temporal variability in living deep-sea benthic...

Ž .Earth-Science Reviews 46 1999 187–212www.elsevier.comrlocaterecorscirev

Temporal variability in living deep-sea benthic foraminifera:a review

Andrew J. Gooday a,), Anthony E. Rathburn b,1

a Southampton Oceanography Centre, Empress Dock, Southampton, SO14 3ZH, UKb Marine Life Research Group, Scripps Institution of Oceanography, 9500 Gilman DriÕe, La Jolla, CA 92093-0218, USA

Abstract

The deep ocean environment is disturbed by various processes, many of which involve episodic inputs of organic matter.Ž .Some inputs e.g., phytodetritus at mid-high latitudes in the North Atlantic and Northeast Pacific are seasonally pulsed,

Ž .others e.g., falls of whale carcasses are irregular and unpredictable, but together, they evoke a variety of responses from thebenthic biota. In the case of deep-sea foraminifera, only those responses arising from seasonal food pulses have been fairly

Ž .well-documented. The population dynamics of deep-sea benthic foraminifera total live populations and individual speciesappear to be controlled largely by two inversely-related parameters, the flux of organic matter to the seafloor and

Ž .concentrations of oxygen in the sediment porewater. Organic matter food inputs are most intense along bathyal continentalmargins, and their oxidation often leads to the depletion of oxygen in surface sediments. Under these conditions,foraminiferal faunas are dominated by low-oxygen tolerant, infaunal species, the abundance of which fluctuate in response to

Ž .seasonally varying amounts of food and oxygen. At some sites e.g., Sagami Bay, off Japan , species migrate up and downŽin the sediments, tracking critical oxygen concentrations. Where oxygen concentrations are consistently low less than about

y1.0.5 ml l , as in parts of the California Borderland, foraminifera may undergo population increases solely in response tofood pulses. In the abyssal North Atlantic, and in some continental margin areas of this ocean, organic matter inputs areweaker and do not lead to oxygen depletion within surface sediments. These systems are food limited and seasonal

Ž .population fluctuations reflect the availability of food phytodetritus rather than oxygen. Here, the species which respond tophytodetritus are mainly epifaunal or shallow infaunal opportunists which represent a small proportion of highly diverse

Ž 2 .communities 2 or 3 out of )120 species per core of 25.5 cm surface area . Seasonal phytodetrital pulses to thedeep-seafloor, and hence, foraminiferal population dynamics, are not entirely predictable. Being dependent on climatic and

Ž Ž .upper-ocean processes, they vary in intensity from year to year and occasionally e.g., at the Porcupine Abyssal Plain PAP. Ž .in 1997 fail to materialise. Foraminiferal responses to irregular non-seasonal organic matter inputs are poorly-known.

However, there is some evidence that whale falls, turbidite deposits, hydrothermal vents and seeps are exploited by speciestypical of organically-enriched, low-oxygen environments rather than by a specialised fauna.

Fossil foraminiferal assemblages from bathyal and abyssal environments may provide evidence for an increase ordecrease in the seasonality of surface production as well as for longer-term changes in palaeoproductivity. However, theaccurate interpretation of this record depends on filling the many gaps which remain in our understanding of relations

) Ž . Ž .Corresponding author. Tel.: q44- 0 1703-596353; Fax: q44- 0 1703-596247; E-mail: [email protected] E-mail: [email protected]

0012-8252r99r$ - see front matter q 1999 Elsevier Science B.V. All rights reserved.Ž .PII: S0012-8252 99 00010-0

( )A.J. Gooday, A.E. RathburnrEarth-Science ReÕiews 46 1999 187–212188

between benthic foraminiferal ecology and seasonal phenomena in the deep ocean. q 1999 Elsevier Science B.V. All rightsreserved.

Keywords: benthic foraminifera; temporal dynamics; deep-sea; phytodetritus; seasonality; oxygen

1. Introduction

Some benthic foraminifera living in easily acces-sible near-shore environments have long been knownto undergo seasonal density fluctuations which affect

Žentire populations and individual species e.g.,.Boltovskoy and Wright, 1976; Murray, 1983 . Coex-

isting species may show different patterns. In some,reproduction peaks at different times of the year, in

Žothers it is spread throughout the year e.g.,.Boltovskoy and Lena, 1969 . These dynamic phe-

nomena have been linked to a variety of physical andbiotic influences and in particular to seasonal changesin temperature and primary production; for example,

Ž .Myers 1943 , one of the earliest authors to docu-ment seasonality in foraminifera, concluded thatgrowth and reproduction are largely confined to thespring in populations of Elphidium crispum living in

Ž .Plymouth Sound SW England . Foraminifera re-Žquire food in order to grow and reproduce Myers,

.1943 and so seasonal cycles in primary productionŽ .i.e., food availability may be responsible for initiat-ing periods of rapid reproduction. Erskian and LippsŽ .1987 described the complex population dynamicsof Glabratella ornatissima in subtidal habitats innorthern California where reproduction is coincidentwith seasonal upwelling and therefore maximum

Ž .phytoplankton production Erskian and Lipps, 1987 .On a smaller scale, centimetre-sized local blooms ofbenthic algae may evoke of a corresponding

Žforaminiferal bloom in intertidal salt marshes Lee et.al., 1969 . Other factors which have been suggested

to influence the population dynamics of shallow-Ž .water foraminifera include salinity Murray, 1967

Ž .and predation Buzas, 1978 .Compared to sublittoral and intertidal environ-

ments, the ocean floor is relatively stable, particu-larly in terms of physico-chemical parameters such

Ž .as temperature and salinity although not pressureŽ .Tyler, 1995 . Hence, deep-sea foraminiferal popula-tions can be expected to display less temporal vari-ability than those living in shallow-water habitatsŽ .Murray, 1967 . However, since the 1980s, evidence

has emerged that parts of the ocean floor are linkedto seasonal processes in the upper water column viatemporal variations in the flux of sinking particlesŽ . ŽTyler, 1988 . In some areas, a pulse of labile reac-

. Ž .tive organic matter phytodetritus , derived from theeuphotic zone, sinks through the water column fol-lowing the spring bloom and forms a patchy depositon the seafloor. This phenomenon has been well-

Ždocumented in the temperate North Atlantic Billettet al., 1983; Rice et al., 1986, 1994; Thiel et al.,

. Ž .1990 and the equatorial Smith et al., 1996 and NEŽ .Pacific Beaulieu and Smith, 1998 . Phytodetrital

pulses may be responsible for seasonal growth andreproduction in some megafaunal invertebratesŽGooday and Turley, 1990; Gage and Tyler, 1991;

.Campos-Creasey et al., 1994; Tyler, 1995 and sea-Žsonal changes in macrofaunal densities Drazen et

.al., 1998 , sediment community respiration ratesŽparticularly in the Pacific: Smith and Baldwin, 1984;

.Smith et al., 1994; Drazen et al., 1998 , bacterialŽ .densities Lochte, 1992 and sediment geochemistry

Ž .Soetaert et al., 1996 .During the last decade, it has become apparent

that populations of some benthic foraminiferal speciesin bathyal and abyssal deep-sea areas are also tempo-rally-dynamic. We begin this paper with an outlineof basic differences between eutrophic continental

Ž .margin bathyal and oligotrophic central oceanicŽ . Ž .abyssal regions. We then review 1 the responsesof foraminifera to seasonally-pulsed food inputs in

Ž .these settings and 2 possible foraminiferal re-Ž .sponses to unpredictable non-seasonal food inputs

to the ocean floor. We consider live faunas, using theterm ‘live’ to refer to specimens which stain withRose Bengal and can therefore be considered to havebeen alive or recently living at the time of collection.

2. Contrasts between marginal and central oceanicareas

The deep sea is not a homogenous environment.In addition to vent and non-vent areas, there are

( )A.J. Gooday, A.E. RathburnrEarth-Science ReÕiews 46 1999 187–212 189

Žmajor differences between continental margins slope. Žand rise and the central oceanic abyss Jahnke et al.,

.1990; Walsh, 1991; Hedges and Keil, 1995 . Al-Žthough some potentially important variables e.g.,

temperature, oxygen concentrations, sediment granu-.lometry change with increasing water depth, many

of the geochemical and biological contrasts betweenbathyal and abyssal habitats are related primarily to

Ž .the intensity of particulate organic carbon POCfluxes to the seafloor. Fluxes are much higher on theslope and rise than on the abyssal plains as a resultof higher phytoplankton productivity in the euphotic

Ž .zone particularly in upwelling regions , shallowerŽbathymetry and hence, less degradation of organic

.matter during its passage through the water column ,lateral advection from the shelf, and direct terrige-

Ž .nous inputs Jahnke et al., 1990; Walsh, 1991 .Recent estimates suggest that, despite their different

Ž .areas, continental margins below 1000 m and cen-tral oceanic gyres receive similar total POC fluxes,about 40% and 50%, respectively of global totalsŽ .table 3 and plate 8 in Jahnke, 1996 . These inputslead to an intensification of organic matter recyclingŽ .Jahnke et al., 1990 and to a higher oxygen con-sumption in continental margin sediments comparedto those from central oceanic regions; Jahnke and

Ž .Jackson 1987 estimate that 50% of deep-sea oxy-gen consumption occurs along continental margins.This results in a shallower redox discontinuity and,

Žin some areas, oxygen-depleted bottom water Diaz.and Rosenberg, 1995 . Because food is more plenti-

Žful, metazoan megafauna, macrofauna, and meio-.fauna biomass is higher along the margin than in theŽabyss e.g., Rowe, 1983; Thiel, 1983; Lampitt et al.,

.1986; Tietjen, 1992 and these regions are inhabitedby different species assemblages, for example, of

Ž .demersal fish Merrett and Haedrich, 1997 andŽ .holothurians Billett, 1991 . Tube-dwelling meta-

zoans have a greater impact in bathyal than in abyssalsettings. Some bathyal polychaetes, for example,rapidly transfer phytodetrital material from the sedi-ment surface into their burrows where it provides a

Žrich food source for infauna Jumars et al., 1990; de.Stigter, 1996; Levin et al., 1997 and influences

Žgeochemical gradients within the sediments Aller.and Aller, 1986 . Sipunculans perform a similar

Ž .function on the Vøring Plateau Norwegian marginŽ .Graf, 1989 .

Marginal and abyssal systems display consider-able regional heterogeneity resulting from variationsin the intensity of organic matter inputs and othercharacteristics such as near-bottom current activity.On the continental slope, regional differences in theorganic matter supply arise from upwelling and ter-

Žrigenous inputs e.g., Schaff et al., 1992; Soltwedel,.1997 . As a result, some parts of the slope are more

organically-enriched than other areas. Differences inthe energy of the benthic boundary layer also cause

Ž .regional heterogeneity Thistle et al., 1985 . Onabyssal plains, regional contrasts may arise fromdifferences in phytodetrital fluxes or sedimentary

Ž .characteristics Thurston et al., 1994 .Ž . ŽAccording to Mackensen et al. 1995 see also

.Schnitker, 1995 , the most important factors deter-mining the broad-scale distribution patterns of liveŽ .stained benthic foraminiferal assemblages in the

Ž .South Atlantic are: 1 lateral advection and bottomŽwater ventilation which influence parameters such

. Ž .as oxygen concentrations and temperature ; 2 in-puts to the seafloor of organic matter, derived largely

Ž .from surface primary productivity; 3 the degree ofundersaturation of bottom water with respect to cal-

Žcium carbonate which will mainly affect calcareous. Ž .species ; 4 the energy of the benthic boundary

Ž .layer. Authors such as Loubere 1991, 1994, 1996Ž .and Fariduddin and Loubere 1997 place particular

emphasis on the link between foraminiferal assem-blages and the organic matter flux, a factor whichprobably accounts for many of the taxonomic andecological differences between live foraminiferalfaunas on continental slopes and abyssal plains. Ingeneral, slope faunas contain a substantially higher

Ž .proportion of calcareous rotaliid and buliminidforaminifera than abyssal faunas. Particularly in ar-eas with a high organic matter flux, slope faunas aretypically dominated by calcareous taxa with infaunalmicrohabitat preferences and, in many cases, anability to tolerate persistent oxygen depletion result-ing from the oxidation of organic carbon. Commongenera are BoliÕina, Bulimina, Cassidulina, Chilos-tomella, Epistominella, Globobulimina, Fursen-

Žkoina, Nonionella and UÕigerina Lutze and Coul-bourne, 1984; Corliss, 1991; Corliss and Emerson,

.1990; Bernhard et al., 1997; Schmiedl et al., 1997 .ŽLarge tubular, agglutinated foraminifera e.g.,

.Bathysiphon, Rhabdammina are also often common


Ž .in slope settings Gooday et al., 1997 . Live faunasin central oceanic areas are characterised by a much

Žlower percentage of calcareous foraminifera even.above the CCD and a larger proportion of aggluti-

nated taxa, including delicate soft-bodied forms suchŽas komokiaceans Kuhnt and Collins, 1995; Gooday,

.1996; Gooday et al., 1997 . The predominant cal-Žcareous foraminifera are near-surface dwelling ‘epi-

.faunal’ species which are apparently intolerant ofŽoxygen depletion Corliss and Emerson, 1990; Joris-

.sen et al., 1995 .

