Post larval development in deep sea echinoderms

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UNIVERSITY OF

SOUTHAMPTON

"Post-larval

development

in

deep-sea

_echinoderms"

Paulo Yukio Gomes Sumida

Doctor of

Philosophy

SCHOOL OF OCEAN AND EARTH SCIENCE

DECLARATION

UNIVERSITYOF _SOUTHAMPTON

ABSTRACT

FACULTYOF SCIENCE

SCHOOL OF OCEAN_{AND EARTH SCIENCE}

Doctor of

Philosophy

POST-LARVAL DEVELOPMENTIN DEEP-SEAECHINODERMS

Paulo Yukio Gomes Sumida

The _{post-larval phase is}

an essential period in the life _history of marine _{invertebrates;} vulnerable to _high

mortality, it

ultimately

_{influences the distribution and}

abundance of adult _populations. The

post-metamorphic ontogenesis of _{thirty species} of _{deep-sea echinoderms,}

belonging

_{to three}

classes

(Ophiuroidea, Asteroidea and _Echinoidea), is described _{using scanning electron}

microscopy.

The life

historyof_{Ophiocten gracilisis also examined}

asacase_studyfor futureresearchon_{post-larvalorganisms.}

The_analysisof

development

in_ophiuroidsreveals that_speciescanbeidentifiedfroma_veryearly

post-metamorphicstage, even in_{congeneric species, contraryto}the _{findingsof other authors. The}

ontogenyof

homologous

structures _{is similar within related groups, but may}

give rise to different adultstructures in differenttaxa. The mouth_papillaewithin the ophiurids are _{serially homologous,}

originating

_{from the}

jaw,

but the fourth mouth _{papillamay have} adifferent_{origin. In the families}

Ophiactidae, Ophiacanthidae and

Amphilepididae

examined, the mouth papillae have different _{origins, as,} for _{instance, the adoral shield}

spine ortentacle scale. Dataonthe_{post-larval development}of_{Ophiura affinissuggest that this}

species is

morecloselyrelatedto_{the genus Ophiocten}andachangein the_genericstatus is_proposed.

Ophiocten gracilis is a bathyal brittle star _occurring on both sides of the North Atlantic and its life

history is studied in the eastern side of the North Atlantic. In this _area, O. _gracilis

spawns in

February/Marchof each_yearproducinga_{largenumber of eggs. Fecundityis estimated}

tobe around40,000

eggs

ind"1,

with thepopulationof the Hebridean_{Slope being}ableto_{produceprobably}

upto _{16 million eggs}

m"2.

Post-larvae start_settling in Mayand numbers settlingreachedover_{3,200 post-larvae}m"2. The _settling

speedof_post-larvae in thewatercolumn isestimatedto bearound 500 m

day"1,

_settlingfaster inwarmer

thancolderwater. _{Settling speeds appear}to be similar for_{post-larvae ranging from 0.6 to 0.9}

mm in disk

diameter. Size at settlement is around 0.6 mm in disk diameter and 5-6 arm _{segments. The settlement of}

post-larvalO. _gracilisonthe bottom of the Hebridean_Slopealso_representedaconsiderable fraction of the

particulate organiccarbon_(POC)flux in the_{area,reaching}over7% of the total dailyflux. Thisis likelyto

have a considerable

impact

in the benthic _community as competition and _predation and as an additional

food sourcefor demersal and benthic_organisms. The occurrenceof_post-larvaeof O. _gracilis in sediment

traps also_represented a_{largeproblem for POC flux measurements, with}

ophiuroidsconsumingpart of the flux. In futureworkswith sedimenttraps, such errors mustbetaken into accountand ophiuroids mustbe included in thetotalPOC flux.

The_{deep-seajuvenileasteroids of theNEAtlantic could be}

distinguishedto _species level from a_very

earlystageof_development. The _{ontogenesisof Porcellanaster ceruleus shows that this}

species is _likelyto

undergo

a shift in habitat and diet _duringthe_{juvenile phase.} This is evidenced _{bythe appearance of the}

epiproctal cone, the

changing

of the furrow and _{apical spines,} the _early

development

_{of the cribriform} organadjacenttothe_madreporiteand the_{appearanceof sediment in the stomach. P. ceruleus is}

probablya

predator on meiofauna and small macrofaunal organisms

during

the _{early stages} of _life,

changing

to a

burrowed life _style

ingesting

sediment_particles.Most_juvenileseastars _{analysed duringthe presentstudy} showed wider_bathymetricdistributionthan their adult_{counterparts,suggestingthatevents}

occurringduring

the_earlystages of lifeare importantfor the maintenance of the local _populationstructureand_diversityin the_deepNE Atlantic.

The _{post-metamorphic development of three}

deep-sea spatangoid echinoids is _very similar, but the

morphology and formation of fascioles facilitate the distinction of the species examined. Whereas in Hemiaster _expergitus and_Spatangus raschi the fascioles _present in the post-larvae

develop

to form the adult _fascioles, in _{Brissopsis lyrifera post-larvae there is}

a juvenile fasciole, which _{disappears during}

ontogenesis giving way to the adult fascioles. The function ofthe _{juvenile fasciole is unknown in B.}

lyrifera. The_developmentofthe_periproctin all_{spatangoidsexamined is similartothatdescribed}

byother

authors, with the _{periproct being initially endocyclic and}

migrating

towards the rear ofthe animal as

development progresses. Post-larvae ofthe _{genus Echinus could not} be _separated into different _species, which may be linkedtotherecentdiversificationof_{the genus in}theNorth Atlantic.

The_widespreadsettlementofechinoderm _{post-larvae reported}inthe_{present thesis}andin other works is

thought to have been _{very important} forthe colonization of the _{deep-sea through} the_supply of_stages to

Contents

Chapter One-General_introduction

and aims

ChapterOne

I 1.1 Thedeep-sea

r 1

1.1.1 The_physicalenvironment

2 1.1.1.1 _Hydrothermalventsandcold_{methane/sulphide}

seeps 3

1.2 _{The North-east Atlantic}

3 1.2.1 Historic

background

3

Figure 1.1._{Mapof the cruise of'the HMS}

Lightning 4

Figure1.2._Mapof the cruise of the HM_{Surveying-vessel Porcupine 6} 1.2.2

Physiography

_{and sediments}

8

Figure1.3._Mapofthe NE Atlantic ₉

1.2.3 Watermassesandcirculation

10

Figure1.4. _{Surface and bottom circulation in theNEAtlantic}

12 1.2.4 _{Primary productivity}and_{inputoforganicmatter tothe sediments}

13 1.2.5 Benthic_{community composition}

14 1.3 _{Reproductionanddevelopmentin}

deep-seainvertebrates 16

Table1.1.Modes ofdevelopmentin_{deep-seaspecies}

18 1.3.1 _Hydrothermalventsand cold_seeps

21 1.3.2 Post-larval_{developmentindeep-seainvertebrates}

23

Figure1.5._Complexlife_cycleofanophiuroid 24

1.3.3 _Approachesusedto_infermodes_{ofdevelopment}

24 1.5 Aims of the presentwork

26

Chapter Two-Material

and methods

ChapterTwo

27 2.1 _Samplingmaterial

27

Figure2.1._MapoftheNE Atlantic_showingthe_{sampling points 27} 2.1.1 _{Ophiuroidpost-larvae}

