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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

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Invertebrate Biology 116(3): 262-276.? 1997 American Microscopical Society, Inc.

Agnezia monnioti and Styela gagetyleri, new deep-sea ascidians specializedfor life within and below the oxygen minimum layer in the Arabian Sea

Craig M. Youngl a and Elsa Vaizquez21Department f LarvalEcology, HarborBranchOceanographicnstitution,Ft. Pierce,Florida34946, USA2 Departamento e 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. Whereasmany deep-sea ascidians have reduced branchial ciliation and exploit the velocity gradient inthe benthic boundary layer to induce internal flow, this species has strong ciliation and asiphonal 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 persistentoxygen minimum zone. The branchial sac of this species has a reduced number of folds andtherefore fewer cilia for food collection and less surface area for oxygen exchange than shallow-water congeners. We hypothesize that reduced filtration capacity is made possible by an un-usually high flux of organic material to the sea floor in this region. The observed reduction inbranchial surface area in a persistent hypoxic zone suggests that branchial complexity in as-cidians is more important for feeding efficiency than gas exchange. Affinities of these specieswith other members of their respective genera are discussed and an appendix with the synonymsand localities of species in the genus Agnezia is included.

Additionalkey words: filterfeeding, IndianOcean,monsoons, Tunicata,Urochordata,Ascidiacea

Deep-sea ascidians show a number of unusual mor-phological and functional modifications, includinglong 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 fewexceptions, abyssal ascidians tend to have smallerbody sizes than their shallow-water counterparts(Monniot 1979). All of these trends and features havebeen attributed to low food supplies (Monniot 1979).Although plankton and other suspended organic par-ticles are indeed scarce in most of the deep sea (Gage& Tyler 1991), seasonal plankton blooms can producemajor pulses of detrital food at abyssal depths both inmid-oceanic regions and near continental land masses(Lampitt 1985; Rice et al. 1986). If food limitation isindeed responsible for the many unusual feedingmodes that have evolved in deep-sea ascidians, onemight predict that species more similar to shallow-a Author for correspondence:Dept. of LarvalEcology, Har-bor BranchOceanographicnstitution,5600 U.S. Hwy. 1N., Ft. Pierce,FL 34946, USA. E-mail:[email protected]

water forms would be found in deep-sea regions wherefood is plentiful.The deep-sea tunicate fauna is known mostly fromspecimens dredged or trawled during major oceano-graphic expeditions, beginning with the Challenger ex-pedition and continuing to the present day (Monniot& Monniot 1978). Collections of ascidians from theIndian Ocean were obtained by the John Murray/Ma-bahiss Expedition in 1933 (Kott 1957), by the Inter-national Indian Ocean Expedition in 1963-64 (Millar1988), and by three French expeditions between 1977and 1981 (Monniot & Monniot 1984). Several speciesof interstitial sorberaceans were described by Monniot& Monniot (1984) from the latter cruises, and Kott(1957) tentatively assigned a single ascidian speciesfrom 2000 m to the genus Hexacrobylus. With thesefew exceptions, the tunicate fauna of the Indian Oceanis known only for depths less than 200 m.Recent interest in oceanographic processes influenc-ing global change and the flux of nutrients in the worldocean prompted the selection of a dynamic region offthe coast of Oman in the Arabian Sea as a major sitefor international cooperative research (Smith et al.


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Fig. 1. A portion of the northern Arabian Sea off Oman, showing the general location of the sampling effort (delimitedby square in A) and bathymetric contours (B) with the type localities of Styela gagetyleri and Agnezia monnioti indicatedby asterisks.1991). This region is strongly influenced by an annualnortheast monsoon, which causes coastal upwelling ofnutrients. The upwelling, coupled with aeolian dustsfrom the deserts of the Middle East and North Africa,fuels strong primary production in the surface layers.Plankton sinking below the mixed layer decompose toform a persistent zone of very low oxygen betweenapproximately 50 and 1300 m depth. The John Mur-ray/Mabahiss Expedition sampled in this zone with anAgassiz trawl and, finding very little life, concludedthat the zone was virtually azoic (Rice 1986). Duringa recent cruise on the British research vessel RRS Dis-covery, zoologists focusing on various components ofthe benthic fauna resampled this zone and discoveredan abundant and surprisingly diverse fauna there.Many of the species, notably molluscs, appear to havetraits (e.g., hemoglobin) that permit occupation of azone with very low oxygen (G. Oliver, pers. comm.).The deep-sea floor below the oxygen minimum zonehas an unusually high content of both organic and in-organic carbon (Smith et al. 1991); indeed, the surfacesediment of undisturbed box cores from abyssal depthsoften appears green because of the large amount ofphytoplankton detritus arriving at the bottom (J. Gage,pers. comm.; CMY, pers. ob.). Whereas flux of organiccarbon to the abyssal sea floor typically amounts toonly about 1 mg m-2d-1 in low-latitude oceanic sys-