3. Temporal variability arising from organic mat-ter inputs

3.1. Seasonal patterns on continental margins

Most data on deep-sea foraminiferal seasonalityare from bathyal continental margins, within the

Ž .depth range 500–1450 m Table 1; Fig. 1 . StudiesŽhave been conducted off California Bernhard and

Reimers, 1991; Corliss and Silva, 1993; Rathburn,.1996, 1998; Silva et al., 1996 , in Sagami Bay, Japan

Ž .Kitazato and Ohga, 1995; Ohga and Kitazato, 1997Ž .and in the Porcupine Seabight PSB off SW Ireland

Ž .Gooday and Lambshead, 1989 . Kaminski et al.Ž .1997 discuss aspects of seasonality at a 3000-m-deep site on the New Jersey continental margin.Most of these sites are eutrophic and the bottomwater is more or less oxygen depleted for at leastpart of the year. Values considerably less than 1 mlly1 are found on the California Borderland, some-

Ž y1 .what higher values around 1 ml l characteriseSagami Bay. The 1340-m-deep PSB site of Gooday

Ž .and Lambshead 1989 , is less organically enrichedand is overlain by Mediterranean Water which hasminimum oxygen concentrations of approximately

y1 Ž .4 ml l Cooper, 1952 . The New Jersey marginŽ .site of Kaminski et al. 1997 is presumably also

well-oxygenated, although no data are available. De-Ž .posits of ‘fluffy’ non-aggregated phytodetritus have

been observed in Sagami Bay and deposits of aggre-gated phytodetritus are present at the PSB site; inboth cases, deposition occurs mainly in the spring.

Many of these studies describe seasonal fluctua-tions in foraminiferal population densities. Fluctua-tions were most dramatic in the central Santa Bar-

bara Basin where they were linked to a reduction inbottom water oxygenation. The highest densities of

ŽRose Bengal stained specimens 2176 individualsy3 .cm in the 0–0.25 cm interval in October 1988

coincided with severely dysoxic bottom water anddetectable H S in near-surface sediments. There was2

no replacement of bottom water during the winter of1998r1989 and by the following July, stained

Žforaminifera had been virtually-eliminated 3 indi-y3 . Ž .viduals cm Bernhard and Reimers, 1991 . In

Sagami Bay, the population fluctuations coincidedwith changes in the thickness of the oxygenated

Ž .layer i.e., migrations of the redox front followingŽ .phytodetritus deposition Ohga and Kitazato, 1997

Ž .Fig. 2 . They ranged from 1500–2000 individualsy2 Ž .10 cm in the spring March–May to 200–500

y2 Ž .individuals 10 cm in the summer June–July . Inthe PSB, the increase in foraminiferal abundancebetween April and July 1983 was less dramatic, from385 " 77 to 713 " 281 individuals 3.45 cmy2

Ž y2 . Žs1116–2067 individuals 10 cm Gooday and.Lambshead, 1989 . Redox fluctuations did not ap-

pear to be a factor at this reasonably well-oxygenatedsite and the changes were mainly accounted for byindividuals inhabiting the phytodetritus layer.

Underlying these changes are the population dy-Ž .namics of individual species Table 1 . At the Cali-

fornia Borderland and Sagami Bay sites, most of thespecies reported to undergo density fluctuations werecalcareous; they include BoliÕina pacifica, B. spissa,Buliminella tenuata, Chilostomella oolina, Epis-tominella smithi, Eponides leÕiculus, Fursenkoinaapertura, F. bramletti, F. seminuda, Globobuliminapacifica, Nonionella stella, N. fragilis and ValÕu-lineria araucana. One species, Textularia katte-

Ž .gatensis, is agglutinated Ohga and Kitazato, 1997 .Many of these species typically occur in areas with ahigh organic matter input and most can tolerate

Žreduced oxygen concentrations Bernhard andReimers, 1991; Sen Gupta and Machain-Castillo,

.1993; Bernhard et al., 1997 . The majority are shal-low infaunal species with peak abundances in theupper 0–1 cm or 0–2 cm, but some are more deeply

Žinfaunal, typically residing )2 cm Silva et al.,.1996; Ohga and Kitazato, 1997 . The latter include

C. oolina, Globobulimina spp. and F. bramletti. InSagami Bay, most species occurred down to 5 cmdepth and were concentrated in the top 2 cm during


April and May, whereas in November and Decemberthey occurred down to 10 cm depth and were con-

Ž . Žcentrated at 2–3 cm Ohga and Kitazato, 1997 Fig.. Ž .2 . Silva et al. 1996 , on the other hand, detected no

changes in the vertical distribution of species overŽtime in the California Borderland San Pedro Basin,

.720 m .The foraminifera which exhibit population growth

following phytodetritus deposition at the well-oxygenated PSB site include agglutinated and al-logromiid species in addition to calcareous taxa.

ŽSome Epistominella exigua, Eponides pusillus,GaÕelinopsis lobatulus, Morulaeplecta sp. nov.,Portatrochammina aff. pygmaea, Tinogullmia rie-

.manni inhabit phytodetrital aggregates while othersŽCassidulina teretis, Nonionella iridea, Trifarina

.pauperata occur mainly in the sediment. None aretypical low-oxygen tolerant taxa, although G. lobatu-lus, N. iridea, T. pauperata have been recorded in

Žsediments rich in organic carbon Mackensen and.Hald, 1988; Mackensen et al., 1985 . At the assem-Ž .blage level, Lambshead and Gooday 1990 detected

a decrease in diversity and an increase in heterogene-ity following the phytodetritus pulse at this site.

Ž .Kaminski et al. 1997 compared the vertical dis-tribution of species in a box core subsample col-lected on the New Jersey continental margin in lateFebruary 1990 with the distribution patterns de-

Ž .scribed by Corliss 1985 in a vegematic subcore ofa box core collected in September 1980 at a site

Ž .situated 89.2 km 48.2 nm to the northeast. Thewater depth at both sites was around 3000 m. The

Ž .winter populations 1990 contained a much higherŽproportion of deep infaunal taxa Chilostomella,

.Globobulimina, Melonis and a much lower propor-Ž .tion of epifaunal taxa Hoeglundina elegans than

Ž .those sampled in the summer 1980 . In addition,specimens of Melonis barleenum were found atsubstantially shallower depths in the winter than inthe summer. The lack of replication and the geo-graphical separation of the two samples, however,make it difficult to eliminate the possibility thatthese differences arose from spatial rather than sea-sonal variability.

3.2. Seasonal patterns at abyssal depths

An abyssal benthic foraminiferal response to aphytodetrital pulse was first detected at the German

ŽBIOTRANS site in the northeast Atlantic 4550 m. Ž . Ž .bathymetric depth Fig. 1 . Gooday 1988 observed

that fresh detrital aggregates removed from multiplecore surfaces harboured calcareous and allogromiidspecies, principally Alabaminella weddellensis,Epistominella exigua and Tinogullmia riemanni.Similar observations were made at a nearby site on

Ž Xthe Porcupine Abyssal Plain PAP: 48850 N,X . Ž .16830 W; 4850 m depth Gooday, 1993, 1996 . The

green protoplasm and cytoplasmic inclusions of theŽtwo common calcareous species A. weddellensis

.and E. exigua indicate that they feed on algal cellsŽ .whereas the allogromiid T. riemanni , which has

colourless protoplasm, probably consumes cyanobac-Žteria and bacteria Gooday and Turley, 1990; Turley

.et al., 1993 . While these studies suggested thatpopulations of ‘phytodetritus species’ fluctuate with

Žthe presence and absence of phytodetritus Gooday,.1996 , they provided only snapshots of the living

Žfauna at particular sampling period in both cases,.the summer .

Direct evidence for population fluctuations atabyssal sites is sparse. At BIOTRANS, PfannkucheŽ .1992, 1993 showed that metazoans made up ahigher proportion of the meiofauna than foraminiferabefore the spring bloom whereas foraminifera weremore abundant in the summer samples. Gooday and

Ž .Turley 1990 published some BIOTRANS datashowing that populations of the three above men-tioned species decrease dramatically during the win-ter when their phytodetrital food source is no longer

Ž .available. In a recent study, Drazen et al. 1998showed that the density and biomass of macrofaunalŽ .) 300 mm protozoans, mainly agglutinatedforaminifera, increased significantly over a 4 weekperiod following the deposition of phytodetritus at a4100 m-deep site in the eastern North Pacific. Popu-lation densities increased between October and

ŽFebruary in consecutive years 1989r1990 and.1990r1991 in core samples collected by a free

vehicle grab respirometer. The increases occurredafter phytodetrital aggregates had disappeared fromthe seafloor and about 8 months after peaks insediment community oxygen consumption and POCflux. Analysis of tube cores collected by the sub-mersible AlÕin revealed significant increases in thepopulation densities of total protozoa and calcareousforaminifera during a 4 week period following the

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Table 1Summary of studies describing seasonal fluctuations in bathyal and abyssal foraminiferal faunas

Ž .Site depth in m , sedi- Environmental data Total fauna Species Other observations Referencesment layer, and size frac-tion examined

Ž .1 Sagami Bay, Japan Bottom water O : 1.0 ml Total populations fluctu- BoliÕina pacifica, Fursen- Species migrate vertically Kitazato and Ohga2y1Ž . Ž .1450 m ; 0–15 cm; )28 l . Fluffy phytodetritus ate seasonally with depth koina sp., Textularia katte- through sediment with 1995 , Ohga and Ki-

Ž . Ž .mm deposited in spring. of oxygenated layer gatensis shallow infaunal seasonally fluctuating tazato 1997increase in spring, Globobu- oxygen levels.limina spp., Chilostomella

Ž .oolina deep infaunal in-crease less distinctly in win-ter.

Ž .2 Santa Barbara Basin Bottom water O : fluctu- Total population density Most common species: Bernhard and Reimers2y1 y3Ž . Ž Ž .500, 550 m ; 0–10 cm; ates; -5 mM kg s ind. cm at 550 m sta- Chilostomella oolina, Non- 1991

y1 Ž . Ž .)63 mm 0.11 ml l August tion : 1548 February , ionella stella, Textularia ear-y1. Ž . Ž1988 ; 0.4 mM kg s 442 June , 2176 Oc- landi.

y1 Ž . Ž .-0.01 ml l October tober , 3 July 1989 ..1988 Biomass doubles between

June and October

Ž . y1 Ž .3 West of Santa Bar- O : 0.41–0.47 ml l ; Total population highest Epistominella smithi signifi- Changes in species abun- Rathburn 1996, 19982Ž .bara Basin 1000 m ; 0–1 bottom water tempera- August, October, lowest cant but variable numbers in dances linked to organic

cm layer; )150 mm ture: 48C May all except August samples; flux.fraction Nonionella fragilis abundant

in May 1995, August 1996.

Ž . Ž .4 San Pedro Basin. Bottom water O : 2.5–17 Total aggl and calc densi- ValÕulinaria araucana April No change in species ver- Corliss and Silva 1993 ,2y1 Ž .0–20 cm; )150 mm, mM l s0.06–0.38 ml ties maximum in July. max.; Buliminella tenuata, tical distribution patterns Silva et al. 1996

y163–150 mm data pre- l ; max. organic C flux Bulimina pacifica, Non- between seasons.Žsented separately January terrigenous in- ionella stella, Eponides leÕ-

.put and AprilrMay iculus, Fursenkoina aper-Ž .bloom input tura, Fursenkoina seminuda

October max.; Globobulim-ina pacifica, Fursenkoinabramletti , Epistominellasmithi July max.

Ž . Ž Ž .5 NE Pacific, 220 km Seasonal inputs of phy- Increases on density and Calcareous taxa dominant Drazen et al. 1998Ž .off California 4100 m ; todetritus to seafloor. biomass following phy- species Chilostomella ooli-

.0–4 cm; )300 mm Sediments oxygenated to todetritus deposition. na, Globobulimina affinis;3 cm depth. show significant increase in

0–2 cm layer within 4 weeksof input.

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Ž . Ž Ž .6 New Jersey continen- February 1990 box core No observations Epifaunal species Hoeg- Melonis barleeanum may Corliss 1985 , KaminskiŽ Ž .tal margin 3000–3098 showed distinct colour lundina elegans, Cibicidoides move upwards to occupy et al. 1997

. .m ; 0–15 cm; )150 mm change at 10 cm depth spp. dominant in September near-surface microhabitatŽassociated with major 1980; infaunal species Me- vacated by epifaunal spe-

change in redox condi- lonis barleeanum, Chilos- cies.tions. tomella oolina, Globobulim-

.ina spp. dominant in Febru-ary 1990.

2Ž . Ž .7 Porcupine Seabight Bottom water O : )4 Forams ind. 3.35 cm OÕammina sp. nov., Cri- Epistominella exigua, Al- Gooday and Lambshead2y1Ž . Ž .1345–1361 m ; 0–1 cm; ml l ; aggregated phy- more abundant in July thionina sp. Lagenammina abaminella weddellensis, 1989

Ž .)45 mm todetritus present in July 713"281, ns5 than sp., Reophax micaceous Tinogullmia riemanni,Ž .April 385"79, ns8 . April max; Tinogullmia rie- Morulaeplecta sp., Por-

manni, Epistominella exigua, tatrochammina aff. pyg-Eponides pusillus, GaÕin- maea, Parafissurina fusi-ulinopsis lobatulus, Moru- formis typically inhabitlaeplecta sp., Portatrocham- phytodetritus aggregates.mina aff. pygmaea, ?Ala-baminella sp., Parafissurinafusiformis, Cassidulina tere-tis July max.

Ž . Ž .8 NE Atlantic BIO- Well - oxygenated open- Metazoans dominate Increase in abundance of Al- Epistominella exigua in- Gooday 1988 , GoodayŽ . Ž .TRANS site 4550 m ; ocean site with seasonal meiofauna in March and abaminella weddellensis, gests fresh 2–3 mm-sized and Turley 1990 ,

Ž .0–1 cm layer; )63 mm phytodetritus inputs May, forams dominate in Epistominella exigua, Tino- algal cells. Pfannkuche 1992, 1993July and September. gullmia riemanni following

phytodetritus deposition.