28

Table 2.1. List of stations of BIOFAR ₂₈

Table2.2.List of stations of SAMS ₂₉

2.1.2 Sedimenttrapophiuroidpost-larvae 30

2.1.3 Adult_{Ophioctengracilis :}

30 Table 2.3. List of stations oftheadultOphioctengracilis 31 2.1.4 Asteroidea_juveniles

2.1.5 Echinoideajuveniles

33 Table2.5.List ofstationsofjuvenileechinoids ₃₃ 2.2 _Studyof the_{post-larvaldevelopmentinechinoderms}

35 2.3 _{Reproductive biologyofOphiocten}

gracilis 37

2.4 _Settlingrates_experiment

38 2.5 Estimation of carbon demands of _{Ophiocten gracilis growing in}

deep-sea

sediment_traps

38 2.6 _{Stomach contents}

analysisof_{post-larval Ophiocten gracilis}

40

Chapter Three-Post-larval

developmentin shallow and deep-seaophiuroids

(ECHINODERMATA:OPHIUROIDEA)OF THENE ATLANTIC OCEAN

ChapterThree

41 3.1 Introduction

41

Figure 3.1. Post-larval _development of_{Ophiactis asperula described by Ludwig}

(1899) ₄₂

3.2 Post-larval_development

44

Figure3.2. Mainstructuresfoundinthe_{early ophiuroid post-larvae 45}

Figure3.3._{Ophiacantha abyssicolapost-larval}

development

46

Figure3.4. _Ophiacanthabidentata_post-larval

development

₄₈

Figure 3.5. Some _stages of the _{post-metamorphic}

development

_of

Ophiomyces

grandis ₅₀

Figure3.6._Ophiurasarsi_post-larval

development

52

Figure3.7._Ophiuracornea_post-larval

development

56

Figure3.8. Post-larval

development

of_{Ophiura ljungmani 58}

Figure3.9._Earlystagesof the_post-larval

development

of_Ophiuraalbida 60

Figure3.10. Two_stagesof the_post-larval

development

of_Ophiurascomba 62

Figure3.11.Post-larval_developmentof_{Ophioctenaffinis}comb,nov 64

Figure3.12.

Post-metamorphic

_developmentof_{Ophioctengracilis 66}

Figure3.13.

Post-metamorphic

_{developmentof}

Amphilepisingolfiana 68

Figure3.14. Post-larval_developmentof_{Ophiactisabyssicola 70}

Figure3.15. _Ophiactisballi_post-larval

development

74

Figure3.16._Ophiopholisaculeata_post-larval

development

₇₆ 3.3 Discussion

77 3.3.1 Generalcomments

77 3.3.2 Taxonomicdiscussion

78 3.3.3 The_{systematic positiono/"Ophioctenaffinis}

Table 3.1. _Comparison ofthe main _{adult characters of}

Ophiocten, Ophiura affinis

and_Ophiura

80 Table 3.2. _{Comparison of the main}

post-larval characters of _{Ophiocten gracilis,}

Ophiura affinisand_Ophiurasarsi ₈₂

3.3.4

Phylogenetic

_{considerations}

83 3.3.5 _{Ecologicalconsiderations}

84

Chapter Four-Early

juvenile developmentofdeep-sea asteroidsof theNB Atlantic

Ocean,with notes on the juvenilebathymetric distribution

ChapterFour

86 4.1 Introduction

86 4.2 Juvenile_developmentinseastars

88

Figure4.1._{Morphological}features ofasteroid_{juveniles 89}

Figure4.2._{Bathybiaster vexillifer juveniledevelopment}

90

Figure4.3. Plutonasterbifronsjuvenile

development

94

Figure4.4. Psilaster andromeda andromedajuveniledevelopment 96

Figure4.5._Hyphalasterinermis_{juvenile development 99}

Figure4.6. Porcellanaster ceruleusjuvenile

development

101

Figure4.7._{Benthopecten simplex simplex}

juveniledevelopment 105

Figure4.8. Pectinaster_{filholi juveniledevelopment}

109

Figure4.9. Plinthaster dentatus_{juveniledevelopment}

111

Figure4.10._{Hymenasterpellucidus}

juvenile development 113

Figure4.11. Zoroaster_{fulgens juvenile}

development

115

Figure4.12._Brisingellacoronatajuveniledevelopment 119

Figure4.13. Pedicellariae of_Brisingellacoronata ₁₂₁

4.3 _{OntogeneticchangesintheR/r ratioof}

asteroids ₁₂₂

Figure4.14. Relative_changesin size ofarmand disk radii with_growthin

paxillosidans ₁₂₄

Figure 4.15. Relative _changes in size of arm and disk radii with _growth in

notomyotids and in the goniasterid Plinthaster dentatus and the zoroasterid Zoroaster_fulgens

125 4.4 Juvenile_{bathymetricdistribution in the}

Porcupinearea ₁₂₅

Figure 4.16. General bathymetric distribution of adult_asteroids; of adults collected

during

the IOS_Programme;and of_juvenilesin the_{Porcupinearea}

.... 127

4.5 Discussion

128 4.5.1 Taxonomic discussion

4.5.1.1 _{Family Astropectinidae}

128 4.5.1.2 _{FamilyPorcellanasteridae}

128 4.5.1.3 _{Family Benthopectinidae}

130 4.5.2 _{Phylogeneticconsiderations}

130 4.5.3 Sizeat_{metamorphosis}

131

4.5.4

Changes

intheratioR/r withgrowth ₁₃₂

4.5.5 Juvenile_{bathymetricdistribution}

135

Chapter Five-Post-larval

developmentof somedeep-sea echinoidsof theNB

Atlantic Ocean

ChapterFive

138 5.1 Introduction

138

Figure5.1. Growth_stagesof Brisaster

fragilis

_{depicted byMortensen(1907)}

142 5.2 Echinoid_{post-larvaldevelopment}

143

Figure5.2.

Morphological

_{characteristicsof}

regularand_irregularechinoids 144

Figure5.3. Phormosoma_{placenta juvenile}

development

145

Figure5.4. Echinusjuveniles ₁₄₇

Figure5.5. Hemiaster_{expergitus juveniledevelopment}

149

Figure5.6._Spatangusraschi_juvenile

development

151

Figure5.7. Peristome

development

of

Spatangus

raschi andpedicellariae 154

Figure5.8.Peristome_developmentof_{Brissopsis lyrifera}

156

Figure5.9._{Brissopsis lyrifera juvenile}

development

159

Figure5.10. Pedicellariae of_{Brissopsislyrifera} : ₁₆₁

5.3 Discussion

162 5.3./ Taxonomicdiscussion

162 5.3.1.1 Phormosoma_placenta

162 5.3.1.2 _Spatangoids

162 5.3.2

Development

_ofthe_{apicalsystemandperiproctin}

spatangoids 163

5.3.3 Formation_ofthemouth_andfasciolesin_{spatangoids 164}

5.3.4 The Echinusproblem ₁₆₆

5.3.4.1 _{Ontogenetic changesinthe}

morphology

ofpedicellariaeinEchinus 167

Figure5.11.Pedicellariae_{of the genus Echinus(A-E)}

168 Table5.1.Size ofglobiferousand_{ophicephalouspedicellariaein Echinusjuveniles}

. 170

5.3.4.2 Possiblereasonsforthe_{similarityamong Echinuspost-larvae}

170

Chapter Six-

Reproduction,

dispersal,settlementand carbon demands of the

bathyal ophiuroidophiocten_{gracilis in thene atlantic}

ChapterSix

174 6.1 Introduction

174 6.2 _{Reproductivebiology}

, 176

Table 6.1._{Fecundityand egg size ofspecimensof}

Ophioctengracilis 176

Figure6.1._Changesin the_maturityindex ofthe_gonadsof_{Ophioctengracilis 177} 6.3 Growthof the_{early post-larva}

177

Figure 6.2. Mean _changes in disk diameter of _{post-larval Ophiocten gracilis}

collected in the sedimenttraps 178

6.4 _Settlingrates

179 Table 6.2. ANOVA_testing differences in _settlingtimes of_post-larvae of_Ophiocten

gracilisatdifferent_temperatures

179

Figure 6.3. _Settling rates of _post-larvae of _{Ophiocten gracilis} at different

temperatures ₁₈₀

Table6.3. ANOVA_testingdifferences in _settlingtimes of different size_post-larvae of_{Ophioctengracilis}

180 Table 6.4. Mean _settling rates of_{Ophiocten gracilis} of different sizes at different

temperatures ₁₈₁

Figure6.4. _Settlingrates of_post-larvaeof_{Ophioctengracilis} of different sizes at _2,