tems (Honjo 1980), carbon flux in the Western ArabianSea averages 5 mg m-2d-I for most of the year andpeaks near 20 mg m-2d-1 during the summer months(Haake et al. 1993) because of the influence of themonsoon (Nair et al. 1989). Comparable fluxes havebeen reported in the Panama Basin (Honjo 1982), butthey are not typical of the deep sea as a whole.In this paper we describe two new species of deep-sea ascidians from the Arabian Sea, both of whichhave morphological features that would be viewed asfunctionally inefficient in less productive regions ofthe world ocean. Styela gagetyleri n. sp. lives in theoxygen minimum zone but, paradoxically, has a re-duced branchial apparatus with less surface area forgas exchange than related species living in well-oxy-genated habitats. Agnezia monnioti n. sp. inhabits thesea floor at depths greater than 3000 m. Unlike mostdeep-sea ascidians, its siphons are oriented in such away as to prevent efficient food collection with the aidof ambient water currents.

MethodsThe benthic fauna was sampled off the coast ofOman (Fig. 1) during a cruise of RRS Discovery be-tween 14 October and 2 November 1994. Some 45boxcores and 496 cores from 44 multicore deploy-

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Young & Vazquezments were taken between 94 and 3300 m to samplethe infaunal meiofauna and macrofauna. Megafaunaand macrofauna, including the deep-sea ascidians de-scribed here, were collected by Agassiz trawl (8 de-ployments) and epibenthic sledge (5 deployments) onthe slope and abyssal plain.The entire sample of mud and rock collected in eachAgassiz trawl (at times as much as 2 tons) was sievedthrough a 5-mm mesh sieve and some subsampleswere sieved through a 300-jtm sieve. Ascidians wereseparated, washed, and maintained for short periods oftime in a cold room at 4?C before fixation in 5% buf-fered formalin. After fixation for one week, they weretransferredinto 70% ethyl alcohol. Ascidians were dis-sected and stained using the method of Monniot &Monniot (1972).For scanning electron microscopy (SEM), branchialsacs were dissected from formalin-fixed specimens,rinsed with distilled water, dehydrated through a grad-ed series of ethyl alcohol, and critical point dried. Thetissues were sputter coated with gold and examinedwith a Hitachi S-510 scanning electron microscope.

ResultsFamily Agneziidae MONNIOT& MONNIOT1991Agnezia monnioti n. sp. (Figs. 2, 3)

Species descriptionHolotype. U.S. National Museum of Natural His-tory, Smithsonian Institution, Washington D.C. (Cat-alog number USNM-23069).Type locality. Discovery Station 12719/1(19?07.73'N, 58?38.83'E), 1 November 1994; 3162 mdepth in the Murray Basin of the Arabian Sea (Fig. 1).Paratypes. Harbor Branch Oceanographic Institu-tion, Florida (Catalog number HBOI 096:00133) andMuseum National d'Histoire Naturelle of Paris (Cat-alog number 3 AGN.A 29).Etymology. Agnezia monnioti is named for ClaudeMonniot of the Museum National d'Histoire Naturelle(Paris), who has contributed more than any other in-dividual to our understanding of the systematics, func-tional morphology, distribution, and ecology of deep-sea ascidians.Description. Body dorso-ventrally or laterally flat-tened, attached by hair-like tunic processes in the basal

(posterior) region to the tubes of giant foraminiferansand to small sand grains (Fig. 2A,B). The test is thinand transparent with few adherent sand particles. Ex-cept for the posterior end, sand particles are mostabundant in the region of the siphons. The largest of101 animals collected measured 26 mm in the anterior-posterior axis and 16 mm wide in the sagittal plane.The smallest individual was 15 mm long and 10 mmwide.The branchial siphon is apical (Fig. 2A) with 8lobes. The atrial siphon is positioned dorsally, /2 to 2/3of the length of the animal away from the branchialsiphon (Fig. 2A). Its margin is divided into severalirregularly shaped lobes.The body wall is very thin and transparent (Fig.2C). Muscle bands encircle both siphons, with themusculature surrounding the atrial siphon being mostextensive (Figs. 2C, 3C). Longitudinal muscle bands(-25) extend from the siphons and the intersiphonalarea to each side of the animal (Fig. 3C). Each bandsubdivides on each side into 3 or 4 bands, which jointhe bands on the opposite side of the body posteriorlyand ventrally. There are no transverse muscles.There are 4 rings of oral tentacles (Fig. 3C). Thefirst has very short and numerous tentacles. Tentaclelength increases in each subsequent ring, with the fil-amentous tentacles in the second and third ring beinglonger than the diameter of the siphon. In the animalswe dissected, there were 10 tentacles in the secondring, 11 in the third, and 6 in the fourth. The prebran-chial area is very large: equal to the width of an in-fundibulum. A strong velum, equal in width to thelength of the prebranchial area, is found anterior to theperipharyngeal groove. The peripharyngeal grooveforms a deep "V" on the dorsal side (Fig. 3C). Theopening of the neural gland is marked by a small pieceof tissue resembling a short languet. The dorsal laminais 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 each2 rows of infundibula (Fig. 3A), but intermediatetransverse vessels were not observed. Each vessel has11 large finger-like papillae (Fig. 3A), each corre-sponding to one infundibulum. Each stigma is inter-

