In Situ Spawning of Hydrothermal Vent Tubeworms (Riftia pachyptila)

2 Pages·1994·0.81 MB·English

by  C L Van Dover

Reference: Biol. Bull 186: 134-135. (February, 1994)
In Situ Spawning of Hydrothermal Vent Tubeworms
(Riftia pachyptila)
CINDY LEE VAN DOVER
Department ofMarine Chemistry and Geochemistry, Woods Hole Oceanographic Institution,
Woods Hole, Massachusetts 02543
Riftia pachyptila, thegiant vestimentiferan tubeworm, which were slightly negatively buoyant, were observed to
dominates the biomass ofmany hydrothermal vent sites sink in amongst the tubeworms. Sperm formed an ap-
intheGulfofCalifornia(GuaymasBasin)andontheEast parently neutrally buoyant, milky cloud that dispersed in
Pacific Rise and Galapagos Spreading Center (I). The the current within 10 s. Mixing ofegg and sperm clouds
wormstypicallyoccurinlargeclumpsorthicketsasmixed was not observed. No spawning activity was noted on a
populations ofmales andfemales On a diveseries made visit to the same site 3 days earlier nor on a subsequent
bythesubmersibleAlvin in the vicinity of9 50 Non the divetothesite4dayslater(L. Mullineaux and L. Garland,
East Pacific Rise, I observedspawning tubeworms while pers. comm.).
I was sampling associated fauna. This note presents a Although the above observations are limited, we can
briefaccount ojthe spawning activity. infer several features of the reproductive ecology of hy-
drothermal vent tubeworms;
A population ofadult vestimentiferans (length greater
than 1 m) coloWnizes a 10mm high basalt pillar at 949.59' 1. Spawning in R pachyptila populations is not nec-
N, 104 17.37' (2511 depth) within the Venture Hy- essarily en masse. Only a few individuals out ofa colony
drothermal Fields(2). Tubeworms cover most ofthe sur- ofhundreds were involved in the release ofgametes. This
face ofthe pillar and are relatively uniform in size and so observation does not preclude mass spawning by a large
densely packed that they present a cylindrical face ofred proportion of the population under appropriate condi-
plumes around the pillar. The site, known as Dudley's tions. Concurrent spawning by several individuals, both
Pillar, is marked by a round white lid labeled "2" placed male and female, suggests synchronization ofgamete re-
duringthe Haymon and Fornari expedition in May 1991. lease among sexually mature animals, presumably me-
On Alvin dive #2474 (6 December 1991), several R. diated by a chemical cue.
pachyptila were observed to spawn during an hour ofin- 2. Spawning behavior within tubeworm populations,
termittent observations. Each release ofgametes consisted as described above, is intermittent, not continuous. Al-
ofa small, 10-15 cm cloud ofeggs orsperm; the gametes though this might seem patent from the lack ofspawning
were propelled upward by a rapid, partial withdrawal of observations duringthe accumulated tensofhours ofob-
the worm into its tube. It was not possible to determine servation time over the 15 years since tubeworm popu-
ifthe same individuals were spawning repeatedly. Fewer lationswere firstdiscovered, the possibility ofcontinuous
than 10 individuals comprising a small portion of the but inconspicuous releaseofgametesexists. Observations
tubeworm population (covering about '/i to '/: m:) were here suggest that individual spawning is best described as
observed engaged in spawning activity. The frequency of an acute rather than a chronic event, with the spawning
spawning contractions of individual worms was not de- period lasting on the order ofhours.
termined;theinterval between observed spawnswasabout 3. The negative buoyancy offemale gametesgenerates
2-3 min. Both males and females were observed spawn- a dispersal shadow that initially lies close to the adult.
ing. Afterrelease, thecloudofeggsseparatedandtheeggs. Some featuresoftheseobservationsmustbe reconciled
with other studies. Cary et a/. (3) describe spawning of
Received 20July 1992; accepted 22 November 1993. female R. pachyptila in a shipboard pressure chamber.
134
TUBEWORM SPAWNING 135
