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Home , Alvinellidae, Ampharetidae, Hydrothermal vent

MARINE PROGRESS SERIES Vol. 106: 111-120, 1994 Published March 17 Mar. Ecol. Prog. Ser.

Ecology and reproductive biology of the Amphisamytha galapagensis ()

Damhnait McHugh1~*,Verena Tunnicliffel,

'Department of Biology and 'School of Earth and Sciences, University of Victoria, British Columbia, CanadaV8W 2Y2

ABSTRACT The ampharet~dpolychaete Amphjsamytha galapagensjs Zottoli, 1983 IS known from hydrothermal vent sltes in the eastern and western Pacific, and has been reported from the Atlantic Pacific specimens are apparently conspeclfic but closer examination of the global species is necessary We exanuned ecological and reproductive features for an explanation of the wide distnbution of th~s species which is unusual among vent (unique, if truly global In distnbution) The worm, pre- sent in 95% of the collections from the Juan de Fuca and Explorer Ridges in the northeast Pacific, occurs in a wide variety of vent habltats It appears to take advantage of vestimentiferan tubes to increase substratum area but also colonizes actlve smokers sediments and other anmals A galapa- gensjs IS gonochoric, and all stages of egg and sperm development were present in populat~onssam- pled at different tlmes of the year Eggs reach 240 ].]m in d~ameterand fecundity is relatively hlgh, no modif~cationsIn sperm ultrastructure were seen From comparison with other , we propose that A galapagens~sundergoes continuous reproduction with external fertdization resulting in demer- sal lecithotrophic larvae The proposed reproductive mode of A galapagensis is not unlque among vent animals and shows no unusual adaptahon for long range d~spersaleven though the adult distrib- ution is wide We propose that broad ecological tolerances, flexibility and reduced dispersal may be more important in alloulng establ~shmentof A galapagens~sat new s~tesonce ~tarrives Fur- ther study In populat~ongenetics, systematics and development IS important in a specles that could pro- vide much lns~ghtinto the evolut~onof ecological and hfe history patterns at ephemeral island hab~tats

KEYWORDS: Amphisamytha galapagensls . Polychaete . Hydrothermal vent . Reproduction

INTRODUCTION spreading centers. Discrete vent faunas are recog- nized in different oceanic realms corresponding to Luxuriant biological communities at hydrothermal separation distance and spreading history (TunnicMfe vents are supported by chemosynthetic primary 1988, 1991, Van Dover 1990, D. Desbruyeres pers. . The energy source, however, is unpre- comm.). Vent fields on separate segments of a ridge dictable as it depends on sustained hydrothermal may lie hundreds of kilometers apart. The extreme activity. Hydrothermal vents, which range in age from patchiness of vents is likely to be a major a few to hundreds of years (MacDonald et al. 1980, factor influencing biotic processes anlong the habitat's Lalou et al. 1984, Campbell et al. 1988, Stakes & inhabitants. Moore 1989), have a global distribution that follows Dispersal of species and maintenance of popula- the mid-ocean spreading ridges and isolated back-arc tions at these ephemeral island can be interpreted from histories of hydrothermal vent animals. Few accounts of reproduction and develop- ' Present address: Department of Biology and Institute of Ma~ineSciences, University of California, Santa Cruz, ment of vent fauna have been published (for review California 95064, USA see Tunnicliffe 1991), however, mainly because time-