5, 10and 15C

182 6.5 Stomach contents

182 Table 6.5. _{Percentageof the collected}

post-larvaeof_{Ophioctengracilispresenting}

a

particularkind of food

184

Figure6.5. _{Percentage of the total number ofOphiocten gracilis}

post-larvae with a

determinate typeoffood withinthestomach ₁₈₅ 6.6 Carbon demandsof_post-larvae

186

Figure6.6. Flux of POC_duringthe_{study period}forthe 1000mtrap 186 Table 6.6. _Percentage of the POC flux ₍₁₀₀₀ m _trap) consumed _{by post-larval}

Ophioctengracilis ₁₈₇

Figure 6.7. Estimates ofthe total amount of carbon consumed _by the _Ophiocten

gracilis population assuming a ratio P/R of 3/7 and assimilation

efficiency

of 80% ₁₈₇

Figure 6.8. Relative _{percentages of flux consumed by}the _post-larvae of_Ophiocten

gracilisbasedonP/R of 3/7 andmean_changesin AFDW 188 6.7 Discussion

188 6.7.1 _{Reproductiveecologyandproduction}

6.7.2

Metamorphosis

_{andsettlement:}

revisiting Ophioctengracilis'non-viable settlement.. 190 6.7.3 Juvenile_ecology

192 6.7.4 _{Significance of the}

growth _{of post-larval Ophiocten gracilis for} sediment _trap

measurements

195 6.7.4.1 Problems with the_{sediment traptechnique}

195 6.7.4.2 Evidence_forgrowthinthe_trap

195

Figure 6.9._{Across-slope depthprofilesshowingtheamountof}

suspended particulate

matter _{(SPM) present} in the Hebridean _Slope area

during

the _study

period ₁₉₇

6.7.4.3 Carbon demands ofpost-larvae and directions _{for measurement problems with}

ophiuroids ₁₉₉

Chapter Seven-General_discussion

ChapterSeven

201 7.1 The_importanceof_{morphological}studiesofpost-larva! echinoderms 202 7.2 Post-larvaeand thecolonizationof the_{deep-sea 203}

References References

Acknowledgements

This work would not have been

possible

without the

help

ofanumber of

people,

to whom I am

deeply

grateful.

I would like to thank Prof. Paul A.

Tyler

for his

constant

supervision,

friendship

_and

enthusiasm,

_{which have}

always taught

us never

to lose that thrill for science. _{Financial supportwas}

provided by

_the

"Coordenadoria

de

Aperfeicoamento

_{de Pessoal de Nivel}

Superior"

(CAPES

-

Ministry

of

Education,

Brazil) through

grant No0900/94-1 to whomI amindebted.

A

large

amountofadditional

supervision

and_supportwere

provided by

_{Prof. John}

Gage

(SAMS),

Dr Richard

Lampitt

(SOC),

Dr David Billett

(SOC),

Dr Gordon Paterson

(BMNH),

DrGordon Hendler

(LA

County

Museum),

_{Miss Ailsa Clarkand}

DrThomas

Brey

(AWI).

It hasbeena

pleasure

andanhonourtoworkwith_youall!

My

thanks to Dr Arne

N0rrevang (Kaldbak

_Marine

Biological Laboratory,

Faroe

Islands),

Prof. John

Gage,

Dr David

Billett,

Dr Richard

Lampitt,

Mr Michael Thurston

(SOC)

and Dr Els Flach

(NIOO/CEMO)

and their

respective

Institutions for

providing

thebenthic

samples

_examined

during

_the

present

study.

Thanks also to Mr Robin

Harvey

(SAMS)

for

help

with

samples;

_{Dr Barbara}

Cressey

(SOC)

for the use of the electron

microscope

facilities at

SOC;

and the

library

staff for their

patience

and

support.

Assistance withart workwas

provided

by

Mrs Kate Davis

(SOC).

Dr

Craig

Young

made

possible

the dream of

knowing

the

deep-sea

in

situ,

whichIwilltreasure forever in_mymemory.

Many

thanks to all _my friends in

Southampton

for

making

so

pleasant

_{my stay} in

England

and in

special

_my Brazilian mates

Alexandre,

_{Ronald and Antonio. Our}

research group,

including

Jon,

Cathy,

Eva

R.,

Eva

G.,

Maria,

Lus andDawn has been fantastic

throughout.

You are a_greatteam!!!

Finally,

all _my loveto _my wife Andreia and_my

family

in

Brazil,

_{for their unconditional support and love}

To my

wife

Andreia andto _myparents,

Parase tero direito de

possuir

_para

sempre, e

precise

_querer

pacientemente

epor muito

tempo

P.Y.G. Sumida "Post-larval_developmentin_deep-seaechinoderms" _ChapterOne

Chapter

One

-

General

introduction

and

aims

1.1. The

deep-sea

The

image

of the

deep-sea

as a

huge

and inaccessible environment is present

ever

since scientists set out to

explore

that _area, and

probably

much earlier. It is

interesting

to note

that,

even

though

the

deep-sea

is

today

still a

mysterious

_and

relatively

poorly

known

environment,

its

exploration

began

_{even before the events}

that marked the

beginning

of the science of

Oceanography

itself. If the

circumnavigation

of the British

ship

H.M.S.

Challenger (1872-76)

_{marks the dawn of}

Oceanography,

some _{years before the cruises of the also British}

ships

Lightning

(1868)

and

Porcupine

(1869-70) (section 1.2.1) proved

beyond

_{doubt that}

organisms

thrived in the

deep-sea.

This was

probably

the first _great event in the

history

of the

biological

exploration

of the

deep-sea.

Other

important

eventsmark the 130_years of this

exploration.

After afirst halfof

the 20th

century

marked

by

the _great

expeditions,

_{which collected abundant material} for a

large inventory

of the

fauna,

the

early

196O's

brought

the invention of the submersible

technology, allowing

in situ

exploration

of the

deep-sea

bed,

as well as

the

possibility

of

experimentation

(Sibuet

et

al,

1990).

The invention of

improved

sampling

gear and the use of fine meshes revealed a

extremely

high

diversity

environment, composed by

a

large

number of small-sized

specimens (Sanders

_et

al,

1965).

The 197O's were marked

by

the

discovery

of the

hydrothermal

vents in the volcanic active locations of the Meso-oceanic

Ridges

(Ballard,

1977),

with an

astonishing

fauna and autochtonous source of

organic

matter driven

by geochemical

energy

(Jannasch

&

Wirsen,

1979).

Later,

similar environments were discovered on

continental

slope

areas and called cold seeps, with

production

being

_fuelled

by

hydrocarbon/methane/sulphide

seeping

from the sediments

(Kennicutt

et

al,

1985).

In the

beginning

of the

1980's,

seasonal

pulses

of

phytodetritus originating

from the

euphotic layers

were detected in

deep-sea

areas of the North Atlantic

(Deuser

&

Ross, 1980;

Deuser et

al, 1981;

Billett et

al, 1983; Deuser,

1986).

Such

pulses

of food are

thought

to drive seasonal _processes in

deep-sea

animals

(Rokop,

1974,

ChapterOne

considereda

tranquil environment,

_withconstant

physical

variables anda

continuous,

low

supply

of food.

Nowadays,

the

deep-sea

_{is considered diverse and}

dynamic,

with a multitude of

differentenvironments and difficultto be considereda

single

unit.

Slope

areaswitha

highly dynamic

and,

sometimes,

unstable sediments

(Jenkins

&

Keene,

1992);

abyssal

areas affected

by

seasonal

pulses

of food

(Rice

et

al, 1986)

and those

food-poor under the

large

oceanic _gyres

(Rowe, 19836);

hydrothermal

_{vents and cold}

seeps, with a

high productivity

and

biomass;

and the

relatively

unknown oceanic trenches form this vast

domain,

characterized

by

the

crushing

_pressuresand

complete

absence of solar

light.