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

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BA

Fig. 3. Internal eatures of Agneziamonnioti(cameralucida drawings).A: Portion of the branchial sac,showing two coiled stigmata (CS)between two transverse vessels(TV); parastigmatic vessels (PV)andpapillae(P). B: Gonad(GO)sit-uated in the gut loop (G) showingthe anus (A), spermduct (SD), andoviduct(0). Note thatthegonoductsterminate at a 90? angle. C: Interiorview of thebody wall (branchial acremoved) showing positions of thegut (G), gonad (GO),branchial en-tacles (BT), body wall musculature(M), neuralgland (N), branchialsi-phon (BS), and atrialsiphon(AS).

AS5 mm

rupted by parastigmatic vessels forming an "X" (Figs. of the oviduct forms a 90? angle and faces posteriorly2E, 3A). The only branchial tissue is that surrounding (Fig. 3B).the stigmata.The gut loop is on the left side of the body (Fig.2C). The stomach is smooth, not well defined, and theintestine 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). Theovary is tubular and branching, with testicular lobesattached to the posterior end of the ovary. Genitalducts follow the course of the rectum; the sperm ductends in a papilla just before the anus and the oviductends halfway up the rectum (Fig. 3B). The terminus

Relationship to other species in the genusThe names of the genus Agnesia MICHAELSEN 898and the family Agnesidae HUNTSMAN 1912 werechanged by Monniot & Monniot (1991a) to Agnezianom. nov. and Agneziidae nom. nov. because the gas-

tropod genus Agnesia KONINCK1883 and its familyAgnesiidae had taxonomic priority.All species of Agnezia in the Southern hemispherewere synonymized by Millar (1960) and Kott (1969a)

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New ascidians from the deep Arabian Seabut Monniot & Monniot (1983) separated the antarcticand subantarctic species. The 12 valid species of Ag-nezia with their synonyms and known localities of oc-currence are summarized in the Appendix.These species can be subdivided into two groups.The first group has a single row of stigmata betweeneach pair of consecutive transverse vessels and in-cludes: A. atlantica (MONNIOT MONNIOT973) fromthe North Atlantic at 2100-4452 m depth (Monniot &Monniot 1973, 1974a; Millar 1982), A. biscoei (MON-NIOT& MONNIOT1983) from Antarctica (Monniot &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 (VanName 1945; Millar 1960; Monniot 1978; Monniot &Monniot 1983; Kott 1985), and A. himeboja (OKA1915) from Japan (Tokioka 1949; Nishikawa 1980,1991).The second group, which includes A. monnioti n.sp., consists of species with two infundibula betweeneach pair of transverse vessels. Agnezia monnioti isdistinguished from the other species in this group asfollows. Agnezia arnaudi (MONNIOT & MONNIOT1974b) is an antarctic and subantarctic species from10-61 m depth. It has unperforated branchial tissuebetween the infundibula and the stigmata coil 3 or 4times. The main difference between this species andA. monnioti is that the former has spatially separatedmale and female gonoducts. The male duct terminateson the left side of the atrial chamber and the femaleduct ends on the right side, where the eggs are incu-bated (Monniot 1970, 1978; Monniot & Monniot1983).Agnezia capensis (MILLAR 955) from South Africaand Mozambique lives between 10 and 35 m depth.Its languets are placed towards the left side and theintestine forms a secondary loop (Millar 1955; Mon-niot & Monniot 1976a).

Agnezia celtica (MONNIOT & MONNIOT 1974a) isfrom the North Atlantic and Argentina at 3903-3917m depth. Its musculature does not extend through thedorsal side of the animal and the ventral side has nomusculature at all. The stigmata coil 4 or 5 times andthere is a very small gut loop relative to the total sur-face of the body wall (Monniot & Monniot 1974a,1976b). Agnezia orthenteron (REDIKORZEV1941) isfrom the Sea of Japan between 1900 and 2090 mdepths. It has circular muscles on the siphons and fineradial muscles diverging from the siphons but disap-pearing near the central part of the mantle body (Ni-shikawa 1991). Agnezia septentrionalis (HUNTSMAN1912) lives between 30 and 86 m depths in BritishColumbia, Alaska, and the Bering Sea. Its musculature