0 Inter-Research 1994 112 Mar. Ecol. Prog. Ser. 106: 111-120, 1994

series samples from a vent are difficult to obtain and METHODS culture of vent species in the lab has yet to be achieved. Nonetheless, single samples of animals Ecology and distribution. Specimens of Amphi- from different areas have yielded a great deal of in- samytha galapagensis used in this study came from formation (e.g. Lutz et al. 1980, Le Pennec et al. 1984, Juan de Fuca and Explorer Ridges in the northeast Berg 1985, Turner et al. 1985, Van Dover et al. 1985, Pacific (Fig. 1). h4ost collections were 'grabs-of-oppor- 1987, Berg & Van Dover 1987, Cary et al. 1989, tunity', and none represent targeted collection for this McHugh 1989, Gustafson et al. 1991, Gardiner et al. species. Most often, vestimentiferan tube clumps were 1992). Many of these studies show that vent species grabbed with a submersible claw in a haphazard exhibit a wide range of reproductive and develop- fashion; chimney samples might be worm grabs or the mental modes reflecting phylogeny of the species broken tops of sulphide edifices. Different pilots and rather than the opportunistic life history strategies observers induce different collection biases, so sam- with larval dispersal stages initially predicted for such ples may be poor representatives of the vent fauna. an ephemeral and patchy environment (Desbruyeres Specimens were bulk fixed In 7 % formalin for later & Laubier 1983, Grassle 1985). More information on sorting and storage in 4 % formalin or 70 % ethanol. reproduction, development and growth rates is To examine microdistribution patterns, a high tem- needed to understand the of in- perature smoker on Endeavour Segment was sampled vertebrates that inhabit the vent environment (Tunni- as follows: a flange, measuring 30 X 40 cm, was broken cliffe 1991, Kennish & Lulz 1992). from the side of the smoker; on shipboard, a 2.5 X In this study, features of the ecology and life history 2.5 cm grid was overlaid and the animals within each of an ampharetid polychaete, Amphisamytha galapa- square were preserved separately. Because of loss and gensis Zottoli, 1983, are investigated. A. galapagensis displacement of some animals, results cannot be is of particular interest because it has the widest viewed as complete. Nonetheless, the relative posi- known geographic range of all species reported from tions of 6592 vent animals could be assigned, including hydrothermal vents around the world. In this paper, 266 Amphisamytha galapagensis. we document the distribution, habitats and associa- Reproductive biology. Specimens for study of re- tions of this species, and examine several aspects of its productive biology came from 3 vent sites: Axial - reproductive and developmental biology. mount (August 1983), Endeavour Segment (September 1984) and South (June 1984) (Fig. 1). Oocytes and spermato-

I I I genic stages in formalin-fixed animals were examined under light micro- scopy. Specimens collected in July 1986 from Axial were fixed in 3% glutaraldehyde in Millonig's l phosphate buffer for sperm ultrastruc- - 4a0 N ture examination with transmission electron microscopy (TEM). Gender was determined from coel- omic samples of gametes. In 10 of the largest females from each sample, 80 oocytes were measured for maximum diameter at 100x magnification. The data on oocyte sizes were log trans- formed and analysis of variance -440N (ANOVA) tests were used to identify significant differences among the sam- ple means and to examine differences l in means among females in each sam- ple. To estimate fecundity, all oocytes

I I from the 5 largest females in each sam- 130°w 126Ow 1i20W ple were collected, and the total num- ber of oocytes in each worm was esti- Fig. 1. Ridges of the northeast Pacific where Amphisamytha galapagensiswas collected for thls study. Vent sites are located on each of the segments indicated mated three aliquots and may be spread over tens of kilometers from a 250 ml suspension of all oocytes. McHugh & Tunnicllffe: Ecology and reproductive biology of Amphlsamylha 113