1.1.1. The

Physical

Environment

As

already

discussed,

the

deep-sea

_{environment is far from}

being

constant,

despite

the view ofa 'stable'

environment,

_{where the}

physical

_and

biological

processes are

slow and

unchanged

over

large

time-scales. This is

probably

true for some of the

physical

variables,

e.g.

temperature

and

salinity,

butnot for other events

(see Tyler,

1995).

A series of

unpredictable

events occur in certain areas ofthe ocean

bed,

causing

effects inthe sediment

community.

Benthic storms associatedwith the

global

pattern

in

eddy

kinetic _energy are

highly

erosive events

occurring

atthe bottom

during

few

days

toweeks

(Richardson

et

al, 1993;

Kontar&

Sokov,

1994)

andcan be

important

as a

disturbing

factor in the local benthos

(Aller, 1989,

1997).

Areas such as the

HEBBLE Site

(High

Energy

Benthic

Boundary

Layer

Experiment)

_{on Nova Scotia} Rise

(NW

Atlantic

Ocean)

are

highly

energetic,

opposing sluggish

_{currents found}

elsewhere in the

deep-sea (Weatherly

&

Kelley,

1985;

Gross et

al,

1988).

Other

unpredictable

events include sediment slides and

slumps

occurring

_{on the continental}

slopes

and hadal

trenches,

sometimes

moving

enormous

quantities

of sediment

downslope

either to the continental rise and

abyssal

plain

or to the

deepest

parts

of trenches.

Turbidity

currents _may also occur on

slopes

and submarine _canyons

carrying

amixture of sediments andwater

downslope (Gage

&

Tyler,

1991).

Although

such events occur at variable time-scales and are

unpredictable

over

ChapterOne

periodicity

events, suchasthe

pulses

of

organic

matter

arriving

atthe bottom_maybe detectedatsomeareas

(section 1.1).

1.1.1.1.

Hydrothermal

_{Vents and}

Deep-Sea

Cold

Methane/Sulphide

Seeps

Hydrothermal

vent _systems are

unique

environments associated

commonly

_with tectonic

plate

boundaries in

spreading

_{centres, subduction}

zones, fracture zones and

back-arcbasins

(German

et

at,

1995).

The

temperature

atthese environments canbe as hot as 380C close to black smokers or cooler as warm fluids

(5-250C)

_from

diffuse emissions _{from crevices in the basaltic rocks}

(Gage

&

Tyler, 1991).

Despite

such

high

temperatures

existing

_{at vent}

sites,

the

overlying

seawater

temperature

remains closetothat of the

surrounding deep-ocean

(~ 2C).

At those

sites,

water

percolates

in the

system

where it

acquires

a

variety

of different

minerals,

as metals and

others,

_which

together

_with

hydrogen

sulphide

and

methane are

expelled

in the

surrounding

water column as a

hydrothermal

plume.

Some minerals are

deposited

near the

chimneys

as metalliferous sediments and Fe-Mn crusts and the

hydrogen sulphide

_{and methane}

(highly

toxic for life in

general)

are used as a substrate

(energy

source)

_for

chemosynthetic

bacteria,

which form the basis of the

hydrothermal

vent

trophic

web

(Tunnicliffe,

1991;

_{Van Dover &}

Fry,

1994;

Van

Dover, 1995).

In

deep-sea

_cold

methane/sulphide

seeps,

physical

conditions are more like

non-vent

deep-sea

_areas, with the

exception

_{of the methane and}

sulphide

that seeps from inside the Earth's _crust,

serving

_as

energy source to

chemosynthetic bacteria,

supporting

a faunasimilarto that found in

hydrothermal

vent_systems

(Hecker, 1985;

Gage

&

Tyler, 1991).

1.2. TheNorth-eastAtlantic

1.2.1. Historic

background

The

deep

_{NE Atlantic Ocean is}

probably

one of the best

sampled

deep-sea

_{areas of}

the world's oceans. The first

biological

survey in the area was made

by

the British

ship

H.M.S.

Lightning,

which covered the

region

of the Hebridean

Slope,

Faroe

Bank,

Faroe-Shetland Channel and the northof Feni

Ridge.

The

Lightning

sailed on

uiojj)

opirejiy3N 3XP UT8981 J

Suunp SutuiifSn

sViH3lPJ ssiaioaqjjosuotjboojuopujsaip

Sutavoiis

dßp\[

'x*I

: i

VMS HJ.ilOX

( 01 H a:

1

19

ChapterOne

Thomson,

1874a).

In the

following

_summer, the British KM.

Surveying-vessel

Porcupine

was used for three cruises in a much more

comprehensive sampling

programme. The

sampling

covered mostof the NE Atlantic offthe westand north of

the British Isles. The first cruise

surveyed

the area of the Rockall

Trough,

Rockall

Bank,

Porcupine

Bank and the north _part of the

Porcupine

Seabight (Fig. 1.2a).

During

the second

cruise,

the Celtic

Shelf,

Goban

Spur

and a small section of the

Porcupine Abyssal

Plain were

sampled (Fig. \.2b).

The third cruise

comprised

the

more northern _part,

encompassing

the Hebridean

Slope,

Wyville-Thomson Ridge,

Faroe

Shelf,

Faroe-Shetland Channelandthe Shetlands Shelf

(Fig. 1.2c).

Thosethree cruises

surveyed

a total of 90 stations at

depths

_up to almost 4500 m

(Thomson,

1874a).

The

Porcupine

would be used

again

during

the summer of

1870,

when a fourth

cruise

sampled

9 stations on the south

edge

of the Celtic Shelf and headed southwards to

explore

the west coast of the Iberian Peninsula and the southern Mediterranean Sea

(Fig.

1.2a1;

Thomson, 1874a).

During

the_years

following

these

cruises,

_many

ships

visited the area

including

the

H.M.S.

Knight-Errant (1880),

H.M.S. Triton

(1882),

Lord Bardon

(1885,

1886,

1888), Flying

Fox

(1889),

Research

(1889),

Fingal

(1890), Harlequin (1891),

the Irish

Helga

and

Helga

II

(1901-1914)

and the Michael Sars

(1910) (Gage

et

al,

1983;

Riceet

al,

1991).

More

recently,

the area has been studied

by major

sampling

_programmes. The

region

aroundtheFaroeIslands was

sampled during

the BIOFAR_programme

(1987-90)

at

depths

from 20 to 2420 m,

sampling

over 750 stations

(TSterrevang

et

al,

1994).

The Rockall

Trough

was

subjected

toa

long-term sampling

_programme

by

the

SMBA

(Scottish

Marine

Biological

Association - _now

SAMS),

starting

in 1973

(Gage

et

al,

1980)

and also

explored

during

the cruises of the French

ship

Jean Charcot in 1969

(Cherbonnier

&

Sibuet,

1973)

and 1976

(INCAL

expedition;

Gage,

1986).

Moretothe

south,

theareas

comprising

the

Porcupine Seabight

and

Porcupine

Abyssal

Plain werestudied

by

the IOS

(Institute

of

Oceanographic

Sciences- _now at

the

SOC)

sampling

_programme

(1977-86),

also

including

some areas of the

Porcupine

Bank and Goban

Spur (Rice

et

al, 1991).

The

Bay

of

Biscay

was

surveyed

Figure

1.2.

Map

showing

the stationlocations of the four cruises

(A-D)

ofthe H.M.

Surveying-vessel

Porcupine during

the summers of 1869-70intheNE

I- if***?'' r F 1

1

I

It *

feL

Jl

L

r:

SPAIN

RANCf.

E 1

WKDIT^RRANt

FeIfi

J C

[a

I

ope

1

ChapterOne

(Laubier

&

Monniot,

1985).

Several shortterm

sampling

_programmes are still

being

carried out or

just

finished in the NE

Atlantic,

including

the OMEX and OMEX II

(Ocean Margin EXchange

-

1993-99),

LOIS

(Land

OceanInteraction

Study

-1991-96),

BENBO

(BENthic BOundary layer

-1997-99)

and BENGAL

(High

resolution

temporal

and

spatial study

oftheBENthic

biology

and

Geochemistry

ofanorth-east

Atlantic

abyssal Locality -1996-99).