is not complete and the muscle bands are short. Pres-ent, sometimes, are intermediate transverse vessels andexoinfundibula (funnel-like structures formed of oneto several stigmata which are not found on either thelongitudinal vessels or on the axis of the folds). Thestigmata are coiled 4 or 5 times (Van Name 1945).Agnezia tenue (MONNIOT& MONNIOT 1983) is aninterstitial species collected from 18 m depth in theAntarctic. The stigmata coil one and a half times andthe transverse vessels have just one papilla on the rightside and none on the left (Monniot & Monniot 1983).Agnezia monnioti is only the fourth deep-sea speciesto be described in this genus and the first in the IndianOcean. The other bathyal and abyssal species are:Ag-nezia atlantica from 2100-4452 m in the North At-lantic (Monniot & Monniot 1973, 1974a; Millar 1982),A. celtica from 3903-3917 m in the North Atlantic andArgentina, and A. orthenteron from 1900-2090 m inthe Japan Sea.Habitat and associated fauna

The sediment at the 3162-m site where Agneziamonnioti was collected consisted of very fine silt withno rocks but with frequent large (up to 2-cm long)foraminiferans, Rhabdammina discreta, resting on thesurface of the mud. All individuals of A. monniotiwere attached to one or more foraminiferan tests.These elongate tests apparently form a sort of raft thatmay help prevent the ascidians from sinking into thesoft ooze. The oxygen concentration was 1.0 ml/1,which is about one order of magnitude higher than thatof the oxygen minimum zone (Gage 1995).The fauna collected at depths over 3000 m in theMurray Basin of the Arabian Sea was dominated bymolluscs, including bivalves in the genera Limopsis,Bentharca, Bathyarca, Nucula, Ledella, Propeamus-sium, Vesicomya, Lucina, and Solemya, numeroussmall gastropods including turridsand cephalaspideans(G. Oliver, pers. comm.), and an unusually diverseaplacophoran fauna (A. Scheltema, pers. comm.).Many of the Limopsis supported epizoic inarticulatebrachiopods, Pelagodiscus atlanticus. Ophiuroids inthe families Ophiuridae, Ophiocanthidae, and Am-phiuridae were common, as were at least four speciesof large asteroids and holothuroids in the genus Ypsi-lothuria (A. Campbell, pers. comm.). Zoantharian andactinarian sea anemones were abundant, and one col-ony of a pennatulid, Umbellula sp., was found. Por-tunid and porcellanid crabs were well represented, aswas the eryonid crab Polycheles sp. and the giant am-phipod Eurythene gryllus. Overall, the fauna was notunusual for an abyssal plain and many of the genera

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Young & Vazquezand species are the same as found at comparabledepths elsewhere in the world.

Family Styelidae SLUITER1895Styela gagetyleri n. sp. (Figs. 4, 5)Species description

Holotype. U.S. National Museum of Natural His-tory, Smithsonian Institution, Washington D.C. (Cat-alog number USNM-23070).Type locality. Discovery Station 12697#1(19?11'N, 58?18'E), 24 October 1994; 394 m depth onthe continental slope off Oman, Arabian Sea (Fig. 1).Paratypes. Harbor Branch Oceanographic Institu-tion, Florida (Catalog number HBOI 096:00134) andMuseum National d'Histoire Naturelle of Paris (Cat-alog number S1 STY.A 247).Etymology. This species is named in honor of JohnGage, Principal Scientific Officer on Discovery duringthe Arabesque cruise, and Paul Tyler, his long-timecolleague and co-principal investigator on the samecruise. Gage and Tyler have collaborated closely onmany aspects of deep-sea biology for more than 2 de-cades. Their names are so closely tied to long-termdeep-sea studies and to studies of deep-sea reproduc-tion that it is appropriate to join their names perma-nently in the specific epithet of Styela gagetyleri.Description. The body is hemispherical when con-tracted, and all 54 specimens we examined were at-tached posteriorly to small stones, sharks' teeth (whichare very abundant in this zone), and other hard sur-faces (Fig. 4A). Body size is small, the largest indi-vidual being 4 mm high (anterior-posterior axis) 11mm long (dorso-ventral axis), and 10 mm wide, andthe smallest 3 mm high, 7 mm long, and 4 mm wide.Test is thin but firm and leathery, covered with veryfine brownish sand. Several tiny white sponges werefound encrusting the siphonal region in every speci-men examined (Fig. 4A). The siphons are apical andseparated in the holotype by a distance of 3 mm. Thebasal region of the ascidian, attached firmly to the sub-stratum, is very thin and soft without any hair-like pro-cesses.The body wall is very thin, transparent, and fragile(Fig. 4B). There are -30 oral tentacles in two circlesand a third circlet of very tiny tentacles (Fig. 4C).There is no space between the peripharyngeal grooveand the branchial sac (Fig. 4C). The dorsal tubercle isa round opening situated on a small protuberance ofthe prebranchial area (Fig. 4C). The atrial siphon hasa circlet of small capitate tentacles. This circle extendstwo wide projections as a velum towards the oral si-phon, one to the right and the other to the left (Fig.5). The edge of this projection also has tentacles.

