RESEARCH ARTICLE

E. Ramirez-Llodra Æ W. D. K. Reid Æ D. S. M. Billett

Long-term changes in reproductive patterns of the holothurianOneirophanta mutabilis from the Porcupine Abyssal Plain

Received: 30 April 2004 / Accepted: 7 September 2004 / Published online: 14 October 2004� Springer-Verlag 2004

Abstract Time-series studies (1989–2002) in the NEAtlantic have shown large-scale changes in the compo-sition and structure of the benthic community on thePorcupine Abyssal Plain. Radical changes in the abun-dance of some species in 1996 led to a significant shift inthe way in which organic matter was reprocessed at theseabed. This article examines the reproductive processesof the holothurian Oneirophanta mutabilis collectedduring the time series. The reproductive biology of O.mutabilis is reviewed. No males were evident in any ofthe samples. The sex ratio (females: ‘no gender’) wasbiased significantly towards no-gender individuals. Themaximum egg size was 650 lm and there was no evi-dence of synchrony in reproduction. Significant changesin the oocyte-size distribution and the fecundity of O.mutabilis were noted through time, coinciding with thetime of greatest faunal change in the benthic community.There was an increase in the proportion of previtello-genic oocytes and a decrease in the proportion of maturevitellogenic oocytes in 1997 and 1998, in parallel with asignificant decrease in fecundity of the post-1996 sam-ples. Samples from 2002 showed a reversal in thereproductive trends, with an increase in the proportionof mature vitellogenic oocytes and fecundity. The resultsare discussed in relation to large changes in abundanceof the epibenthos on the Porcupine Abyssal Plain. It issuggested that the superabundance of certain megafa-unal species on the abyssal seafloor affected the avail-ability of trophic resources for O. mutabilis, leading tothe changes in its reproductive effort.

Introduction

With the exclusion of chemosynthetic ecosystems, suchas hydrothermal vents and cold seeps, the deep-seabenthic fauna depends ultimately on the input of sur-face-produced organic matter. Under areas of highsurface production, large, seasonal fluxes of organicmatter couple the surface water and deep-sea benthicecosystems (Billett et al. 1983; Lampitt 1985; Rice et al.1986, 1991, 1994; Thiel et al. 1990; Smith et al. 1994;Smith et al. 1996; Baldwin et al. 1998; Beaulieu andSmith 1998; Lampitt et al. 2001; Beaulieu 2002). Becausethe rapid sinking of phytodetritus prevents its completeutilisation by upper-ocean pelagic grazers, the arrival ofthis organic matter provides deep-sea communities withseasonal, high-quality food resources (Gooday andTurley 1990; Beaulieu and Smith 1998; Ginger et al.2000; Billett et al. 2001; Ramirez-Llodra et al. 2002;Wigham et al. 2003a; Ruhl and Smith 2004).

Over the last few decades, the northeast Atlanticabyssal plains have been the focus of several multidis-ciplinary research programmes (Roe et al. 1987; Sibuetet al. 1993; Rice et al. 1994; Thurston et al. 1994; Billettand Rice 2001). In particular, the Porcupine AbyssalPlain was studied by the BENGAL project (high-reso-lution temporal and spatial study of the BENthic biol-ogy and Geochemistry of a north-eastern Atlanticabyssal Locality; Billett and Rice 2001). This projectshowed that the vertical flux of organic matter to thePorcupine Abyssal Plain seafloor varies on seasonal andinter-annual time scales, in terms of both quantity andquality (Witbaard et al. 2000, 2001; Kiriakoulakis et al.2001; Lampitt et al. 2001). In addition, major long-termchanges in the structure and composition of benthicinvertebrate megafauna were documented (Billett et al.2001).

The megabenthos of the Porcupine Abyssal Plaincomprises 17 major taxa, with holothurians dominatingthe invertebrate megafauna in abundance (81%) andbiomass (91%). Actiniarians, annelids, asteroids, and

Communicated by J.P. Thorpe, Port Erin

E. Ramirez-Llodra (&) Æ W. D. K. Reid Æ D. S. M. BillettSouthampton Oceanography Centre,European Way, Southampton, SO14 3ZH, UKE-mail: ezr@soc.soton.ac.ukFax: +44-2380-593052

Marine Biology (2005) 146: 683–693DOI 10.1007/s00227-004-1470-z

ophiuroids constitute a large part of the remainingmegafauna (Billett et al. 2001). The data analysed fromthe 13-year time-series samples (1989–2002) on thePorcupine Abyssal Plain shows an increase in the totalmean abundances of benthic megafauna after 1996(Billett et al. 2001). In particular, the small elasipodidholothurian Amperima rosea increased in number rap-idly by more than two orders of magnitude, becomingthe dominant species over a vast area of the PorcupineAbyssal Plain. This significant increase, together withpopulation changes in other megafaunal species of thePorcupine Abyssal Plain, has become known as the‘Amperima Event’ (Billett et al. 2001).

