Hydrothermal Vents: A Global Ecosystem

Abstract Known hydrothermal vent

communities cluster in distant corners of the

world. The habitat conditions and trophic basis

of the ecosystem ensure a global similarity in

adaptations but resemblances go beyond

convergence. Taxonomic relations among vents

around the world are greater than those with

seeps or with adjacent deep-sea. Ancient ties

across the northern Pacific via a long-vanished

spreading zone may be revealed in faunal

similarities between northeast and northwest

Pacific vent faunas. Regional character overlies

historical connections.

Introduction

By the late Archaean, the Earth's

lithosphere had differentiated continental and

oceanic crust Plate dynamics similar to the

modem world were in place. Evidence of rifting

systems and hydrothermal deposits are known in

Precambrian uplifted ocean crust (Scott, 1985).

The hydrothermal habitat was well-established

by the time of diversification of the metazoans in

the late Proterozoic. During the evolution of the

major groups of marine animals in the early

Phanaerozoic, hydrothermal vents were available

to colonization. While the Palaeozoic record is

poorly documented, evidence of animal

communities dates from the Silurian and

Devonian (Moore et al., 1986; Zaykov and

Maslennikov, 1987; Little et al. 1997). Hie feet

that so many of the hot vent animals belong to

new taxonomic groups that apparently have

antiquated origin, suggests that part of the vent

fauna may be a hold-over from earlier

(?Mesozoic) times (Newman, 1985; McLean,

1990, Tunnicliffe, 1992). The role of historical

relations and evolution of marine communities

should be considered when describing relations

among modem hot vent communities. Hot vents

have been found on most explored mid-ocean

spreading ridges (Fig. 1). Important recent

discoveries include the highly active areas of the

southern East Pacific Rise near the Easter Island

microplate (Urabe et al., 1995; Auzende et al.

1996) and the Southeast Indian Ridge (Pluger et

al. 1990; Halbach et al. 1996). Areas with little

exploration effort include the Chilean Rise, the

southernmost EPR, the Southwest Indian Ridge,

the southern Mid-Atlantic Ridge and the ridges

north of Iceland. Back-arc basin spreading

associated with subducting oceanic crust in the

western Pacific also provides sites of

hydrothermal emissions that sponsor biotic

communities. This global distribution of the

habitat is unusual in its linear, fairly contiguous

character and very limited spatial extent

Dispersal of the inhabitants must be highly

directional in a deep ocean where currents are

generally not strong.

Ecosystem Character

Much of the fascination with

hydrothermal vents lies in their unusual

production source. The Archaea, the first

evolutionary group of organisms on our planet

(Bult et al., 1996) form the basis of the

ecosystem. While these microbes dominated the

Archaean world, they now produce little biomass

in an oxygenated biosphere in which aerobic

respiration is more energetically efficient and

plant photosynthesis predominates production.

Nonetheless, the reductive energetic reactions

known today at vents are similar to those

proposed for initial autotrophs (Jannasch, 1985).

With deep oxygen penetration into the ocean

(probably in the late Proterozoic), the greater

energetic return of oxidative reactions mediated

by Archaea became possible. Today, sulphide

oxidation appears to fuel the greatest

chemosynthetic biomass at most hot vents. The

abundance of reduced compounds such as

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Verena Tunnicliffe

School of Earth & Ocean Sciences, University of Victoria, Victoria, B.C Canada V8W 2N5

0 180Figure 1. Arrows indicate locations of the major sites of sampling for hydrotherma! vent fauna. The

designations indicate major biogeographic provinces (ATL Atlantic, JMAR Japan-Marians, WPAC

western equatorial Pacific, JdF northeastern Pacific, EPR northern East Pacific Rise, GAL Galapagos,

sEPR souther East Pacific Rise). IND is site of a recent small sample.

hydrogen sulphide and methane in vent fluids

around the world has fostered a common

production base. General similarity in fluid

composition also defines an unusual chemical

habitat that requires specific adaptations in

macrofauna: for instance, mechanisms to

detoxify hydrogen sulfide.

Relations among biogeographic regions

can be examined to determine the biotic

similarities. Aspects of common history and

community functioning promote those

similarities while both biotic character and the

underlying geologic context contribute to the

differences seen. There are now about 400

species known from hydrothermal vents.