1.2.2.

Physiography

and sediments

The NE Atlantic Ocean is delimited on the north-west

by

the

Reykjanes Ridge,

Iceland onthe north andthe Iceland-Faroe-Scotland

Ridge

on the north-east. On the

east, it is limited

by

the

European

Continent

(Van

Aken&

Becker,

1996).

Nexttothe

Reykjanes Ridge, running

from the north-east to

south-west,

the Iceland Basin is

present. On the southern _part ofthe _area, the

Porcupine Abyssal

Plain is

present

as

partofthe West

European

Basin

(Fig. 1.3).

Between the Iceland Basin and the British Isles

Shelf,

a

complex bathymetry

is

generated by

the_presence of the Rockall-Hatton

Plateau,

withthe Rockall and Hatton

Banks. The Rockall-Hatton Plateau delimits the

moderately deep

Rockall Channel

(Rockall Trough)

onthewest-north-west. Theeastborder ofthechannel is

composed

by

the British Isles Shelf and

Slope.

The entrance ofthe Rockall Channel is in the south-west at

depths

of about 3500 m in

53

N latitude

(Ellett

et

al, 1986).

The northern

part

is shallower and delimited

by

a series of smaller banks

(Lousy,

Bill

Bailey's

andFaroe

Banks)

and the

Wyville-Thomson

Ridge.

The

Wyville-Thomson

Ridge

separates

the Rockall Channel from the Faroe-Shetland Channel onthe north¬

east, which is connected with the

Norwegian

Basin

(Fig. 1.3).

Inside the Rockall

Channel,

three

major

topographic

features are the Hebrides

Terrace

Seamount,

Anthon Dohrn Seamount and

Rosemary

Bank

(Fig. 1.3).

The

slope

onthewestof the Rockall Channel ismore

gentle,

withthe_presenceofabroad

sediment drift called Feni

Ridge (Roberts, 1975).

On the east

border,

the

slope

is

relatively

narrowerand

steeper,

following

the

relatively

broad continental shelfofthe

British Isles

(Roberts,

1975,

1979).

Close to the Hebrides Terrace

Seamount,

however,

the

slope

is

gentler owing

to _{the presence} ofthe Barra and

Donegal

ChapterOne

upper

slope

on both sides of the Rockall Channel is

composed by terrigenous

sediments

(Faugeres

et

al,

1981)

andrecentevidence _suggests thata

large

numberof

rock outcrops are _present,

mainly

in the southern _part of the channel

(Tyler

&

Zibrowius, 1992;

Neil

Kenyon, personal communication). Gage (1986) points

_out thatsediments collected with box core and anchor

dredge

in atransect in the Rockall

Trough

from 200-700 m

depth

showed

muddy

sand with

pebbles,

cobbles and some

boulders. Below 700 m the sediment is made _up of an increased

proportion

of

calcareous

particles

of

pelagic origin

(Gage,

1986).

Porcupine AbyssalPlain

P

-35 W -30

Figure

1.3.

Map

of the NE Atlantic

showing

the main

topographic

features.

ADS=Anton Dohrn

Seamount;

BBB=Bill

Bailey's

Bank;

EB=Edoras

Bank;

ES=Eriador

Seamount;

FB=Faroe

Bank;

FBC=Faroe Bank

Channel;

HB=Hatton

Bank;

LB=Lousy

Bank;

LrB=Lorien

Bank;

RB=Rosemary

Bank;

ChapterOne

Towards the south-west ofthe British Isles

Shelf,

the

Porcupine

Bank is _present and a

large embayment

in the

slope adjacent

to

it,

the

Porcupine Seabight,

which

leads,

on the

south-west,

to the

Porcupine

Abyssal

Plain

(Fig.

1.3).

The

Porcupine

Seabight

is characterized

by

_{the presence} of coarse carbonate sediments and rock outcrops

(Faugeres

et

al, 1981).

The

slopes

onthe westof the

Porcupine

Bank and

Porcupine Seabight

are characterized

by

the few number ofcanyons, which reflect the limited sediment

supply

available

(Roberts,

1975;

Rice et

al,

1991).

The

opposite

istrue for the eastern

slope

of the

Porcupine Seabight

and the southern _part of the Celtic Shelf

slope,

where there are numerous _{canyons and} channel _systems

(Rice

et

al, 1991).

The sediments of the centre of the

Seabight

are a

coccolith-foraminiferanmarl

(Lampitt

et

al,

1986).

Rock and mineral

debris,

including

clinker

and

drop

stones, are also _present

(Kidd

&

Huggett, 1981), serving

as substrata for

sessile

organisms (Rice

et

al,

1991).

1.2.3. Watermassesandcirculation

The subsurface

layers

of theNE Atlantic areformed

by

the

Subpolar

ModeWater

(SPMW

- _see

McCartney

&

Talley, 1982),

which may also bear different names in

the literature

(Subarctic

Intermediate Water -

SAIW, Bubnov, 1968;

Eastern North

Atlantic Water -

ENAW,

Harvey,

1982;

North Atlantic Water -

NAW,

Dooley

&

Meincke,

1981;

Modified North Atlantic Water -

MNAW, Hansen, 1985;

Rockall

Channel Mode Water -

RCMW,

Arhan et

al,

1994) (Van

Aken &

Becker,

1996).

This

variety

of names is related to the number of modifications that the SPMW is

subjected, mainly owing

to its

transport

and seasonal

variation,

with

temperatures

varying

from

8-12C.

Van Aken & Becker

(1996)

state that the SPMW forms the

bulk of 'warm' Atlantic water

entering

the

Norwegian

Sea between Iceland and Scotland. The SPMW is formed

by cooling

and

freshening

ofwater from the North Atlantic Current

(NAC)

in winter as aresult ofa

deep

convection driven

by

the heat

loss atthe seasurface

(Van

Aken &

Becker, 1996).

Below the

SPMW,

a

layer

of

salinity

minimum water is

present

at around

1600-1900m

depth, comprising

the Labrador SeaWater

(LSW

- see

Talley

&

McCartney,.

ChapterOne

Water

(MW;

also Gibraltar Water -

GW,

Ellett &

Martin, 1973;

Ellett et

al,

1986;

Lonsdale &

Hollister, 1979)

between 800-1200m

depth.

The

deep

layer

north of the Rockall Channel and Iceland Basin is formed

by

waters

resulting

from the overflow of

Norwegian

Sea

Deep

Water

(NSDW) through

the Iceland-Faroe

Ridge

into the Iceland Basin and

through

the

Wyville-Thomson

Ridge

into the Rockall Channel and Faroe Bank Channel

(Lee

&

Ellett,

1965;

Ellett

&

Roberts,

1973;

Mauritzen, 1996).

The NSDW interacts withthe SPMW

during

the overflow

forming

the Iceland-Scotland Overflow Water

(ISOW;

also called North¬

east Atlantic

Deep

Water -

NEAD,

Ellett &

Roberts,

1973).

The ISOW is a saline

water mass,with

temperatures

around

2.5C.

TheISOW is

gradually

mixed with less

dense waters

along

its

journey

southonthewest side of the Rockall-Hatton

Plateau,

forming

amodifiedwatermass called North-east Atlantic

Deep

Water

(NEADW).

The NEADW is found ina

salinity

maximumat around 2600 m

depth (Van

Aken

&

Becker, 1996).

In the south ofthe Iceland

Basin,

Porcupine Abyssal

Plain and Southern Rockall Channel the NEADW is found between the LSW above and another water _mass, the Lower

Deep

Water

(LDW),

below. The LDW

(<2.5C)

occurs at

depths

below 3000 minthe

Porcupine

Abyssal

Plain and at around 2500m

in the southern

part

of the Rockall Channel

(Van

Aken &

Becker,

1996).