The deposition of phytodetritus to the seafloor trig-gers significant responses in the activity of the benthicfauna (Sibuet 1985; Gooday and Turley 1990;Pfannkuche 1993; Pfannkuche et al. 1999; Thurstonet al. 1994, 1998; Galeron et al. 2001; Witbaard et al.2001; Ruhl and Smith 2004). Recent studies suggest thatapart from the amount of phytodetritus, the quality ofthe organic matter may also affect biological processesof the deep-sea megabenthos (Ginger et al. 2001; Hud-son et al. 2003; Wigham et al. 2003a,b). In the PorcupineAbyssal Plain, variations with time of the concentrationof phytopigments indicate that there is an importantinter-annual variability in the availability of food on theseabed. During the Amperima Event, a six-fold decreasein the pigment concentration was observed between 1996and 1997 (Witbaard et al. 2000, 2001). Although moredetailed biogeochemical studies are necessary to providefurther evidence, these variations in food supply to theabyssal benthic community may have important conse-quences in the feeding and life-history strategies ofindividual species, resulting in long-term communitychanges such as the Amperima Event (Billett et al. 2001;Ginger et al. 2001; Wigham et al. 2003a,b).

Apart from variability in the supply of quantity andquality of organic matter (OM), deposit feeders may alsobe affected by competition for OM on the seabed. If onespecies increases in abundance by three orders of mag-nitude, as in the Amperima Event, then competition forresources will be intense, particularly in a food-limitedenvironment. Time-lapse photography showed that therate at which organic matter was reprocessed at thesediment surface was greatly different before and afterthe Amperima Event (Bett et al. 2001). Whereas it tookover 2.5 years for the megafauna to rework the sedimentsurface before 1996, after the onset of the communitychanges this was reduced to less than 6 weeks. Prior to1996, phytodetritus gathered as a layer on the seabed(Thiel et al. 1990; Rice 1995), but after 1996 no phy-todetritus was seen. This was thought to be the result ofenhanced megafaunal activity (Bett et al. 2001). Vari-ability in phytodetritus deposition has been shown toaffect reproductive patterns of some deep-sea mega-fauna, mainly echinoderms (Tyler and Gage 1980, 1984;Tyler and Pain 1982; Tyler et al. 1982a, 1982b, 1984,1990, 1993, 1994; Campos-Creasey et al. 1994; Ramirez-Llodra et al. 2002; Wigham et al. 2003a,b). If recycling

of organic matter on the seabed was changed so radi-cally during the Amperima Event, it is possible that life-history characteristics of deep-sea deposit feeders, suchas growth and reproductive processes, would be im-pacted significantly. This article uses Oneirophantamutabilis as a test case.

O. mutabilis is a cosmopolitan abyssal holothurianbelonging to the family Deimatidae (Hansen 1975). It iscommon on the Porcupine Abyssal Plain and prior tothe Amperima Event it was one of the dominant me-gafaunal species (Billett et al. 2001). The basic repro-ductive patterns of O. mutabilis from the western IndianOcean, the Kermadec Trench, the Panama Basin, andthe Porcupine Abyssal Plain were described by Hansen(1968, 1975) and Tyler and Billett (1987). In females, themaximum oocyte size reported was 950 lm, suggestinglecithotrophic or direct development. Hansen (1968,1975) reported intra-ovarian brooding in specimens ofO. mutabilis affinis from the Panama Basin and sug-gested that there might be reproductive periodicity atthis locality coupled to upwelling events (Hansen 1975).Conversely, Tyler and Billett (1987) did not find intra-ovarian brooding and an analysis of gametogenesissuggested continuous reproduction. Furthermore, whilethe populations of O. mutabilis affinis sampled by the‘Galathea Expedition’ in the Panama Basin containedboth ripe male and female specimens (Hansen 1975), thepopulations of O. mutabilis mutabilis analysed by Tylerand Billett (1987) from the Porcupine Abyssal Plain,sampled between 1973 and 1982, contained no males. Inthese cases about 50% of the population were females,but the sex in the remaining individuals could not bedetermined. No valid explanation has been found todate to account for the lack of males in the PorcupineAbyssal Plain samples and for the differences inbrooding aspects across ocean basins.