Maximum oocyte size was recorded from each other vent species (Tunnicliffe 1991 and unpubl. data) coelomic sample. shows that A. galapagensis is recorded at more sites In males, the occurrence frequencies of 3 stages of than any other species. sperm development were noted: early rosettes of sper- On a provincial scale, it is equally ubiquitous. We matocytes (4 to 16 stage), later rosettes of sperma- have sorted collections from 56 vents along the tocytes (> 16 cell stage) and clusters of spermatids with Explorer and Juan de Fuca Ridges that span a dis- tail pieces. In coelomic samples from each of 5 males, tance of 550 km, and Amphisamytha galapagensis all stages in 4 randomly assigned squares of a hemocy- was present at 52 vents (Table 2, Fig. 1) that range tometer slide were recorded. The nephromixia of from diffuse low temperature flows on new males were checked for the presence of free spermato- to large high temperature sulphide structures in a zoa. For examination of sperm ultrastructure under mature field. The 4 vents with no A. galapagensis TEM, gluteraldehyde-fixed worms were post-fixed in specimens hold no obvious common features. Often 1 % osmium tetroxide at 4 "C for 1 h. After dehydration the worm has a clumped distribution and a single in a graded series of ethanol and propylene oxide, they grab might not contain it, therefore we may have were embedded in EPON 812 and sectioned on a missed sampling it. The proportion of the total fauna Reichert ultramicrotome using glass knives. Sections represented by this species (Table 2) varied from neg- were stained in citrate and uranyl acetate before ligible to 67 %; in half the ennumerated samples, this viewing on a Philips EM-300. species represented over 4 % of the total count. The few samples in which it was found in great abun- dance (over 25 Yo)were old chimneys with diminished RESULTS flow and many dead tubeworms. Collections from Cleft Segment (Fig. 1) spanned many Distribution vent types, and they were analyzed together as collec- tion methods tended to be uniform. Ridgeia piscesae, Table 1 documents the sites at which Anlphisamytha Paralvinella sulfincola and Amphisamytha galapagensis galapagensis has been found. The ampharetid are 3 of the most abundant species at Cleft Segment reported from Snake Pit of Mid-Atlantic Ridge (Segon- (6 species comprise over 90 % of all collections: B. zac 1992) resembles A. galapagensis; however, speci- Milligan pers. comm.). The abundances of A. galapa- mens from the Florida Escarpment were apparently genslsare significantly correlated with those of R. pisce- misidentified and do not belong to the sae, the vestimentiferan (Spearman correlation coeffi- Amphisamytha (D, Desbruyeres pers, comm.). To date, cient = 0.488, n = 28, p < 0.01). No significant the species is known for sure only from the Pacific, relationship was found with abundances of the poly- Nonetheless, comparison with the distributions of chaete P sulfincola, however. Fine-scale distribution of An~phisamytha Table 1. Reports of presence of the polychaete Amphisamytha galapa- galapagensis was examined On the gensis. Note that the Florida Escarpment is a seep, not a vent site flange collected from Endeavour Segment. Hot pooling under the flange mea- Site Source sured a maximum of 260°C from where it trickled upward over the nose of the flange Equatorial Eastern Pacific and bathed a dense mat of animals on the Galapagos hft Zottoli (1983) upper side (J. Holden pers. comm.). The 13"N. Desbruyeres et al. (1985) occurrence of species across the flange 21°N. East Pacific Rise Grassle (1985) Guaymas Basin, EPR Grassle (1985) corresponded to water flow: where hot water Northeastern Pacific emerged around one side, the polychaete Juan de Fuca and Explorer Ridges Tunnicliffe (1991) Paralvinella sulfincola predominated; on the Western Pacific cooler side, Ridgela piscesae tubes were Marianas Back-Arc Basin Hessler & Lonsdale (1991) abundant. A. galapayensis occurred on both Manus Back-Arc Basin Galkin (1992) sides. Within the sample, A, galapagensis Lau and Back-Arc Basins D. Desbruyeres pers. ~omrn.~ abundances are correlated to those of Atlantic the vestimentiferan (Spearman correlation Mid-Atlantic Ridge Segonzac (1992) coefficient 0.400, 108, p 0.001) and Florida Escarpment Petrecca & Grassle (1990) C = n = < again showed no significant relationship "Reported as Arnphisamytha aff. galapagensis with P sulfincola. The ratio of adult A. gala- bReported as Ampharetidae gen. sp.; see text CSpecin~ensapparently misidentified (D. Desbruyeres pers. comm.) pagensis to 'juveniles' (<5 mm length, but see 'Reproductive biology' section below) in 114 Mar. Ecol. Prog. Ser. 106: 11 1-120, 1994

crawl actively. At 13" N on East Pacific Rise, we found this species free-living around the mouth- parts of the vent crab Cyanograea praedator; it has also been noted on the crab Bythograea thermy- dron (Desbruyeres & Laubier 1983). Like other ampharetids, A. galapagensis apparently uses its buccal tentacles for deposit feed- ing; several specimens had sul- phide particles and bacterial fila- ments in the gut.

