Agnezia monnioti and Styela gagetyleri, New Deep-Sea Ascidians Specialized for Life within and below the

Oxygen Minimum Layer in the Arabian Sea Author(s): Craig M. Young and Elsa Vzquez Source: Invertebrate Biology, Vol. 116, No. 3, (Summer, 1997), pp. 262-276 Published by: Blackwell Publishing on behalf of American Microscopical Society Stable URL: http://www.jstor.org/stable/3226903 Accessed: 30/05/2008 09:57
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Invertebrate Biology 116(3): 262-276. ? 1997 American Microscopical Society, Inc.

Agnezia monnioti and Styela gagetyleri, new deep-sea ascidians specialized for life within and below the oxygen minimum layer in the Arabian Sea
Craig M. Youngl
a

and Elsa Vaizquez2

1Departmentof Larval Ecology, HarborBranchOceanographic Institution, Ft. Pierce, Florida34946, USA 2 Departamento de Ecoloxia e Bioloxia Animal, Facultadede Ciencias do Mar,Universidadede Vigo, 36200 Vigo, Spain Abstract. Two new species of solitary ascidians from the deep sea off Oman, Arabian Sea, are described. Agnezia monnioti n. sp. is from the abyssal plain at 3162 m depth. Whereas many deep-sea ascidians have reduced branchial ciliation and exploit the velocity gradient in the benthic boundary layer to induce internal flow, this species has strong ciliation and a siphonal arrangement that appears inappropriate for using ambient water currents for filtration. Styela gagetyleri n. sp. is found at a depth of 368 m, which is in the middle of a persistent oxygen minimum zone. The branchial sac of this species has a reduced number of folds and therefore fewer cilia for food collection and less surface area for oxygen exchange than shallowwater congeners. We hypothesize that reduced filtration capacity is made possible by an unusually high flux of organic material to the sea floor in this region. The observed reduction in branchial surface area in a persistent hypoxic zone suggests that branchial complexity in ascidians is more important for feeding efficiency than gas exchange. Affinities of these species with other members of their respective genera are discussed and an appendix with the synonyms and localities of species in the genus Agnezia is included. Additionalkey words: filter feeding, IndianOcean, monsoons, Tunicata,Urochordata, Ascidiacea

Deep-sea ascidians show a number of unusual morphological and functional modifications, including long stalks, simplification of the branchial apparatus, unciliated branchial sacs, and carnivory (Monniot & Monniot 1975, 1978, 1985, 1991a; Monniot 1979). Colonial species are rare in deep water, and with few exceptions, abyssal ascidians tend to have smaller body sizes than their shallow-water counterparts (Monniot 1979). All of these trends and features have been attributed to low food supplies (Monniot 1979). Although plankton and other suspended organic particles are indeed scarce in most of the deep sea (Gage & Tyler 1991), seasonal plankton blooms can produce major pulses of detrital food at abyssal depths both in mid-oceanic regions and near continental land masses (Lampitt 1985; Rice et al. 1986). If food limitation is indeed responsible for the many unusual feeding modes that have evolved in deep-sea ascidians, one might predict that species more similar to shallow-

water forms would be found in deep-sea regions where food is plentiful. The deep-sea tunicate fauna is known mostly from specimens dredged or trawled during major oceanographic expeditions, beginning with the Challenger expedition and continuing to the present day (Monniot & Monniot 1978). Collections of ascidians from the Indian Ocean were obtained by the John Murray/Mabahiss Expedition in 1933 (Kott 1957), by the International Indian Ocean Expedition in 1963-64 (Millar 1988), and by three French expeditions between 1977 and 1981 (Monniot & Monniot 1984). Several species of interstitial sorberaceans were described by Monniot & Monniot (1984) from the latter cruises, and Kott (1957) tentatively assigned a single ascidian species from 2000 m to the genus Hexacrobylus. With these few exceptions, the tunicate fauna of the Indian Ocean is known only for depths less than 200 m. Recent interest in oceanographic processes influencing global change and the flux of nutrients in the world a Authorfor correspondence: Dept. of Larval Ecology, Har- ocean prompted the selection of a dynamic region off bor Branch Oceanographic Institution,5600 U.S. Hwy. 1 the coast of Oman in the Arabian Sea as a major site N., Ft. Pierce, FL 34946, USA. E-mail:youngc@hboi.edu for international cooperative research (Smith et al.

New ascidians from the deep Arabian Sea

263

'.. ':.':

; ':

~ ,'

'

0.

'.

' ?

Fig. 1. A portion of the northern Arabian Sea off Oman, showing the general location of the sampling effort (delimited by square in A) and bathymetric contours (B) with the type localities of Styela gagetyleri and Agnezia monnioti indicated