Ž . Ž .9 Porcupine Abyssal Well-oxygenated open- No obvious seasonal Alabaminella weddellensis, Possible increase in abun- Gooday 1996 ; this pa-Ž .Plain 4850 m ; 0–1 cm ocean site with seasonal changes in live foramini- Epistominella exigua, Tino- dance of Trochammina per

layer; )63 mm phytodetritus inputs feral densities. gullmia riemanni colonise sp. between 1989 andŽ .fresh phytodetritus 1989 ; 1996.

Quinqueloculina sp. colo-nise degraded phytodetritusŽ .1996 .

The numbers in the first column correspond to the numbers used in Fig. 1.

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Fig. 1. Map showing the locations of localities mentioned in Table 1 and the text. 1sSagami Bay; 2–4sSanta Barbara and San Pedro Basin sites; 5sNE Pacific site ofŽ .Drazen et al. 1998 ; 6sNew Jersey continental margin; 7sBIOTRANS site; 8sPAP; 9sPSB.


Ž . Ž . Ž .Fig. 2. Seasonal changes over a 4 year period March 1991 to December 1994 in a the thickness of the oxygenated layer, b the totalŽ .population density of live benthic foraminifera and c the abundance of the most common species at a 1450 m-deep site in Sagami Bay,

Ž .Japan. Fig. 2 in Ohga and Kitazato 1997 .


deposition of phytodetritus in August 1994. LargeŽ .)300 mm calcareous foraminifera, dominated byChilostomella oolina and Globobulimina affinis,showed a particularly marked increase. A corre-sponding increase in the biomass of these taxa wasmost clearly expressed in the top 2 cm of the cores.This site, which lies 220 km offshore at the base ofthe Monterey deep-sea fan and below the Californiacurrent, is relatively eutrophic compared to, for ex-ample, the PAP in the NE Atlantic.

In order to improve our knowledge of temporalvariability in abyssal systems, a study is in progress

Ž .of foraminifera )63 mm fraction in time-seriesŽ .samples from the PAP Rice et al., 1998 . Multiple

cores, obtained in September 1996 and in March,July and October 1997, were sliced into 0.5-cm-thicklayers down to 2 cm depth and into 1-cm-thicklayers from 2 to 15 cm. A small volume of materialŽ .‘topmost sediment’ was removed directly from thesurface sediment using a plastic Pasteur pipette. Phy-todetritus aggregates with a degraded appearancewere present in September 1996, but in July 1997,only occasional lumps of fresh, gelatinous materialwere observed on a few cores. Population densities

Žin the 0–1 cm sediment layer 0–0.5 and 0.5–1.0 cm

.layers combined show no clear seasonal trend, sam-ples from March 1997 and September 1996 yielding

Ž .the highest and lowest values, respectively Fig. 3 .There was, however, a higher concentration of stainedforaminifera in the ‘topmost sediment’ during

Ž .September 1996 than in the 1997 samples Fig. 4 .Although these foraminiferal populations are very

Ždiverse )120 species present in the upper 1 cm.layer , the only species to show a clear temporal

trend is Quinqueloculina sp. which is the dominantspecies in September 1996, common in one of theMarch 1997 samples, but fairly uncommon in the

Ž .remaining samples Fig. 5 . In September 1996, itwas concentrated in the ‘topmost sediment’ and theupper 0.5 cm layer, indicating that most specimenslived on or just below the sediment surface. In the1997 samples, however, it was absent from the ‘top-most sediment’ and more common in the 0.5–1.0 cm

Žlayer than in the 0–0.5 cm layer although the. Ž .numbers are generally small Fig. 6 . Thus, Quin-

queloculina sp. appears to be a shallow infaunalspecies which migrates towards the sedimentrwaterinterface in order to feed on phytodetritus and toreproduce. Many specimens from the 0.5–1.0 cm

Ž .layer 1997 samples were encased in cocoons and

Ž . Ž X X .Fig. 3. Abundance of total live benthic foraminifera i.e., the entire stained population in cores from the PAP 48850 N, 16830 W, 4850 mŽ . Ž .collected during August 1989 DiscoÕery Stn 11908, three samples , September 1996 DiscoÕery Stn 12930, three samples , March

Ž . Ž . Ž .DiscoÕery Stn 13200, two samples , July DiscoÕery Stn 13077, two samples , October 1997 Challenger Stn 54301, one sample . NoteŽ .that for one of the September 1996 samples indicated by an asterisk , the data are derived from the 0–0.5 cm layer only; in all other cases,

the data are derived from the 0–1 cm layer.


Ž . ŽFig. 4. Distribution of total live foraminifera i.e., the entire stained population among phytodetrital aggregates, ‘topmost’ sediment surface. Ž X X .material removed using a Pasteur pipette , 0–0.5 and 0.5–1.0 cm layers of multiple cores from the PAP 48850 N, 16830 W, 4850 m

Ž . Ž . Žcollected during September 1996 DiscoÕery Stn 12930, three samples , March DiscoÕery Stn 13200, two samples , July DiscoÕery Stn. Ž .13077, two samples and October 1997 Challenger Stn 54301, one sample . Note the greater abundance of foraminifera in the topmost

Ž .sediment during September. For one of the September 1996 samples indicated by an asterisk , there are no data from the 0.5–1.0 cm layer.

Ž . Ž X X .Fig. 5. Abundance of important species live populations in 1996r1997 multiple cores from the PAP 48850 N, 16830 W, 4850 mŽ . Ž . Žcollected during September 1996 DiscoÕery Stn 12930, three samples , March DiscoÕery Stn 13200, two samples , July DiscoÕery Stn

. Ž . Ž .13077, two samples , October 1997 Challenger Stn 54301, one sample and August 1989 DiscoÕery Stn 11908, three samples . Note thatŽ .for one of the September 1996 samples indicated by an asterisk , the data are derived from the 0–0.5 cm layer only; in all other cases, the

data are derived from the 0–1 cm layer.


Ž . ŽFig. 6. Abundance of live stained specimens of Quinqueloculina sp. in phytodetrital aggregates, ‘topmost’ sediment surface material. Ž X X .removed using a Pasteur pipette , 0–0.5 and 0.5–1.0 cm layers of multiple cores from the PAP 48850 N, 16830 W, 4850 m collected

Ž . Ž . Žduring September 1996 DiscoÕery Stn 12930, three samples , March DiscoÕery Stn 13200, two samples , July DiscoÕery Stn 13077, two. Ž .samples , October 1997 Challenger Stn 54301, one sample . Note that specimens are abundant in the topmost sediment from the

Ž .September 1996 samples but not in later samples. For one of the September 1996 samples indicated by an asterisk , there are no data fromthe 0.5–1 cm layer.

Ž .may have been dormant Linke and Lutze, 1993 .Ž . Ž .Linke 1992 and Linke et al. 1995 described how

some deep-sea species switch from a dormant to anactive state when food becomes available followinga period of starvation.

In addition to these changes in the abundance ofQuinqueloculina sp., there is a clear difference be-tween the 1996r1997 foraminiferal assemblages andthose sampled during August 1989 when fresh phy-todetritus was present on many core surfaces. TheAugust 1989 samples yielded large populations ofAlabaminella weddellensis and E. exigua, most indi-viduals of which were found embedded within the

Ž .phytodetrital aggregates Gooday, 1996 . Neither ofŽ .these species was common in 1996r1997 Fig. 5 .

This can probably be attributed to the degradednature of the aggregates present in September 1996and the virtual absence of phytodetritus in subse-quent samples. Thus, in a negative way, the newobservations support the view that these species areopportunists and suggests the following sequence ofevents may be associated with phytodetrital pulses:Ž .1 Fresh phytodetritus is colonised by A. weddellen-

sis, E. exigua, Tinogullmia riemanni and other lessŽ .common species; 2 as phytodetritus is degraded in

the late summer, these species are replaced by Quin-queloculina sp. which migrates up from a shallowinfaunal microhabitat to feed and reproduce at the

Ž .sediment surface; 3 the Quinqueloculina popula-tions decline during the winter and move back down

Žinto the sediment, remaining cocooned and dor-. Ž .mant? until food again becomes available; 4

foraminiferal populations remain fairly stable in theabsence of pulsed inputs of organic matter. However,this is a speculative scenario and further observationsare required. Moreover, even if broadly correct, thereis unlikely to be an exact repetition of this sequencefrom year to year.

3.3. Non-seasonal patterns

Foraminifera also respond to irregular inputs oforganic matter to deep-sea systems, but these re-sponses are poorly documented and little is knownabout temporal trends. These will presumably de-pend on the magnitude and nature of the input and


the time scale over which the organic matter decom-poses.

3.3.1. Patterns associated with organically-enrichedpatches

Organic matter reaches the seafloor in a variety offorms in addition to phytodetritus and othermacroaggregates; these include large animal remainsŽ .e.g., whale carcasses and smaller packages of ani-

Žmal and plant material such as invertebrate e.g.,. Žsalp carcasses, Sargassum and wood Rowe and

Staresinic, 1979; Grassle and Morse-Porteous, 1987;Smith and Hessler, 1987; Gooday and Turley, 1990;

.Gage and Tyler, 1991 . The impact of these organicpackages on seafloor communities depends on theirsize and nature. Whale carcasses are stripped of their

Ž .flesh by scavengers Smith, 1985, 1986 and thefresh, exposed skeletons are colonised by chemosyn-thetically-based communities similar to those occur-

Ž .ring around vents Smith et al., 1989 . Recent studiesof a whale skeleton in the Santa Catalina BasinŽ .1240 m depth, California Borderland indicate that,after an estimated 4 years on the seafloor, chemicaland microbiological effects on the surrounding sedi-ments were modest and the impact on the macrofau-

Žnal sediment community a sharp reduction in theabundance of the dominant macrofaunal species, and

.in bioturbation rates was limited to a region withinŽ .0.5 m of the skeleton Smith et al., 1998 . Cattle

Žbones placed on the seafloor near Japan 1445 m.depth initially attracted scavengers and, after 1 year,

were covered with patches of filamentous bacteriaand surrounded by sediments smelling of hydrogen

Ž .sulphide Kitazato and Shirayama, 1996 . Studies ofnatural inputs and experiments using enriched sedi-ment trays demonstrate that small, localised patchesof organic enrichment are colonised by macrofaunal

Žinvertebrates e.g., Grassle and Morse-Porteous,.1987; Snelgrove et al., 1994, 1996 . In the Atlantic

Ocean, although apparently not in the Pacific, theseŽare predominantly opportunistic species e.g.,

capitellid, spionid and hesionid polychaetes, bi-.valves, cumaceans, leptostracans which are rare in

the normal sediment community.These organic matter inputs are unpredictable and

in most cases are highly localised. The ways inwhich foraminifera and other meiofauna respond to

Ž .them are largely unknown. Wada et al. 1994 found

that sediment rich in fatty acids, collected beneaththe spine of a Bryde’s Whale skeleton on the Tor-ishima Seamount south of Japan, contained aforaminiferal assemblage characterised by Cassiduli-noides parkerianus. Other species present were

Ž .‘Rhabdammina’ ?sSaccorhiza ramosa, Reophaxscorpiurus, RecurÕoides parkerae, Cystammina pau-ciloculata, Textularia kattegatensis, Textularia sp.Ž .all agglutinated species , Gyroidina quinqueloba,Tosaia hanzawai, Fursenkoina sp., Melonis pompil-

Ž .ioides, Epistominella exigua all rotaliids andŽ .Spiroloculina miliolid . Preliminary observations by

Ž .Rathburn unpublished suggest that whale fallsŽfavour common species e.g., UÕigerina peregrina.and Globobulimina spp. which are typically found

in eutrophic conditions. In local patches, populationsof these species can be expected to undergo tempo-

Ž .rary increases duration of months or years? whichare unpredictable in both space and time. Whalecarcasses represent an intense form of organic en-richment and persist for much longer than phytode-trital aggregates. It is possible, therefore, that asuccession of foraminiferal species may respond todifferent phases of the decomposition process.

3.3.2. Patterns associated with turbiditesTurbidites provide another ephemeral source of

organic matter in the deep-sea. They are common onŽsome abyssal plains e.g., Weaver et al., 1992 and

.earlier papers; Masson et al., 1996 and can containsubstantial amounts of organic material. Griggs et al.Ž .1969 postulated that deep-sea macrofaunal commu-nities in the Cascadia Channel are affected by theincreased supply of labile organic material broughtin by turbidity flows. These inputs, which may be

Ž .periodic over long time scales Weaver et al., 1992 ,also seem to influence foraminiferal assemblages.For example, organic-rich turbidite sediments from3980 m in the South China Sea contained deepinfaunal specimens of Chilostomella oolina whereassurface sediments were inhabited by agglutinated

Ž .taxa Rathburn et al., 1996 . At 4515 m in the SuluSea, turbidite sediments yielded ValÕulineria mexi-cana, C. oolina, and Globobulimina species, again in

Ž .deep infaunal microhabitats. Rathburn et al. 1996suggested that these foraminifera are able to avoidthe corrosive bottom waters by residing below theuppermost sediment, and, at the same time, could


take advantage of organic matter within the sedi-ments. Total abundances of calcareous taxa weremuch higher than expected for these water depths. Itis unknown how long the faunal influence of thismaterial lasts. One possibility is that calcareous in-faunal species may persist in deep-sea areas where

Žlight turbide deposition is frequent assuming they.can survive the emplacement process , while tempo-

rary blooms occur in situations where turbidite depo-sition is less frequent.