The surface circulation

pattern

in the NE Atlantic shows anoverall trendtowards

the

transport

of

Subpolar

Mode Water north-eastwards into the

Norwegian

Sea

(Fig.

1.4a).

The SPMW is

transported by

the NAC from the

south,

passing

onthewest of

the Rockall-Hatton Plateau and on the east into the Rockall

Channel,

entering

the

Norwegian

Sea overthe Iceland-Faroe and

Wyville-Thomson

Ridges (Van

Aken &

Becker, 1996).

More to the west, over the Iceland

Basin,

part

of the SPMW is

diverted into thewesternNorth Atlanticoverthe

Reykjanes Ridge

(Fig.

1

Aa).

The

deep

circulation is more

complicated,

with the overflow of NSDW

(in

the

form of

ISOW) through

the Iceland-Faroe

Ridge

flowing

south-westwards on the

west-north-west

part

of the Iceland

Basin,

next to the

Reykjanes Ridge (Fig.

I

Ab).

The overflow

through

the

Wyville-Thomson Ridge

flows into the Rockall

Channel,

ChapterOne

-35 -30 -25 -20 -15 -10 -5 0

65

N

-60

-55

-50

-35

y\l

-30 -25 -20 -15

Figure

1.4.

Map showing

the circulation in the NE Atlantic and the estimated

geostrophic

transport

(1

Sv=106

m3

s"1).

A. surface

circulation;

B. bottom circulation. Abbreviations of water current names are

according

to the text

ChapterOne

Inthe

south,

next tothe

Porcupine

Bank,

the LDW andNEADWflow

northwards,

dividing

into twobranches. One followsthecontoursof the

Porcupine

Bankuntil the

contours

change

to an east-west direction. At this

point,

the LDW and NEADW

diverttothe north-westand thentothe

south-west,

recirculating along

the SouthFeni

Ridge,

where

they

meet the waters

flowing

from the north ofthe Rockall Channel

(Fig.

l

Ab).

The second branch of LDW and NEADW diverts earlier in the

Porcupine

Bankto the _west,

meeting

the first branch

just

south ofthe Lorien Bank.

Then,

the

waters follow the contours ofthe south-western _part of the Rockall-Hatton Plateau untiltheEdoras

Bank,

where

they

divide

again.

Onebranch flowsto the

south,

where

it either recirculates

again

in theeasternNorth Atlanticorleaves the area

through

the

Charles-Gibbs Fracture

Zone,

flowing

into the western North Atlantic. The other branch flows north-eastwards

along

the west

part

of the Rockall-Hatton Plateau and

at around

60N

it

recirculates,

joining

the ISOW

flowing

south-westwards. This branch_may also recirculate or leave the easternNorth Atlantic

through

the Charles-GibbsFracture Zone

(Fig.

1.46;

VanAken&

Becker,

1996).

1.2.4.

Primary productivity

and

input

of

organic

matterto thesediments

The NE Atlantic

region

is

subject

to the seasonal bloom of

phytoplankton during

the

spring

and summer

(Lochte

et

ai,

1993).

This bloom drives an

export

of

carbon,

as well as other

biogenic

and detrital

material,

from the surface ocean to

deeper

layers (Newton

et

al,

1994).

However,

the arrival of this material onthe bottom was

only

detected

relatively recently (Billett

et

al,

1983;

Rice et

al,

1986).

The amount

of the

primary

production

that arrivesonthe bottom is

generally

around 2-4% of the

surface

productivity (Turley

et

al,

1995)

and _{may vary}

spatially

and

temporally

(Lampitt,

1985;

Newton et

al,

1994;

Riceet

al,

1994).

The

majority

of the flux is in the form of fast

sinking (-60-500

m

day"1

-

Turley

et

al, 1995) aggregated

particles

commonly

called 'marine snow'

(Aldredge

&

Silver, 1988;

Lampitt

et

al, 1993a,

b).

Evidence also _suggests that once on the

bottom,

this material _{may be}

resuspended

backto the water column

(Lampitt, 1985).

The

phytodetritus

arriving

on the seabed

ChapterOne

1.2.5. Benthic

community composition

The benthic fauna of the

deep

NE Atlantic is

composed by

a

large

number of

species,

of which the echinoderms are some of the most

conspicuous (Gage

et

al.,

1983,

1985).

The zonation of the fauna in the Rockall

Trough

is described

by Gage

(1986)

and seems to be similar to that found in the

Bay

of

Biscay

and

Porcupine

Seabight (LeDanois,

1948; Sibuet,

1977).

The fauna onthe west side of the Rockall

Trough

is richer in number of

species

than that of the east side

(Gage

et

al.,

1983),

witha

large

number of

suspension

feeders.

On the east

side,

_{the upper}

slope

down to 700 m

depth

is characterized

by

coral

banks of

Lophelia

_pertusa and

Madrepora oculata,

and the echinoderms Cidaris

cidaris, Spatangus

raschi,

Stichopus

tremulus and Luidia sarsi. Other echinoderms with wider

bathymetric

distributions also occur at these

sites,

such as

Gorgonocephalus

caputmedusae,

Pseudarchaster

parelli

and

Ophiacantha

abyssicola (Gage, 1986).

From 700 to 1300 m

depth,

onthe

Hebrides-Donegal slope,

aricher

megafauna

is

found

composed

mainly by

the sea urchin Echinus acutus var.

norvegicus

and the

crustaceans Nematocarcinus

ensifer,

Pontophilus

norvegicus,

Geryon

tridens and

Nephropsis

atlantica. The echinoderms

Ophiocten gracilis,

Calveriosoma

hystrix,

Bathyplotes

natans,

Laetmogone

violacea,

Benthogone

rosea, Psilaster andromeda

and Plutonaster

bifrons

are also _present. A number of

ahermatypic

corals and the

pycnogonid

Collosendeis clavata also inhabit thisarea, aswell as

deeper

ones

(Gage,

1986).

A

large

number of echinoderms inhabit the zonebetween 1400 and 2000 m

depth,

including

Echinus

alexandri,

E.

affinis,

Persephonaster patagiatus,

Plinthaster

dentatus,

Bathybiaster

vexillifer,

Zoroaster

fulgens,

Ophiacantha

bidentata,

Ophiomusium lymani, Ophiura ljungmani

and Phormosoma

placenta.

Munidopsis

curvirostra,

Polycheles sculptus,

Neolithodes

grimaldi,

Colus

jeffreysianus

and Troschelia bernicensis are among the other

species

that live at those

depths (Gage,

1986).

In the _upper

abyssal, Hymenaster pellucidus, Dytaster

insignis,

Porcellanaster

ChapterOne

Hygrosoma

petersii,

Benthothuria

funebris

and

Oneirophanta

mutabilis

figure

among the echinodermspresent

(Gage, 1986).

In the

slope

areas rich in rock

outcrops

to the western_partof the

Porcupine

Bank,

Tyler

& Zibrowius

(1992)

describe a rich

suspension feeding

fauna,

mainly

composed by

sponges,

cnidarians,

stalked and comatulid

crinoids,

and

brisingid

asteroids,

among others

(see

also

Tyler

&

Lampitt, 1988).

The factors

affecting

the benthic distribution in the NE Atlantic are

probably

related to the

hydrography

and

dynamics

ofwater masses in the area. The

depth

of

winter

mixing

is around 600 m

(Ellett

&

Martin,

1973)

and may influence the presence of the 'mud line'

(Gage

&

Tyler,

1991),

where

Gage (1986) reported

a

maximuminrateof faunal

change

ataround 1000m

depth (Gage

et

al,

1984).

Intermsof biomass and

abundance,

the

general

pattern

_appears tobeadecrease of

both

parameters

with

increasing

depth,

for both the

megafauna (Laubier

&

Sibuet,

1979;

Sibuet,

1984;

Lampitt

et

al,

1986)

and macrofauna

(Flach

&

Heip,

1996;

Cosson et

al,

1997).

