benthic foram-2001

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BENTHIC FORAMINIFERA

A. J. Gooday, Southampton Oceanography Centre,

Southampton, UK

Copyright & 2001 Elsevier Ltd.

This article is reproduced from the 1st edition of Encyclopedia of Ocean

Sciences, volume 1, pp 274286, & 2001, Elsevier Ltd.

Introduction

Foraminifera are enormously successful organismsand a dominant deep-sea life form. These amoeboidprotists are characterized by a netlike (granulor-eticulate) system of pseudopodia and a life cycle thatis often complex but typically involves an alternationof sexual and asexual generations. The most obvious

characteristic of foraminifera is the presence of ashell or test that largely encloses the cytoplasmicbody and is composed of one or more chambers. Insome groups, the test is constructed from foreignparticles (e.g., mineral grains, sponge spicules, shellsof other foraminifera) stuck together (agglutinated)by an organic or calcareous/organic cement. In oth-ers, it is composed of calcium carbonate (usuallycalcite, occasionally aragonite) or organic materialsecreted by the organism itself.

Although the test forms the basis of foraminiferalclassification, and is the only structure to survive

fossilization, the cell body is equally remarkable andimportant. It gives rise to the complex, highly mo-bile, and pervasive network of granuloreticulosepseudopodia. These versatile organelles perform avariety of functions (locomotion, food gathering, testconstruction, and respiration) that are probablyfundamental to the ecological success of foraminiferain marine environments.

As well as being an important component ofmodern deep-sea communities, foraminifera have anoutstandingly good fossil record and are studiedintensively by geologists. Much of their research usesknowledge of modern faunas to interpret fossilassemblages. The study of deep-sea benthic for-aminifera, therefore, lies at the interface betweenbiology and geology. This articles addresses boththese facets.

History of Study

Benthic foraminifera attracted the attention of somepioneer deep-sea biologists in the late 1860s. Themonograph of H.B. Brady, published in 1884 and

based on material collected in the Challenger round-

the-world expedition of 187276, still underpins ourknowledge of the group. Later biological expeditionsadded to this knowledge. For much of the 1900s,

however, the study of deep-sea foraminifera wasconducted largely by geologists, notably J.A. Cush-man, F.B. Phleger, and their students, who amassedan extensive literature dealing with the taxonomyand distribution of calcareous and other hard-shelledtaxa. In recent decades, the emphasis has shiftedtoward the use of benthic species in paleoceano-graphic reconstructions. Interest in deep-sea for-aminifera has also increased among biologists sincethe 1970s, stimulated in part by the description ofthe Komokiacea, a superfamily of delicate, soft-shelled foraminifera, by O.S. Tendal and R.R.

Hessler. This exclusively deep-sea taxon is a domin-ant component of the macrofauna in some abyssalregions.

Morphological and Taxonomic

Diversity

Foraminifera are relatively large protists. Their testsrange from simple agglutinated spheres a few tens ofmicrometers in diameter to those of giant tubular

species that reach lengths of 10 cm or more. How-ever, most are a few hundred micrometers in size.They exhibit an extraordinary range of morphologies(Figures 1 and 2), including spheres, flasks, varioustypes of branched or unbranched tubes, and cham-bers arranged in linear, biserial, triserial, or coiled(spiral) patterns. In most species, the test has anaperture that assumes a variety of forms and issometimes associated with a toothlike structure. Thekomokiaceans display morphologies not tradition-ally associated with the foraminifera. The test formsa treelike, bushlike, spherical, or lumpish body that

consists of a complex system of fine, branchingtubules (Figure 2AC).

The foraminifera (variously regarded as a sub-phylum, class, or order) are highly diverse witharound 900 living genera and an estimated 10 000described living species, in addition to large numbersof fossil taxa. Foraminiferal taxonomy is based verylargely on test characteristics. Organic, agglutinated,and different kinds of calcareous wall structure serveto distinguish the main groupings (orders or sub-orders). At lower taxonomic levels, the nature andposition of the aperture and the number, shape, and

arrangement of the chambers are important.

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Methodology

Qualitative deep-sea samples for foraminiferal stud-ies are collected using nets (e.g., trawls) that aredragged across the seafloor. Much of the Challengermaterial studied by Brady was collected in this way.

Modern quantitative studies, however, require the

use of coring devices. The two most popular corersused in the deep sea are the box corer, which obtainsa large (e.g., 0.25 m2) sample, and the multiple corer,which collects simultaneously a battery of up to 12smaller cores. The main advantage of the multiplecorer is that it obtains the sedimentwater interface

in a virtually undisturbed condition.