Materials and methods

Study area and sampling

The Porcupine Abyssal Plain is situated off the southwestcoast of Ireland in the northeast Atlantic. The study areawas located in the middle of the Porcupine Abyssal Plain(approximately 4,850 m depth). The study site wassampled regularly between 1989 and 2002, within 20nautical miles of the central point (48�50¢N and16�30¢W). This locality became known as the BENGALstation (Billett and Rice 2001; Fig. 1). Sampling wasundertaken with a semi-balloon otter-trawl (OTSB 14)with a wing-end spread of 8.6 m and a net height ofapproximately 1.5 m from the footrope to the headline.The samples were sorted at sea, fixed with 5% borax-buffered formaldehyde in seawater, and subsequentlytransferred to 80% methylated spirit after 3–5 days.

The samples analysed in this study were collectedduring two cruises prior to the Amperima Event

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(September 1989 and May 1991) and four cruises afterthe Amperima Event (July 1997, March 1998, October1998, and October 2002; Table 1).

Processing

Sex ratio

Between 30 and 40 individuals of Oneirophanta mutabiliswere selected at random from each of six cruises cov-ering the period 1989 to 2002. The holothurians wereweighed and their length was measured on the ventralside from the mouth to the anus. The individuals weresexed by direct observation of the gonads. A chi-squaredtest was employed to examine the sex ratio in eachpopulation and between pre- and post-Amperima Eventpopulations.

Gametogenesis

Gametogenesis was investigated from light-histologicalsections. The gonads were dehydrated in graded alcoholsand then the tissues were cleared with xylene andembedded in paraffin wax. Gametogenesis was describedfrom 7-lm sections stained with haematoxylin and eo-sin. The ovaries of ten females were examined persample. At least 100 oocytes that had been sectionedthrough the nucleus were measured (Feret diameter)using an image-analysis package (Sigma Scan Pro 4).The oocyte sizes were grouped into 100-lm classes andoocyte-size-frequency diagrams constructed for eachindividual and for the composite data for each sample.The oocyte-size distributions were compared between

Fig. 1 Bathymetric chart of the Porcupine Abyssal Plain area withthe BENGAL site (black square)

Table 1 Station data for samples used in this study

Station Date Position start Position end Depth (m)

Latitude (N) Longitude (W) Latitude (N) Longitude (W)

R.R.S. ‘‘Discovery’’ cruise 18511908#44 05 September 1989 48�47.30¢ 16�29.90¢ 48�56.80¢ 16�27.60¢ 4,843–4,84911908#51 07 September 1989 48�45.30¢ 16�32.20¢ 48�51.00¢ 16�29.40¢ 4,839–4,85411908#68 12 September 1989 48�46.90¢ 16�24.70¢ 48�42.50¢ 16�39.60¢ 4,853–4,877R.R.S. ‘‘Challenger’’ cruise 7952701#17 18 May 1991 48�51.30¢ 16�30.30¢ 48�47.00¢ 16�43.10¢ 4,842–4,84552701#42 24 May 1991 48�52.70¢ 16�38.50¢ 48�51.20¢ 16�28.50¢ 4,843–4,845R.R.S. ‘‘Discovery’’ cruise 22913200#09 06 July 1997 48�51.96¢ 16�24.61¢ 48�46.21¢ 16�31.63¢ 4,840–4,84413200#27 10 July 1997 48�52.50¢ 16�39.31¢ 48�42.44¢ 16�41.00¢ 4,839–4,84813200#35 11 July 1997 48�44.03¢ 16�32.82¢ 48�55.85¢ 16�40.22¢ 4,842–4,84513200#60 17 July 1997 48�52.11¢ 16�26.66¢ 48�48.34¢ 16�42.01¢ 4,843–4,847R.R.S. ‘‘Discovery’’ cruise 23113368#23 10 March 1998 48�50.70¢ 16�28.34¢ 48�44.84¢ 16�40.44¢ 4,842–4,84413368#24 11 March 1998 48�50.31¢ 16�37.30¢ 48�57.01¢ 16�46.02¢ 4,802–4,84413368#50 17 March 1998 48�49.58¢ 16�27.72¢ 48�48.25¢ 16�15.91¢ 4,840–4,84013368#51 18 March 1998 48�49.71¢ 16�28.42¢ 48�48.88¢ 16�20.61¢ 4,840–4,84013368#01 22 March 1998 48�55.79¢ 15�44.66¢ 48�52.33¢ 15�38.85¢ 4,826–4,84113368#02 23 March 1998 48�54.37¢ 15�39.93¢ 48�50.72¢ 15�32.86¢ 4,828–4,837R.R.S. ‘‘Discovery’’ cruise 23713627#10 30 September 1998 48�53.06¢ 16�42.06¢ 49�02.00¢ 16�53.03¢ 4,835–4,83713627#23 05 October 1998 48�58.09¢ 16�45.02¢ 49�03.09¢ 16�40.07 4,814–4,837R.R.S. ‘‘Discovery’’ cruise 26615054#6 03 October 2002 48�51.85¢ 16�40.91¢ 48�48.71¢ 16�52.80¢ 4,843–4,84415054#22 09 October 2002 48�53.72¢ 16�54.13¢ 48�58.42¢ 17�02.02 4,842–4,84515054#24 11 October 2002 48�01.89¢ 16�53.41¢ 49�09.80¢ 16�58.50 4,843–4,84915054#25 12 October 2002 48�54.24¢ 16�29.52¢ 48�55.20¢ 16�39.25¢ 4,844–4,84515055#2 13 October 2002 49�29.34¢ 16�52.32¢ 49�29.51¢ 16�58.66 4,783–4,822