The branchial sac has just one fold on the right side(Fig. 4D). On the left sides of most individuals, thereare no true folds, but only longitudinal vessels situatedvery close to each other where the folds would be (Fig.4D). However, in a few individuals, there is a singletrue fold on the left side. In others, there is no evidenceof a left fold at all. There are two columns of stigmatabetween every adjacent pair of longitudinal vessels.The branchial formulas of three adult animals (show-ing the number of longitudinal vessels lying betweenthe Dorsal Lamina, "DL," and Endostyle, "E," oneach side of the body) for three different observedcases of branchial reduction are:DL right 7-13-18 EDL left 0-11-26 EDL right 8-8-21 EDL 0-7-9-9-4 E

DL right 8-10-22 EDL left 27 EThe gut forms a very pronounced S-shaped second-ary loop and the first loop is nearly closed (Fig. 5).The stomach is in the shape of an elongate olive, with18 longitudinal folds, a gastric caecum at the posteriorend, and a gastro-intestinal connective from the middlepart of the stomach to the intestine. The anus ends verynear the atrial siphon (Figs. 4B, 5). The edge of theanus is smooth.There are 10 large endocarps on the right side and5 on the left side, scattered over the body wall (Fig.

5).Each side of the body has a single gonad, situatedanteriorly. Each ovary is long and convoluted and hasat least 14 testicular lobes situated at the posterior end(Figs. 4B, 5). A sperm duct arises from each male lobeand the ducts all join together in a common sperm ductat the posterior end of the ovary. The sperm ductcourses along the ovary to open in the atrial cavity justbehind the female opening (Fig. 5).Relationship to other species in the genus

Reduction of the branchial sac as observed in Styelagagetyleri has been described only in antarctic andabyssal species. Among the abyssal species, S. tenui-branchia MONNIOT, MONNIOT, & MILLAR1976 and S.ordinaria MONNIOT& MONNIOT 1985 have no bran-chial folds whatsoever, and S. polypes MONNIOT,MON-NIOT,& MILLAR 1976 has one fold on each side, withthe right fold being lower than the left one (Monniotet al. 1976). Styela longiducta MONNIOT& MONNIOT1985 from Comores has only one fold on each side ofthe branchial sac and only one endocarp on the body

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s

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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: Bodywall and attached structures, following removal of branchial sac and tunic. Siphons, gut loop, gonads, and endocarps arevisible (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 rightside. 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 (SLUITER1912) and Cnemidocarpa sericata (HERDMAN 1888)have no branchial folds. Styela schmitti simplex MIL-LAR 1960 has three folds on the right side and two onthe left (Kott 1969b).Styela asterogama MILLAR 1975 from a depth of 70

m off Bali has two folds on the right and one on theleft, with one gonad on each side. The grouped testic-ular lobes are separate from the ovary. The test hashair-like processes on the lower half of the body, thebranchial sac has one row of stigmata between eachpair of longitudinal vessels, and the rows of stigmataare crossed by parastigmatic transverse vessels (Millar1975).

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Fig. 5. Internalbodywall (branchialsac removed) of Styela gagetyleri(camera ludica drawing), showingthe gut (G), testes (T), ovary (0),endocarps (E), neural gland (N),branchial iphon(BS), and atrialsi-phon (AS) with attachedvelum.Habitat and associated fauna

Styela gagetyleri occurred on small pebbles andsharks' teeth (Fig. 4A) in a muddy habitat between340 and 400 m depth. Oxygen concentrations in thisgeneral depth zone ranged from 0.15 ml/l on the bot-tom at 400 m (measured on the supernatant of tubecores) to 0.63 ml/1 in the water column at 300 m (Gage1995). The oxygen level near the surface (5 m) wasabout 1 order of magnitude higher (4.1-4.3 ml/1). Thefauna in the hypoxic zone was more abundant thanexpected. Styela gagetyleri and a nest-building mussel,Amygdalum sp., were the dominant organisms. Otheranimals occurring at the same site included the spidercrab Encephaloides armstrongi, a vesicomyid clam,and two species of gastropods.Discussion

Many of the convergences in body form and func-tion that characterize deep-sea tunicates are unknownor uncommon in shallow water. These include carniv-ory in the families Octacnemidae and Ascidiidae, ex-ploitation of interstitial habitats in the diminutivemembers of the class Sorberacea, reduction of thebranchial sac, elimination of cilia, and reduction inbody organs not directly used for reproduction or foodcollection (Monniot & Monniot 1978, 1991a,b; Kott1989). Long stalks for exploiting ambient water cur-rents are found in shallow-water species (Young &Braithwaite 1980) but are especially common in the

deep sea. One of the species we describe here, Styelagagetyleri, has a reduced branchial sac even though itlives at bathyal depths in an oxygen minimum zone.The other species, Agnezia monnioti, has a fully de-veloped branchial apparatuswith ciliation and a siphonorientation similar to those of shallow-water conge-ners, even though it lives at abyssal depths. Thus, bothspecies deviate from the expected morphologies ofdeep-sea ascidians.Branchial reduction in Styela gagetyleri