by asterisks. 1991). This region is strongly influenced by an annual northeast monsoon, which causes coastal upwelling of nutrients. The upwelling, coupled with aeolian dusts from the deserts of the Middle East and North Africa, fuels strong primary production in the surface layers. Plankton sinking below the mixed layer decompose to form a persistent zone of very low oxygen between approximately 50 and 1300 m depth. The John Murray/Mabahiss Expedition sampled in this zone with an Agassiz trawl and, finding very little life, concluded that the zone was virtually azoic (Rice 1986). During a recent cruise on the British research vessel RRS Discovery, zoologists focusing on various components of the benthic fauna resampled this zone and discovered an abundant and surprisingly diverse fauna there. Many of the species, notably molluscs, appear to have traits (e.g., hemoglobin) that permit occupation of a zone with very low oxygen (G. Oliver, pers. comm.). The deep-sea floor below the oxygen minimum zone has an unusually high content of both organic and inorganic carbon (Smith et al. 1991); indeed, the surface sediment of undisturbed box cores from abyssal depths often appears green because of the large amount of phytoplankton detritus arriving at the bottom (J. Gage, pers. comm.; CMY, pers. ob.). Whereas flux of organic carbon to the abyssal sea floor typically amounts to only about 1 mg m-2d-1 in low-latitude oceanic systems (Honjo 1980), carbon flux in the Western Arabian Sea averages 5 mg m-2d-I for most of the year and peaks near 20 mg m-2d-1 during the summer months (Haake et al. 1993) because of the influence of the monsoon (Nair et al. 1989). Comparable fluxes have been reported in the Panama Basin (Honjo 1982), but they are not typical of the deep sea as a whole. In this paper we describe two new species of deepsea ascidians from the Arabian Sea, both of which have morphological features that would be viewed as functionally inefficient in less productive regions of the world ocean. Styela gagetyleri n. sp. lives in the oxygen minimum zone but, paradoxically, has a reduced branchial apparatus with less surface area for gas exchange than related species living in well-oxygenated habitats. Agnezia monnioti n. sp. inhabits the sea floor at depths greater than 3000 m. Unlike most deep-sea ascidians, its siphons are oriented in such a way as to prevent efficient food collection with the aid of ambient water currents. Methods The benthic fauna was sampled off the coast of Oman (Fig. 1) during a cruise of RRS Discovery between 14 October and 2 November 1994. Some 45 boxcores and 496 cores from 44 multicore deploy-

264 ments were taken between 94 and 3300 m to sample the infaunal meiofauna and macrofauna. Megafauna and macrofauna, including the deep-sea ascidians described here, were collected by Agassiz trawl (8 deployments) and epibenthic sledge (5 deployments) on the slope and abyssal plain. The entire sample of mud and rock collected in each Agassiz trawl (at times as much as 2 tons) was sieved through a 5-mm mesh sieve and some subsamples were sieved through a 300-jtm sieve. Ascidians were separated, washed, and maintained for short periods of time in a cold room at 4?C before fixation in 5% buffered formalin. After fixation for one week, they were transferred into 70% ethyl alcohol. Ascidians were dissected and stained using the method of Monniot & Monniot (1972). For scanning electron microscopy (SEM), branchial sacs were dissected from formalin-fixed specimens, rinsed with distilled water, dehydrated through a graded series of ethyl alcohol, and critical point dried. The tissues were sputter coated with gold and examined with a Hitachi S-510 scanning electron microscope. Results
Family Agneziidae MONNIOT& MONNIOT1991

Young & Vazquez (posterior) region to the tubes of giant foraminiferans and to small sand grains (Fig. 2A,B). The test is thin and transparent with few adherent sand particles. Except for the posterior end, sand particles are most abundant in the region of the siphons. The largest of 101 animals collected measured 26 mm in the anteriorposterior axis and 16 mm wide in the sagittal plane. The smallest individual was 15 mm long and 10 mm wide. The branchial siphon is apical (Fig. 2A) with 8 lobes. The atrial siphon is positioned dorsally, /2 to 2/3 of the length of the animal away from the branchial siphon (Fig. 2A). Its margin is divided into several irregularly shaped lobes. The body wall is very thin and transparent (Fig. 2C). Muscle bands encircle both siphons, with the musculature surrounding the atrial siphon being most extensive (Figs. 2C, 3C). Longitudinal muscle bands (-25) extend from the siphons and the intersiphonal area to each side of the animal (Fig. 3C). Each band subdivides on each side into 3 or 4 bands, which join the bands on the opposite side of the body posteriorly and ventrally. There are no transverse muscles. There are 4 rings of oral tentacles (Fig. 3C). The first has very short and numerous tentacles. Tentacle length increases in each subsequent ring, with the filamentous tentacles in the second and third ring being longer than the diameter of the siphon. In the animals we dissected, there were 10 tentacles in the second ring, 11 in the third, and 6 in the fourth. The prebranchial area is very large: equal to the width of an infundibulum. A strong velum, equal in width to the length of the prebranchial area, is found anterior to the peripharyngeal groove. The peripharyngeal groove forms a deep "V" on the dorsal side (Fig. 3C). The opening of the neural gland is marked by a small piece of tissue resembling a short languet. The dorsal lamina is reduced, consisting of 3 long, wide languets. The branchial sac has 12 rows of 11 infundibula (Fig. 2D), with strongly ciliated stigmata (Fig. 2F) coiled 8 times to form a nearly perfect square (Figs. 2D, 3A, 4). Primary transverse vessels separate each 2 rows of infundibula (Fig. 3A), but intermediate transverse vessels were not observed. Each vessel has 11 large finger-like papillae (Fig. 3A), each corresponding to one infundibulum. Each stigma is inter-

Agnezia monnioti n. sp. (Figs. 2, 3) Species description Holotype. U.S. National Museum of Natural History, Smithsonian Institution, Washington D.C. (Catalog number USNM-23069). Station 12719/1 Type locality. Discovery (19?07.73'N, 58?38.83'E), 1 November 1994; 3162 m depth in the Murray Basin of the Arabian Sea (Fig. 1). Paratypes. Harbor Branch Oceanographic Institution, Florida (Catalog number HBOI 096:00133) and Museum National d'Histoire Naturelle of Paris (Catalog number 3 AGN.A 29). Etymology. Agnezia monnioti is named for Claude Monniot of the Museum National d'Histoire Naturelle (Paris), who has contributed more than any other individual to our understanding of the systematics, functional morphology, distribution, and ecology of deepsea ascidians. Description. Body dorso-ventrally or laterally flattened, attached by hair-like tunic processes in the basal

Fig. 2. External and internal anatomy of Agnezia monnioti. A: External view showing locations of branchial (BS) and atrial (AS) siphons B: Close-up of giant foraminiferans (arrowheads) adhering to posterior end of the ascidian. C: Body wall and visceral mass (V) with branchial sac removed, showing muscle bands (M) illustrated in Fig. 3C. D: Spiral stigmata forming infundibula in the branchial sac. E: Portion of the branchial sac, showing ciliated stigmata in the background and crossed parastigmatic vessels in the foreground. SEM. F: Close-up view of the lateral cilia on a stigma. SEM.