(A) (B)

(C) (D) (E)

(F) (G) (H)

Figure 1 Scanning electron micrographs of selected deep-sea foraminifera (maximum dimensions are given in parentheses).

(A) Epistominella exigua; 4850 m water depth, Porcupine Abyssal Plain, NE Atlantic (190mm). (B) Nonionella iridea; 1345 m depth,

Porcupine Seabight, NE Atlantic (110 mm). (C) Nonionella stella; 550 m depth, Santa Barbara Basin, California Borderland (220 mm).

(D) Brizalina tumida; 550 m depth, Santa Barbara Basin, California Borderland (680mm). (E) Melonis barleaanum; 1345 m depth,

Porcupine Seabight, NE Atlantic (450 mm). (F) Hormosina sp., 4495 m depth, Porcupine Abyssal Plain (1.5 mm). (G) Pyrgoella

sp.; 4550 m depth, foothills of Mid-Atlantic Ridge (620mm). (H) Technitella legumen; 9971037m depth, NW African margin (8 mm).

(A)(E) and (G) have calcareous tests, (F) and (H) have agglutinated tests. (C) and (D), photographs courtesy of Joan Bernhard.

BENTHIC FORAMINIFERA 337


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Foraminifera are extracted from sieved sedimentresidues. Studies are often based on dried residuesand concern total assemblages (i.e. including bothlive and dead individuals). To distinguish individualsthat were living at the time of collection from deadtests, it is necessary to preserve sediment samples in

either alcohol or formalin and then stain them with

rose Bengal solution. This colors the cytoplasm redand is most obvious when residues are examined inwater. Stained assemblages provide a snapshot of theforaminifera that were living when the samples werecollected. Since the live assemblage varies in bothtime and space, it is also instructive to examine the

dead assemblage that provides an averaged view of

(A) (B)

(C) (D) (E)

(F)

(G)

(H)

(I) (J)(K)

Figure 2 Light micrographs of deep-sea foraminifera (maximum dimensions are given in parentheses). (A) Species of Lanain which

pad-like test consists of tightly meshed system of fine tubules; 5432 m water depth, Great Meteor East region, NE Atlantic (7.4 mm).

(B) Septumasp.; same locality (2 mm). (C) Edgertoniamudball; same locality (3.8 mm). (D) Hormosina globulifera; 4004 m depth, NW

African margin (6.4 mm). (E) Rhabdammina parabyssorum; 3392 m depth, Oman margin, NW Arabian Sea (18mm). (F) Leptohalysis

sp.; 3400 m depth, Oman margin, NW Arabian Sea (520 mm). (G) Minute species of Hyperammina; 3400 m depth, Oman margin, NW

Arabian Sea (400 mm). (H) Lenticulariasp.; 9971037 m depth, NW African margin (2.5 mm). (I, J) Biloculinellasp.; 4004m depth, NW

African margin (3 mm). (K) Spherical allogromiid; 3400 m depth, Oman margin, NW Arabian Sea (105 mm). Specimens illustrated in

(A)(G) have agglutinated tests, in (H)(J) calcareous tests and in (K) an organic test. (A)(C) belong to the superfamily Komokiacea.

338 BENTHIC FORAMINIFERA


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the foraminiferal fauna. Deep-sea foraminiferalassemblages are typically very diverse and thereforefaunal data are often condensed mathematically byusing multivariate approaches such as principalcomponents or factor analysis.

The mesh size of the sieve strongly influences thespecies composition of the foraminiferal assemblageretained. Most deep-sea studies have been based on>63mm, 125 mm, 150mm, 250mm, or even 500 mmmeshes. In recent years, the use of a fine 63 mm meshhas become more prevalent with the realization thatsome small but important species are not adequatelyretained by coarser sieves. However, the additionalinformation gained by examining fine fractions mustbe weighed against the considerable time and effortrequired to sort foraminifera from them.

Ecology Abundance and Diversity

Foraminifera typically make up >50% of the soft-bottom, deep-sea meiofauna (Table 1). They arealso often a major component of the macrofauna.

In the central North Pacific, for example, for-aminifera (mainly komokiaceans) outnumber allmetazoans combined by at least an order of mag-nitude. A few species are large enough to be easilyvisible to the unaided eye and constitute part of themegafauna. These include the tubular speciesBathysiphon filiformis, which is sometimes abun-dant on continental slopes (Figure 3). Some xeno-phyophores, agglutinated protists that are probablyclosely related to the foraminifera, are even larger(up to 24 cm maximum dimension!). These giantprotists may dominate the megafauna in regions ofsloped topography (e.g., seamounts) or high surfaceproductivity. In well-oxygenated areas of the deep-seafloor, foraminiferal assemblages are very speciesrich, with well over 100 species occurring in rela-tively small volumes of surface sediment (Figure 4).Many are undescribed delicate, soft-shelled forms.