3.3.3. Patterns associated with seeps and ÕentsSome specialised metazoans derive food from

symbiotic bacteria which depend on reduced com-pounds emanating from seeps and vents on theseafloor. Seeps and vents may persist for some years,although they are ephemeral over longer time scales.They harbour a characteristic epibiota that includessymbiont-bearing clams, pogonophoran or vestimen-tiferan tube worms and sometimes mussels or gas-

Žtropods Grassle, 1986; Høvland and Judd, 1988;.Gage and Tyler, 1991; Sibuet and Olu, 1998 . Rela-

tively little is known about benthic foraminifera inthese environments. Studies carried out so far havebeen opportunistic, using sampling strategies andmethodologies designed for the collection of macro-fauna or sediment samples, and have rarely distin-

Žguished living from dead specimens Arnold et al.,1985; Kaminski, 1988; Molina-Cruz and Ayala-Lopez, 1988; Nienstedt and Arnold, 1988; van Doverét al., 1988; Akimoto et al., 1992, 1994; Jones, 1993,1996; Quinterno, 1994; Jonasson et al., 1995; Ki-

.tazato, 1996 . However, benthic foraminifera can besignificant components of seep and vent communi-ties. In a study of recruitment patterns on hardsubstrates near hydrothermal vents, van Dover et al.Ž .1988 found a single agglutinated foraminiferalspecies to be one of the most abundant colonisers atlong-term deployments in one area. This species,Abyssotherma pacifica, may be endemic to vent

Ženvironments Bronnimann et al., 1989; Lee et al.,¨.1991 . The limited data available suggest that seep

and vent areas which do not produce high tempera-ture and corrosive fluids can support calcareousforaminiferal communities that differ substantially interms of density, diversity, and species compositionfrom adjacent non-seeprvent communities. How-ever, apart perhaps from A. pacifica, few such taxa

Ž .are endemic to these unusual areas Kitazato, 1996 .Most of the calcareous species are also normallyfound in non-vent environments characterised by

Žorganic enrichment andror low oxygen e.g., BoliÕ-.ina, Bulimina, Trifarina, and UÕigerina species

ŽMolina-Cruz and Ayala-Lopez, 1988; Nienstedt andÁrnold, 1988; Sen Gupta and Aharon, 1994; Sen

. Ž .Gupta et al., 1997 . Vanreusel et al. 1997 came to asimilar conclusion regarding the lack of endemicnematode genera around vents in the SW Pacific. Itis possible, however, that some foraminifera havehigher tolerances to the stressful environmental con-ditions associated with seeps and vents. For example,

Ž .Akimoto et al. 1994 suggest that the occurrence ofRutherfordoides cornuta is related to high methanegas content of the sediments and is associated withCalyptogena clam communities, while Bulimina stri-ata distributions are influenced by the hydrogensulphide gas content of ambient waters. Sen Gupta et

Ž .al. 1997 suggested that BoliÕina albatrossi is toler-ant of high levels of sulphides associated with somehydrocarbon seeps.

3.4. Longer-term trends

In bathyal environments, temporal changes overlonger time scales may be linked to climatic oroceanographic events which shift thermal boundariesand the position of the oxygen minimum zoneŽ . ŽOMZ . These shifts may be cyclic e.g., due to El

. Ž .Nino or directional e.g., due to global warming .Ãlthough the effects of changes caused by El Nino˜have been examined for certain benthic taxa in up-

Žwelling areas e.g., off Peru by Arntz et al., 1985,.1991; Gallardo, 1985 , their influence on the tempo-

ral dynamics of benthic foraminifera is unknown.However, since the characteristics of foraminiferalcommunities are related to the amounts of organicmaterial and oxygen available, temporal changes inthe extent or location of the OMZ probably havesignificant effects on the distribution and composi-tion of bathyal assemblages. Such changes may beparticularly evident near the edges of OMZs wheresubstantial gradients in abundances and assemblagecompositions occur for both macrofauna andforaminifera, for example, off the Californian and

ŽPeruvian coasts Mullins et al., 1985; Resig and.Glenn, 1997 . Since El Nino events suppress diatom˜


production, they could also influence the depositionof phytodetritus in the equatorial Pacific, where thephytodetrital production has been linked to the pas-

Ž .sage of tropical instability waves Smith et al., 1996 .Longer-term changes in abyssal environments are

also possible. Recent work at the PAP suggests thatan important faunal shift, for which there is noobvious cause, has occurred in metazoan megafaunal

Žpopulations sampled using an otter trawl with a 4. Ž .mm mesh over a period of years Rice et al., 1998 .

The changes are particularly evident among theholothurians, the most abundant and conspicuousmegafauna at this locality. In 1989, 1991 and 1994,holothurian populations consisted mainly of several

Žlarge species Psychropotes longicauda, Oneiro-.phanta mutabilis, Pseudostichopus sp. , whereas in

1996r1997, these species had been overtaken, interms of biomass as well as abundance, by a small

Ž .holothurian Amperima sp. which had been rare inthe earlier otter trawls. A change may have occurredamong the foraminifera during the same period. Asmall trochamminacean species is consistently abun-

Ž .dant either first or second ranked in all the1996r1997 BENGAL samples but is relatively un-common in three samples collected during 1989Ž . Ž .DiscoÕery Station 11908 Fig. 5 . Whether there isany link between the obvious change in theholothurian fauna over a two and a half year periodŽ .1994r1996 , and the more modest change in theforaminiferal fauna at PAP between 1989 and 1996,is unknown. However, these observations do suggestthe possibility that population densities of somedeep-sea foraminiferal species may fluctuate in away that cannot presently be attributed to any envi-ronmental cue. Examination of further material fromthe PAP site, including cores collected during 1991and 1994, may help to clarify this issue. Meanwhile,it is interesting to note that a similar shift inforaminiferal assemblage composition has been re-

Žported from an intertidal site in Bahrain Basson and.Murray, 1995 .

4. Discussion

4.1. Some problems

Spatial heterogeneity is a feature of most, perhapsall, benthic communities and is particularly impor-

tant in the deep-sea where small-scale features, forexample, faecal casts and patches of organic matter,persist for longer periods than in more energetic

Žcontinental shelf systems e.g., Bernstein et al., 1978;Jumars and Eckman, 1983; Grassle and Morse-Porte-

.ous, 1987; Gage and Tyler, 1991 . This complicatesthe study of temporal change. In bathyal systems,seasonal inputs may be sufficiently intense to gener-ate obvious fluctuations in foraminiferal faunas. Inabyssal systems, where inputs are much lower, it isparticularly difficult to discriminate between thetemporal and spatial components of population vari-ability. For example, the abundance of ‘phytodetritusspecies’ in the abyssal NE Atlantic is closely linkedto the occurrence and thickness of the phytodetrital

Ž .layer Gooday, 1996 , which is discontinuous in bothŽ .space and time Rice et al., 1994 . It is therefore

highly desirable in studies of modern temporal pro-cesses to examine at least two replicates, preferably

Žmore, from each sampling period e.g., Douglas,.1981 , although the time-consuming nature of

foraminiferal sorting will place constraints on howmany samples can be examined on a realistic timescale. It is reassuring, however, to find that temporalpatterns in deep-sea foraminiferal communities,which can be plausibly related to seasonal events, are

Žapparent even in single-sample time series Ohga.and Kitazato, 1997 .

A number of authors have pointed out that stain-able protoplasm persists after the death of the

Žforaminiferal cell e.g., Bernhard, 1989; Corliss and.Emerson, 1990; Jorissen et al., 1995 . In some cases,

foraminifera take up Rose Bengal for several monthsafter death which casts doubt on the assumed equiva-lence of stained and living populations. Protoplasmicdecay rates are likely to be further reduced in oxygendeficient sediments which may trap dormantforaminifera, leading to an exaggeration of popula-tion densities and a blurring of seasonal changesŽ .Jorissen et al., 1995 . Nevertheless, as Corliss and

Ž .Silva 1993 recognise, the fact that seasonal patternsŽare discernible at all, even in low-oxygen O F0.12

y1 . Ž .ml l settings Bernhard and Reimers, 1991 , sug-gest that protoplasm decays relatively quickly. Thisis consistent with the generally fast rate of bacterialgrowth and microbial decomposition in the deep-seaŽ .Lochte and Turley, 1988; Turley and Lochte, 1990 .Using conservative methods to recognise stained


specimens seems to provide adequate resolution ofdeep-sea foraminiferal populations. Rose Bengal iseasy to use and remains the stain of choice forstudies of community-scale processes among deep-

Ž .sea foraminifera Lutze and Altenbach, 1991 .

4.2. Controls on temporal dynamics

4.2.1. The importance of food and oxygenIn general, the deep sea is a food-limited environ-

ment and relatively stable in terms of its physicaland chemical characteristics. Thus, in quiescent ar-eas, the spatial and temporal patchiness of availablefood exerts an important influence on the ecologyand population structure of deep-sea benthic organ-

Ž .isms Grassle and Morse-Porteous, 1987 , includingforaminifera. As discussed above, oxygen availabil-ity may also be an important ecological factor, par-

Žticularly on continental margins Diaz and Rosen-.berg, 1995 . However, it seems that oxygen becomes

limiting for many foraminifera and metazoans onlywhen bottom water concentrations fall below about

y1 Ž .0.5 ml l Levin and Gage, 1998 . At higher con-centrations, the organic carbon supply plays a deci-

Žsive ecological role Rathburn and Corliss, 1994;.Jorissen et al., 1995; Levin and Gage, 1998 .

ŽThe vertical distribution of live foraminifera en-.tire populations and individual species within the

sediment is controlled largely by a combination ofŽthese two parameters Shirayama, 1984; Corliss and

Emerson, 1990; Jorissen et al., 1995; de Stigter,.1996 . In eutrophic regions, oxygen is depleted close

to the sediment surface and becomes limiting,favouring low-oxygen tolerant species. In olig-otrophic regions, most of the organic matter is rem-ineralised close to the sediment surface and thesediment is well-oxygenated to a considerable depth.Such systems are food-limited and favour near-

Ž .surface dwelling epifaunal species which are intol-erant of low oxygen concentrations. This modelŽ .called the TROX model by Jorissen et al., 1995explains many of the differences between forami-niferal faunas inhabiting the continental margins and

Ž .the central oceanic abyss Fig. 7 .Foraminiferal population dynamics can also be

largely explained by the interplay between oxygenŽand food availability. In eutrophic e.g., sublittoral

.and bathyal systems, population fluctuations will be

Ž .Fig. 7. Conceptual model the TROX model of the depth towhich foraminifera live within the sediment as a function of theavailability of food and oxygen. Modified after Jorissen et al.Ž .1995 .

driven mainly by changes in both food and oxygenŽ .availability; in oligotrophic mainly abyssal sys-

tems, they will be driven solely by changes in theŽ . Ž .food supply Jorissen et al., 1995 . de Stigter 1996 ,

who modelled oxygen-dependent population fluctua-tions, recognised three categories of species: A, withhigh reproductive potential, short life-cycle and lowtolerance to anoxia; B, with low reproductive poten-tial, relatively long life-cycle, tolerance of anoxia; C,with high reproductive potential, short life cycle,tolerance of dysoxia but poor competitive ability.With food availability held constant, population den-sities change according to the intensity and length ofperiods of oxygen deficiency. Species A flourishes

Ž y1 .under well-oxygenated conditions 5 ml l or whenoxygen minima dip down to 1 ml ly1 for only shortperiods, species B becomes dominant when oxygenminima are more persistent, whereas the opportunis-tic but poorly competitive species C can only flour-ish for short periods in systems recovering fromperiods of anoxia which are prolonged enoughŽ .several months to eliminate species A and B. As de

Ž .Stigter 1996 acknowledges, this model is simplis-tic; for example, it does not take into account habitatpartitioning which will allow less competitive speciesto avoid complete elimination. However, it does


show how fluctuating oxygen concentrations can ex-plain some of the changes in population densities

Žseen in bathyal and sublittoral systems Barma-.widjaja et al., 1992 .

Changes in organic matter inputs and oxygenavailability may lead to a migrating redox front inthe sediments which some bathyal species are able to

Žtrack Kitazato and Ohga, 1995; Ohga and Kitazato,.1997 . For example, Chilostomella oolina, a deep

infaunal species associated with levels in the sedi-ment where oxygen concentrations diminish to zero,must migrate in order to remain in its preferredmicrohabitat. This behaviour is similar to that of

Žsublittoral species in natural Barmawidjaja et al.,. Ž1992 and experimental systems Alve and Bernhard,. Ž1995 . However, in some benthic settings e.g., the

. ŽSan Pedro Basin , there is no change at a 0.5 cm.resolution in vertical distribution patterns followingŽ .food inputs Silva et al., 1996 . This may be because

oxygen hardly penetrates highly organic-rich sedi-ments such as those of the Californian Borderlandbasins and so additional organic inputs have littleimpact on pore-water oxygen profiles.

The dynamics of foraminiferal populations inlow-oxygen environments are not always dictated bysediment oxygen profiles. Some species which arehighly tolerant of oxygen deficiency, for example,

Ž .Nonionella fragilis Bernhard et al., 1997 , bloomafter increases in surface productivity in the Califor-

Ž .nia borderland e.g., Rathburn, 1998 . At the muchbetter oxygenated bathyal PSB site of Gooday and

Ž .Lambshead 1989 , species such as Eponides pusil-lus, which are not known to tolerate low oxygenlevels, also bloom following phytodetrital pulses. Aslong as they have sufficient oxygen, these oppor-tunistic bathyal foraminifera resemble their abyssal

Ž .counterparts see below by responding quickly tophytodetrital inputs.