Although some remain to be described, it

appears that about 83 to 90% are new species

unknown from other marine habitats. In

addition, about 50% of the genera are endemic

(Tmmicliffe & Fowler, 1996).

Sulfophilic Systems

The discovery of other

chemosynthetically-based habitats has raised the

possibility of animal dispersal from sites such as

seeps and whale carcasses to hot vents (Hecker,

1985; Kennicutt et al., 1985; Smith et al., 1989).

The production source and utilization is similar

to vents and similar adaptations such as sulphide

tolerance and complete dependence on microbial

symbionts for organic carbon are found - at least

at seeps. At continental margin cold seeps, the

use of methane appears more important

(Childress et al. 1986). There are many

similarities in groups of organisms found at

vents and seeps. In the northeast Pacific, three

species, including a vestimentiferan (Southward

et al., 1996), are known to inhabit both seeps and

vents. In the western Pacific, three species of

mussel and one shrimp species are known from

both seeps off Japan and vents in the Okinawa

Trough. Craddock et al. (1994) present a

phylogenetic analysis of mussels

(Bathymodiolvs) from eastern Pacific and

Atlantic vents and also fiom Atlantic seeps.

While seep and vent 'stocks' fall out separately,

there is a clear evolutionary link. An analysis of

genetic similarity among vestimentiferan groups

identifies vent and seep tubeworms as sister

clades with separate diversification paths (M.

Black, pers. comm.).

Whale bones are extremely rich in oils

and take many decades to decay. They generate

a sulphide-rich habitat in the immediate vicinity

that attracts microbes and attendant grazers

(Fujioka et al., 1993; Bennett et al., 1994).

― 106 ―

While whales have a marine history since the

Eocene, it is possible that the 'carcass' fauna

may have an evolutionary history originating

with Mesozoic marine reptiles (Hogler, 1994).

In areas of the world with long-established whale

migration routes near ridge-crests (e.g. west

coast of the Americas), some sulfophilic species

may exploit both whale and vent habitats.

An examination of known taxonomic

information from whales and seeps, identifies a

very small overlap of species with vents

(Tunnicliffe et al. 1996). Only 3% of vent

species are also found at seeps and another 1.5%

on carcasses. Modern species dispersal among

these habitats must be very limited.

Nonetheless, the evolutionary connections are

again found in the systematic listings; for

instance, five families of vent worms and

molluscs are known nowhere but vents and

seeps. While species have diverged, a common

past is evident. Much more work at seeps is

needed to explore these connections. An area of

particular interest is around Japan where seep

faunas are known in both deep and shallow

waters while the distance to vent communities

south of Japan is not great (Laubier et al., 1986;

Hashimoto etal., 1989; 1993).

Biogeographic Relations

Because most vent species seem to have

evolved in situ, a similarity analysis of different

biogeographic regions can be performed without

including faunas of other environments. Not

surprisingly, regions close to each other tend to

show greater similarity (Tunnicliffe and Fowler,

1996). However, direct distance alone does not

tell the whole story. It appears that past

geographic relations among regions may be very

important. Spreading ridges occupied different

positions throughout the Mesozoic and

Cenozoic. The character of the modem vent

faunas reflects these past relationships (Van

Dover, 1995; Tunnicliffe and Fowler, 1996).

Examination of distribution routes along

spreading ridges of the past contributes a great

deal to understanding modern similarities among

regions.

It is interesting to compare the known

vent faunas of the northeast and northwest

Pacific. A world map shows the northern Pacific

as a contiguous ocean. The North Pacific Drift

from west to east in subtemperate latitudes and

northwesterly return in the Alaskan Gyre tends

to ensure a dispersion of shallow marine

organisms throughout the northern ocean. In the

deep-sea, there are relatively few barriers to

dispersion across an abyssal plain dotted with

seamounts. Numerous species of deep-water

echinoderms, corals and sponges, among others,

are found throughout the northern Pacific. The

spider crab that populates Juan de Fuca Ridge

and scavenges on the periphery of hot vents there

was first described from the Emperor Seamounts

(Sakai, 1978; Tunnicliffe and Jensen, 1987).

That same abyssal plain, however, is a barrier to

dispersal of hot vent organisms. There are no

way-stations for these animals across 8000 km of

the world's largest ocean. The Northeast Pacific

ridges presently foim the end of a long ridge

pathway that runs along North America,

southern EPR to the southern Australasian

region. At this point, several back-arc spreading

centres form distribution stepping stones

northward past Australia and New Guinea to

Japan. Thus, via ridge crests, the distance from

eastern to western Pacific vents is about 32,000

km.