New ascidians from the deep Arabian Sea

265

266

Young & Vazquez

B A

Fig. 3. Internalfeaturesof Agnezia monnioti (camera lucida drawings). A: Portion of the branchial sac, showing two coiled stigmata (CS) between two transverse vessels (TV); parastigmatic vessels (PV) and papillae(P). B: Gonad(GO) situated in the gut loop (G) showing the anus (A), sperm duct (SD), and oviduct (0). Note thatthe gonoducts
terminate at a 90? angle. C: Interior

view of the body wall (branchialsac removed) showing positions of the gut (G), gonad (GO), branchialtentacles (BT), body wall musculature (M), neural gland (N), branchialsiphon (BS), and atrialsiphon (AS).

AS
5 mm

rupted by parastigmatic vessels forming an "X" (Figs. 2E, 3A). The only branchial tissue is that surrounding the stigmata. The gut loop is on the left side of the body (Fig. 2C). The stomach is smooth, not well defined, and the intestine and rectum do not form a secondary loop (Fig. 3B). The anus opens near the cloacal siphon. The gonad is situated in the gut loop (Fig. 3B). The ovary is tubular and branching, with testicular lobes attached to the posterior end of the ovary. Genital ducts follow the course of the rectum; the sperm duct ends in a papilla just before the anus and the oviduct ends halfway up the rectum (Fig. 3B). The terminus

of the oviduct forms a 90? angle and faces posteriorly (Fig. 3B). Relationship to other species in the genus
1898 The names of the genus Agnesia MICHAELSEN HUNTSMAN 1912 were and the family Agnesidae

changed by Monniot & Monniot (1991a) to Agnezia nom. nov. and Agneziidae nom. nov. because the gastropod genus Agnesia KONINCK 1883 and its family

Agnesiidae had taxonomic priority. All species of Agnezia in the Southern hemisphere were synonymized by Millar (1960) and Kott (1969a)

New ascidians from the deep Arabian Sea but Monniot & Monniot (1983) separated the antarctic and subantarctic species. The 12 valid species of Agnezia with their synonyms and known localities of occurrence are summarized in the Appendix. These species can be subdivided into two groups. The first group has a single row of stigmata between each pair of consecutive transverse vessels and includes: A. atlantica (MONNIOT MONNIOT & 1973) from the North Atlantic at 2100-4452 m depth (Monniot & Monniot 1973, 1974a; Millar 1982), A. biscoei (MONNIOT & MONNIOT 1983) from Antarctica (Monniot &

267 is not complete and the muscle bands are short. Present, sometimes, are intermediate transverse vessels and exoinfundibula (funnel-like structures formed of one to several stigmata which are not found on either the longitudinal vessels or on the axis of the folds). The stigmata are coiled 4 or 5 times (Van Name 1945). Agnezia tenue (MONNIOT & MONNIOT 1983) is an interstitial species collected from 18 m depth in the Antarctic. The stigmata coil one and a half times and the transverse vessels have just one papilla on the right side and none on the left (Monniot & Monniot 1983). Agnezia monnioti is only the fourth deep-sea species to be described in this genus and the first in the Indian Ocean. The other bathyal and abyssal species are: Agnezia atlantica from 2100-4452 m in the North Atlantic (Monniot & Monniot 1973, 1974a; Millar 1982), A. celtica from 3903-3917 m in the North Atlantic and Argentina, and A. orthenteron from 1900-2090 m in the Japan Sea. Habitat and associated fauna

Monniot 1983, 1994; Kott 1969a,b as A. glaciata; Monniot & Monniot 1974b as A. glaciata), A. glaciata (Michaelsen 1898) from Antarctica, the subantarctic, and Southern California from 23-150 m depth (Van Name 1945; Millar 1960; Monniot 1978; Monniot & Monniot 1983; Kott 1985), and A. himeboja (OKA 1915) from Japan (Tokioka 1949; Nishikawa 1980,
1991).