Reproductive biology

Amphisamytha galapagensis is gonochoric and chi-square tests of the 3 samples showed no sig- nificant difference from a 1: 1 male: female sex ratio (p < 0.001). Gametes are released at an early Fig. 2. Amphisamytha galapagensis. Live worms on shipboard. Anterior filaments are stage into the coelom, where branchiae. Black mass is coalesced tubes made of sulphide particulates and mucus. proceeds. COelOmic Scale bar = 1 cm gametes are found in worms as small as 3.5 mm in length, which is approximately 20 % of the max- this sample is 1.2: 1.0. Abundances of the 2 size classes imum length. Fig. 3 shows size frequencies of coelomic examined over the gridded flange are correlated gametes in females from the 3 sites. A similar wide (Spearman correlation coefficient = 0.530, n = 108, range of oocyte sizes is recorded from each site and p < 0.001). this size range is repeated in each female in the 3 sam- Amphisarnytha galapagensis occurs in a wide vari- ples. The ANOVA test reveals significant differences ety of vent habitats. We found it most commonly between sample means and the overall mean (F = attached to vestimentiferan worms in a flexible partic- 63.43, df = 2, p < 0.0001). This difference indicates vari- ulate tube bound by mucus, and usually free at the ability in the reproductive cycle among the 3 popula- upper end (Fig. 2). The worm may also construct tions; both the and the Explorer Ridge recumbent tubes on rock surfaces, and was seen on populations have higher proportions of larger oocytes active sulphide chimneys near the venting spout. than the Endeavour Segment population (Fig. 3). Tubes were also found projecting from sediments at Significant differences exist between individual the base of smoker chimneys. However, A. galapagen- means of oocyte size and sample means (Axial sis is frequently without a tube and specimens can Seamount: F= 2.39, df = 9, p < 0.0113; Explorer Ridge:

Table 2. Occurrence of the ampharetid polychaete Amphisamytha galapagensis at vents on the spreading ridges in the northeast Pacific. Listing indicates the numbers of vents at which the worm was found and, for enumerated samples, the proportion of the fauna (> 5 mm size) represented by A. galapagensls. n: sample size; na: not available

hdge: Explorer Juan de Fuca Site; South Segment Mlddle Valley Endeavour Segment Ax~alSeamount Cleft Segment

No. of vents sampled 6 3 12 If 18 No. of vents with A galapagensis 6 3 12 16 15 Proportion of A. galapagensis na na 18.8 % 6.6 % 4.3 % (n, SD) (8. 24.2) (1,-1 (28, 8.7) McHugh & Tunnicliffe: Ecology and reproductive biology of Amphisamytha

Axial Seamount Early N=10 Rosettes

Rosettes

Endeavour Segment Endeavour Segment N=10

O/O Occurrence

Fig. 4. Amphisanlytha yalapagensls. Percent occurrence of spermatogenic stages in 5 males from each of the 3 samples of worms