Work in the last decade has defined a

distinct character for vent faunas in the

equatorial western Pacific (Hessler and

Lonsdale, 1991; Galkin, 1992; Desbruyeres et

al., 1994). Recent discoveries in the New

Ireland areas (near Lihir Island) extend this

regional fauna (Herzig et al., 1994). Here,

venting through sediments on the flank of a

shallow seamount sponsors large communities of

large snails (Sysoev and Kantor 1995), limpets

(Beck, 1996), vesicomyid clams, neolepadid

barnacles, and a variety of polychaetes (unpubl.

data). It is a relatively large distance from this

site to known vents in the Marianas Back-Arc

Basin - some 2000 km. Together, Marianas and

Okinawa vents form a distinct assemblage of

species with minor overlap with more southerly

-107-

vents. As further data accumulate, it may be that

Marianas and the sites near Japan will also be

treated as separate biogeographic provinces.

Table 1. Animals that are found at both

northeast Pacific and northwest Pacific

hydrothermal vents.

GROUP GENUS

Polychete

Polychete

Polychete

Polychete

Polychete

Polychete

Polychete

Polychete

Polychete

Polychete

Limpet

Limpet

Snail

Snail

Clam

Spider

Copepod

Lobsters

Nicomache (Maldanidae)

Capitella (Maldanidae)

Ophryotrocha (Dorvilleidae)

Branchinotogluma (Polynoidae)

Lepidonotopodium (Polynoidae)

Levensteiniella (Polynoidae)

Opistkotrochopodus (Polynoidae)

Amphisamytha (Ampharetida)

Paralvinella (Alvinellidae)

Helicoradomenia (Simrothiellidae)

Puncturella (Fissurellidae)

Lepetodrilus (Lepetodrilidae)

Provanna (Provannidae)

Buccinum (Buccinidae)

Calyptogena (Vesicomyidae)

Sericosura (Ammotheidae)

Stygiopontius (Dirivultidae)

Munidopsis (Galatheidae)

Despite extensive sampling in the Juan

de Fuca Ridge area ("Northeast Pacific) the

number of vent species is relatively small (about

80). Species lists from Marianas (Hessler &

Lonsdale, 1991) and Okinawa (Hashimoto et al.,

1995) vents document only a few less; further

expeditions will likely lengthen the northwest

Pacific lists extensively. As taxonomic

descriptions from these sties are incomplete,

comparisons of 60 identified genera can be

made. Of these, 18 are genera known from the

Northeast Pacific and most of these are endemic

to vents (Table 1). In comparison, only a few

more genera (21) are held in common with the

Australasian vents (Lihir, Manus, Lau, Fiji) that

are much closer to the Japan area. Nine species

are shared indicating a subset of animals that are

widely dispersed. However, the generic level

remains interesting because it holds a longer

history: species differentiate faster.

Hessler & Lonsdale (1991) and

Tunnicliffe et al. (1996) discuss the historical

relations between the east and west Pacific. A

broad plate, the Kula, used to exist between

northern Asia and Canada/Alaska. A ridge

between the Kula and Pacific plates transsected

the northern Pacific connecting what is now Juan

de Fuca Ridge with a ridge just south of Japan in

the early Tertiary (Hibbard & Karig, 1990;

Osozawa, 1994). The Kula Plate is now gone,

being subducted beneath Japan and the Bering

Sea. Thus nothing remains of this late

Cretaceous/early Tertiary ridge (Fig. 2)

Nonetheless, the pathway likely existed for

dispersion of vent animals and may explain the

high similarity at generic levels between east and

west vent faunas in the northern Pacific. Most of

the northeast Pacific fauna is presumed to have

derived from a trans-Farallon fauna prior to the

splitting of Juan de Fuca from East Pacific Rise

about 30 million years ago (Tunnicliffe et al.,

1996) and most genera shared with the

Japan/Marianas are also found on EPR. The

actual site of origination for many of these

groups, however, remains unknown. Only

further systematic work and phylogenetic studies

of relations among the taxa can help to answer

such a question.

Figure 2. Possible Eocene northern Pacific plate

boundaries (from Tunnicliffe et al., 1996).

Acknowledgments. 1 thank C. M. Fowler and

L. Franklin for their help.

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