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samples using the G-test of independence. Analysis ofvariance (ANOVA) was used to examine variations inthe mean percentage of previtellogenic oocytes (100–200 lm) and vitellogenic oocytes nearing maturation(500–700 lm) amongst samples. Three ‘non-female’ go-nads were sectioned per sample to identify potentialsigns of spermatogenesis.

Fecundity

Ten females were selected randomly from each cruise.Their gonads were dissected and wet-weighed to a pre-cision of 0.001 g, allowing time for significant evapora-tion to cease. Three tubules were selected andindividually weighed to 0.001 g. The tubules wereopened, showing the oocytes to the naked eye. Thenumber of oocytes within the three tubules, the weight ofthe tubules, and the weight of the gonads were then usedto calculate the potential fecundity of the individual.ANOVAs were used to examine the difference infecundity between cruises and periods (pre-1995 andpost-1995).

Gonad index

The body mass of O. mutabilis varied considerablydepending on the amount of sediment within the stom-ach. Therefore the gut was removed before the wetweight of the specimen was determined. The regressionof body weight (gut-free) to length was calculated from55 individuals. The relationship between gut-free bodyweight and length was found to be significant (r2=0.727,P<0.001). The following formula was used to estimategut-free weight (W) where L was the length of an indi-vidual:

W ¼ 0:352L� 10:8

Once gut-free weight was estimated, the gonad indices(GI) were calculated as

GI ¼ Gonad mass gð ÞEstimated female mass gð Þ � 100

The mean GI were calculated for each cruise and com-pared using an ANOVA.

Results

Sex ratio

Two types of gonad were identified in Oneirophantamutabilis. Ovaries were easily recognised by macroscopicobservation. Developing oocytes were seen clearlythrough the ovary wall. The ovaries had an opaque basefrom which a number of tubules developed distally.These tubules had thin transparent walls and the oocytescould be seen lying free in the lumen (Fig. 2A,B). Dif-

ferent sizes of oocytes were seen though the ovary walls.The largest oocytes were dark orange in colour. A sec-ond type of gonad was present in all populations ofO. mutabilis from the Porcupine Abyssal Plain. Thesegonads were composed of empty, translucent tubules.There was no evidence of spermatogenesis or oogenesis,as seen macroscopically and microscopically. Thehistological sections of these tubules showed the gonadwall and germinal epithelium but no associated devel-oping germinal cells, and no gametes were observed inthe lumen (Fig. 2C).

A total of 230 specimens of O. mutabilis were sexedfrom six samples. Of these, 96 were female while theother 134 could not be classed as female or male.Females ranged from 54 to 130 mm in length, andindividuals that could not be sexed (identified as ‘no-gender’ hereafter) ranged from 48 to 120 mm inlength. The ratio of no-gender:females differed signifi-cantly from the 1:1 expected ratio between males andfemales (v2=6.278, df=1, P<0.05), with approxi-mately 1.4 no-gender individuals per female. This ratiodid not differ significantly between pre- and post-Amperima Event samples (v2=1.208, df=1, P>0.05).The smallest individual dissected with a developedovary was 41 mm in length, suggesting that size at firstmaturity in females of O. mutabilis is around 40 mmin length.

Long-term patterns of gametogenesis and oocyte-sizedistribution

The ovaries of O. mutabilis contained oocytes in allstages of development at any single time, suggestingcontinuous production of eggs throughout the year. Inall samples, the ovaries of some individuals containedonly a small number of oocytes, mainly previtellogenic,suggesting perhaps a recent (individual) spawning event.

The oogenetic patterns observed under light micros-copy in specimens of O. mutabilis from the PorcupineAbyssal Plain collected between 1989 and 2002 weresimilar to the patterns described by Tyler and Billett(1987) from samples collected between 1973 and 1982.The oogonia developed from the germinal epitheliuminto primary oocytes. These primary oocytes werebasophilic and anchored to the germinal epithelium by alayer of follicle cells (Fig. 2A). The pre-vitellogenicoocytes reached 200 lm diameter before undergoingvitellogenesis. Vitellogenetic oocytes were acidophilic,staining pale pink with eosin, and exhibited yolk gran-ules in the cytoplasm (Fig. 2B). The maximum oocytesize for the specimens analysed from the BENGAL sitewas 625 lm.