The sediment at the 3162-m site where Agnezia monnioti was collected consisted of very fine silt with 1974b) is an antarctic and subantarctic species from 10-61 m depth. It has unperforated branchial tissue no rocks but with frequent large (up to 2-cm long) between the infundibula and the stigmata coil 3 or 4 foraminiferans, Rhabdammina discreta, resting on the times. The main difference between this species and surface of the mud. All individuals of A. monnioti A. monnioti is that the former has spatially separated were attached to one or more foraminiferan tests. male and female gonoducts. The male duct terminates These elongate tests apparently form a sort of raft that on the left side of the atrial chamber and the female may help prevent the ascidians from sinking into the duct ends on the right side, where the eggs are incu- soft ooze. The oxygen concentration was 1.0 ml/1, bated (Monniot 1970, 1978; Monniot & Monniot which is about one order of magnitude higher than that of the oxygen minimum zone (Gage 1995). 1983). The fauna collected at depths over 3000 m in the Agnezia capensis (MILLAR 1955) from South Africa and Mozambique lives between 10 and 35 m depth. Murray Basin of the Arabian Sea was dominated by Its languets are placed towards the left side and the molluscs, including bivalves in the genera Limopsis, intestine forms a secondary loop (Millar 1955; Mon- Bentharca, Bathyarca, Nucula, Ledella, Propeamussium, Vesicomya, Lucina, and Solemya, numerous niot & Monniot 1976a). small gastropods including turrids and cephalaspideans Agnezia celtica (MONNIOT & MONNIOT 1974a) is from the North Atlantic and Argentina at 3903-3917 (G. Oliver, pers. comm.), and an unusually diverse m depth. Its musculature does not extend through the aplacophoran fauna (A. Scheltema, pers. comm.). dorsal side of the animal and the ventral side has no Many of the Limopsis supported epizoic inarticulate musculature at all. The stigmata coil 4 or 5 times and brachiopods, Pelagodiscus atlanticus. Ophiuroids in there is a very small gut loop relative to the total sur- the families Ophiuridae, Ophiocanthidae, and Amface of the body wall (Monniot & Monniot 1974a, phiuridae were common, as were at least four species 1976b). Agnezia orthenteron (REDIKORZEV1941) is of large asteroids and holothuroids in the genus Ypsifrom the Sea of Japan between 1900 and 2090 m lothuria (A. Campbell, pers. comm.). Zoantharian and depths. It has circular muscles on the siphons and fine actinarian sea anemones were abundant, and one colradial muscles diverging from the siphons but disap- ony of a pennatulid, Umbellula sp., was found. Porpearing near the central part of the mantle body (Ni- tunid and porcellanid crabs were well represented, as shikawa 1991). Agnezia septentrionalis (HUNTSMAN was the eryonid crab Polycheles sp. and the giant am1912) lives between 30 and 86 m depths in British phipod Eurythene gryllus. Overall, the fauna was not Columbia, Alaska, and the Bering Sea. Its musculature unusual for an abyssal plain and many of the genera
follows. Agnezia arnaudi (MONNIOT & MONNIOT

The second group, which includes A. monnioti n. sp., consists of species with two infundibula between each pair of transverse vessels. Agnezia monnioti is distinguished from the other species in this group as

268 and species are the same as found at comparable depths elsewhere in the world.
Family Styelidae SLUITER1895

Young & Vazquez The branchial sac has just one fold on the right side (Fig. 4D). On the left sides of most individuals, there are no true folds, but only longitudinal vessels situated very close to each other where the folds would be (Fig. 4D). However, in a few individuals, there is a single true fold on the left side. In others, there is no evidence of a left fold at all. There are two columns of stigmata between every adjacent pair of longitudinal vessels. The branchial formulas of three adult animals (showing the number of longitudinal vessels lying between the Dorsal Lamina, "DL," and Endostyle, "E," on each side of the body) for three different observed cases of branchial reduction are: DL right 7-13-18 E DL left 0-11-26 E DL right 8-8-21 E DL 0-7-9-9-4 E DL right 8-10-22 E DL left 27 E The gut forms a very pronounced S-shaped secondary loop and the first loop is nearly closed (Fig. 5). The stomach is in the shape of an elongate olive, with 18 longitudinal folds, a gastric caecum at the posterior end, and a gastro-intestinal connective from the middle part of the stomach to the intestine. The anus ends very near the atrial siphon (Figs. 4B, 5). The edge of the anus is smooth. There are 10 large endocarps on the right side and 5 on the left side, scattered over the body wall (Fig. 5). Each side of the body has a single gonad, situated anteriorly. Each ovary is long and convoluted and has at least 14 testicular lobes situated at the posterior end (Figs. 4B, 5). A sperm duct arises from each male lobe and the ducts all join together in a common sperm duct at the posterior end of the ovary. The sperm duct courses along the ovary to open in the atrial cavity just behind the female opening (Fig. 5). Relationship to other species in the genus Reduction of the branchial sac as observed in Styela gagetyleri has been described only in antarctic and abyssal species. Among the abyssal species, S. tenuibranchia MONNIOT, MONNIOT, & MILLAR 1976 and S. ordinaria MONNIOT & MONNIOT 1985 have no branchial folds whatsoever, and S. polypes MONNIOT,MONNIOT, & MILLAR 1976 has one fold on each side, with

Styela gagetyleri n. sp. (Figs. 4, 5) Species description Holotype. U.S. National Museum of Natural History, Smithsonian Institution, Washington D.C. (Catalog number USNM-23070). Station 12697#1 Discovery Type locality. (19?11'N, 58?18'E), 24 October 1994; 394 m depth on the continental slope off Oman, Arabian Sea (Fig. 1). Paratypes. Harbor Branch Oceanographic Institution, Florida (Catalog number HBOI 096:00134) and Museum National d'Histoire Naturelle of Paris (Catalog number S1 STY.A 247). Etymology. This species is named in honor of John Gage, Principal Scientific Officer on Discovery during the Arabesque cruise, and Paul Tyler, his long-time colleague and co-principal investigator on the same cruise. Gage and Tyler have collaborated closely on many aspects of deep-sea biology for more than 2 decades. Their names are so closely tied to long-term deep-sea studies and to studies of deep-sea reproduction that it is appropriate to join their names permanently in the specific epithet of Styela gagetyleri. Description. The body is hemispherical when contracted, and all 54 specimens we examined were attached posteriorly to small stones, sharks' teeth (which are very abundant in this zone), and other hard surfaces (Fig. 4A). Body size is small, the largest individual being 4 mm high (anterior-posterior axis) 11 mm long (dorso-ventral axis), and 10 mm wide, and the smallest 3 mm high, 7 mm long, and 4 mm wide. Test is thin but firm and leathery, covered with very fine brownish sand. Several tiny white sponges were found encrusting the siphonal region in every specimen examined (Fig. 4A). The siphons are apical and separated in the holotype by a distance of 3 mm. The basal region of the ascidian, attached firmly to the substratum, is very thin and soft without any hair-like processes. The body wall is very thin, transparent, and fragile (Fig. 4B). There are -30 oral tentacles in two circles and a third circlet of very tiny tentacles (Fig. 4C). There is no space between the peripharyngeal groove and the branchial sac (Fig. 4C). The dorsal tubercle is a round opening situated on a small protuberance of the prebranchial area (Fig. 4C). The atrial siphon has a circlet of small capitate tentacles. This circle extends two wide projections as a velum towards the oral siphon, one to the right and the other to the left (Fig. 5). The edge of this projection also has tentacles.