At abyssal locations, it is the epifaunal or nearŽ .epifaunal species species A in de Stigter’s model

which respond to phytodetrital deposits, reflectingthe fact that most biological activity and biomass

Žoccur close to the sediment surface Snider et al.,1984; Corliss and Emerson, 1990; Jorissen et al.,

.1995 . Since the sediment column remains well-oxygenated to a substantial depth, foraminiferalspecies are less likely to move up and down in thesediment. However, preliminary evidence from the

Ž .PAP suggests that one species Quinqueloculina sp.migrates though at least the upper 1 cm of sedimentto the sediment–water interface when phytodetritusis present, presumably as a response to the arrival offood. Foraminifera are well-adapted to take advan-tage of these sudden food pulses. Some deep-seaspecies have physiological mechanisms which allowthem to close down their metabolism and then ‘re-

Žawaken’ quickly when presented with food Alten-.bach, 1992; Gooday et al., 1992; Linke et al., 1995 .

Time-series studies extending over more than 1year have been conducted recently at abyssal sites in

Žthe Pacific and Atlantic Oceans Baldwin et al.,.1998; Rice et al., 1998 . In both cases, there were

considerable year to year differences in the seasonalflux of organic matter to the ocean floor, suggestingthat, to some extent, each annual cycle is unique andcannot be used to predict the dynamics offoraminiferal populations during other years.

4.2.2. Other factorsThis review has been concerned largely with the

response of foraminifera to organic-matter inputs tothe ocean floor, but other disturbances may also leadto population fluctuations. Bottom current activityplays an important role in structuring benthic com-

Žmunities Thistle et al., 1985; Tyler, 1995; Aller,.1997; Gage, 1997; Thistle, 1998 and in determining

Žthe nature of foraminiferal assemblages Kaminski,.1985; Kuhnt and Collins, 1995 . The high energy

HEBBLE site, on the Nova Scotia continental rise, issubject several times a year to periods of strong

Ž .current activity ‘benthic storms’ . The foraminiferawhich live here include hormosinaceans which areknown to be good colonisers of defaunated sedi-

Žments Kaminski and Schroder, 1987; Kaminski et¨.al., 1988 . These populations are likely to undergo

fluctuations resulting from cycles of defaunation andrecolonisation, and possibly also from associatedchanges in sediment granulometry. Population densi-

Žties of isopods and harpacticoid copepods although.not polychaetes, bivalves and tanaids are reduced

following benthic storms at the HEBBLE site, proba-Ž .bly as a result of erosion Thistle et al., 1991 .

Similar processes may operate in submarine canyonsŽ .Jorissen et al., 1994 . Volcanic eruptions whichdeposit a layer of ash on the ocean floor may initiate


Žcycles over longer time scales Cita and Podenzani,.1980; Hess and Kuhnt, 1996 .

Parameters such as temperature and salinity, whichŽare virtually constant on the ocean floor Gage and

.Tyler, 1991; Tyler, 1995 , are unlikely to influenceforaminiferal population dynamics as they do inshallow water. Similarly, although specialistforaminiferal predators certainly exist in the deep-seaŽe.g., Arnold et al., 1985; Gooday et al., 1992;

.Svavarsson et al., 1993 , there is no evidence thatpredation underlies any of the temporal changes indeep-sea foraminiferal populations so far reported.However, macrofaunal exclusion experiments haveshown that predation reduces live foraminiferal den-

Žsities in shelf settings Buzas et al., 1989 and earlier.papers and so the high foraminiferal densities char-

acteristic of organically-enriched, low-oxygen sitesŽmay reflect a scarcity of macrofauna Phleger and

Soutar, 1973; Douglas, 1981; Bernhard and Reimers,.1991 . Patterns of species diversity have also been

linked to variations in the intensity of macrofaunalŽ .predation Douglas, 1981 .

4.3. Species Õs. community responses

Most deep-sea foraminiferal faunas are highlyŽ .diverse Gooday et al., 1998 . Live assemblages at

Ž .the PAP site 4850 m depth typically contain moreŽ .than 120 species Gooday, 1996 and samples from

the bathyal PSB site have yielded a similar numberŽ .Gooday, 1986; Gooday and Lambshead, 1989 . Atthese well-oxygenated localities, the seasonally fluc-tuating species are part of much larger foraminiferal

Ž .communities. As predicted by Murray 1967 , themajority of species seem to have population densitieswhich are relatively stable, or at least change in arandom, non-seasonal manner which may reflect spa-tial patchiness rather than temporal change. Someforaminiferal taxa common at abyssal depths seemparticularly unlikely to undergo population fluctua-tions. For example, komokiaceans and other large,soft-bodied taxa with diffuse protoplasm and largeaccumulations of stercomata, are probably slow-growing, equilibrium species which are well-adapted

Ž .to oligotrophic conditions Gooday et al., 1997 . Wesuggest that in well-oxygenated, food-limited deep-sea settings, only a few opportunistic species respondto ephemeral food pulses. These species appear, in a

sense, to be decoupled from the rest of the diverseforaminiferal community, most members of whichdo not show a clear, immediate response to inputs oflabile food. However, phytodetrital inputs lead to a

Žslight increase in diversity measures e.g.,.Shannon–Weiner index and a slight decrease in the

Ždominance of the top ranked species Rank 1 domi-.nance if foraminiferal populations in the phytodetri-

Žtus and sediment are treated as one entity Gooday et.al., 1998 . Whether this model applies generally to

abyssal, central oceanic foraminiferal communities isunclear.

Faunas at oxygen-limited bathyal localities aremuch less diverse than those in well-oxygenatedareas and are typically dominated by one or two

Žcalcareous species e.g., Phleger and Soutar, 1973;.Sen Gupta and Machain-Castillo, 1993 . Population

fluctuations in relation to a seasonally varying foodsupply appear to involve most of the foraminiferalspecies present, rather than a small subset of oppor-tunists. This results in sometimes substantial changesin live population densities. Presumably, there arecorresponding changes in population parameters suchas species diversity and dominance, although theseremain undocumented at present.

4.4. Palaeoceanographic significance

Seasonal and other ephemeral events leave fewdirect traces in bioturbated deep-sea sediments.Foraminiferal species which react to these eventstherefore provide valuable proxies for them in the

Žpalaeoceanographic record Schmiedl, 1995; Smart.et al., 1994 . Benthic and pelagic systems are cou-

pled to a greater or lesser extent at sublittoral, bathyalŽand abyssal depths Tyler, 1988; Graf, 1989, 1992;.Smith et al., 1994 . Hence, benthic foraminiferal

faunas will reflect the influence of short-term pro-cesses operating in the upper water column as well

Ž .as on the ocean floor Altenbach, 1992 . The follow-ing examples illustrate why the recognition of theseprocesses in ancient sediments is important.

4.4.1. Quantification of surface primary productiÕitySeveral methods which employ benthic

foraminifera to estimate the flux of organic matter tothe ocean floor, and hence, primary productivity inthe euphotic zone, have recently been developed.


These include the benthic foraminiferal accumulationŽ . Ž .rate BFAR of Herguera and Berger 1991 , based

on total foraminiferal abundance )150 mm, andvarious methods based on principal component anal-ysis of species assemblages in the )150 mmŽ . ŽGuichard et al., 1997 or )63 mm Loubere, 1991,

.1994, 1996 fractions. In central oceanic areas, andin seasonally upwelling areas on continental margins,where most primary production is concentrated withinthe spring bloom, much of the productivity signalwill be carried by small opportunistic species re-

Ž .tained in finer 63–150 mm residues. These will bemissed by analyses of palaeoproductivity which ex-clude the 63–150 mm fraction.

4.4.2. Recognition of changing climatic systemsThe change from non-seasonal to seasonal pelagic

regimes may be associated with major geologicalŽ .and climatic events. Thomas and Gooday 1996

Žshowed that around 33.5 million years ago Berggren.et al., 1995 , the relative and absolute abundance of

Žabyssal phytodetritus species Alabaminella weddel-.lensis and Epistominella exigua increased in ODP

cores from the Weddell Sea. There was no corre-sponding increase in low latitude cores. They relatedthis increase to the establishment of the AntarcticConvergence and the build up of ice on the Antarcticcontinent which possibly led to the development of amore seasonal pelagic ecosystem and the generation

Ž .of episodic phytodetrital inputs. Thomas et al. 1995also recognised an increase in the relative and abso-lute abundance of phytodetritus species during the

Žlast deglaciation in the NE Atlantic about 15,000.BP . This change was apparently associated with an

enhanced phytodetrital flux following the northwardretreat of the polar front.

The recent focus on high-resolution geologicalrecords, such as those in laminated sediments oncontinental margins, will yield palaeoenvironmentaldata which include a seasonal signal. Modern ana-logue data will be particularly valuable for interpret-ing the fossil and geochemical record of these envi-ronments.

4.4.3. Isotope studiesThe isotope and elemental chemistry of

foraminiferal tests are important tools in palaeo-ceanographic reconstructions. The assumption is usu-

ally made that shell chemistry depends largely onlong-term benthic processes, e.g., deep-ocean circu-lation. However, species with seasonally fluctuatingpopulations are strongly influenced by short-termprocesses, particularly inputs of phytodetritus origi-nating from surface primary productivity. Thesespecies probably grow mainly during short periodsof the year and their shell chemistry will reflect

Žconditions during these intervals Corliss and Silva,.1993 . The deposition of labile, isotopically light

Ž .i.e., carbon 12-enriched phytodetritus could influ-ence the shell chemistry of seasonally fluctuating

Ž . Ž .species in two ways Gooday, 1996 : 1 by theincorporation of ingested carbon into the carbonate

Ž .shell and 2 by the provision of organically-enrichedmicrohabitats. In both cases, the effect would be toincrease the carbon 12 content of the shell carbonatesecreted during periods of growth. Mackensen et al.Ž .1993 attributed anomalously light Cibicideswuellerstorfi carbon isotope values associated withhighly productive frontal zones in the Southern Ocean

Žto the influence of phytodetritus the ‘Mackensen.effect’ of McCorkle et al., 1997 . The close relation-

ship between foraminiferal carbon and oxygen iso-tope chemistry and ambient conditions may alsoprovide a means to examine palaeoenvironmentalchanges by focusing on interspecific differences in

Žisotope values. For example, McCorkle et al. 1990,.1997 suggested that long-term changes in the depth

of the oxic zone in ancient porewaters could bedetermined from differences between carbon isotopevalues in fossil epifaunal and infaunal taxa.

The use of benthic foraminifera for solving prob-lems in palaeoceanography depends on sound infor-mation regarding the autecology of modern speciesand the factors which control their abundance and

Ždistribution patterns at larger scales Gooday, 1994;.Murray, 1995 . There are many important gaps in

our understanding of these issues.

5. Conclusions

Ž .1 Strong environmental and faunal contrasts ex-Žist between bathyal continental margin slope and

.rise and abyssal central oceanic regions of the deepsea. In particular, continental margin systems experi-

Žence a much higher organic matter flux originating


.from primary production and terrigenous inputs thancentral oceanic systems which are distant from landand are overlain by a deeper water column. Thesecontrasts are reflected in the taxonomic and ecologi-cal characteristics of the foraminiferal faunas.

Ž .2 Evidence for temporal fluctuations in deep-seaforaminifera is sparse and most of it originates from

Ž .bathyal depths -1450 m on continental margins,particularly the California Borderland. At all but oneof these marginal sites, oxygen concentrations areF1.0 ml ly1. An exception is the PSB site of

Ž .Gooday and Lambshead 1989 where oxygen con-centrations are G4 ml ly1.

Ž .3 On eutrophic continental margins, where oxy-gen is limiting, foraminiferal faunas are dominatedby infaunal, high productivityrlow-oxygen tolerantspecies. Changes in the population densities of suchspecies can often be related to fluctuating pore-water

Žoxygen concentrations resulting from episodic sea-.sonal organic matter inputs. As in sublittoral sys-

tems, foraminifera may migrate up and down in thesediment, tracking critical oxygen concentrations.However, these migrations do not occur where oxy-gen penetration of the sediment is minimal through-out the year.

Ž .4 At oxygen-depleted sites where oxygen con-Žcentrations are consistently low e.g., parts of the

.California Borderland , some low-oxygen tolerantŽtaxa respond mainly to influxes of food phytodetri-

.tus originating from surface primary production.Ž .5 In typical abyssal central oceanic settings, and

more oligotrophic parts of the continental margin,the organic matter flux is not usually sufficient tocause oxygen depletion in the underlying sediments.These systems are food limited and changes in thepopulation densities of foraminiferal species arelinked to phytodetrital pulses. Unlike those at eu-trophic continental margin sites, the species con-cerned are epifaunal or shallow infaunal and can beinferred to be intolerant of low-oxygen conditions.We emphasise that the intensity of phytodetritalpulses, and hence, the population dynamics of oppor-tunistic species, varies from year to year at anyparticular locality; occasionally, they may fail en-tirely.

Ž .6 Many foraminifera which undergo seasonalfluctuations are probably opportunists. At abyssallocalities, they constitute a very small proportion of

Žhighly diverse faunas e.g., 2–3 out of )120.foraminiferal species at the PAP . Eutrophic bathyal

communities, particularly those subject to oxygendepletion, are less diverse and probably contain ahigher proportion of seasonally dynamic species. In

Žabyssal as well as bathyal systems, many but by no. Žmeans all of the foraminifera both species and.specimens which respond to food pulses are calcare-

ous. This is despite the strong decrease in the relativeand absolute abundances of calcareous foraminiferafrom the continental margin to the central oceanicabyss.