In small abyssal styelids, reduction in body sizegenerally also involves reduction in the volume andnumber of the gonads and reduced complexity of thebranchial sac (Monniot & Monniot 1978). Solitaryshallow-water styelids normally have 4 branchial foldson each side. In the small abyssal species, the bran-chial folds become less numerous and less marked, andmay disappear, leaving only groups of vessels (Styelacrinita, Cnemidocarpa sericata, and Styela minima).Often, the branchial sac seems to remain in a juvenilestate (Monniot & Monniot 1978). This reduction inbranchial sac complexity is somewhat puzzling. Onemight argue that a reduction in branchial folds is nec-essary in species with small body size because thereis insufficient room to accommodate extra folds. How-ever, small solitary styelids in shallow water do havea full complement of 8 branchial folds. The branchialsac is almost certainly the major surface for oxygen

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Pharyngodictyoncaulifos

Araneumpedunculatum

Culeoluselegans

Fig. 6. Examples of deep-seastalked and unstalkedascidianswithunciliatedbranchial acs or reducedbranchial ciliation, showing thearrangementsof the incurrent andFungulus excurrent siphons. Outlines areredrawn from the original speciesdescriptions,so some are probablynot good representations of theposturesof the living animals.

exchange in ascidians (Goodbody 1974), so one mightexpect that this structure would increase in size tocompensate for hypoxic conditions. Because the bran-chial surface area in S. gagetyleri is reduced ratherthan expanded, we must conclude that the surface areafor gas exchange is not limiting even at very low ox-ygen concentrations. With a decrease in temperature,the rate of oxygen diffusion across a membrane shoulddecrease more slowly (Qlo < 2) than metabolic rate(QIo > 2) (Giese 1968), so a relatively smaller bran-chial sac may be adequate in deeper waters. Small filter-feeding bivalves show a similar reduction in complex-ity and size of the filtering apparatus in the deep sea(Allen 1979) and this reduction has been attributedtoa reduced metabolic oxygen demand in deep-sea spe-cies (Allen 1979).

One strategy for a filter-feeder living in a nutrient-poor habitat is to reduce the amount of somatic tissuethat must be nourished while simultaneously increas-ing the efficiency or size of the food collection appa-ratus. Monniot & Monniot (1989) documented an ex-ample of this phenomenon within a single species ofHalocynthia from the Galapagos Islands. The deep-water form had less massive tissues than the shallow-water form, but the complexity of the branchial sac,as measured by the number of stigmata per mesh, in-creased as a function of depth. Complex, folded bran-chial sacs increase efficiency of particle capture (Fiala-Medioni 1974). Even if increased feeding efficiency isnot required in the Arabian Sea, it is difficult to en-vision selective pressures that would result in branchialreduction in S. gagetyleri. Perhaps in a low oxygen

I

LCnemidocarpadigonas

Miniperapapillosa

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Young & Vazquez

Agneziaatlantica Agnezia celtica Proagneziadepressar

Fig. 7. Siphon arrangements in thefamily Agneziidae. See Table 1 forbathymetric distributions. Top row:deep-sea species with siphons di- Agneziamonniotirected dorsally and ventrally. Agne-zia atlantica is depicted with ante-rior siphons in this drawing, but theliterature description (Monniot &Monniot 1973) indicates that the si-phons are spatially separated, on t Atwo angles of a triangular body.Middle row: Agnezia monnioti fromthe deep sea and two shallow-waterspecies having a similar siphon ar-rangement. Bottom row: shallow-water species with siphons insertedon the anterior end and directed ei-ther anteriorly or dorsally and ven-trally. Agneziacapensisenvironment, selection favors reduction of tissues, in-cluding the branchial sac itself, that consume oxygen.Siphon orientation and feeding in Agneziamonnioti

Many deep-sea species orient siphons to take ad-vantage of ambient water currents for filtration, there-by minimizing the energy expenditure required forfeeding (Young & Braithwaite 1980; Kott 1989) (Fig.6). Stalked forms generally have the branchial (incur-rent) siphon pointed posteriorly and the atrial (excur-rent) siphon pointed anteriorly. By swaying with eachchange of current direction, the branchial siphon is al-ways presented to the current and flow through thebranchial sac is induced by dynamic pressure (Young& Braithwaite 1980; Kott 1989).Unstalked ascidians may use ambient water currents