the right fold being lower than the left one (Monniot et al. 1976). Styela longiducta MONNIOT& MONNIOT 1985 from Comores has only one fold on each side of the branchial sac and only one endocarp on the body

New ascidians from the deep Arabian Sea

269

3mm

Fig. 4. External and internal anatomy of Styela gagetyleri. A: External view of an individual attached to a shark tooth, showing locations of the siphons (arrowheads). Note the white sponges encrusting the anterior end of the animal. B: Body wall and attached structures, following removal of branchial sac and tunic. Siphons, gut loop, gonads, and endocarps are visible (see Fig. 5 for labels). C: Close-up of incurrent siphon region viewed from the inside. Note branchial tentacles (T) and neural gland (N). D: Branchial sac, stained and removed from the body wall, showing a single fold (F) on the right side. A second concentration of longitudinal vessels (L) on the same side does not form a true fold.

wall. Also the gonoducts are longer than the gonads (Monniot & Monniot 1985). The antarctic species Styela insinuosa (SLUITER 1912) and Cnemidocarpa sericata (HERDMAN 1888) have no branchial folds. Styela schmitti simplex MILLAR 1960 has three folds on the right side and two on the left (Kott 1969b). Styela asterogama MILLAR 1975 from a depth of 70

m off Bali has two folds on the right and one on the left, with one gonad on each side. The grouped testicular lobes are separate from the ovary. The test has hair-like processes on the lower half of the body, the branchial sac has one row of stigmata between each pair of longitudinal vessels, and the rows of stigmata are crossed by parastigmatic transverse vessels (Millar 1975).

270

Young & Vazquez

Fig. 5. Internalbody wall (branchial sac removed) of Styela gagetyleri (camera ludica drawing), showing the gut (G), testes (T), ovary (0), endocarps (E), neural gland (N), branchialsiphon (BS), and atrialsiphon (AS) with attachedvelum. Habitat and associated fauna

3mm deep sea. One of the species we describe here, Styela gagetyleri, has a reduced branchial sac even though it lives at bathyal depths in an oxygen minimum zone. The other species, Agnezia monnioti, has a fully developed branchial apparatus with ciliation and a siphon orientation similar to those of shallow-water congeners, even though it lives at abyssal depths. Thus, both species deviate from the expected morphologies of deep-sea ascidians. Branchial reduction in Styela gagetyleri In small abyssal styelids, reduction in body size generally also involves reduction in the volume and number of the gonads and reduced complexity of the branchial sac (Monniot & Monniot 1978). Solitary shallow-water styelids normally have 4 branchial folds on each side. In the small abyssal species, the branchial folds become less numerous and less marked, and may disappear, leaving only groups of vessels (Styela crinita, Cnemidocarpa sericata, and Styela minima). Often, the branchial sac seems to remain in a juvenile state (Monniot & Monniot 1978). This reduction in branchial sac complexity is somewhat puzzling. One might argue that a reduction in branchial folds is necessary in species with small body size because there is insufficient room to accommodate extra folds. However, small solitary styelids in shallow water do have a full complement of 8 branchial folds. The branchial sac is almost certainly the major surface for oxygen

Styela gagetyleri occurred on small pebbles and sharks' teeth (Fig. 4A) in a muddy habitat between 340 and 400 m depth. Oxygen concentrations in this general depth zone ranged from 0.15 ml/l on the bottom at 400 m (measured on the supernatant of tube cores) to 0.63 ml/1 in the water column at 300 m (Gage 1995). The oxygen level near the surface (5 m) was about 1 order of magnitude higher (4.1-4.3 ml/1). The fauna in the hypoxic zone was more abundant than expected. Styela gagetyleri and a nest-building mussel, Amygdalum sp., were the dominant organisms. Other animals occurring at the same site included the spider crab Encephaloides armstrongi, a vesicomyid clam, and two species of gastropods. Discussion Many of the convergences in body form and function that characterize deep-sea tunicates are unknown or uncommon in shallow water. These include carnivory in the families Octacnemidae and Ascidiidae, exploitation of interstitial habitats in the diminutive members of the class Sorberacea, reduction of the branchial sac, elimination of cilia, and reduction in body organs not directly used for reproduction or food collection (Monniot & Monniot 1978, 1991a,b; Kott 1989). Long stalks for exploiting ambient water currents are found in shallow-water species (Young & Braithwaite 1980) but are especially common in the

New ascidians from the deep Arabian Sea

271

Pharyngodictyon caulifos

Araneum pedunculatum

I
`J
Culeolus elegans

Cnemidocarpa digonas

L
Fig. 6. Examples of deep-sea stalkedand unstalkedascidianswith unciliatedbranchialsacs or reduced branchial ciliation, showing the arrangementsof the incurrent and
Fungulus

excurrent

siphons.