Ž .7 Other patterns of change in deep-seaforaminiferal populations are likely to occur in re-

Žsponse to unpredictable organic matter inputs e.g.,the deposition of whale carcasses, turbidite depositsand chemosynthetically-based primary production

.associated with seeps and vents which are ephemeralon a variety of time scales. Responses to these inputsare poorly-documented but the limited available evi-dence suggests that they are exploited mainly by

Ž .species adapted to low oxygen and or high produc-tivity environments. In addition, longer term fluctua-tions possibly occur over time scales of severalyears, for example, in response to oceanographic andclimatic changes which cause shifts in the extent orlocation of OMZ.

Acknowledgements

AJG thanks Professor G.J. van der Zwaan forinviting him to present a paper at the Drooger Sym-posium. AER appreciates the support of the UCshipfunds committee and is grateful to Prof. C.R.Smith for access to his whale fall samples. Themanuscript benefited from the comments of Profs.J.W. Murray and G.J. van der Zwaan, Drs. E. Alve,A.L. Rice, F. Jorissen, E. Thomas and an anonymousreviewer. We are grateful to Drs. H. Kitazato and F.Jorissen for providing copies of their published illus-

Žtrations reproduced herein as Figs. 2 and 7, respec-.tively . AJG is partly supported by the European

Union under the Marine Science and TechnologyŽ .Programme MAST III , contract MAS3-CT95-0018.

ŽAER is partly supported by the CALCOFI Cali-.fornia Cooperative Oceanic Fisheries Investigations

program, and from NOAArNURP Grants aUAF


97-0037 and 66RUO181 awarded to Levin, Rath-burn, Geiskes and Hessler. This is DEEPSEAS Pub-lication No. 39.

References

Akimoto, K., Tanaka, T., Hattori, M., Hotta, H., 1992. Recentbenthic foraminiferal assemblages around hydrothermal ventsin the Okinawa Trough, Ryukyu Islands, Japan. In: Takayanagi,

Ž .Y., Saito, T. Eds. , Studies in Benthic Foraminifera. TokaiUniv. Press, Tokyo, pp. 211–225.

Akimoto, K., Tanaka, T., Hattori, M., Hotta, H., 1994. Recentbenthic foraminiferal assemblages from the cold seep commu-nities—a contribution to the methane gas indicator. In: Tsuchi,

Ž .R. Ed. , Pacific Neogene Events in Time and Space. Univ. ofTokyo Press, Tokyo, pp. 11–25.

Aller, J.Y., 1997. Benthic community response to temporal andspatial gradients in physical disturbance within a deep-seawestern boundary region. Deep-Sea Research 44, 39–69.

Aller, J.Y., Aller, R.C., 1986. Evidence for localized enhancementof biological activity associated with tube and burrow struc-tures in deep-sea sediments at the HEBBLE site, westernNorth Atlantic. Deep-Sea Research 33, 755–790.

Altenbach, A.V., 1992. Short term processes and patterns in theforaminiferal response to organic flux rates. Marine Micropa-leontology 19, 119–129.

Alve, E., Bernhard, J.M., 1995. Vertical migratory response ofbenthic foraminifera to controlled oxygen concentrations in anexperimental mesocosm. Marine Ecology Progress Series 116,137–151.

Arnold, A.J., D’Escrivan, F., Parker, W.C., 1985. Predation andavoidance responses in the foraminifera of the Galapagoshydrothermal mounds. Journal of Foraminiferal Research 15,38–42.

Arntz, W.E., Flores, L.A., Maldonado, M., Carbajal, G., 1985.Cambios de los factores ambientales, macrobentos y bacteriasfilamentosas en la zone de minimo de oxigeno frente al Perudurante El Nino 1982–1983. In: Arntz, W.E., Landa, A.,˜

Ž .Tarazona, J. Eds. , El Nino v su impacto en la fauna marina.˜Ž .Boletin Instituto del Mar del Peru special issue , pp. 65–757.´

Arntz, W.E., Tarazona, J., Gallardo, V., Flores, L.A., Salzwedel,H., 1991. Benthos communities in oxygen deficient shelf andupper slope areas of the Peruvian and Chilean Pacific coastand changes caused by El Nino. In: Tyson, R.V., Pearson,˜

Ž .T.H. Eds. , Modern and Ancient Continental Shelf Anoxia.Geological Society, Tulsa Oklahoma, pp. 131–154.

Baldwin, R.J., Glatts, R.C., Smith, K.L. Jr., 1998. Particulatematter fluxes into the benthic boundary layer at a long time-series station in the abyssal NE Pacific: composition andfluxes. Deep-Sea Research II 45, 643–665.

Barmawidjaja, D.M., Jorissen, F.J., Puskaric, S., Van der Zwaan,G.J., 1992. Microhabitat selection by benthic Foraminifera inthe Northern Adriatic Sea. Journal of Foraminiferal Research22, 297–317.

Basson, P.W., Murray, J.W., 1995. Temporal variations in four

species of intertidal foraminifera, Bahrain, Arabian Gulf. Mi-cropaleontology 41, 69–76.

Beaulieu, S.E., Smith, K.L., 1998. Phytodetritus entering thebenthic boundary layer and aggregated on the sea floor in theabyssal NE Pacific: macro- and microscopic composition.Deep-Sea Research II 45, 781–815.

Berggren, W.A., Kent, D.V., Swisher, C.C. III, Aubry, M.-P.,1995. A revised Cenozoic geochronology and chronostratigra-phy. Society of Economic Paleontologists and Mineralogists54, 129–212.

Bernhard, J.M., 1989. The distribution of benthic Foraminiferawith respect to oxygen concentration and organic carbonlevels in shallow-water Antarctic sediments. Limnology andOceanography 34, 1131–1141.

Bernhard, J.M., Reimers, C., 1991. Benthic foraminiferal popula-tion fluctuations related to anoxia: Santa Barbara Basin. Bio-geochemistry 15, 127–149.

Bernhard, J.M., Sen Gupta, B.K., Borne, P.F., 1997. Benthicforaminiferal proxy to estimate dysoxic bottom-water oxygenconcentrations: Santa Barbara Basin, US Pacific continentalmargin. Journal of Foraminiferal Research 27, 301–310.

Bernstein, B.B., Hessler, R.R., Smith, R., Jumars, P.A., 1978.Spatial dispersion of benthic Foraminifera in the abyssal Cen-tral Pacific. Limnology and Oceanography 23, 401–416.

Billett, D.S.M., 1991. Deep-sea holothurians. Oceanography andMarine Biology Annual Review 29, 259–317.

Billett, D.S.M., Lampitt, R.S., Rice, A.L., Mantoura, R.F.C.,1983. Seasonal sedimentation of phytodetritus to the deep-seabenthos. Nature 302, 520–522.

Boltovskoy, E., Lena, H., 1969. Seasonal occurrences, standingcrop and production in benthic foraminifera of Puerto De-seado. Contributions from the Cushman Foundation forForaminiferal Research 20, 87–95.

Boltovskoy, E., Wright, R., 1976. Recent Foraminifera. Junk, TheHague, 515 pp.

Bronnimann, P., Van Dover, C.L., Whittaker, J.E., 1989.¨Abyssotherma pacifica, n. gen., n. sp.: a Recent remaneicidŽ .Foraminifera, Remaneicacea from the East Pacific Rise.Micropaleontology 35, 142–149.

Buzas, M.A., 1978. Foraminifera as prey for benthic depositfeeders: results of predator exclusion experiments. Journal ofMarine Research 36, 617–625.

Buzas, M.A., Collins, L.S., Richardson, S.L., Severin, K.P., 1989.Experiments on predation, substrate preference, and coloniza-tion of benthic foraminifera at the shelfbreak off the Ft. PierceInlet, Florida. Journal of Foraminiferal Research 19, 146–152.

Campos-Creasey, L.C., Tyler, P.A., Gage, J.D., John, A.W.G.,1994. Evidence for coupling the vertical flux of phytodetritusto the diet and seasonal life history of the deep-sea echinoidEchinus affinis. Deep-Sea Research 41, 188–369.

Cita, M.B., Podenzani, M., 1980. Destructive effects of oxygenstarvation and ash falls on benthic life: a pilot study. Quater-nary Research 13, 230–241.

Cooper, L.H.N., 1952. Physical and chemical oceanography of thewaters bathing the continental slope of the Celtic Sea. Journalof the Marine Biological Association of the United Kingdom30, 465–510.


Corliss, B.H., 1985. Microhabitats of benthic foraminifera withindeep-sea sediments. Nature 314, 435–438.

Corliss, B.H., 1991. Morphology and microhabitat preferences ofbenthic foraminifera from the northwest Atlantic Ocean. Ma-rine Micropaleontology 17, 195–236.

Corliss, B.H., Emerson, S., 1990. Distribution of Rose Bengalstained deep-sea benthic foraminifera from the Nova Scotiancontinental margin and Gulf of Maine. Deep-Sea Research 37,381–400.

Corliss, B., Silva, K.A., 1993. Rapid growth of deep-sea benthicforaminifera. Geology 21, 991–994.

de Stigter, H.C., 1996. Recent and fossil benthic foraminifera inthe Adriatic Sea: distribution patterns in relation to organiccarbon flux and oxygen concentration at the seabed. GeologicaUltraiectina. Mededelingen van de Faculteit Aardwetenschap-pen Universiteit Utrecht, No. 44, 254 pp.

Diaz, R.J., Rosenberg, R., 1995. Marine benthic hypoxia: a reviewof its ecological effects and the behavioural responses of thebenthic macrofauna. Oceanography and Marine Biology An-nual Review 33, 245–303.

Douglas, R.G., 1981. Paleoecology of continental margin basins: amodern case history from the borderland of Southern Califor-

Ž .nia. In: Douglas, R.G., et al. Eds. , Depositional Systems ofActive Continental Margin Basins. Society of Economic Pale-ontologists and Mineralogists, Pacific Section, Bakersfield,CA, pp. 121–156.

Drazen, J.C., Baldwin, R.J., Smith, K.L., 1998. Sediment commu-nity response to a temporally varying food supply at anabyssal station in the NE Pacific. Deep-Sea Research II 45,893–913.

Erskian, M.G., Lipps, J.H., 1987. Population dynamics of theŽ .foraminiferan Glabratella ornatissima Cushman in northern

California. Journal of Foraminiferal Research 17, 240–256.Fariduddin, M., Loubere, P., 1997. The surface ocean productivity

response of deeper water benthic foraminifera in the AtlanticOcean. Marine Micropaleontology 32, 289–310.

Gage, J.D., 1997. High benthic species diversity in deep-seasediments: the importance of hydrodynamics. In: Ormond,

Ž .R.F.G., Gage, J.D., Angel, M.V. Eds. , Marine Biodiversity:Patterns and Processes. Cambridge Univ. Press, pp. 148–177.

Gage, J.D., Tyler, P.A., 1991. Deep-Sea Biology. A NaturalHistory of Organisms at the Deep-Sea Floor. Cambridge Univ.Press, Cambridge, 504 pp.

Gallardo, V.A., 1985. Efectos del fenomeno de El Nino sobre el´ ˜bentos sublitoral frente a Concepcion, Chile. In: Arntz, W.,´

Ž .Landa, A., Tarazona, J. Eds. , El Nino y su impacto en la˜fauna marina. Instituto del Mar del Peru, Boletin Extraordi-´nario, pp. 79–85.

Gooday, A.J., 1986. Meiofaunal foraminiferans from the bathyalŽ .Porcupine Seabight northeast Atlantic : size structure, stand-

ing stock, taxonomic composition, species diversity and verti-cal distribution in the sediment. Deep-Sea Research 33, 1345–1373.

Gooday, A.J., 1988. A response by benthic foraminifera to phy-todetritus deposition in the deep-sea. Nature 332, 70–73.

Gooday, A.J., 1993. Deep-sea benthic foraminiferal species whichexploit phytodetritus: characteristic features and controls ondistribution. Marine Micropaleontology 22, 187–205.

Gooday, A.J., 1994. The biology of deep-sea foraminifera: areview of some advances and their applications in paleo-ceanography. Palaios 9, 14–31.

Gooday, A.J., 1996. Epifaunal and shallow infaunal foraminiferalcommunities at three abyssal NE Atlantic sites subject todiffering phytodetritus regimes. Deep-Sea Research 43, 1395–1431.

Gooday, A.J., Lambshead, P.J.D., 1989. Influence of seasonallydeposited phytodetritus on benthic foraminiferal populations inthe bathyal northeast Atlantic. Marine Ecology Progress Series58, 53–67.

Gooday, A.J., Turley, C.M., 1990. Responses by benthic organ-isms to inputs of organic material to the ocean floor. Philo-sophical Transactions of the Royal Society of London, SeriesA 331, 119–138.

Gooday, A.J., Levin, L.A., Linke, P., Heeger, T., 1992. The roleof benthic foraminifera in deep-sea food webs and carbon

Ž .cycling. In: Rowe, G.T., Pariente, V. Eds. , Deep-Sea FoodChains and the Global Carbon Cycle. Kluwer Academic Pub-lishers, The Netherlands, pp. 63–91.

Gooday, A.J., Shires, R., Jones, A.R., 1997. Large deep-seaagglutinated foraminifera: two differing kinds of organisationand their possible ecological significance. Journal ofForaminiferal Research 27, 278–291.

Gooday, A.J., Bett, B.J., Shires, R., Lambshead, P.J.D., 1998.Deep-sea benthic foraminiferal species diversity in the NEAtlantic and NW Arabian Sea: a synthesis. Deep-Sea ResearchII 45, 165–201.