Agneziaseptentrionalis

Agneziaglaciata

Agnezia enue

Agneziaarnaudi Agneziabiscoei

for filtration if the siphons are positioned at differentheights in the velocity gradient of the benthic bound-ary layer. Specifically, if the branchial siphon is posi-tioned nearer the bottom than the atrial siphon, theBernoulli effect will result in a pressure difference thatwill draw water through the branchial sac. This Ber-noulli effect is augmented by viscous entrainment and,if the incurrent siphon is facing upstream, by dynamicpressure (Vogel 1978). If the atrial siphon faces di-rectly upward, flow will be induced regardless of thedirection from which the current comes. However,none of these passive filtration mechanisms will workif the siphons are of equal length and inserted on theanterior end, as in some shallow-water phlebobranchs(Kott 1989) or if the branchial siphon opens higher inthe water column than the atrial siphon.If Agnezia monnioti followed the typical deep-sea

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New ascidians from the deep Arabian SeaTable 1. Siphon arrangements and bathymetric distribu-tions of Agnezia and Proagnezia species. References anddetailed bathymetric data are given in the Appendix.

Bathymetric distributionSpecies (m)Siphons anterior, but directed dorsally and ventrally liketwo angles of a triangle:Agnezia atlantica 2,100-4,680Agnezia celtica 3,903-4,758Proagnezia depressa 5,850-5,860Both siphons on anterior end and directed anteriorly:Agnezia arnaudi 20-61Agnezia biscoei 37-121Agnezia capensis 10-35Agnezia glaciata 10-115Branchial siphon on anterior end, atrial siphon on dorsalside:

Agnezia monnioti 3,162Agnezia septentrionalis 30-86Agnezia tenue 18Unknown siphon arrangement:Agnezia himeboja 5-39Agnezia krausei unknownAgnezia orthenteron 1,900-2,090

pattern, it would have reduced cilia in the branchialsac and siphons oriented for the capture of currents(Fig 6). However, this species is unusual in that itsbranchial siphon is pointed directly upward and theatrial siphon is directed to the side (Figs. 2A, 7). Thissiphonal arrangement cannot be used for exploitingambient flows; indeed, in the absence of ciliary cur-rents, any flow should drive water through the animalin reverse, from atrial to branchial siphon. We have nodata on the current speeds in the benthic boundarylayer at the site where A. monnioti was found. If cur-rents are very weak, then the unusual siphon arrange-ment may be inconsequential. If they are strong, how-ever, then A. monnioti must feed only during periodsof low or slack flow, or its ciliation must be strongenough to counteract the adverse Bernoulli and vis-cous entrainment effects.

Perhaps, during times of slack water, A. monnioticollects particles like a sediment trap, by opening theupward facing branchial siphon and allowing food tofall in. Given estimates of metabolic rate and flux offood particles to the sea floor, we can estimate thepotential importance of this mechanism. Vertical fluxof particulate organic matter at 3000 m depth in theWestern Arabian Sea has been documented by Haakeet al. (1993). During the four months or so of theSouthwest Monsoon, flux of organic carbon can reachvalues as high as 20 Ijg m-2d-1 (Haake et al. 1993),

which amounts to roughly 9.5 X 105 mj m-2d-' ofavailable energy (conversion factor: 47.7 j/mg C forphytoplankton; Platt & Irwin 1973). A typical individ-ual of A. monnioti has an incurrent siphon diameter of-2 mm (3.14 mm2 siphon area), so it should be ableto collect passively enough particulate carbon to yieldabout 3 Lj of energy per day. Metabolic rate has notbeen measured for any deep-sea ascidian, so we mustestimate the mass-specific metabolic rate of A. mon-nioti by scaling the metabolic rate of a shallow-waterrelative to an appropriately lower temperature, usingQlo = 2. Phallusia mamillata consumes maximally 846jLg 02 h-Ig dry wt-2 at a temperature of 15?C (Fiala-Medioni 1979). Converting this value to energy withan oxyenthalphic equivalent of 484 mj/tmol 02(Gnaiger 1983) and scaling with the Qloequation, weestimate that an individual of A. monnioti of 0.0086 gdry weight (empirically determined on a single aver-age-sized specimen) should consume about 1074 mj of02 per day at 2?C. Even this is likely to be an under-estimate, since mass-specific oxygen consumptiontends to be inversely related to body mass (Newell &Northcroft 1967) and we have assumed an unrealisticassimilation efficiency of 100%. Thus, the passive rainof particles into an upward facing siphon should pro-vide no more than about 0.3% of the animal's energyrequirements. Because A. monnioti would receive in-adequate nutrition from passive collection and is notequipped to use ambient currents, it must rely almostentirely on cilia to move water for filtration.