Explorer Ridge tinct peaks in oocyte sizes are evident in the Ax~al N = 10 Seamount sample and, to a lesser extent, in the other 2 samples (Fig. 3). The maximum fecundity of Amphisamytha galapagensis is 12 500 oocytes in a worm of 18 mm length (0.0684 g) and mean fecundity ranges from 5600 to 9600 oocytes per worm among the 3 populations (Table 3). Maximum oocyte size of 0 50 100 150 200 250 A. galapagensis from the 3 samples ranges from 215 to Oocyte Diameter (pm) 240 pm diameter (Table 3). While free spermatozoa were not found In the Fig 3 Arnph~sarnythagalapagenvs Size-frequency histo- nephromixia, the 3 spermatoyenic stages were well grams of maximum oocyte diameter for the 3 samples of represented in the coeloms of males from the 3 sites worms N number of females in each sample (Fig. 4), and mature sperm were found in males fixed for TEM. In mature sperm from the coelom, the nuclear F = 6.031, df = 9, p < 0.0001;Endeavour Ridge: F= 4.92, material is condensed to a bullet-shaped nucleus and df = 9, p < 0.0001), which indicate a lack of synchro- the acrosomal vesicle is thimble-shaped with a thin nization of oocyte development among individuals in opaque cap (Fig. 5A). Longitudinal and cross-sectional each population. In the Axial Seamount and Endeav- views of the vesicle reveal regional differences in elec- our Segment populations, however, 1 and 2 females tron opacity: an electron-translucent inner border lines account for the significant differences among individu- the main portion of the vesicle, within which a regular als in each sample, respectively (p < 0.05). Three dis- granular substructure is apparent in some sections; a thin layer of electron-opaque material, perhaps sub- acrosomal in origin, apposes the inner proximal end of Table 3. Amphlsarnytha galapagensis. Maximum oocyte di- ameter and maximum fecund~ty(no of oocytes in an indiv- the acrosomal vesicle. A prominent gap of ca 0.1 pm idual) recorded for worms from the 3 sites n: sample size separates the base of the acrosome and the anterior tip of the nucleus, and the fully condensed nucleus mea- Site Maximum Maxlrnum sures ca 2.7 pm by ca 1.6 pm (Fig. 5A). The middle oocyte diameter fecundity piece contains 5 mitochondna surrounding the proxi- (pm) In, F, SDI mal and distal centrioles, and the flagellurn has a 9 + 2 - microtubular arrangement (Fig. 5B). Ax~alSeamount 215 11412 (5, 5956, 3624)

Endeavour Segment DISCUSSION

The wide distribution of Amphisamytha galapagen- Explorer R~dge 240 12500 (5, 9893, 2200) sis is unique among vent species, apparently ranging across the Pacific and possibly the Atlantic. A re- Mar. Ecol. Prog. Ser 106: 111-120. 1994