The individual oocyte-size distributions showed noevidence of synchrony in gamete development in any ofthe samples. In general, there was a high proportion ofprevitellogenic (100–200 lm) and medium-sized vitello-genic oocytes (400–500 lm), and a smaller proportion oflarge vitellogenic oocytes (>600 lm). There was some

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variation between the oocyte-size distributions amongstindividuals within each sample, indicating a lack ofsynchrony in oocyte production within the population.

The composite oocyte-size distributions for eachsample did not show evidence of seasonality, suggestinga continuous production of oocytes (Fig. 3). Whenanalysing the composite data for each sample, therewere significant differences in the distributions ofoocyte sizes amongst samples (G-test, G=46.308,df=25, P<0.01). The samples collected prior to 1996exhibited a relatively constant proportion of oocytes inthe size classes between 200 lm (pre-vitellogenic) and500 lm (vitellogenic), which accounted for 75–85% ofall oocytes. After 1996, the oocyte-size distributions ofsamples collected in July 1997 and March and October1998 were skewed towards previtellogenic oocytes, witha significantly higher proportion of oocytes in the 200-lm size class (40–60%) and a decrease in the propor-tion of developing vitellogenic oocytes (300–500 lm).In the sample from October 2002, however, the patternwas reversed and oocyte sizes were similar to thoseobserved before 1996. A relatively constant proportionof oocytes was seen in all size classes from 200 to600 lm (Fig. 3).

To investigate further the differences found in theoocyte-size distribution between years, the percentageof previtellogenic oocytes (<200 lm) and large vitell-ogenic oocytes nearing maturation (500–700 lm) wereplotted (Fig. 4). In September 1989 and May 1991, thepercentages of previtellogenic and vitellogenic oocyteswere similar. The mean percentage of previtellogenicoocytes was significantly greater after 1996, reaching amaximum (51%) in the March 1998 sample (ANOVA,F=4.113, df=5, P<0.005). The percentage of pre-vitellogenic oocytes from March 1998 was significantlyhigher than the percentage of these oocytes in thesamples from September 1989 and October 2002(Tukey’s HSD multiple comparisons, P<0.05). Whenthe samples were compared between pre-AmperimaEvent and post-Amperima Event, the percentage ofprevitellogenic oocytes was significantly lower in thesamples prior to 1996 than in the post-1996 samples(t-test, t=�2.201, df=55, P<0.05), but the meanpercentage of large vitellogenic oocytes nearing ma-turation did not show significant differences betweensamples (ANOVA, F=1.881, df=5, P>0.05). How-ever, the October 2002 sample shows a reverse in thetrend observed in the time series. In 2002, the oocyte-size distribution exhibited a decrease in the percentageof previtellogenic oocytes (25%) and an increase in thepercentage of vitellogenic oocytes (41%) in relation tothe specimens analysed in July 1997, March 1998, andOctober 1998.

Fig. 2A–C Light-histology sections of gonads of Oneirophantamutabilis. A Ovary of a young female showing proliferation ofoogonia (oo) and previtellogenic oocytes (pvo) surrounded byfollicle cells (fc); gw gonad wall. B Ovary of mature female showinglarge vitellogenic oocytes (vo) and previtellogenic oocytes (pvo).C Section of empty gonad from ‘no-gender’ specimen; gw gonadwall, lu gonad lumen

b

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Ovary index

The mean ovary index ranged between 4.7 and 8.2(Table 2). There were significant differences in the meanovary index between samples (ANOVA, F=3.675, df=5,P<0.05). The variation was caused by the 2002 popu-lation, which exhibited a significantly higher mean ovaryindex than the July 1997, March 1998, and October 1998populations (Tukey’s multiple comparisons, P<0.05;Fig. 5). There were no significant differences in the meanovary index between samples collected before and afterthe Amperima Event (t-test, t=�0.011, df=58, P>0.05).