The family Agneziidae includes species living inboth deep and shallow water, and species with variousspatial arrangements of incurrent and excurrent si-phons. To determine if siphon arrangement is corre-lated with depth, we have tabulated the informationavailable in the taxonomic literature (Table 1, Fig. 7).Several species of shallow-water agneziids with fullciliation have both siphons inserted anteriorly, an ar-rangement that does not allow exploitation of ambientcurrents, but also does not allow flow to reduce ciliaryfeeding efficiency. The three deep-sea species forwhich information is available all have triangularbod-ies with the siphons pointed laterally in opposite di-rections (Table 1, Fig. 7). This arrangement would al-low exploitation of a prevailing current, given appro-priate body orientation. The only two species with thesame siphonal arrangement as A. monnioti are fromshallow water, where there is presumably enough foodto offset any adverse effects of having an anteriorbranchial siphon and an atrial siphon directed dorsally.Presumably, A. monnioti can feed in exactly the sameway as its shallow-water relatives because food is suf-ficiently plentiful in the deep Arabian Sea.

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Young & VazquezAcknowledgments. We thank J.D. Gage and P.A. Tyler forinviting us to participate in the Arabian Sea work and Cap-tain J. Long and the crew of Discovery for their efficiencyand professionalism. The Arabesque cruise was funded bythe National Environmental Research Council of the UnitedKingdom. Participation by C.M.Y. was supported by the Na-tional Science Foundation (OCE-9116560). E.V. was sup-ported by a postdoctoral fellowship from EP.U. Ministeriode Educacion y Ciencia (Spain). We thank G. Oliver, L. Lev-in, and A. Scheltema for assistance in picking ascidian spec-imens from sediment samples; A. Gooday for identifying theforaminiferal substratum; and J. Piraino for assistance withthe SEM. 0. Hoegh-Guldberg provided useful comments onthe 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-seaascidians, for comments on portions of the manuscript, andfor loaning specimens of deep-sea agneziids and styelids.This is Harbor Branch Contribution 1179.

AppendixSpecies belonging to the genus Agnezia (MICHAEL-SEN1898) with their synonyms, known distributions,and known bathymetric ranges.

A. arnaudi (MONNIOT MONNIOT974)A. arnaudi: Monniot & Monniot 1974b, p. 720:Kerguelen 20-61 m; Monniot 1978, p. 174: Ker-guelen; Monniot & Monniot 1983, p. 57: Islas Or-cadas 37-55 m; Monniot & Monniot 1994, p. 25:Weddell Sea.A. glaciata: Monniot 1970: Kerguelen 10-15 m.A. atlantica (MONNIOT& MONNIOT1973)A. atlantica: Monniot & Monniot 1973, p. 421:Azores from 2100-4680; Monniot & Monniot1974a, p. 741: North Atlantic from 2100-4452 m;Millar 1982, p. 165: Northeast Atlantic from2540-2900 m.A. biscoei (MONNIOT& MONNIOT1983)A. biscoei: Monniot & Monniot 1983, p. 56: Ant-arctica, 87-121 m; Monniot & Monniot 1994, p.25: Weddell Sea.A. glaciata: Kott 1969a, p. 97; Kott 1969b, p. 450;Monniot & Monniot 1974b, p. 373.

A. capensis (MILLAR1955)A. capensis: Millar 1955, p. 191: South Africa;Monniot & Monniot 1976a, p. 364: Mozambiquefrom 10-15 m; Monniot & Monniot 1983; Kott1985, p. 76.A. glaciata: Millar 1960, p. 92 (part): South Africafrom 35 m.A. glaciata: Millar 1962, p. 174.A. celtica (MONNIOT& MONNIOT1974)A. celtica: Monniot & Monniot 1974a, p. 743: North

Atlantic 4100-4758 m; Monniot & Monniot1976b, p. 633: Argentina from 3903-3917 m.A. glaciata (MICHAELSEN898)A. glaciata: Michaelsen 1898, p. 370: Tierra delFuego 10 m; Michaelsen 1900, p. 6; Michaelsen1907, 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; Mon-niot & 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 23-115 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-kawa 1980, Table 1: Japan from 10 m; Nishikawa1991, p. 59: Japan.A. sabulosa: Oka 1929, p. 152: Japanfrom 20-30 m.A. krausei (MICHAELSEN 912)A. krausei: Michaelsen 1912, p. 181: Patagonia.A. monnioti n. sp.A. monnioti: (this paper) off Oman, Arabian Sea.A. orthenteron (REDIKORZEV941)A. orthenteron: Redikorzev 1941, p. 199: Japan Seafrom 1900-2090 m; Nishikawa 1991, p. 60.A. septentrionalis (HUNTSMAN1912)A. septentrionalis: Huntsman 1912a, p. 118, Hunts-man 1912b, p. 106: British Columbia.A. beringia: Ritter 1913, p. 493: Bering Sea andAlaska 30-86 m.

A. tenue (MONNIOT& MONNIOT1983)A. tenue: Monniot & Monniot 1983, p. 57: Antarc-tica from 18 m.References

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