Lampitt

et al

(1986)

found that the biomass of the

megabenthos

in the

Porcupine Seabight

is dominated

by suspension

feeders and

crustaceans in the _upper

slope,

whereas in the middle and lower

slope

the biomass is dominated

by

echinoderms. Recent observations on the

Porcupine

Abyssal

Plain

revealed a dramatic

change

in the relative abundance of

megafaunal

species, mainly

in the

elasipodid

holothurian

Amperima

rosea

(David

Billett,

personal

communication).

The

megabentbic

biomass _appears to be more sensitive to

changes

in food

input

than the macrofauna

(Lampitt

et

al, 1986;

Flach &

Heip, 1996).

On the other

hand,

the seasonal

input

of

organic

matter _appearsto affect the

density

of the macrofauna

(Flach

&

Heip,

1996).

The meiofauna is also affected

by

food

pulses,

with individuals

being

larger

insize

during

food-rich

periods

(Soltwedel

et

al,

1996).

Diversity

also _appears to decrease with

depth.

Sibuet

(1977) points

out that

asteroid

diversity

decreases with

increasing

depth

in the

Bay

of

Biscay.

Paterson &

Lambshead

(1995)

show that

polychaetes

have a

parabolic

distribution in

species

richness,

with

peak

at 1800 m

depth

in the Rockall

Trough.

Data collected on the

benthos of the NE Atlantic _appearto be inconcertwith data found elsewhere

(Rowe,

ChapterOne

1.3.

Reproduction

and

development

in

deep-sea

invertebrates

Throughout history

the

deep-sea

has

being

marked

by

untested

hypotheses,

most

of whichwere

subsequently

discarded. Oneof themostfamouswasthe

concept

ofan

'azoic zone' below 600 m

depth (Forbes, 1844),

which was formulated even

though

the first animal to be retrieved from the

deep-sea,

the

ophiuroid Gorgonocephalus

caputmedusae (as

Astrophyton

linkii),

was collected much earlier in 1818

(Tyler,

1988).

During

the first half of the 20th _century, another

important

untested

hypothesis, stating

that

deep-sea organisms

should not

undergo pelagic development

was

being

erected

(see Young, 1994).

Two works were

remarkably important

in

consolidating

those ideas on the

development

of

deep-sea organisms.

The first was

suggestion by

Orton

(1920)

that

animals

living

in a

temperature-stable

environment,

as the

deep-sea

and

polar

regions,

should breed

continuously.

The secondwasthe

comprehensive

_{paper written}

by

Thorson

(1936),

which

supports

that

deep-sea

and

polar

animals should

develop

directly,

withoutalarval

stage.

Despite

the

early

evidence

present

in the literature

(Prouho,

1888;

Shearer et

al.,

1914; Mortensen,

1921), only by

the late 1960sand 1970s these ideaswere found to

flawed.

Rokop (1977) reported

that the

deep-sea brachiopod

Frieleia halli and the

scaphopod

Cadulus

californicus reproduce seasonally

and that the most obvious factor

influencing

breeding

was

probably

periodicity

in food

supply (for

F.

halli).

The same was earlier

put

forward

by

Schoener

(1968),

who found

seasonality

intwo

species

of

deep-sea ophiuroids

and

probably

the_presence ofa

free-living

larval _stage

for those

species.

Those

findings

were

important

not

only

as anevidence for

pelagic

development,

but that

seasonality

was also

present

in

deep-sea

organisms (see

also

George

&

Menzies, 1967, 1968;

and

Tyler,

1988 for a

review).

Later on,

during

the

1980s,

seasonal cues and events were discovered for different

deep-sea

areas in the

form of

particulate

organic

material

falling

to the seabed

(Deuser

&

Ross, 1980;

Deuseret

al,

1981;

Billettet

al, 1983; Deuser,

1986).

Itseemsthat

only

a

minority

of the

deep-sea

species

studiedso far haveaseasonal

reproduction,

with the _presence of a

planktotrophic

larva. In the Rockall

Trough

region (NE

Atlantic,

~ 2000 m

depth),

where much work have been done on the

ChapterOne

Ophiura ljungmani

and

Ophiocten

gracilis,

the seastars Plutonaster

bifrons

and

Dytaster grandis (formerly

identifiedas D.

insignis

-

Tyler

et

al,

1990)

and the sea

urchin Echinus

affinis produce seasonally

a

large

number of small _eggs,

indicating

probably

the _presence of

planktotrophic

larval

development (see

also

Tyler

&

Gage,

1979;

Gage

&

Tyler,

1981a;

Tyler

&

Pain, 1982a;

Tyler

et

al,

1993).

Inaddition to

Echinus

affinis,

Tyler

&

Gage (1984a)

note that the closer related

species

E.

alexandri and E.acutusvar.

norvegicus

also

possessed

a

planktotrophic

development

based on the egg

size,

fecundity

and the presence of larvae

(Shearer

et

al, 1914;

Hagström

&

L0nning,

1961;

Gage

et

al,

1986).

The same was found for the cidarid seaurchin Cidaris cidaris

(Tyler

&

Gage, 19846),

which

already

had aknown larva

(Prouho,

1888,

as Dorocidaris

papillata).

Young

(1991)

working

in the Bahamian

continental

slope

found that all the 21 different

species

of echinoids collected

presented

a

long-lived

planktonic

larvae,

with the

majority

being planktotrophic.

Young

et al

(1989)

raised larvae of the

bathyal

urchin

Aspidodiadema jacobyi

and

found that

they

were

obligate

planktotrophs,

but with an extended

pre-feeding

lecithotrophic

stage. Unfed larvaeremained alive for80

days

at 12C andtheir mouth

did not _openuntil 3 weeks after fertilization!

Young

& Cameron

(1989)

also _report

planktotrophic development

for

Linopneustes longispinus,

a

bathyal irregular

sea

urchinfrom theBahamas.

Other

deep-sea

_groups also show

planktotrophic

development.

Muirhead et al.

(1986)

notethattwo

species

of

Epizoanthus (E.

paguriphilus

andE.

abyssorum)

from the

deep-sea

have

planktotrophic

development

mainly owing

to the

specialized

commensal

lifestyle, despite

the latter

possessing

oocytes

with

only

one

quarter

of the volume ofthat ofE.

paguriphilus

(see

also

Tyler

et

al, 19856).

Van Praet

(1990)

reports

seasonality

in the

deep-sea

anemoneParacalliactis

stephensoni (see

alsoVan

Praet et

al,

1990 for

Phelliactis).

Bronsdon et al.

(1993)

also found

reproductive

seasonality

in the

deep-sea

epizoic

anemone

Amphianthus

inornata. Dataon

deep-sea

pennatulids

reveals that the

development

is

likely

to be

lecithotrophic (Rice

et

al,

1992;

Tyler

er

a/.,

19956).

Databased onthe

embryonic

and larval shells reveal that

planktotrophy

is _present amongst

deep-sea gastropods (Bouchet

&

Waren,

1979a).

Rex & Waren

(1982)

ChapterOne

suggested

this_maybe linkedtothe

ability

to track

patch

prey. In the Rockall

Trough,

Colmanet al.

(1986a)

estimate that43% of the 14

neogastropods

examined showed shell

morphologies

indicative of

planktotrophic development.

Evidence citedabove showed that Thorson's Rule

(named by Mileikovsky, 1971)

was nottrue, since

planktotrophy, although

not

dominant,

is common_amongst

deep-sea

species.

Moreover,

the statementthatdirect

development

wouldbethemain_type

of

development proved

also not to be _{true, since direct}

development

_appears to be

rare in the

deep-sea

and a

lecithotrophic pelagic

development

is

probably

most commonin that environment

(Pearse, 1994).

Table 1.1 shows the

probable

mode of

development

for some of the

deep-sea

species

and

higher

taxa. The mode of

development

is inferred _{from egg} size and

fecundity,

shell

morphology

or cultured larvae

(or

information on more than one

approach).

Data on the

development

of some

hydrothermal

vent and cold _seep invertebratesarealso included.