Graf, G., 1989. Benthic–pelagic coupling in a deep-sea commu-nity. Nature 341, 437–439.

Graf, G., 1992. Benthic–pelagic coupling: a benthic view.Oceanography and Marine Biology Annual Review 30, 149–190.

Grassle, J.F., 1986. The ecology of deep-sea hydrothermal ventcommunities. Advances in Marine Biology 23, 301–362.

Grassle, J.F., Morse-Porteous, N.J., 1987. Macrofaunal colonisa-tion of disturbed deep-sea environments and the structure ofdeep-sea benthic communities. Deep-Sea Research 20, 643–659.

Griggs, G.B., Carey, A.G. Jr., Kulm, L.D., 1969. Deep-sea sedi-mentation and sediment–fauna interaction in Cascadia Chan-nel and on Cascadia Abyssal Plain. Deep-Sea Research 16,157–170.

Guichard, S., Jorissen, F., Bertrand, P., Gervais, A., Martinez, P.,Peypouquet, J.-P., Pujol, C., Vergnaud-Grazzini, 1997.Foraminiferes benthiques et paleoproductivite: reflexions sur` ´ ´ ´

Ž .une carotte de l’upwelling NW africain . Compte RenduesAcademie des Sciences Paris, Sciences de la terre et des`planetes 325, 65–70.`

Hedges, J.I., Keil, R.G., 1995. Sedimentary organic matter preser-vation: an assessment and speculative synthesis. MarineChemistry 49, 81–115.

Herguera, J.C., Berger, W.H., 1991. Paleoproductivity from ben-thic foraminifera abundance: glacial to postglacial change inthe west-equatorial Pacific. Geology 19, 1173–1176.

Hess, S., Kuhnt, W., 1996. Deep-sea benthic foraminiferal recolo-nization of the 1991 Mt. Pinatubo ash layer in the South ChinaSea. Marine Micropaleontology 28, 171–197.


Høvland, M., Judd, A.G., 1988. Seabed Pockmarks and Seepages,Impact on Geology, Biology and the Marine Environment.Graham and Trotman Publ., London, 293 pp.

Jahnke, R.A., 1996. The global ocean flux of particulate organiccarbon: areal distribution and magnitude. Global Biogeochem-ical Cycles 10, 71–88.

Jahnke, R.A., Jackson, G.A., 1987. Role of sea floor organisms inthe deep North Pacific Ocean. Nature 329, 621–623.

Jahnke, R.A., Reimers, C.E., Craven, D.B., 1990. Intensificationof recycling of organic matter at the sea floor near oceanmargins. Nature 348, 50–54.

Jonasson, K.E., Schroder-Adams, C.J., Patterson, R.T., 1995.¨Benthic foraminiferal distribution at Middle Valley, Juan deFuca Ridge, a northeast Pacific hydrothermal venting site.Marine Micropaleontology 25, 151–167.

Jones, R.W., 1993. Preliminary observations on benthonicforaminifera associated with biogenic gas seep in the North

Ž .Sea. In: Jenkins, D.G. Ed. , Applied Micropaleontology.Kluwer Academic Publishers, The Netherlands, pp. 69–91.

Jones, R.W., 1996. Preliminary observations on benthonicforaminifera associated with petroleum seeps. In: Jones, R.W.Ž .Ed. , Micropaleontology in Petroleum Exploration. OxfordUniv. Press, New York, pp. 179–196.

Jorissen, F.J., Buzas, M.B., Culver, M.B., Culver, S.J., Kuehl,S.A., 1994. Vertical distribution of living benthic foraminiferain submarine canyons off New Jersey. Journal of ForaminiferalResearch 24, 28–36.

Jorissen, F.J., de Stigter, H.C., Widmark, J.G.V., 1995. A concep-tual model explaining benthic foraminiferal microhabitats. Ma-rine Micropaleontology 26, 3–15.

Jumars, P.A., Eckman, J.E., 1983. Spatial structure within deep-seaŽ .benthic communities. In: Rowe, G.T. Ed. , The Sea, Vol. 8.

Wiley, New York, pp. 399–451.Jumars, P.A., Mayer, L.M., Deming, J.W., Baross, J.A.,

Wheatcroft, R.A., 1990. Deep-sea deposit-feeding strategiessuggested by environmental and feeding constraints. Philo-sophical Transactions of the Royal Society of London, SeriesA 331, 85–101.

Kaminski, M.A., 1985. Evidence for control of abyssal aggluti-nated foraminiferal community structure by substrate distur-bance: results from the HEBBLE area. Marine Geology 66,113–131.

Kaminski, M.A., 1988. Cenozoic deep-water agglutinatedforaminifera in the North Atlantic. Unpublished Doctoral Dis-sertation, CambridgerWoods Hole, MA, MITrWoods HoleOceanographic Inst., 262 pp.

Kaminski, M.A., Schroder, C.J., 1987. Environmental analysis of¨deep-sea agglutinated foraminifera: can we distinguish tranquilfrom disturbed environments? Gulf Coast Section SEPMFoundation Eighth Annual Research Conference. Selected pa-pers and illustrated abstracts, pp. 90–93.

Kaminski, M.A., Grassle, J.F., Whitlach, R.B., 1988. Life historyand recolonisation among agglutinated foraminifera in the

Ž .Panama Basin. In: Gradstein, M.F., Rogl, F. Eds. , Second¨Workshop on Agglutinated Foraminifera. Abhandlungen derGeologischen Bundesanstalt, Wien 41, 229–243.

Kaminski, M.A., Al Hassawi, A.M., Kuhnt, W., 1997. Seasonality

in microhabitats of rose bengal stained deep-sea benthicforaminifera from the New Jersey continental margin. In:

Ž .Hass, H.C., Kaminski, M.A. Eds. , Contributions to the Mi-cropaleontology and Paleoceanography of the Northern NorthAtlantic. Grzybowski Foundation Special Publication, No. 5,pp. 245–248.

Kitazato, H., 1996. Benthic foraminifera associated with coldseepages: discussion of their faunal characteristics and adapta-tions. Fossils 60, 48–52.

Kitazato, H., Ohga, T., 1995. Seasonal changes in deep-sea ben-thic foraminiferal populations: results of long-term observa-

Ž .tions at Sagami Bay, Japan. In: Sakai, H., Nozami, Y. Eds. ,Biogeochemical Processes and Ocean Flux in the Western

Ž .Pacific. Terra Scientific Publishing TERRAPUB , Tokyo, pp.331–342.

Kitazato, H., Shirayama, Y., 1996. Rapid creation of a reducedenvironment and an early stage of a chemosynthetic commu-nity on cattle bones at the deep-sea bottom in Sagami Bay,central Japan. Vie Milieu 46, 1–5.

Kuhnt, W., Collins, E.S., 1995. Fragile abyssal foraminifera fromthe northwestern Sargasso Sea: distribution, ecology, and pale-oceanographic significance. In: Kaminski, M.A., Geroch, S.,

Ž .Gasinski, M.A. Eds. , Proceedings of the Fourth InternationalWorkshop on Agglutinated Foraminifera, Krakow Poland,´September 12–19, 1993, Vol. 3. Grzybowski Foundation Spe-cial Publication, pp. 159–172.

Lambshead, P.J.D., Gooday, A.J., 1990. The impact of seasonallydeposited phytodetritus on epifaunal and shallow infaunalbenthic foraminiferal populations in the bathyal northeast At-lantic: the assemblage response. Deep-Sea Research 37, 1263–1283.

Lampitt, R.S., Billett, D.M.S., Rice, A.L., 1986. Biomass of theinvertebrate megabenthos from 500 m to 4100 m in thenortheast Atlantic. Marine Biology 93, 69–81.

Lee, J.J., Muller, W.A., Stone, R.J., McEnery, M.E., Zucker, W.,1969. Standing crop of foraminifera in sublittoral epiphyticcommunities of a Long Island salt marsh. Marine Biology 4,44–61.

Lee, J.J., Anderson, O.R., Karim, B., Beri, J., 1991. Additionalinsight into the structure and biology of Abyssotherma paci-

Ž .fica Bronnimann, Van Dover and Whittaker . Micropaleontol-¨ogy 37, 303–312.

Levin, L.A., Gage, J.D., 1998. Relationships between oxygen,organic matter and the diversity of bathyal macrofauna. Deep-Sea Research II 45, 129–163.

Levin, L.A., Blair, N., DeMaster, D., Plaia, G., Fornes, W.,Martin, C., 1997. Rapid subduction of organic matter bymaldanid polychaetes on the North Carolina Slope. Journal ofMarine Research 55, 595–611.

Linke, P., 1992. Metabolic adaptations of deep-sea benthicforaminifera to seasonally varying food input. Marine EcologyProgress Series 81, 51–63.

Linke, P., Lutze, G.F., 1993. Microhabitat preferences of benthicforaminifera—a static concept or a dynamic adaptation tooptimize food acquisition. Marine Micropaleontology 20,215–234.

Linke, P., Altenbach, A.V., Graf, G., Heeger, T., 1995. Response


of deep-sea benthic foraminifera to a simulated sedimentationevent. Journal of Foraminiferal Research 25, 75–82.

Lochte, K., 1992. Bacterial standing stock and consumption oforganic carbon in the benthic boundary layer of the abyssal

Ž .North Atlantic. In: Rowe, G.T., Pariente, V. Eds. , Deep-SeaFood Chains and the Global Carbon Cycle. Kluwer AcademicPublishers, The Netherlands, pp. 1–10.

Lochte, K., Turley, C.M., 1988. Bacteria and cyanobacteria asso-ciated with phytodetritus in the deep-sea. Nature 333, 67–69.

Loubere, P., 1991. Deep-sea benthic foraminiferal assemblageresponse to a surface ocean productivity gradient: a test.Paleoceanography 6, 193–204.

Loubere, P., 1994. Quantitative estimation of surface ocean pro-ductivity and bottom water oxygen concentration using ben-thic foraminifera. Paleoceanography 9, 727–737.

Loubere, P., 1996. The surface ocean productivity and bottomwater oxygen signals in deep water benthic foraminiferalassemblages. Marine Micropaleontology 28, 247–261.

Lutze, G.F., Altenbach, A., 1991. Technik und Signifikanz derLebendfarbung benthischer Foraminiferen mit Bengalrot. Ge-¨ologisches Jahrbuch 128, 251–265.

Lutze, G.F., Coulbourne, W.T., 1984. Recent benthic foraminiferafrom the continental margin of northwest Africa: communitystructure and distribution. Marine Micropaleontology 8, 361–401.

Mackensen, A., Hald, M., 1988. Cassidulina teretis Tappan andC. laeÕigata d’Orbigny: their modern and late Quaternarydistribution in northern Seas. Journal of Foraminiferal Re-search 18, 16–24.

Mackensen, A., Sejrup, H.P., Jansen, E., 1985. The distribution ofliving benthic foraminifera on the continental margin and riseoff southwest Norway. Marine Micropaleontology 9, 275–306.

Mackensen, A., Hubberten, H.-W., Bickert, T., Fischer, G.,Futterer, D.K., 1993. The d

13C in benthic foraminiferal tests¨Ž . 13of Fontbotia wuellerstorfi Schwager relative to the d C of

dissolved inorganic carbon in Southern Ocean deep water:implications for glacial ocean circulation models. Paleo-ceanography 8, 587–610.

Mackensen, A., Schmiedl, G., Harloff, J., Giese, M., 1995. Deep-sea foraminifera in the South Atlantic Ocean: ecology andassemblage generation. Micropaleontology 41, 342–358.

Masson, D.G., Kenyon, N.H., Weaver, P.P.E., 1996. Slides, debrisflows, and turbidity currents. In: Summerhayes, C.P., Thorpe,

Ž .S.A. Eds. , Oceanography, An Illustrated Guide. MansonPublishing, London, pp. 136–151.

McCorkle, D.C., Keigwin, L.D., Corliss, B.H., Emerson, S.R.,1990. The influence of microhabitats on carbon isotopic com-position of deep-sea benthic foraminifera. Paleoceanography5, 161–185.

McCorkle, D.C., Corliss, B.H., Farnham, C., 1997. Vertical distri-Ž .butions and stable isotopic compositions of live stained

benthic foraminifera from the North Carolina and Californiacontinental margins. Deep-Sea Research 44, 983–1024.

Merrett, N.R., Haedrich, R.L., 1997. Deep-Sea Demersal Fish andFisheries. Chapman & Hall, London, 282 pp.

Molina-Cruz, A., Ayala-Lopez, A., 1988. Influence of hydrother-´mal vents on the distribution of benthic foraminifera from theGuaymas Basin, Mexico. Geo-Marine Letters 8, 49–56.

Mullins, H.T., Thompson, J.B., McDougall, K., Vercoutere, T.L.,1985. Oxygen-minimum zone edge effects: evidence from thecentral California coastal upwelling system. Geology 13, 491–494.

Murray, J.W., 1967. Production in benthic foraminiferids. Journalof Natural History 1, 61–68.

Murray, J.W., 1983. Population dynamics of benthic foraminifera:results from the Exe Estuary, England. Journal of ForaminiferalResearch 13, 1–12.

Murray, J.W., 1995. Microfossils as indicators of oceanic watermasses, circulation and climate. In: Bosence, D.W., Allison,

Ž .P.A. Eds. , Marine Palaeoenvironmental Analysis from Fos-sils, Vol. 83. Geological Society of London Special Publica-tion, pp. 245–264.

Myers, E.H., 1943. Life activities of foraminifera in relation tomarine ecology. Proceedings of the American PhilosophicalSociety 86, 439–458.