Outlines

are

Minipera papillosa

redrawn from the original species descriptions, so some are probably not good representations of the posturesof the living animals. One strategy for a filter-feeder living in a nutrientpoor habitat is to reduce the amount of somatic tissue that must be nourished while simultaneously increasing the efficiency or size of the food collection apparatus. Monniot & Monniot (1989) documented an example of this phenomenon within a single species of Halocynthia from the Galapagos Islands. The deepwater form had less massive tissues than the shallowwater form, but the complexity of the branchial sac, as measured by the number of stigmata per mesh, increased as a function of depth. Complex, folded branchial sacs increase efficiency of particle capture (FialaMedioni 1974). Even if increased feeding efficiency is not required in the Arabian Sea, it is difficult to envision selective pressures that would result in branchial reduction in S. gagetyleri. Perhaps in a low oxygen

exchange in ascidians (Goodbody 1974), so one might expect that this structure would increase in size to compensate for hypoxic conditions. Because the branchial surface area in S. gagetyleri is reduced rather than expanded, we must conclude that the surface area for gas exchange is not limiting even at very low oxygen concentrations. With a decrease in temperature, the rate of oxygen diffusion across a membrane should decrease more slowly (Qlo < 2) than metabolic rate (QIo > 2) (Giese 1968), so a relatively smaller branchial sac may be adequate in deeper waters. Small filterfeeding bivalves show a similar reduction in complexity and size of the filtering apparatus in the deep sea (Allen 1979) and this reduction has been attributed to a reduced metabolic oxygen demand in deep-sea species (Allen 1979).

272

Young & Vazquez

Agnezia atlantica

Agnezia celtica

Proagneziadepressa

Fig. 7. Siphon arrangements in the family Agneziidae. See Table 1 for bathymetric distributions. Top row: deep-sea species with siphons directed dorsally and ventrally. Agnezia atlantica is depicted with anterior siphons in this drawing, but the literature description (Monniot & Monniot 1973) indicates that the siphons are spatially separated, on two angles of a triangular body. Middle row: Agnezia monnioti from the deep sea and two shallow-water species having a similar siphon arrangement. Bottom row: shallowwater species with siphons inserted on the anterior end and directed either anteriorly or dorsally and ventrally.

monnioti Agnezia

Agnezia septentrionalis

Agneziatenue

Agnezia capensis

Agneziaglaciata

Agnezia arnaudi

Agneziabiscoei

environment, selection favors reduction of tissues, including the branchial sac itself, that consume oxygen. Siphon orientation and feeding in Agnezia monnioti Many deep-sea species orient siphons to take advantage of ambient water currents for filtration, thereby minimizing the energy expenditure required for feeding (Young & Braithwaite 1980; Kott 1989) (Fig. 6). Stalked forms generally have the branchial (incurrent) siphon pointed posteriorly and the atrial (excurrent) siphon pointed anteriorly. By swaying with each change of current direction, the branchial siphon is always presented to the current and flow through the branchial sac is induced by dynamic pressure (Young & Braithwaite 1980; Kott 1989). Unstalked ascidians may use ambient water currents

for filtration if the siphons are positioned at different heights in the velocity gradient of the benthic boundary layer. Specifically, if the branchial siphon is positioned nearer the bottom than the atrial siphon, the Bernoulli effect will result in a pressure difference that will draw water through the branchial sac. This Bernoulli effect is augmented by viscous entrainment and, if the incurrent siphon is facing upstream, by dynamic pressure (Vogel 1978). If the atrial siphon faces directly upward, flow will be induced regardless of the direction from which the current comes. However, none of these passive filtration mechanisms will work if the siphons are of equal length and inserted on the anterior end, as in some shallow-water phlebobranchs (Kott 1989) or if the branchial siphon opens higher in the water column than the atrial siphon. If Agnezia monnioti followed the typical deep-sea

New ascidians from the deep Arabian Sea

Table 1. Siphon arrangements and bathymetric distributions of Agnezia and Proagnezia species. References and detailed bathymetric data are given in the Appendix. Bathymetric distribution (m)

273 which amounts to roughly 9.5 X 105 mj m-2d-' of available energy (conversion factor: 47.7 j/mg C for phytoplankton; Platt & Irwin 1973). A typical individual of A. monnioti has an incurrent siphon diameter of -2 mm (3.14 mm2 siphon area), so it should be able to collect passively enough particulate carbon to yield about 3 Lj of energy per day. Metabolic rate has not been measured for any deep-sea ascidian, so we must estimate the mass-specific metabolic rate of A. monnioti by scaling the metabolic rate of a shallow-water relative to an appropriately lower temperature, using
Qlo = 2. Phallusia mamillata consumes maximally 846 jLg 02 h-Ig dry wt-2 at a temperature of 15?C (Fiala-

Species

Siphons anterior, but directed dorsally and ventrally like two angles of a triangle: 2,100-4,680 Agnezia atlantica 3,903-4,758 Agnezia celtica 5,850-5,860 Proagnezia depressa Both siphons on anterior end and directed anteriorly: 20-61 Agnezia arnaudi 37-121 Agnezia biscoei 10-35 Agnezia capensis 10-115 Agnezia glaciata Branchial siphon on anterior end, atrial siphon on dorsal side: 3,162 Agnezia monnioti 30-86 Agnezia septentrionalis 18 Agnezia tenue Unknown siphon arrangement: 5-39 Agnezia himeboja unknown Agnezia krausei 1,900-2,090 Agnezia orthenteron

pattern, it would have reduced cilia in the branchial sac and siphons oriented for the capture of currents (Fig 6). However, this species is unusual in that its branchial siphon is pointed directly upward and the atrial siphon is directed to the side (Figs. 2A, 7). This siphonal arrangement cannot be used for exploiting ambient flows; indeed, in the absence of ciliary currents, any flow should drive water through the animal in reverse, from atrial to branchial siphon. We have no data on the current speeds in the benthic boundary layer at the site where A. monnioti was found. If currents are very weak, then the unusual siphon arrangement may be inconsequential. If they are strong, however, then A. monnioti must feed only during periods of low or slack flow, or its ciliation must be strong enough to counteract the adverse Bernoulli and viscous entrainment effects. Perhaps, during times of slack water, A. monnioti collects particles like a sediment trap, by opening the upward facing branchial siphon and allowing food to fall in. Given estimates of metabolic rate and flux of food particles to the sea floor, we can estimate the potential importance of this mechanism. Vertical flux of particulate organic matter at 3000 m depth in the Western Arabian Sea has been documented by Haake et al. (1993). During the four months or so of the Southwest Monsoon, flux of organic carbon can reach values as high as 20 Ijg m-2d-1 (Haake et al. 1993),