There is an urgent need to describe at least some ofthese species as a step toward estimating globallevels of deep-sea species diversity. The commonspecies are often widely distributed, particularly atabyssal depths, although endemic species un-doubtedly also occur.

Table 1 The percentage contribution of foraminifera to the deep-sea meiofauna at sites where bottom water is well oxygenated

Area Depth (m) Percentage of foraminifera Number of samples

NW AtlanticOff North Carolina 5002500 11.090.4 14

Off North Carolina 4004000 7.685.9 28

Off Marthas Vineyard 146567 3.410.6 4

NE Atlantic

Porcupine Seabight 1345 47.059.2 8

Porcupine Abyssal Plaina 4850 61.876.3 3

Madeira Abyssal Plaina 4950 61.476.1 3

Cape Verde Abyssal Plaina 4550 70.2 1

Off Mauretania 2504250

427

26

461N, 16171W 40004800 0.58.3 9

Indian Ocean

NW Arabian Sea

b

3350 54.4 1Pacific

Western Pacific 20006000 36.069.3 11

Central North Pacific 58215874 49.5 2

Arctic 10002600 14.584.1 74

Southern Ocean 16611680 2.223.7 2

aData from Gooday AJ (1996) Epifaunal and shallow infaunal foraminiferal communities at three abyssal NE Atlantic sites subject to

differing phytodetritus input regimes. Deep-Sea Research I 43: 13951421.bData from Gooday AJ, Bernhard JM, Levin LA and Suhr SB (2000) Foraminifera in the Arabian Sea oxygen minimum zone and other

oxygen-deficient settings: taxonomic composition, diversity, and relation to metazoan faunas. Deep-Sea Research II 47: 2554.

Based on Gooday AJ (1986) Meiofaunal foraminiferans from the bathyal Porcupine Seabight (northeast Atlantic): size structure,

standing stock, taxonomic composition, species diversity and vertical distribution in the sediment. Deep-Sea Research 35: 1345

1373; with permission from Elsevier Science.



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Foraminifera are also a dominant constituent ofdeep-sea hard-substrate communities. Dense popu-lations encrust the surfaces of manganese nodules as

well as experimental settlement plates deployed on

the sea floor for periods of months. They includevarious undescribed matlike taxa and branchedtubular forms, as well as a variety of small coiledagglutinated species (many in the superfamily Tro-chamminacea), and calcareous forms.

Role in Benthic Communities

The abundance of foraminifera suggests that they playan important ecological role in deep-sea communities,although many aspects of this role remain poorlyunderstood. One of the defining features of theseprotists, their highly mobile and pervasive pseudopo-dial net, enables them to gather food particles veryefficiently. As a group, foraminifera exhibit a widevariety of trophic mechanisms (e.g., suspension feed-ing, deposit feeding, parasitism, symbiosis) and diets(herbivory, carnivory, detritus feeding, use of dis-

solved organic matter). Many deep-sea species appearto feed at a low trophic level on organic detritus,sediment particles, and bacteria. Foraminifera areprey, in turn, for specialist deep-sea predators (sca-phopod mollusks and certain asellote isopods), andalso ingested (probably incidentally) in large numbersby surface deposit feeders such as holothurians. Theymay therefore provide a link between lower andhigher levels of deep-sea food webs.

Some deep-sea foraminifera exhibit opportunisticcharacteristics rapid reproduction and populationgrowth responses to episodic food inputs. Well-

known examples are Epistominella exigua, Alaba-minella weddellensis and Eponides pusillus. Thesesmall (generally o200mm), calcareous species feedon fresh algal detritus (phytodetritus) that sinksthrough the water column to the deep-ocean floorafter the spring bloom (a seasonal burst of phyto-plankton primary production that occurs moststrongly in temperate latitudes). Utilizing energyfrom this labile food source, they reproduce rapidlyto build up large populations that then decline whentheir ephemeral food source has been consumed.Moreover, certain large foraminifera can reduce

their metabolism or consume cytoplasmic reserveswhen food is scarce, and then rapidly increase theirmetabolic rate when food again becomes available.These characteristics, together with the sheer abun-dance of foraminifera, suggest that their role in thecycling of organic carbon on the deep-seafloor is verysignificant.