east to west Pacific, and is doubtful about the exact affinities of the Atlantic specimens. While even sub-species or sister-species rela- tionships have biogeographic interest, further speculation on a global perspective is prema- ture. Even with the most conservative approach, however, the wide eastern Pacific distribution remains intriguing. The highly adaptable nature of the worm may partly explain its wide distribution. It appears to have few requirements other than proximity to a chemosynthetic source, and the extremes of habitats it occupies are impres- sive. We have found this under a 10 cm thick cracked basalt crust some 50 m distant from a vent; no other were found there. It was also collected from atop a black smoker in a zone just below Paralvinella sulfincola, the northeast Pacific species that occupies the hottest zone (Tunnicliffe et al. 1993). Amphisamytha gala- pagensis is reported in seeping Guayrnas sedi- ments with several other polychaetes, and as the only animal in sediments at the foot of a smoker (Grassle et al. 1985). The wide range of habitats reported here and by Desbruyeres et al. (1985) is seen in no other vent species to our knowledge. Unlike other vent species with wide distribu- tions, Amphisamytha galapagensis is not a rare or minor species. At over 5 % mean abun- dance in collections, it ranks as a dominant species on . Petrecca & Grassle (1990) record densities of 2267 m-' in Guaymas sediments, and we estimate a mini- mum density of 2995 m-2 on the smoker flange collected from Endeavour Segment. At such high abundances, some interactions with other species can be expected. The significant posi- tive correlation with vestimentiferan abun- dances is most likely due to the increased sub- stratum area provided by the vestimentiferan tubes. The same correlation existed whether or not the vestimentiferan tubes were occupied Fig. 5. Amphisamytha galapagensis. Transmission electron micrographs (tested using the flange samples). On bare of sperm ultrastructure. (A)Medlan longitudinal section through a sperm chimney surfaces additional substrate is also cell. a = acrosome; m = mitochondria; n = nucleus. Scale bar = 1.0 pm. available to this ampharetid, In neither the (B)Longitudinal section through the flagellar apparatus showing the between-vent analysis (Cleft Segment collec- proximal (pc) and distal (dc) centrioles. The unlabeled arrow points tions) the within-vent (Endeavour to a lateral satellite. Inset shows a cross section throuahd a flaaellum., If).. , m = mitochondria; n = nucleus. Scale bar = 0.5 pm flange) did we identify a negative correlation with the alvinellid Paralvinella sulfincola. Nonetheless, substratum may oc- examination of the species characters is advisable, cur, even though the alvinellid tends to locate within however, as D. Desbruyeres (pers. comm.) expresses centimeters of the hottest flow (Tunnicliffe et al. 1993) some concern over the variability of characters from while the ampharetid stays more distal. ~McHugh& Tunnicliffe: Ecology and reproductive biology of .4mphisamytha 117