Medioni 1979). Converting this value to energy with an oxyenthalphic equivalent of 484 mj/tmol 02 (Gnaiger 1983) and scaling with the Qlo equation, we estimate that an individual of A. monnioti of 0.0086 g dry weight (empirically determined on a single average-sized specimen) should consume about 1074 mj of 02 per day at 2?C. Even this is likely to be an underestimate, since mass-specific oxygen consumption tends to be inversely related to body mass (Newell & Northcroft 1967) and we have assumed an unrealistic assimilation efficiency of 100%. Thus, the passive rain of particles into an upward facing siphon should provide no more than about 0.3% of the animal's energy requirements. Because A. monnioti would receive inadequate nutrition from passive collection and is not equipped to use ambient currents, it must rely almost entirely on cilia to move water for filtration. The family Agneziidae includes species living in both deep and shallow water, and species with various spatial arrangements of incurrent and excurrent siphons. To determine if siphon arrangement is correlated with depth, we have tabulated the information available in the taxonomic literature (Table 1, Fig. 7). Several species of shallow-water agneziids with full ciliation have both siphons inserted anteriorly, an arrangement that does not allow exploitation of ambient currents, but also does not allow flow to reduce ciliary feeding efficiency. The three deep-sea species for which information is available all have triangular bodies with the siphons pointed laterally in opposite directions (Table 1, Fig. 7). This arrangement would allow exploitation of a prevailing current, given appropriate body orientation. The only two species with the same siphonal arrangement as A. monnioti are from shallow water, where there is presumably enough food to offset any adverse effects of having an anterior branchial siphon and an atrial siphon directed dorsally. Presumably, A. monnioti can feed in exactly the same way as its shallow-water relatives because food is sufficiently plentiful in the deep Arabian Sea.

274
Acknowledgments. We thank J.D. Gage and P.A. Tyler for inviting us to participate in the Arabian Sea work and Captain J. Long and the crew of Discovery for their efficiency and professionalism. The Arabesque cruise was funded by the National Environmental Research Council of the United Kingdom. Participation by C.M.Y. was supported by the National Science Foundation (OCE-9116560). E.V. was supported by a postdoctoral fellowship from EP.U. Ministerio de Educacion y Ciencia (Spain). We thank G. Oliver, L. Levin, and A. Scheltema for assistance in picking ascidian specimens from sediment samples; A. Gooday for identifying the foraminiferal substratum; and J. Piraino for assistance with the SEM. 0. Hoegh-Guldberg provided useful comments on the manuscript and W. Jaeckle, I. Bosch, M. Sewell, and A. Pile assisted with calculations. We are much indebted to Dr. C. Monniot for sharing his extensive knowledge of deep-sea ascidians, for comments on portions of the manuscript, and for loaning specimens of deep-sea agneziids and styelids. This is Harbor Branch Contribution 1179.

Young & Vazquez

Atlantic 4100-4758 m; Monniot & Monniot 1976b, p. 633: Argentina from 3903-3917 m. A. glaciata (MICHAELSEN 1898) A. glaciata: Michaelsen 1898, p. 370: Tierra del Fuego 10 m; Michaelsen 1900, p. 6; Michaelsen 1907, p. 75; Van Name 1945, p. 200; Millar 1960, p. 92 (part): Patagonial Shelf from 110-115 m; Millar 1962, p. 174 (part); Monniot 1978; Monniot & Monniot 1983; Kott 1985, p. 76.
A. septentrionalis: Van Name 1945, p. 201 (part):

Southern California. not A. glaciata: Michaelsen 1898; Kott 1969a, p. 97: Antarctic Peninsula; Kott 1969b, p. 450: Queensland; Monniot 1970, p. 341; Monniot & Monniot 1974a, p. 373: Isla Decepcion from 23115 m. A. himeboja (OKA 1915) A. himeboja: Oka 1915, p. 1: Japan from 10-14 m;
Tokioka 1949, p. 6: Japan from 5-39 m; Nishi-

Appendix

Species belonging to the genus Agnezia (MICHAELSEN 1898) with their synonyms, known distributions, A. krausei (MICHAELSEN 1912) and known bathymetric ranges. A. krausei: Michaelsen 1912, p. 181: Patagonia. A. monnioti n. sp. A. arnaudi (MONNIOT MONNIOT & 1974) A. monnioti: (this paper) off Oman, Arabian Sea. A. arnaudi: Monniot & Monniot 1974b, p. 720: A. orthenteron (REDIKORZEV 1941) Kerguelen 20-61 m; Monniot 1978, p. 174: KerA. orthenteron: Redikorzev 1941, p. 199: Japan Sea guelen; Monniot & Monniot 1983, p. 57: Islas Orfrom 1900-2090 m; Nishikawa 1991, p. 60. cadas 37-55 m; Monniot & Monniot 1994, p. 25: A. septentrionalis (HUNTSMAN1912) Weddell Sea. A. septentrionalis: Huntsman 1912a, p. 118, HuntsA. glaciata: Monniot 1970: Kerguelen 10-15 m. man 1912b, p. 106: British Columbia. A. atlantica (MONNIOT& MONNIOT 1973) A. beringia: Ritter 1913, p. 493: Bering Sea and A. atlantica: Monniot & Monniot 1973, p. 421: Alaska 30-86 m. Azores from 2100-4680; Monniot & Monniot A. tenue (MONNIOT& MONNIOT1983) 1974a, p. 741: North Atlantic from 2100-4452 m; A. tenue: Monniot & Monniot 1983, p. 57: AntarcMillar 1982, p. 165: Northeast Atlantic from tica from 18 m. 2540-2900 m. A. biscoei (MONNIOT& MONNIOT1983) References A. biscoei: Monniot & Monniot 1983, p. 56: AntAllen JA 1979. The adaptations and radiation of deep-sea arctica, 87-121 m; Monniot & Monniot 1994, p. bivalves. Sarsia 64: 19-27. 25: Weddell Sea. Fiala-Medioni A 1974. Ethologie alimentaire d'invert6bres A. glaciata: Kott 1969a, p. 97; Kott 1969b, p. 450; benthiques filtreurs (ascidies). II. Variations des taux de Monniot & Monniot 1974b, p. 373. filtration et de digestion en fonction de l'espece. Mar. Biol.
A. capensis (MILLAR 1955) 28: 199-206.