Table 1.1. Modes of

development

in

deep-sea

species.

Hydrothermal

vents andcold

seeps section modified from Cannetal.

(1994)

and

Copley

(1998).

Taxon _EggDiameter Development Source

'Normal'_Deep-Sea Cnidaria Epizoanthus paguriphilus Epizoanthus abyssorum Kophobelemnon stelliferum Umbellula lindahli Paracalliactisstephensoni Phelliactishertwigi Pheuiactis robusta Amphianthusinornata Kadosactis commensalis Mollusca Gastropoda Colus_{Jeffreysianus} Calliotropisottoi Benthonella tenella Benthomangeliamacra Tacita danielsseni Tacitaabyssorum Mohnia mohni Oenopotaovalis Oenopota graphica Anachis haliaeeti Trophonsp. Typhlomangeliasp.

Upto_{280 m}

Upto180_m Upto800m

Upto800m

Upto 180_m Upto180_m Upto210_m Upto205_m Upto 150_m

Planktotrophic Planktotrophic Lecithotrophic,'continuous' Lecithotrophic Seasonal Seasonal Seasonal Seasonal 'Continuous'

Upto170 m Lecithotrophic,'continuous'

150-260_{m Lecithotrophic,} 'continuous' Planktotrophic Planktotrophic Lecithotrophic,contained Lecithotrophic Lecithotrophic,contained Lecithotrophic,contained Lecithotrophic Planktotrophic Lecithotrophic Lecithotrophic Muirheade/a/.,1986 Muirheadefa/., 1986 Riceetal, 1992 Tylere<a/.,19956

VanPraet, 1990

VanPraete?a/.,1990

Van Praetetal,1990 Bronsdone/a/., 1993 BronsdoneJa/., 1993

Colmanetal, 1986a,6 Colman &Tyler, 1988 Bouchet &Waren, 1979a Bouchet &Waren,1979a

Bouchet&Waren,19796

Colmanetal, 1986a Bouchet &_Waren,19796 Bouchet&Waren, 19796; Colmanetal,1986a Colmanetal.,1986a Bouchet&Warön, 1979a; Colmanetal,1986a Colmanetal,1986a

ChapterOne Gymnobela frielei Gymnobelasubaraneosa Pleurotomellapackardi Pleurotomella lottae Taranis moerchi Lusitanops sp.A Turridaesp.A Belomitraquadruplex Iphitellatuberata Epitoniumformosissimum Bivalvia Malletiacuneata Ledella_pustulosa Ledellamessanensis Yoldiellajeffreysi Scaphopoda Caduluscalifornicus Echinodermata Ophiuroidea Ophiura ljungmani Ophiomusium lymani Ophiocten gracilis Ophiacanthabidentata Echinoidea Echinusaffinis Echinus alexandri Echinusacutusvar.

norvegicus Echinuselegans Phormosomaplacenta Calveriosoma_hystrix Araeosomafenestratum Sperosoma grimaldii Hygrosoma petersii Poriocidarispurpurata Cidariscidaris Stylocidarislineata Pourtalesiajeffreysi Pourtalesia miranda Echinosigraphiale Aspidodiademajacobyi Linopneustes longispinus Asteroidea Hymenaster pellucidus Hymenaster gennaeus'' Brisingaendecacnemos Brisingellacoronata Freyella spinosa Zoroasterfulgens Dytaster grandis Plutonasterbifrons

Upto_{240 m}

Upto120 m

Upto109_m Upto 120_m

Upto240m

Upto110_^i Upto450_m

Upto650m

Upto_ll(^m

Upto 110_m Upto 110_^i Upto60_m

1100-1500_m 1100-1500m 1100-1500_m 1100-1500m 1100-1500_^i 1100-1500_m Upto110m

Upto225_m 173-357m

250-335m

Upto98_m Upto109_m

Upto110(^m Upto1200m

Upto1250m

Upto1250_m

Upto1250_^i

Upto950m

Upto 120_m Upto 120_m

Planktotrophic Planktotrophic Planktotrophic Planktotrophic Lecithotrophic Planktotrophic Planktotrophic Lecithotrophic Planktotrophic Planktotrophic Lecithotrophic,'continuous' Lecithotrophic,seasonal Lecithotrophic,seasonal Lecithotrophic,seasonal .

Lecithotrophicordirect, seasonal

Planktotrophic,seasonal Lecithotrophic, 'continuous',

butseasonalityinrecruitment Planktotrophic,seasonal Lecithotrophic,'continuous' Planktotrophic,seasonal Planktotrophic,seasonal Planktotrophic,seasonal Planktotrophic,seasonal Lecithotrophic, 'continuous' Lecithotrophic,continuous Lecithotrophic, 'continuous' Lecithotrophic,'continuous' Lecithotrophic,'continuous' Lecithotrophic,'continuous' Planktotrophic,seasonal Planktotrophic,seasonal Lecithotrophic Lecithotrophic,'continuous' Lecithotrophic,'continuous' Planktotrophic,seasonal Planktotrophic,seasonal Lecithotrophic,'continuous' Lecithotrophic, 'continuous' Lecithotrophic,'continuous' Lecithotrophic,'continuous'

Direct_demersal,'continuous' Lecithotrophic, (seasonal?) Planktotrophic,seasonal Planktotrophic,seasonal

Colma.net_al,1986a

Colmanetai, 1986a Bouchet&Waren, 1979a; Colmanetal, 1986a Bouchet&Waren, 1979a Colmanetal, 1986a Colmanetal,1986a Colmanetah,1986a Colmanetal.,1986a Bouchet &_Waren,1979a Bouchet&Waren, 1979a Tyleretal,1992 Tyleretal.,1992 Lightfootefa/., 1979 Lightfootefa/., 1979;Tyler

etal.,1992 Rokop, 1977

Tyler&_Gage, 1979, 1980;

Gage&_Tyler, 19816

Gage&Tyler, 1982c Gage&Tyler, 1981a;Tyler

&Gage,19826 Tyler&_Gage, 1982a

Tyler&_Gage,1984a Tyler&_Gage,1984a Tyler&_{Gage, 1984a,Gage} etal,1986

Gageetal., 1986 Tyler&Gage, 19846 Tyler&Gage,19846 Tyler&Gage,19846 Tyler&Gage,19846 Tyler&_Gage,19846 Tyler&_Gage,19846 Tyler&Gage,19846 Youngetal, 1992 Harvey&Gage,1984 Harvey&Gage, 1984 Harvey&_Gage, 1984 Youngetal,1989 Young&Cameron, 1989 Painetal,1982a_(usH. membranaceus) Painetal,1982a Tyleretal,19846 Tyleretal, 19846 Tyleretal, 19846 Tyleretal,19846 Tyler&Pain, 1982a;Tyler etal, 1990

ChapterOne Psilaster andromeda Benthopecten simplex Pectinasterfilholi Pontastertenuispinis Bathybiaster vexillifer Pseudarchasterparelli Paragonastersubtilis Holothuroidea Ypsilothuriabitentaculata Laetmogoneviolacea Benthogonerosea Pentagoneazorica Pentagone diaphana Cherbonniera utriculus Molpadiablähet Deimavalidum Oneirophantamutabilis Bathyplotesnatans Benthodites sordida Psychropotes longicauda Psychropotes depressa Psychropotessemperiana Brachiopoda Frieleia hallt

HydrothermalVentsand Cold_Seeps Crustacea Ventiellasulfuris Bythograea thermydron Munidopsissp. Alvinocarislusca Rimicarisexoculata Polychaeta Alvinella Paralvinellapandorae Paralvinella_palmiformis Paralvinella_grasslei Paralvinellasulflncola A_mphisamytha Galapagensis MoUusca Gastropoda Alvinoconcha Bivalvia Bathymodiolus Thermophilus Calyptogena magnifica

Upto950_m Upto950_m Upto850_m Upto800_m Upto1000 m

Upto900_m Upto900_m

Upto350 _m

Upto400 _m Upto750 m