Fecundity

O. mutabilis has a low fecundity, ranging from a fewhundred to under 2,000 eggs per female. There were

significant differences in the mean fecundity of thepopulations sampled in different years (ANOVA,F=12.992, df=5, P<0.001; Table 2, Fig. 6). Post-hocanalysis revealed that the fecundity of the specimensfrom September 1989 and May 1991 was significantlydifferent from other sampling periods (Tukey’s multiplecomparisons, P<0.05). There were no significant dif-ferences in the mean fecundity of the two populationssampled before the Amperima Event (t-test, t=�0.059,df=18, P>0.05). Similarly, there were no significantdifferences in the mean fecundity between the fourpopulations sampled after the Amperima Event (ANO-VA, F=2.821, df=3, P>0.05), although the data indi-cated a lower fecundity in the two populations sampledin 1998 (March and October; Fig. 6). When comparingpre- and post-Amperima Event samples, the meanfecundity of O. mutabilis was significantly different,

Pre "Amperima Event" samples

September 1989

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Oocyte diameter (µm)

Oocyte diameter (µm)

Fig. 3 Oocyte-size distributionof O. mutabilis from thePorcupine Abyssal Plain.Composite data in each sample.Error bars: standard deviation

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decreasing from 1,568±226 oocytes per female before1996 to 641±130 oocytes per female after 1996 (t-test,t=7.466, df=58, P<0.001).

Discussion

Reproductive biology of Oneirophanta mutabilis

One of the most striking and constant observations instudies of Oneirophanta mutabilis from the PorcupineAbyssal Plain has been the lack of mature males in anysample collected to date (Tyler and Billett 1987; thisstudy). Only mature females and individuals of ‘nogender’ have been found. The sex ratio of no-genderindividuals to females was about 1.4. There were nosignificant differences in the sex ratio of the populationssampled before and after the Amperima Event. Theabsence of mature males in O. mutabilis and the lowerproportion of females to no-gender individuals contrastwith other deep-sea holothurians. In general, deep-seaholothurians exhibit a male:female sex ratio of 1:1 andmales have mature sperm in the testes throughout theyear. The constant production of sperm increases thepotential for fertilisation success in chance encounterswith mature females in habitats characterised by lowfaunal abundance (Billett and Hansen 1982; Tyler et al.

1985a, 1985b, 1992; Tyler and Billett 1987; Young et al.1992; Wigham et al. 2003a).

Tyler and Billett (1987) suggested several hypothesesthat might explain the lack of mature males in O. mut-abilis, but none of the suggestions have been supportedby samples taken in recent years. Spawning on capturecan be ruled out, because some spermatozoa are almostalways evident, even in spawned-out testes. The possi-bility of O. mutabilis being a sequential hermaphrodite isnot supported either, as males should have been foundat least in some of the samples. No evidence of season-ality was found in the reproductive patterns of femalesbetween 1973 and 1982 (Tyler and Billett 1987). Thiswas confirmed by the present study (1989–2002). In thecase of males, Tyler and Billett (1987) suggested thatperiodic reproduction might occur on a time scalegreater than an annual cycle and that this might explainthe lack of mature males. The samples analysed in thisstudy extended over a period of 13 years and, althoughthe time series was imperfect, no males were found.

% p

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Fig. 4 Mean percentages (±SE) of previtellogenic oocytes(<200 lm; triangles) and vitellogenic oocytes nearing maturation(500–700 lm; circles) of O. mutabilis from the Porcupine AbyssalPlain

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Fig. 6 Mean fecundity (number of oocytes per female; ± SD) ofO. mutabilis from the Porcupine Abyssal Plain

Table 2 Mean ovary index (± standard deviation) and fecundity(± standard deviation) of Oneirophanta mutabilis from the Por-cupine Abyssal Plain

Date Ovary index ± SD Fecundity ± SD

September 1989 6.1±3.3 1,561.1±613.5May 1991 5.4±1.0 1,575±429.2July 1997 5.0±1.6 818.1±461.3March 1998 4.7±2.1 513.6±435.9October 1998 5.0±1.4 414.3±395.9October 2002 8.2±2.7 819.2±241.6

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Nevertheless, juvenile O. mutabilis, 20–30 mm long,were collected frequently (Billett et al. 2001), suggestingthat individuals were recruited regularly to the popula-tion. The apparent lack of mature males through long-term periodicity in maturation, therefore, would appearto be unlikely.

Asexual reproduction by parthenogenesis could ex-plain the lack of males in the populations of O. muta-bilis. Parthenogenesis is a mode of reproduction inwhich zygotic development of eggs is not induced byfertilisation from another individual. Parthenogenesiscan be meiotic, with genetic crossing over during mei-osis in an unfertilised ovum, or ameiotic, with clonalproduction of offspring (Bell 1982). A number ofmarine invertebrates exhibit parthenogenetic reproduc-tion, but it is rare in echinoderms (Mladenov 1996). Inthis phylum evidence for parthenogenesis has beenfound only in the ophiuroid Ophiomyxa brevisima(Garrett et al. 1997). The lack of male specimens inOneirophanta mutabilis could be indicative of parthe-nogenesis, as suggested for three species of Antarcticophiuroids (Mortensen 1936) and the coral-reef aster-oid Ophidiaster granifer (Yamaguchi and Lucas 1984).However, the presence of gravid O. mutabilis males inthe Panama Basin (Hansen 1975) calls this interpreta-tion into question and molecular studies on females andtheir offspring would be necessary to confirm thishypothesis.