The tests of large foraminifera are an importantsource of environmental heterogeneity in the deepsea, providing habitats and attachment substrates forother foraminifera and metazoans. Mobile infaunalspecies bioturbate the sediment as they move through

it. Conversely, the pseudopodial systems of

Species ordered by rank0

20

40

60

80

100

120

Numbersper25cm

2

Figure 4 Deep-sea foraminiferal diversity: all species from a

single multiple corer sample collected at the Porcupine Abyssal

Plain, NE Atlantic (4850 m water depth), ranked by abundance.

Each bar represents one live (rose Bengal-stained) species. The

sample was 25.5 cm2 surface area, 01 cm depth, and sieved on

a 63 mm mesh sieve. It contained 705 live specimens and 130

species.

Figure 3 Bathysiphon filiformis, a large tubular agglutinated

foraminifer, photographed from the Johnson Sealink submersible

on the North Carolina continental slope (850 m water depth). The

tubes reach a maximum length of about 10 cm. (Photograph

courtesy of Lisa Levin.)



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foraminifera may help to bind together and stabilizedeep-sea sediments, although this has not yet beenclearly demonstrated.

Microhabitats and Temporal Variability

Like many smaller organisms, foraminifera resideabove, on and within deep-sea sediments. Variousfactors influence their overall distribution patternwithin the sediment profile, but food availability andgeochemical (redox) gradients are probably the mostimportant. In oligotrophic regions, the flux of organicmatter (food) to the seafloor is low and most for-aminifera live on or near the sediment surface wherefood is concentrated. At the other extreme, in eu-trophic regions, the high organic-matter flux causespore water oxygen concentrations to decrease rapidlywith depth into the sediment, restricting access to the

deeper layers to those species that can tolerate lowoxygen levels. Foraminifera penetrate most deeplyinto the sediment where organic inputs are of inter-mediate intensity and the availability of food andoxygen within the sediment is well balanced.

Underlying these patterns are the distributions ofindividual species. Foraminifera occupy more or lessdistinct zones or microenvironments (microhabitats).For descriptive purposes, it is useful to recognize anumber of different microhabitats: epifaunal andshallow infaunal for species living close to the sedi-ment surface (upper 2 cm); intermediate infaunal for

species living between about 1 cm and 4 cm (Figure 5);and deep infaunal for species that occur at depths

down to 10 cm or more (Figure 6). A few deep-waterforaminifera, including the well-known calcareousspecies Cibicidoides wuellerstorfi, occur on hardsubstrates (e.g., stones) that are raised above thesedimentwater interface (elevated epifaunal micro-habitat). There is a general relation between testmorphotypes and microhabitat preferences. Epifaunaland shallow infaunal species are often trochospiralwith large pores opening on the spiral side of the test;infaunal species tend to be planispiral, spherical, orovate with small, evenly distributed pores. It is im-portant to appreciate that foraminiferal microhabitatsare by no means fixed. They may vary between sitesand over time and are modified by the burrowingactivities of macrofauna. Foraminiferal microhabitatsshould therefore be regarded as dynamic rather thanstatic. This tendency is most pronounced in shallow-water settings where environmental conditions are

more changeable and macrofaunal activity is moreintense than in the deep sea.The microhabitats occupied by species reflect the

same factors that constrain the overall distributionpatterns of foraminifera within the sediment. Epi-faunal and shallow infaunal species cannot toleratelow oxygen concentrations and also require a diet ofrelatively fresh organic matter. Deep infaunal for-aminifera are less opportunistic but are more tolerantof oxygen depletion than are species living close tothe sedimentwater interface (Figure 6). It has beensuggested that species of genera such as Globobuli-

mina may consume either sulfate-reducing bacteriaor labile organic matter released by the metabolic

0 20 400

1

2

3

4

5

0 5 0 5 10 5

0 20 0 10

0

1

2

3

4

5

(A) (B) (C)

(F)(E)(D)

Number of specimens

Depthinsediment(cm)

Figure 5 Vertical distribution patterns within the top 5 cm of sediment of common foraminiferal species (live, rose Bengal-stained

specimens) in the Porcupine Seabight, NW Atlantic (511360N, 131000W; 1345 m water depth). Based on 463mm sieve fraction. (A)

Ovammina sp. (mean of 20 samples). (B) Nonionella iridea (20 samples). (C) Leptohalysis aff. catenata (7 samples). (D) Melonis

barleeanum (9 samples). (E) Haplophragmoides bradyi (19 samples). (F) Turritellella laevigata (21 samples). (Amended and

reprinted from Gooday AJ (1986) Meiofaunal foraminiferans from the bathyal Porcupine Seabight (northeast Atlantic): size structure,

standing stock, taxonomic composition, species diversity and vertical distribution in the sediment. Deep-Sea Research 35: 1345

1373; permission from Elsevier Science.)