Arnphisarnytha galapagensis is a deposit-feeder that 1989, Rice 1992). Specializations for the mode of fertil- appears to prefer a tubicolous habit but frequently ization (e.g. within the tube, spermatophore transfer, vacates its tubes; it may be free-living when tube pseudocopulation, copulation) are usually associated material is scarce. It seems to have little problem colo- with spermatozoan modifications such as an elongated nizing vents and maintaining populations. One Cleft nucleus, a complex acrosome or fused mitochondria. Segment field is known to be young - about 10 yr at Sperm ultrastructure is known in few polychaetes of collection time (Chadwick et al. 1991, Milligan & Tun- the and we report the first nicliffe in press) - and several Endeavour chimneys in observations for an ampharetid. The invaginated coni- an old field are almost extinct; A. galapagensis was cal acrosomal vesicle of Amphisamytha galapagensis abundant at the first and predominated at the second. is reported in other polychaete families, including the Like almost all other ampharetid polychaetes that terebellid Streblosoma acymatun~(Jamieson & Rouse have been studied, Amphisamytha galapagensis is 1989). The variation in acrosomal electron opacity seen gonochoric and its gametes develop freely in the in A. galapagensis is common in polychaetes and may coelom from an early stage. The presence of gametes reflect compositional differences of acrosome compo- in small worms indicates that maturity is reached at a nents (Eckelbarger & Grassle 1987). The nucleus, mid- relatively early stage in the life cycle. Mature speci- dle piece and tail of A. galapagensis sperm show no mens were recovered from panels deployed on the unusual characteristics. The condensed nucleus length East Pacific Rise and Galapagos spreading center for to width ratio of 1.8 lies within the range observed 1216 d (Van Dover et al. 1988),implying that growth to among polychaetes with external fertilization (Sawada maturity takes at the most 3.3 yr in this species. The 1984). Only the acrosome of A. galapagensis sperm presence of a full range of oocyte sizes and all sper- shows any complexity which may be related to egg matogenic stages in worms from 3 vents sampled envelope specializations rather than the fertilization in different months of different years suggests that mode. Based on these results, it is proposed that A. A. galapagensis produces gametes continuously or galapagensis has neither internal fertilization nor sper- semi-continuously. ANOVA results imply a lack of matophore formation. We can only speculate whether synchrony of oogenesis among females in the 3 popu- fertilization occurs in the water or in the tube. In the lation~,although multiple comparison tests indicate terebellids Ramex californiensis and Nicolea zosteri- that this result can be accounted for by a small propor- cola eggs are fertilized in the tube and in a mucus mass tion of the individuals in 2 cases. Peaks in the oocyte at the tube opening, respectively (Eckelbarger 1974, size-frequency histograms may represent intermittent McHugh 1993), and both species have elongated release of oocytes into the coelom, which may cause sperm nuclei (ca 10 pm; pers. ohs.); the terebellid peaks in reproductive activity when eggs mature. In Streblosoma acymatum fertilizes in the the shallow water ampharetid acutifrons,2 and has a sperm head of ca 2 pm (Jamieson & Rouse spawning peaks in the females are separated by 2 mo 1989). If such characteristics can be generalized, then (Clavier 1984), and peaks are also known in the con- broadcast spawning seems likely for A. galapagensis. tinuous reproduction of the brackish water ampharetid While polychaete larvae have been sampled in the Hypaniola kowalewskii (Marinescu 1964). The alvinel- at and near vents on the East Pacific Rise and lid polychaete Paralvinella pandorae, found at north- in the Guaymas Basin, their identification has not been eastern Pacific vents, is thought to reproduce continu- possible because of their early stages of development ously (McHugh 1989). Reproductive potential in the and damaged condition (Berg & Van Dover 1987). vent bivalve may be high Therefore, we base our predictions of the development because it becomes reproductively active at a small mode of Amphisamytha galapagensis on indirect size and apparently reproduces continuously over a evidence. In , maximum oocyte long time (Berg 1985). Also, gametogenesis occurs size correlates well with type of larval development continuously in the vestimentiferan (Thorson 1950, Strathmann & Vedder 1977). In poly- (Gardiner et al. 1992). chaetes, small eggs (1150 pm) are usually associated The Polychaeta exhibit a variety of sperm morphol- with planktotrophy while larger eggs (>l50 pm) give ogies, which generally correspond to fertilization rise to lecithotrophic larvae or brooded embryos modes. In species with ect-aquasperm (sensu Rouse & (Hermans 1979). Among ampharetids, oocytes greater Jamieson 1987), the spermatozoon generally has a than 150 pm in diameter give rise to lecithotrophic, short, rounded or conical head, a middle piece con- demersal larvae (Okuda 1947, Nyholm 1951, Hutch- taining 4 to 6 mitochondria and a long flagellum with a ings 1973, Guillou & Hily 1983) or to direct developing 9 + 2 microtubular arrangement. Broadcast spawning larvae (Wesenberg-Lund 1934, Marinescu 1964, polychaetes from many families have such characteris- Zottoli 1974, Cazaux 1982, Clavier 1984). The eggs of tics (for reviews see Sawada 1984, Jamieson & Rouse shallow water ampharetids sink, in some cases sticking 118 Mar. Ecol Prog Ser.

