pacific Rise Gal.

 Latitude

 13[deg- 9[deg- 17[deg- 21[deg-
Species rees]N rees]N rees]S rees]S 0[degrees]

H.juani
H. acredema + ? ? +
H. bisquama
Helico. sp. 1
Helico. sp. 2 + + +
Helico. sp. 3 ?
Helico. sp. 4 +

Gal. = Galapagos Rift.

TABLE 2.
Helicoradomia species examined from the southwest Pacific
back-arc basins and Indian Ocean Triple Junction. Specimens
provided by Robert Hessler, Cindy Van Dover, and IFREMER.

 Southwest Pacific

No. Fiji Back-Arc 16[degrees]-18[degrees]S,
 Basin 173[degrees]-179[degrees]W
Lau Back-Arc Basin 22[degrees]S, 176[degrees]W
Mariana Back-Arc
 Basin 18[degrees]S, 144[degrees]E
 Indian Ocean Triple Junction
Kairei mussel field 25[degrees]S, 70[degrees]E

 Southwest Pacific

No. Fiji Back-Arc 2-3 species, 8 specimens
 Basin
Lau Back-Arc Basin 1 species, 3 specimens
Mariana Back-Arc
 Basin 1 species, 3 specimens
 Indian Ocean Triple Junction
Kairei mussel field 1 species, 3 specimens

TABLE 3.
Diversity of genera and species of limpets on the northern and
southern sectors of the East Pacific vent and ridge systems,
enumerated as occurring in both sectors or as restricted to only
one sector or the other. Comparison is made to the aplacophoran
genus Helicoradomenia, with the same diversity but with fewer
species. Limpet data compiled from Desbruyeres et al. (2006).

 North & South North Only

 No. No. No. No.
Taxon genera species genera species

Lepetsoidea 1 1 -- --
Lepetodriloidea 3 -- 1 5
Neomphalina
 Neomphalidae 1 -- 1 2
 Peltospiridae -- -- 1 1
Totals 5 1 3 8
Helicoradomenia 1 -- -- 1

 South Only

 No. No.
Taxon genera species

Lepetsoidea 1 5
Lepetodriloidea 2 13
Neomphalina
 Neomphalidae 5 8
 Peltospiridae 7 13
Totals 15 39
Helicoradomenia -- 6
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Author:Scheltema, Amelie H.
Publication:Journal of Shellfish Research
Article Type:Report
Geographic Code:1USA
Date:Mar 1, 2008
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