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activities of these bacteria. These species move closerto the sediment surface as redox zones shift upwardin the sediment under conditions of extreme oxygendepletion. Although deep-infaunal foraminifera mustendure a harsh microenvironment, they are exposedto less pressure from predators and competitors thanthose occupying the more densely populated surfacesediments.

Deep-sea foraminifera may undergo temporalfluctuations that reflect cycles of food and oxygenavailability. Changes over seasonal timescales in theabundance of species and entire assemblages havebeen described in continental slope settings (Fig-ure 7). These changes are related to fluctuations inpore water oxygen concentrations resulting fromepisodic (seasonal) organic matter inputs to the sea-floor. In some cases, the foraminifera migrate up anddown in the sediment, tracking critical oxygen levelsor redox fronts. Population fluctuations also occur inabyssal settings where food is a limiting ecological

factor. In these cases, foraminiferal population dy-namics reflect the seasonal availability of phytode-tritus (food). As a result of these temporalprocesses, living foraminifera sampled during oneseason often provide an incomplete view of the livefauna as a whole.

Environmental Controls on Foraminiferal

Distributions

Our understanding of the factors that control thedistribution of foraminifera on the deep-ocean floor

is very incomplete, yet lack of knowledge has not

prevented the development of ideas. It is likely thatforaminiferal distribution patterns reflect a combin-ation of influences. The most important first-orderfactor is calcium carbonate dissolution. Above thecarbonate compensation depth (CCD), faunas in-clude calcareous, agglutinated, and allogromiid taxa.Below the CCD, calcareous species are almost en-tirely absent. At oceanwide or basinwide scales, the

organic carbon flux to the seafloor (and its season-ality) and bottom-water hydrography appear to beparticularly important, both above and below theCCD.

Studies conducted in the 1950s and 1960s em-phasized bathymetry (water depth) as an importantcontrolling factor. However, it soon became apparentthat the bathymetric distribution of foraminiferalspecies beyond the shelf break is not consistentgeographically. Analyses of modern assemblages inthe North Atlantic, carried out in the 1970s, revealeda much closer correlation between the distribution of

foraminiferal species and bottom-water masses. Forexample, Cibicidoides wuellerstorfi was linked toNorth Atlantic Deep Water (NADW) and Nuttallidesumbonifera to Antarctic Bottom Water (AABW). Atthis time, it was difficult to explain how slightphysical and chemical differences between watermasses could influence foraminiferal distributions.However, recent work in the south-east Atlantic,where hydrographic contrasts are strongly de-veloped, suggests that the distributions of certainforaminiferal species are controlled in part by thelateral advection of water masses. In the case of

N. umboniferus there is good evidence that the main

0 10 20 30 40 50

Intermediate anddeep infauna, number of specimens

0.25

1.25

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3.25

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5.25

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Oxygen ( mol l )_1

0 20 40 60 80100120140160

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10Nitrate ( mol l )

_1

(A) (B) (C)

0 100 200 300 400 500

Number of stainedforaminifera

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Depth

insediment(cm)

Figure 6 Vertical distribution of (A) total live (rose Bengal-stained) foraminifera), (B) pore water oxygen and nitrate concentrations,

and (C) intermediate and deep infaunal foraminiferal species within the top 10 cm of sediment on the north-west African margin

(21128.80N, 17157.20W, 1195 m). All foraminiferal counts based on 4150 mm sieve fraction, standardized to a 34 cm3 volume. Species

are indicated as follows: Pullenia salisburyi(black), Melonis barleeanum(crossed pattern), Chilostomella oolina(honeycomb pattern),

Fursenkoina mexicana (grey), Globobulimina pyrula (diagonal lines), Bulimina marginata (large dotted pattern). (Adopted and

reprinted from Jorissen FJ, Wittling I, Peypouquet JP, Rabouille C and Relexans JC (1998) Live benthic foraminiferal faunas off Cape

Blanc, northwest Africa: community structure and microhabitats. Deep-Sea Research I 45: 21572158; with permission from Elsevier

Science.)



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factor is the degree of undersaturation of the bottomwater in calcium carbonate. This abyssal species isfound typically in the carbonate-corrosive (and

highly oligotrophic) environment between the calcitelysocline and the CCD, a zone that may coincideapproximately with AABW. Where water masses aremore poorly delineated, as in the Indian and PacificOceans, links with faunal distributions are less clear.