Nienstedt, J.C., Arnold, A.J., 1988. The distribution of benthicforaminifera on seamounts near the East Pacific Rise. Journalof Foraminiferal Research 18, 237–249.

Ohga, T., Kitazato, H., 1997. Seasonal changes in bathyalforaminiferal populations in response to the flux of organic

Ž .matter Sagami Bay, Japan . Terra Nova 9, 33–37.Pfannkuche, O., 1992. Organic carbon flux through the benthic

community in the temperate abyssal northeast Atlantic. In:Ž .Rowe, G.T., Pariente, V. Eds. , Deep-Sea Food Chains and

the Global Carbon Cycle. Kluwer Academic Publishers, TheNetherlands, pp. 183–198.

Pfannkuche, O., 1993. Benthic foraminiferal response to the sedi-mentation of particulate organic matter at the BIOTRANSstation 478N, 208W. Deep-Sea Research II 40, 135–149.

Phleger, F.B., Soutar, A., 1973. Production of benthic foraminiferain three east Pacific oxygen minima. Micropaleontology 19,110–115.

Quinterno, P., 1994. Quaternary foraminifers from EscanabaTrough, Northeast Pacific Ocean. In: Morton, J.L., Zierenberg,

Ž .R.A., Reiss, C.A. Eds. , Geologic, Hydrothermal and Bio-logic Studies at Escanaba Trough, Gorda Ridge, OffshoreNorthern California. US Geological Survey Bulletin 2022, pp.337–359.

Ž .Rathburn, A.E., 1996. Inter-annual variation in living staineddeep-sea benthic foraminiferal assemblages from the Southern

Ž .Californian Margin abstract . EOS, Transactions AmericanGeophysical Union 77, 308.

Ž .Rathburn, A.E., 1998. Living stained deep-sea benthicforaminifera from the Southern California margin: relationship

Ž .to productivity abstract . EOS, Transactions of the AmericanGeophysical Union 79, 4.

Rathburn, A.E., Corliss, B.H., 1994. The ecology of deep-seabenthic foraminifera from the Sulu Sea. Paleoceanography 9,87–150.

Rathburn, A.E., Corliss, B.H., Tappa, K.D., Lohmann, K.C.,1996. Comparisons of the ecology and stable isotopic compo-

Ž .sitions of living stained deep-sea benthic foraminifera fromthe Sulu and South China Seas. Deep-Sea Research 43, 1617–1646.

Resig, J.M., Glenn, C.R., 1997. Foraminifera encrusting phos-phatic hardgrounds of the Peruvian upwelling zone: taxonomy,


geochemistry, and distribution. Journal of Foraminiferal Re-search 27, 133–150.

Rice, A.L., Billett, D.S.M., Fry, J., John, A.W.G., Lampitt, R.S.,Mantoura, R.F.C., Morris, R.J., 1986. Seasonal deposition ofphytodetritus to the deep-sea floor. Proceedings of the RoyalSociety of Edinburgh B 88, 265–279.

Rice, A.L., Thurston, M.H., Bett, B.J., 1994. The IOSDLDEEPSEAS programme: introduction and photographic evi-dence for the presence and absence of a seasonal input ofphytodetritus at contrasting abyssal sites in the northeast At-lantic. Deep-Sea Research 41, 1305–1320.

Rice, A.L., Gage, J.D., Lampitt, R.S., Pfannkuche, O., Sibuet, M.,1998. BENGAL: High resolution temporal and spatial study ofthe benthic biology and geochemistry of a north-east Atlanticabyssal locality. In: Third European Marine Science and Tech-nology Conference, Lisbon 23–27 May 1998. Project Syn-opses: Volume 1. Marine Systems. Luxembourg Office forOfficial Publications of the European Communities, pp. 23–27.

Rowe, G.T., 1983. Biomass and production of the deep-sea ben-Ž .thos. In: Rowe, G.T. Ed. , The Sea, Vol. 8. Wiley-Intersci-

ence, New York, pp. 97–121.Rowe, G.T., Staresinic, N., 1979. Sources of organic matter to the

deep-sea benthos. Ambio Special Report 6, 19–24.Schaff, T., Levin, L., Blair, N., DeMaster, D., Pope, R., Boehme,

S., 1992. Spatial heterogeneity of benthos on the North Car-Ž .olina continental slope: large 100 km-scale variation. Marine

Ecology Progress Series 88, 143–160.Schmiedl, G., 1995. Rekonstruktion der spatquartaren Tiefen-¨ ¨

wasserzirkulation und Productivitat im ostlichen Sudatlantik¨ ¨ ¨anhand von benthischen Foraminiferenvergesellschaftungen.Berichte zur Polarforschung, No. 160, pp. 1–207.

Schmiedl, G., Mackensen, A., Mller, P.J., 1997. Recent benthicforaminifera from the eastern South Atlantic Ocean: depen-dence on food supply and water masses. Marine Micropaleon-tology 32, 49–287.

Schnitker, D., 1995. Deep-sea benthic foraminifera: food andbottom water masses. In: Zahn, R., Pederson, T., Kaminski,

Ž .M., Labeyrie, L. Eds. , Carbon Cycling in the Glacial Ocean:Constraints on the Oceans Role in Global Change. Springer,Berlin, Heidelberg, pp. 539–554.

Sen Gupta, B.K., Aharon, P., 1994. Benthic foraminifera ofbathyal hydrocarbon vents of the Gulf of Mexico: initial reporton communities and stable isotopes. Geo-Marine Letters 14,88–96.

Sen Gupta, B.K., Machain-Castillo, M.L., 1993. Benthicforaminifera in oxygen-poor habitats. Marine Micropaleontol-ogy 20, 183–201.

Sen Gupta, B.K., Platon, E., Bernhard, J.M., Aharon, P., 1997.Foraminiferal colonization of hydrocarbon-seep bacterial matsand underlying sediment, Gulf of Mexico slope. Journal ofForaminiferal Research 27, 292–300.

Shirayama, Y., 1984. Vertical distribution of meiobenthos in thesediment profile in bathyal, abyssal and hadal deep sea sys-tems of the Western Pacific. Oceanologica Acta 7, 120–129.

Sibuet, M., Olu, K., 1998. Biogeography, biodiversity and fluiddependence of deep-sea cold-seep communities at active andpassive margins. Deep-Sea Research II 45, 517–567.

Silva, K.A., Corliss, B.C., Rathburn, A.E., Thunnell, R.C., 1996.Seasonality of living benthic foraminifera from the San PedroBasin, California Borderland. Journal of Foraminiferal Re-search 26, 71–93.

Smart, C.W., King, S.C., Gooday, A.J., Murray, J.W., Thomas,E., 1994. A benthic foraminiferal proxy of pulsed organicmatter paleofluxes. Marine Micropaleontology 23, 89–99.

Smith, C.R., 1985. Food for the deep sea: utilization, dispersal andflux of nekton falls at the Santa Catalina Basin floor. Deep-SeaResearch 32A, 417–442.

Smith, C.R., 1986. Nekton falls, low-intensity disturbance andcommunity structure of infaunal benthos in the deep sea.Journal of Marine Research 44, 567–600.

Smith, K.L., Baldwin, R.J., 1984. Seasonal fluctuations in deep-seasediment community oxygen consumption: central and easternNorth Pacific. Nature 307, 624–625.

Smith, C.R., Hessler, R.R., 1987. Colonisation and succession indeep-sea ecosystems. Trends in Ecology and Evolution 2,359–363.

Smith, C.R., Kukert, H., Wheatcroft, R.A., Jumars, P.A., Deming,J.W., 1989. Vent fauna on whale remains. Nature 341, 27–28.

Smith, K.L., Kaufmann, R.S., Baldwin, R.J., 1994. Coupling ofnear-bottom pelagic and benthic processes at abyssal depths inthe eastern North Pacific Ocean. Limnology and Oceanogra-phy 39, 1101–1118.

Smith, C.R., Hoover, D.J., Doan, S.E., Pope, R.H., DeMaster,D.J., Dobbs, F.C., Altabet, M.A., 1996. Phytodetritus at theabyssal seafloor across 108 of latitude in the central equatorialPacific. Deep-Sea Research 43, 1309–1338.

Smith, C.R., Maybaum, H.L., Baco, A.R., Pope, R.H., Carpenter,S.D., Yager, P.L., Macko, S.A., Deming, J.W., 1998. Sedi-ment community structure around a whale skeleton in the deepNortheast Pacific: macrofaunal, microbial and bioturbationeffects. Deep-Sea Research II 45, 335–364.

Snelgrove, P.V.R., Grassle, J.F., Petrecca, R.F., 1994. Macrofau-nal response to artificial enrichments and depressions in adeep-sea habitat. Journal of Marine Research 52, 45–369.

Snelgrove, P.V.R., Grassle, J.F., Petrecca, R.F., 1996. Experimen-tal evidence for ageing of food patches as a factor contributingto high deep-sea macrofaunal diversity. Limnology andOceanography 41, 605–614.

Snider, L.J., Burnett, B.R., Hessler, R.R., 1984. The compositionand distribution of meiofauna and nanobiota in a central NorthPacific deep-sea area. Deep-Sea Research 31, 225–1249.

Soetaert, K., Herman, P.M.J., Middelburg, J.J., 1996. Dynamicresponse of deep-sea sediments to seasonal variations: a model.Limnology and Oceanography 41, 1651–1668.

Soltwedel, T., 1997. Meiobenthos distribution pattern in the tropi-cal East Atlantic: indication for fractionated sedimentation oforganic matter to the sea floor?. Marine Biology 129, 747–756.

Svavarsson, J., Gudmundsson, G., Brattegard, T., 1993. FeedingŽ . Ž .by asellote isopods Crustacea on foraminifers Protozoa in

the deep sea. Deep-Sea Research 40, 1225–1239.Thiel, H., 1983. Meiobenthos and nanobenthos of the deep sea. In:

Ž .G.T. Rowe Ed. , The Sea, Vol. 8. Wiley-Interscience, NewYork, pp. 167–230.

Thiel, H., Pfannkuche, O., Schriever, G., Lochte, K., Gooday,


A.J., Hemleben, Ch., Mantoura, R.F.C., Turley, C.M., Patch-ing, J.W., Riemann, F., 1990. Phytodetritus on the deep-seafloor in a central oceanic region of the northeast Atlantic.Biological Oceanography 6, 203–239.

Thistle, D., 1998. Harpacticoid diversity at two physically re-worked sites in the deep sea. Deep-Sea Research 45, 13–24.

Thistle, D., Yingst, J.Y., Fauchald, K., 1985. A deep-sea benthiccommunity exposed to strong bottom currents on the Scotian

Ž .Rise Western Atlantic . Marine Geology 66, 91–112.Thistle, D., Ertman, S.C., Fauchald, K., 1991. The fauna of the

HEBBLE site: patterns in standing stock and sediment-dy-namic effects. Marine Geology 99, 413–422.

Thomas, E., Gooday, A.J., 1996. Cenozoic deep-sea benthicforaminifera: tracers for changes in oceanic productivity?Geology 24, 355–358.

Thomas, E., Booth, L., Maslin, M., Shackelton, N.J., 1995. North-eastern Atlantic benthic foraminifera during the last 45,000years: changes in productivity seen from the bottom up.Paleoceanography 10, 545–562.

Thurston, M.H., Bett, B.J., Rice, A.L., Jackson, P.A.B., 1994.Variations in the invertebrate abyssal megafauna in the NorthAtlantic Ocean. Deep-Sea Research 41, 1321–1348.

Tietjen, J.H., 1992. Abundance and biomass of metazoanmeiobenthos in the deep sea. In: Rowe, G.T., Pariente, V.Ž .Eds. , Deep-Sea Food Chains and the Global Carbon Cycle.Kluwer Academic Publishers, The Netherlands, pp. 45–62.

Turley, C.M., Lochte, K., 1990. Microbial response to the input offresh detritus to the deep-sea bed. Palaeogeography, Palaeocli-matology, Palaeoecology 89, 3–23.

Turley, C.M., Gooday, A.J., Green, J.C., 1993. Maintenance ofabyssal benthic foraminifera under high pressure and lowtemperature: some preliminary results. Deep-Sea Research 40,643–652.

Tyler, P.A., 1988. Seasonality in the deep sea. Oceanography andMarine Biology Annual Review 26, 227–258.

Tyler, P.A., 1995. Conditions for the existence of life at thedeep-sea floor: an update. Oceanography and Marine BiologyAnnual Review 33, 221–244.

van Dover, C.L., Berg, C.J., Turner, R.D., 1988. Recruitment ofmarine invertebrates to hard substrates at deep-sea hydrother-mal vents on the East Pacific Rise and Galapagos spreadingcenter. Deep-Sea Research 35, 1833–1849.

Vanreusel, A., Van den Bossche, I., Thiermann, F., 1997. Free-living marine nematodes from hydrothermal sediments: simi-larities with communities from diverse reduced habitats. Ma-rine Ecology Progress Series 157, 207–219.

Wada, H., Naganuma, T., Fujioka, K., Kitazato, H., Kawamura,K., Akazawa, Y., 1994. The discovery of the Torishima whale

Ž .bone animal community TOWBAC and its meaning. JAM-STEC Journal of Deep-Sea Research 10, 37–47.

Walsh, J.J., 1991. Importance of the continental margins in themarine biogeochemical cycling of carbon and nitrogen. Nature350, 53–55.

Weaver, P.P.E., Rothwell, R.G., Ebbing, J., Gunn, D., Hunter,P.M., 1992. Correlation, frequency of emplacement and sourcedirections of megaturbidites on the Madeira Abyssal Plain.Marine Geology 109, 1–20.

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