The gametogenetic patterns of female O. mutabiliscollected from the Porcupine Abyssal Plain during theAmperima Event are similar to those of individualsanalysed by Tyler and Billett (1987) between 1973 and1982. The maximum size of vitellogenic oocytes of O.mutabilis collected between 1989 and 2002 was650 lm, contrasting with a maximum of 950 lm col-lected prior to 1982 (Tyler and Billett 1987). This sizedisparity probably reflects differences in the method-ologies used to measure oocytes. Oocytes from histo-logical sections used by Tyler and Billett (1987) werere-measured as part of this study with better imageanalysis techniques now available. No significant dif-ferences were found in the mean maximum oocyte sizeof O. mutabilis in the sampling periods 1973 to 1982and 1989 to 2002.

The overall distribution of oocyte sizes did not showevidence of seasonal synchrony in the samples studiedbetween 1989 and 2002, reinforcing the results obtainedby Tyler and Billett (1987). Most specimens exhibited ahigh number of previtellogenic (<200 lm) and devel-oping vitellogenic oocytes (200–500 lm) that accountedfor 75–80% of the oocytes, and a smaller percentage (3–8%) of large vitellogenic oocytes nearing maturation(>600 lm). This distribution suggests that the femalesof O. mutabilis produce eggs continuously throughoutthe year, undergoing periodic, asynchronous spawningevents. This is supported by the observation in allsamples of some individuals with ovaries that containedmainly pre-vitellogenic oocytes, possibly indicating arecent spawning event.

Long-term change in the fecundity of O. mutabilis

The Porcupine Abyssal Plain benthos is subjected to astrong seasonal pulse of phytodetritus. Most of the or-ganic matter deposition occurs in mid-summer and thereis significant seasonal and inter-annual variability inboth the quantity and the quality of the organic matterflux (Lampitt et al. 2000, 2001; Kiriakoulakis et al.2001). It has been suggested that the long-term persistentchanges in the benthic community of the PorcupineAbyssal Plain and, in particular, the rapid increase in theabundance of the holothurians Amperima rosea andEllipinion molle (Billett et al. 2001) might be related tointer-annual variability in the quality of organic mattersupply (Billett and Rice 2001; Billett et al. 2001; Ikenet al. 2001; Wigham et al. 2003a, 2003b).

Changes in both abundances and population size-structures were observed in many of the major megafa-unal species on the Porcupine Abyssal Plain between1989 and 2002. The increase in the abundance ofA. rosea was associated with a significant decrease in itsbody size. Before the Amperima Event in 1996 there werefour dominant holothurians; Oneirophanta mutabilis,Psychropotes longicauda, Pseudostichopus villosus, andPeniagone diaphana. During the Amperima Event,P. diaphana almost disappeared, O. mutabilis andPsychropotes longicauda remained at similar abun-dances, but decreased in mean body size, while Pseu-dostichopus villosus appeared to be unaffected (Billettet al. 2001). Changes in body size were particularlyevident in O. mutabilis. Prior to 1996, the populationwas dominated by specimens of approximately 100 mmbody length. Post-1996 the populations showed a sig-nificant increase of individuals in small ( £ 50 mm) andintermediate (60–80 mm) size classes (Billett et al. 2001;Wigham et al. 2003a,b).

Within the lifespan of an organism, its life-historystrategy integrates the demands of competing functions,such as growth and reproduction, resulting in the opti-misation of fitness for a specific environment (Stearns1992; Giangrande et al. 1994; Olive et al. 1997, 2000;Ramirez-Llodra 2002). Individuals must maintain aminimum allocation of energy to locomotion and sur-vival to ensure their feeding potential. However, energyallocation to growth and reproduction may be highlyvariable. To respond to changing environmental factors,many life-history variables are highly polytypic, havingthe capacity to display different functional abilities inresponse to different environmental situations (Hadfieldand Strathmann 1996). Oocyte development and fecun-dity are of the most flexible of these variables.

The oocyte-size distributions of O. mutabilis popula-tions collected before and after the Amperima Eventwere analysed to investigate potential long-term varia-tions in the gametogenetic cycles induced by changes inenvironmental factors. There was an increase in theproportion of previtellogenic oocytes post-1996, to-gether with a slight decrease in the number of vitello-genic oocytes nearing maturation. These data suggest

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that, during the megafaunal community changes at theonset of the Amperima Event, the females of O. mutabilisallocated less energy to reproduction, constraining thenumber of oocytes undergoing vitellogenesis andreaching maturity. This, ultimately, resulted in the sig-nificantly lower fecundity observed in the populations ofO. mutabilis post-1996. The changes in the oocyteproduction exhibited by O. mutabilis after 1996 werereversed in October 2002. This population had anoocyte-size distribution similar to that of the pre-Amperima Event populations, characterised by relativelyconstant proportions of previtellogenic and developingvitellogenic oocytes and, in this case, a high proportion(around 40%) of vitellogenic oocytes nearing matura-tion. The decrease in both the body size and the fecun-dity of O. mutabilis during the Amperima Event suggestsa limitation in the allocation of energy to both growthand reproduction.