During the past 15 years, attention has focused onthe impact on foraminiferal ecology of organicmatter fluxes to the seafloor. The abundance of deadforaminiferal shells 4150mm in size correlates wellwith flux values. There is also compelling evidencethat the distributions of species and species associ-ations are linked to flux intensity. Infaunal species,

such as Melonis barleeanum, Uvigerina peregrina,

Chilostomella ovoidea and Globobulimina affinis,predominate in organically enriched areas, e.g. be-neath upwelling zones. Epifaunal species such as

Cibicidoides wuellerstorfi and Nuttallides umboni-fera are common in oligotrophic areas, e.g. the cen-tral oceanic abyss. In addition to flux intensity, thedegree of seasonality of the food supply (i.e., whetherit is pulsed or continuous) is a significant factor.Epistominella exigua, one of the opportunists thatexploit phytodetritus, occurs in relatively oligo-trophic areas where phytodetritus is depositedseasonally.

Recent analysis of a large dataset relating therelative abundance of live (stained) foraminiferalassemblages in the north-east Atlantic and Arctic

Oceans to flux rates to the seafloor has provided a

0

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Totalnumbersof

livingbenthicforaminifera(per10cm

)2

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3.03.5 Oxygenatedlayer(cm)

345 8 1112 2 3 5 7 9 11 4 6 12 5 9 12

1991 1992 1993 1994

(A)

(B)

(C)

Others

Fursenkoinasp.1

Bolivina pacifica

Textularia kattegatensis

Uvigerinaspp.

Bolivina spissa

Bulimina aculeata

Globobuliminaspp.

Chilostomella ovoidea

Figure 7 Seasonal changes over a 4-year period (March 1991 to December 1994) in (A) the thickness of the oxygenated layer, (B)

the total population density of live benthic foraminifera, and (C) the abundances of the most common species at a 1450 m deep site in

Sagami Bay, Japan. (Reprinted from Ohga T and Kitazato H (1997) Seasonal changes in bathyal foraminiferal populations in response

to the flux of organic matter (Sagami Bay, Japan). Terra Nova 9: 3337; with permission from Blackwell Science Ltd.)



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quantitative framework for these observations. Al-though species are associated with a wide flux range,this range diminishes as a species become relativelymore abundant and conditions become increasinglyoptimum for it. When dominant occurrences (i.e.,where species represent a high percentages of thefauna) are plotted against flux and water depth,species fall into fields bounded by particular flux anddepth values (Figure 8). Despite a good deal ofoverlap, it is possible to distinguish a series ofdominant species that succeed each other bath-ymetrically on relatively eutrophic continental slopesand other species that dominate on the more oligo-trophic abyssal plains.

Other environmental attributes undoubtedlymodify the species composition of foraminiferalassemblages in the deep sea. Agglutinated specieswith tubular or spherical tests are found in areas

where the seafloor is periodically disturbed by strongcurrents capable of eroding sediments. Forms pro-jecting into the water column may be abundantwhere steady flow rates convey a continuous supplyof suspended food particles. Other species associ-ations may be linked to sedimentary characteristics.

Low-Oxygen Environments

Oxygen availability is a particularly important eco-logical parameter. Since oxygen is consumed during

the degradation of organic matter, concentrations ofoxygen in bottom water and sediment pore water areinversely related to the organic flux derived fromsurface production. In the deep sea, persistent oxy-gen depletion (O2o1 m l l

1) occurs at bathyal depths(o1000 m) in basins (e.g., on the California Bor-derland) where circulation is restricted by a sill andin areas where high primary productivity resultingfrom the upwelling of nutrient-rich water leads to thedevelopment of an oxygen minimum zone (OMZ;e.g., north-west Arabian Sea and the Peru margin).Subsurface sediments also represent an oxygen-lim-ited setting, although oxygen penetration is generallygreater in oligotrophic deep-sea sediments than infine-grained sediments on continental shelves.

On the whole, foraminifera exhibit greater toler-ance of oxygen deficiency than most metazoan taxa,although the degree of tolerance varies among species.

Oxygen probably only becomes an important limitingfactor for foraminifera at concentrations well below1 ml l1. Some species are abundant at levels of 0.1 mll1 or less. A few apparently live in permanently an-oxic sediments, although anoxia sooner or later re-sults in death when accompanied by highconcentrations of hydrogen sulfide. Oxygen-deficientareas are characterized by high foraminiferal densitiesbut low, sometimes very low (o10), species numbers.This assemblage structure (high dominance, low spe-cies richness) arises because (i) low oxygen

0.1 1 10 100

Flux of organic carbon (g m y )_ 2 _1

20

1000

100

Waterdepth(m)

1 Tetragonostomia rhombiformis2 Nonion asterizans3 Trifarina fornasinii4 Rupertina stabilis5 Bolivina albatrossi

6 Sphaeroidina bulloides7 Hoeglundina elegans8 Pyrgo murrhina9 Eponides tumidulus and

Stetsonia arctica

10 30 100

300

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4 5

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Figure 8 Dominant live (rose Bengal-stained) occurrences of foraminiferal species in relation to water depth and flux or organic

carbon to seafloor in the North Atlantic from the Guinea Basin to the Arctic Ocean. Each open circle corresponds to a data point. The

polygonal areas indicate the combination of water depth and flux conditions under which nine different species are a dominant faunal

component. The diagonal lines indicate levels of primary production (10, 30, 100, 300 g m2 y1) that result in observed flux rates.