to the bottom for a few days after fertilization, and However, there are numerous examples of marine spe- emerging lecithotrophic larvae are demersal (Thorson cies with short-lived or brooded larvae that have wide 1946, Nyholm 1951, Clavier 1984). The relatively large geographic ranges; some authors describe mecha- eggs of A. galapagensis (200 pm) probably produce nisms of adult dispersal by rafting or wafting (e.g. non-feeding demersal larvae or develop directly into Highsmith 1985, 6 Foighil 1989, Martel & Chia 1991). crawl-away juveniles. We have yet to find larvae or If this highly adaptable species has located a dispersal early stage juveniles of A. galapagensis; the earliest agent in the , it is not yet known. juvenile stages retrieved have 9 setigers (pers. obs.). The ecology of Amphisamytha galapagensis may We propose, therefore, that A. galapagensis undergoes contribute to its ability to become widely established. lecithotrophic larval development near the bottom. In addition to having the widest distribution, it also has The longest planktonic period recorded for ampharetid the widest ecological range presently documented larvae is 3 to 5 d in Melinna cristata (Nyholm 1951). among the common vent species. Vent animals may Metabolism may be reduced at the low ambient tem- enter distant provinces frequently but be unable to perature around vents (ca 2"C), making it impossible locate an appropriate habitat. The key to the wide to confidently predict the length of larval life of vent distribution of A. galapagensis may lie in its ability to polychaetes based on studies of shallow water species. adapt to whatever habitat is available in a new site. The maximum fecundity of Amphisamytha galapa- Indeed, long-lived larvae may not be an advantage gensis, 12500 oocytes, is comparable to estimates for to a hot-vent animal with a localized habitat. As shallow water polychaetes that undergo non-feeding Johannesson (1988)points out, the colonizing potential larval development (George 1964, Olive 1970, Fauchald of short dispersers may be higher, as they can maintain 1983, Gremare & Olive 1986), and the vent alvinellid a population once it becomes established. polychaete Paralvinella palmiformis (McHugh 1989). Amphisamytha galapagensis is an exception to the If A. galapagensis does reproduce continuously, then high species shown by vent communities of each breeding event may involve just a portion of the different provinces. A better understanding of its biol- eggs in the coelom. Nonetheless, fecundity in A. gala- ogy would contribute to interpretation of many aspects pagensis is much higher than that of the only other of vent biology, such as the roles of dispersal, habitat ampharetid for which an estimate exists; Hypaniola specialization, speciation and population structure in kowalevvskii, which is comparable in size and repro- the development of vent communities. Studies on the duces continuously, spawns 40 to 110 eggs at a time systematics and population genetics of this species (Marinescu 1964) and undergoes direct development would make valuable contributions. within the maternal tube. The proposed life history features of Amphisamytha Acknowledgements. We thank NOAA Vents Program, Geo- galapagensis are continuous reproduction, external logical Survey of Canada and Department of Fisheries & Canada for logistic support in collecting samples. fertilization and non-feeding, demersal larval develop- Support by submersible crews of 'Alvin', 'Pisces IV' and ment. A short larval life would ensure that a vent pop- 'Ropos' are gratefully acknowledged. Further contnbutions ulation is maintained. We find large numbers of small were made J. Delaney, University of Washington. Information individuals (<5 mm) associated with adults, which on species counts was provided by S. Mah, B Milligan and T. Parker. D. Desbruyeres kindly advised us on the Identification indicates more than 1 event, and recruit- of Atlantic and western Pacific specimens. The original man- ment experiments at and near vents confirm local uscript was improved by the comments of 3 anonymous repopulation (Van Dover et al. 1988, Tunnicliffe 1990). reviewers. This research was supported by the Natural Sci- Recruitment to new sites within a ridge requires a dis- ences and Engineering Research Council of Canada. persal mechanism of larvae. The strong along-ridge component to the movements of deep water (Thomson LITERATURE CITED et al. 1990, Cannon et al. 1991) around vents may be important in providing such a mechanism. Berg, C. J. Jr (1985).Reproductive strategies of mollusks from The proposed life history does not explain the abyssal hydrothermal vent communities. In: Jones. M. L. unique distribution of Amphisamytha galapagensis. (ed.) The hydrothermal vents of the eastern Pacific: an While it has been suggested that long planktonic devel- overview. Bull. biol. Soc. Wash. 6: 185-197 Berg, C. J., Van Dover, C. L. (1987).Benthopelagic macrozoo- opment promotes wide dispersal (e.g. Mileikovsky plankton communities at and near deep-sea hydrothermal 1971, Scheltema 1986), the observation is not universal vents in the eastern Pacific Ocean and the Gulf of Califor- and many other factors may influence distribution pat- nia. Deep Sea Res. 34A: 379-401 terns (Johannesson 1988). Active dispersal of A. gala- Campbell, A. C., Bowers, T. S., Measure, C I,Falkner, K K., Khadem, M,, Edmond, J. M. (1988).A tlme senes of vent pagensis between northern and equatorial Pacific vent fluid composition from 21°N, East Pacific kse (1979, 1981, fields would be compromised by a short larval life; fur- 1985) and the Guaymas Basin, (1982, ther dispersal across the Pacific is even less probable. 1985).J. geophys. Res. 93: 4537-4549 McHugh & Tunnicliffe. Ecology and reproductive biology of Amphlsanlytha 119

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This article was submitted to the editor Manuscript first received: June 8, 1993 Revised version accepted: October 26, 1993