Fine-scale selectivity among deposit-feeding holothu-rians could allow for the partitioning of phytodetritalfood sources and the selective exploitation of specificnutrients deposited on the seabed (Ginger et al. 2001;Witbaard et al. 2001; Wigham et al. 2003a,b). In Porcu-pine Abyssal Plain megafaunal communities Amperimarosea appears to be highly selective for fresh, potentiallychlorophyll-a-richmaterial (Iken et al. 2001) and is able tometabolise phytosterols that are not utilised by otherholothurians (Ginger et al. 2000, 2001). This, togetherwith photographic evidence that indicates A. rosea con-tributes to the removal of large amounts of newlydeposited phytodetritus as a direct result of its highabundance andmobility (Bett et al. 2001), suggests thatA.rosea and other megafauna (e.g. the ophiuroid Ophioctenhastatum) consume most of the fresh material arriving atthe seabed (Bett et al. 2001;Gage et al. 2004), forcing otherabundant fauna, such asO.mutabilis, to subsistmainly ondegraded products (Wigham et al. 2003a,b).

Carotenoid pigments, such as zeaxanthin, echine-none, and b-carotene, appear to play a central role in thereproductive success of echinoderms (Tsushima et al.1997; Bandaranayake and Des Rocher 1999; Plank et al.2002; Hudson et al. 2003; Wigham et al. 2003a,b). It hasbeen proposed that changes in the composition of phy-todetritus deposited on the seabed, and hence theavailability of carotenoids, might affect the reproductiveprocesses of benthic species (Hudson et al. 2003) andthat long-term changes in the composition of phytode-tritus may have driven the sudden increase in theabundance of the opportunistic holothurian A. rosea(Billett et al. 2001; Wigham et al. 2003a, 2003b).

To investigate this hypothesis further, Wigham et al.(2003b) analysed the pigments in the guts and gonads offive holothurian species from the Porcupine AbyssalPlain. Their data showed that the ovaries of all thespecies contained the same major pigments: zeaxanthin,b-carotene, echinenone, and an unidentified pigment.A. rosea and O. mutabilis exhibited high concentrationsof zeaxanthin and b-carotene. In addition, A. rosea alsohad high levels of echinenone, a carotenoid that appears

to promote successful early development in shallow-water echinoids (Tsushima et al. 1997). Wigham et al.(2003a,b) suggested that by selective feeding on freshphytodetritus, species like A. rosea can accumulate spe-cific pigments providing them with a reproductiveadvantage. The corollary to this is that the utilisation ofcritical compounds by superabundant species, such asAmperima, may reduce their availability to other species.

If deep-sea holothurians are unable to synthesisecertain critical large organic molecules de novo (Gingeret al. 2000, 2001) it is likely that there is competition forcomplex organic compounds vital for growth andreproduction, particularly in the food-limited deep sea.While it cannot be discounted that changes in the flux oforganic matter to the deep-sea bed might have led to areduction in the fecundity of O. mutabilis, it is possiblethat the superabundance of A. rosea led to a reduction incritical compounds needed for reproduction, in turnreducing the fecundity of O. mutabilis. Recently, Ruhland Smith (2004) have reported long-term megafaunalcommunity changes at 4,100 m in Station M in thenortheast Pacific, similar to those on the PorcupineAbyssal Plain. These authors suggest a correlation be-tween faunal changes and climate fluctuations duringmajor El Nino/La Nina events linked to variations in thefood supply to the abyssal seabed. While variations inthe quantity, quality, and timing of organic mattersupply might be responsible for some of the faunalchanges in the northeast Atlantic and in the northeastPacific, we believe that biotic interactions and competi-tion for resources might also be responsible for ecosys-tem change on the abyssal seafloor.

Acknowledgements The authors would like to thank the partners ofthe BENGAL programme as well as the officers and crew of R.R.S.‘‘Discovery’’ and R.R.S. ‘‘Challenger’’ for assistance at sea. Thecomments and suggestions of two anonymous reviewers improvedthe manuscript considerably. The samples were collected duringBENGAL cruises, partly funded by EC contract MAS-3 950018.The studies on which this article is based complied with the currentlaws of the United Kingdom, where the studies were performed.

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