Based on 4250mm sieve fraction plus 63250 mm fraction from Guinea Basin and Arctic Ocean. (Reprinted from Altenbach AV,

Pflaumann U, Schiebel R et al. (1999) Scaling percentages and distribution patterns of benthic foraminifera with flux rates of organic

carbon. Journal of Foraminiferal Research 29: 173185; with permission from The Cushman Foundation.)



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concentration acts as a filter that excludes non-toler-ant species and (ii) the tolerant species that do surviveare able to flourish because food is abundant andpredation is reduced. Utrastructural studies of somespecies have revealed features, e.g., bacterial sym-bionts and unusually high abundances of peroxi-somes, that may be adaptations to extreme oxygendepletion. In addition, mitachondria-laden pseudo-podia have the potential to extend into overlyingsediment layers where some oxygen may be present.

Many low-oxygen-tolerant foraminifera belong tothe Orders Rotaliida and Buliminida. They oftenhave thin-walled, calcareous tests with either flat-tened, elongate biserial or triserial morphologies(e.g., Bolivina, Bulimina, Globobulimina, Fursen-koina, Loxotomum, Uvigerina) or planispiral/len-ticular morphologies (e.g., Cassidulina,Chilostomella, Epistominella, Loxotomum, Nonion,

Nonionella). Some agglutinated foraminifera, e.g.,

Textularia, Trochammina (both multilocular), Bath-ysiphon, and Psammosphaera (both unilocular), arealso abundant. However, miliolids, allogromiids, andother soft-shelled foraminifera are generally rare inlow-oxygen environments. It is important to notethat no foraminiferal taxon is currently known to beconfined entirely to oxygen-depleted environments.

Deep-Sea Foraminifera in

Paleo-Oceanography

Geologists require proxy indicators of importantenvironmental variables in order to reconstruct an-cient oceans. Benthic foraminifera provide goodproxies for seafloor parameters because they arewidely distributed, highly sensitive to environmentalconditions, and abundant in Cenozoic and Cret-

aceous deep-sea sediments (note that deep-sea

Table 2 Benthic foraminiferal proxies or indicators (both faunal and chemical) useful in paleo-oceanographic reconstruction

Environmental parameter/property Proxy or indicator Remarks

Water depth Bathymetric ranges of abundant

species in modern oceans

Depth zonation largely local although

broad distinction between shelf,

slope and abyssal depth zones

possible

Distribution of bottom water masses Characteristic associations of epifaunal

species

Relations between species and water

masses may reflect lateral advection

Carbonate corrosiveness of bottom

water

Abundance of Nuttallides umbonifera Corrosive bottom water often broadly

corresponds to Antarctic Bottom

Water

Deep-ocean thermohaline circulation Cd/Ca ratios and d13C values for

calcareous tests

Proxies reflect age of bottom

watermasses; i.e., period of time

elapsed since formation at ocean

surface

Oxygen-deficient bottom-water and

pore water

Characteristic species associations;

high-dominance, low-diversity

assemblages

Species not consistently associated

with particular range of oxygen

concentrations and also found in

high-productivity areas

Primary productivity Abundance of foraminiferal tests

4150mm

Transfer function links productivity to

test abundance (corrected for

differences in sedimentation rates

between sites) in oxygenatedsediments

Organic matter flux to seafloor (i) Assemblages of high productivity

taxa (e.g. Globobulimina, Melonis

barleeanum)

Assemblages indicate high organic

matter flux to seafloor, with or without

corresponding decrease in oxygen

concentrations

(ii) Ratio between infaunal and epifaunal

morphotypes

(iii) Ratio between planktonic and

benthic tests

Seasonality in organic matter flux Relative abundance of phytodetritus

species

Reflects seasonally pulsed inputs of

labile organic matter to seafloor

Methane release Large decrease (23%) in d13C values

of benthic and planktonic tests

Inferred sudden release of 12C enriched

methane from clathrate deposits

following temperature rise



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sediments older than the middle Jurassic age havebeen destroyed by subduction, except where pre-served in ophiolite complexes).