kawa 1980, Table 1: Japan from 10 m; Nishikawa 1991, p. 59: Japan. A. sabulosa: Oka 1929, p. 152: Japan from 20-30 m.

A. capensis: Millar 1955, p. 191: South Africa; Monniot & Monniot 1976a, p. 364: Mozambique from 10-15 m; Monniot & Monniot 1983; Kott 1985, p. 76. A. glaciata: Millar 1960, p. 92 (part): South Africa from 35 m.
A. glaciata: Millar 1962, p. 174. A. celtica (MONNIOT& MONNIOT 1974)

1979. Effects of oxygen tension on pumping,filtration, and oxygen uptake in the ascidian Phallusia mammillata. Mar. Ecol. Prog. Ser. 1: 49-53. Gage JD 1995. Benthic community and fluxes in relation to the oxygen minimum zone in the Arabian Sea. Cruise Report: RRS Discovery 211/94. Scottish Association for Marine Science, Oban, U.K. 71 pp. Gage JD & Tyler PA 1991. Deep-Sea Biology. A Natural History of Organisms at the Deep-Sea Floor. Cambridge University Press, Cambridge. 504 pp.

A. celtica: Monniot & Monniot 1974a, p. 743: North

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275 Millar RH 1955. On a collection of ascidians from South Africa. Proc. Zool. Soc. Lond. 125(1): 169-221. 1960. Ascidiacea. Discovery Reports 30: 1-160. 1962. Further descriptions of South African ascidians. Ann. S. Afric. Mus. 56(7): 113-221. 1975. Ascidians from the Indo-West-Pacific region in the Zoological Museum, Copenhagen (Tunicata, Ascidiacea). Steenstrupia 3: 205-336. 1982. Ascidians from the Rockall Trough area of the Northeast Atlantic. J. Nat. Hist. 16: 165-182. 1988. Ascidians collected during the international Indian Ocean Expedition. J. Nat. Hist. 22: 823-848. Monniot C 1970. Ascidies Phl6bobranches et Stolidobranches des Iles Kerguelen r6coltees par P. Grua. Bull. Mus. Natl. Hist. Nat., Paris, ser. 2, 42(2): 340-354. 1978. Ascidies Phlebobranches et Stolidobranches du sud de l'Oc6an Indien. Ann. Inst. Oc6anogr., Paris, 54(2): 171-224. 1979. Adaptations of benthic filtering animals to the scarcity of suspended particles in deep water. Ambio Special Report 6: 73-74. Monniot C & Monniot F 1972. C1e mondiale des genres d'ascidies. Arch. Zool. Exp. Gen. 113: 311-367. 1973. Ascidies abyssal recoltees au cours de la campagne oceanographique Biaores par Jean Charcot. Bull. Mus. Natl. Hist. Nat., Paris, ser. 3, Zool. 93, 121: 389-475. 1974a. Ascidies abyssaux de l'Atlantique r6coltees par le '"Jean Charcot" (campagnes Noratlante, Walda, Polygas A). Bull. Mus. Natl. Hist. Nat., Paris, ser. 3., Zool. 226, 154: 721-786. 1974b. Ascidies des Iles Kerguelen recoltees par P.M. Arnaud. Tethys 5(4): 715-734. 1975. Abyssal tunicates: an ecological paradox. Ann. Inst. Oceanogr. Paris 51(1): 99-129. 1976a. Ascidies de la c6te du Mozambique. Revue Zoologie africaine, 90(2): 357-392. 1976b. Tuniciers abyssaux du bassin argentin recoltees par l'Atlantis IL Bull. Mus. Natl. Hist. Nat., Paris, ser. 3, Zool. 387, 269: 629-662. 1978. Recent work on the deep-sea tunicates. Oceanogr. Mar. Biol. Ann. Rev. 16: 181-228. 1983. Ascidies antarctiques et subantarctiques, morphologie et biogeographie. Mem. Mus. Natl. Hist. Nat., Paris, ser. A, Zool. 125: 1-168. 1984. Nouvelle Sorberacea (Tunicata) profondes de l'Atlantique sud et de l'Ocean Indien. Cah. Biol. Mar. 25: 197-215. 1985. Ascidies profondes au large de Mayotte (Archipiel des Comores). Cah. Biol. Mar. 26: 35-52. 1989. Ascidians collected around the Galapagos Islands using the Johnson-Sea-Link research submersible. Proc. Biol. Soc. Wash. 102: 14-32. 1991 a. Tunicata, Peuplements d' ascidies profondes en Nouvelle-Cal6donie. Diversite des strategies adaptatives. In: Resultats des Campagnes Musorstom, Volume 8. Crosnier A, ed., Mem. Mus. Natl. Hist. Nat., Paris (A), 151: 357-448.

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