Females released streams ofeggs, bound by mucus, from (3) fertilization occurs internally immediately before
the gonopores over a period of 30 min. The eggs were spawningorexternally(within the vestimental chamber?)
retained in the vestimental cavity fora few minutes before just after release of the eggs; (4) accumulated eggs are
the mucous binding dissolved and the eggs, positively forcefully ejected into the watercolumn where, negatively
buoyant, floated upward. In unpressurized aquaria, the buoyant, theyspendashort period nearthesiteofrelease:
same authors (3) observed male tubeworms spawning, (5)advectiveconditionsoftheturbulent, warm-watervent
with semen continuously flowing from the male gono- environmentdispersegametesanddevelopinglarvaeaway
pores. Though it is conceivable that release ofa stream from the adult population.
ofgametes, ratherthan punctuated and forceful expulsion
of gametes as observed /// xilu. is an alternative repro- Acknowledgments
ductive strategy, the observations ofCary el at. (3) may Thisnotebenefited from discussion andreviewbySteve
representanomalousbehaviorasa result oftraumaduring Gardiner, Robert Messier, and Stein Kaartvedt. I am
collection, ascent, anddepressurization. Ifthis isthecase, grateful to Paul McCaffrey, Alvin Pilot-in-Training on
the positive buoyancy ofthe eggs may be an artifact of Dive2474, who first observed "something unusual" about
prematuregamete release. Southward andCoates(4)sug- the tubeworms. This work was supported in part by a
gest, based on characteristics ofthe acrosome, that Cary grant from the National Science Foundation.
ft a/, witnessed expulsion ofimmature sperm.
Based on morphological criteria ofmodified sperm in Literature Cited
R. pachyptila. Gardiner and Jones (5) suggest that this
species hassome form ofdirect sperm transferorinternal 1 fVaaunnaDlocvoemrp,osC.itLi.o,naonfdhRy.drRo.thMeersmsailerv.en1t99c0o.mmuSnpiattiiaelsvoanritahtieoEnasitn
fertilization. Likewise, thepresenceofsperm togetherwith PacificRiseandGalapagosSpreadingCenter.Pp.253-264inGorda
eggs in the female genital tracts ofR. pachyptila suggests Ridge:A SeafloorSpreadingCenterinthe UnitedStatesEconomic
the possibility ofinternal fertilization (6). Cary el al. (3) Zone, G. R. McMurray, ed. Sponger Verlag. New York.
demonstratethat R.pachyptilasperm bundlesareeffective 2. Haymon, R. M., D. J. Fornari, M. H. Edwards, S. Carbotte, D.
swimmers and suggest that the bundles may become an- Wburtiigohnt,alaonndgKt.heC.EasMtacPdaocinfailcdR.is1e99c1r.est (H9y0d9r'o-t5h4e'rmNa)lavnedntitsdirsetlrai--
chored in the vicinity ofthe female gonopores or within tionshiptomagmaticandtectonicprocessesonfast-spreadingmid-
theanteriorregionsoftheoviducts. SouthwardandCoates ocean ridges. Earth PlanetarySci. Let 104: 513-534.
(4) suggest that active sperm transfer is likely in a group 3. Cary, S. C., H. Felbeck, and N. D. Holland. 1989. Observations
of related vestimentiferans (Ridgeia spp.), and that this on the reproductive biology ofthe hydrothermal vent tube worm
transfertakes placewhen theplumesofcloselyjuxtaposed 4. SRiofuttihawpaarcdh,ypEt.iCl.a,.aMnadr.K.EAc.olC.oaPtreosg. 1S9e8r9.52:S8p9e-r9m4.massesandsperm
animals may brush against each other. transfer in a vestimentiferan, RidgeiapiscesaeJones, 1985 (Pogo-
//; situobservations reconciled with the literature cited nophora: Obturata). Can.J. Zool.67: 2776-2781.
above suggest the following spawning scenario in R. pa- 5. Gardiner, S. L., and M. L. Jones. 1985. Infrastructure ofsper-
chyptila:(1)Neutrallybuoyantsperm bundlesareexpelled gmoinogoepnheosrias:iOnbttuhreavteas)t.imTernatnisf.erAamn.tMuibcerwosocr.mSRoicf.ti1a04p:ach1y9p-t4i4l.a(Po-
forcefully enough to be dispersed over a field of tube- 6. Jones, M.L. 1981. Riftiapachyptila. newgenus,newspecies,the
worms; (2)the sperm bundles swim and attach to females, vestimentiferan worm from the Galapagos Rift geothermal vents
somehow mediating a spawning response in the female; (Pogonophora). Proc. Biol Sue. Wash. 93: 1295-1313.