Foraminiferal faunas, and the chemical tracerspreserved in the tests of calcitic species, can be usedto reconstruct a variety of paleoenvironmental par-ameters and attributes. The main emphasis has beenon organic matter fluxes and bottom-water/porewater oxygen concentrations (inversely related par-ameters), the distribution of bottom-water masses,and the development of thermohaline circulation(Table 2). Modern deep-sea faunas became estab-lished during the Middle Miocene (1015 millionyears ago), and these assemblages can often be in-terpreted in terms of modern analogues. This ap-proach is difficult or impossible to apply to sedimentsfrom the Cretaceous and earlier Cenozoic, whichcontain many foraminiferal species that are now ex-

tinct. In these cases, it can be useful to work with testmorphotypes (e.g., trochospiral, cylindrical, biserial/triserial) rather than species. The relative abundanceof infaunal morphotypes, for example, has been usedas an index of bottom-water oxygenation or relativeintensities of organic matter inputs. The trace element(e.g., cadmium) content and stable isotope (d13C; i.e.,the deviation from a standard 12C : 12C ratio)chemistry of the calcium carbonate shells of benthicforaminifera provide powerful tools for makingpaleo-oceanographic reconstructions, particularlyduring the climatically unstable Quaternary period.

The cadmium/calcium ratio is a proxy for the nutrient(phosphate) content of sea water that reflects abyssalcirculation patterns. Carbon isotope ratios also reflectdeep-ocean circulation and the strength of organicmatter fluxes to the seafloor.

It is important to appreciate that the accuracy withwhich fossil foraminifera can be used to reconstructancient deep-sea environments is often limited. Theselimitations reflect the complexities of deep-sea for-aminiferal biology, many aspects of which remainpoorly understood. Moreover, simple relationshipsbetween the composition of foraminiferal assemblagesand environmental variables are elusive, and it is oftendifficult to identify faunal characteristics that can beused as precise proxies for paleo-oceanographic par-ameters. For example, geologists often wish to es-tablish paleobathymetry. However, the bathymetricdistributions of foraminiferal species are inconsistent

and depend largely on the organic flux to the seafloor,which decreases with increasing depth (Figure 8) andis strongly influenced by surface productivity. Thus,foraminifera can be used only to discriminate in ageneral way between shelf, slope, and abyssal faunas,but not to estimate precise paleodepths. Oxygenconcentrations and organic matter inputs are par-ticularly problematic. Certain species and morpho-types dominate in low-oxygen habitats that also areusually characterized by high organic loadings.However, the same foraminifera may occur in or-ganically enriched settings where oxygen levels are

0

5000

10000

15000

20000

25000

30000

35000

40000

45000

0 3000 6000 9000

Number per gramPhytodetritus species,

YD

0 25 50 75 1000

5000

10000

15000

20000

25000

30000

35000

40000

45000

Phytodetritus species,Relative abundance

YD

H1

H2

H3

H4

Figure 9 (A) Absolute (specimens per gram of dry sediment) and (B) relative (percentage) abundances of Alabaminella

weddellensis and Epistominella exigua (463 mm fraction) in a long-sediment core from the North Atlantic (50141.30N, 21151.90W,

3547 m water depth). In modern oceans, these two species respond to pulsed inputs of organic matter (phytodetritus) derived from

surface primary production. Note that they increased in abundance around 15 000 years ago, corresponding to the main Northern

Hemisphere deglaciation and the retreat of the Polar Front. Short period climatic fluctuations (YDYounger Dryas; H14Heinrich

events, periods of very high meltwater production) are also evident in the record of these two species. (Reprinted from Thomas E,

Booth L, Maslin M and Shackleton NJ (1995). Northeast Atlantic benthic foraminifera during the last 45 000 years: change in

productivity seen from the bottom up. Paleoceanography: 10: 545562; with permission from the American Geophysical Union.)



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not severely depressed, making it difficult for paleo-oceanographers to disentangle the influence of thesetwo variables. Finally, biological factors such asmicrohabitat preferences and the exploitation ofphytodetrital aggregates (floc) influence the stableisotope chemistry of foraminiferal tests.

There are many examples of the use of benthicforaminiferal faunas to interpret the geological his-tory of the oceans. Only one is given here. Corescollected at 501410N, 211520W (3547 m water depth)and 581370N, 191260W (1756 m water depth) wereused by E. Thomas and colleagues to study changesin the North Atlantic over the past 45 000 years. Thecores yielded fossil specimens of two foraminiferalspecies, Epistominella exigua and Alabaminellaweddellensis, both of which are associated withseasonal inputs of organic matter (phytodetritus) inmodern oceans. In the core from 511N, these phy-

todetritus species were uncommon during the lastglacial maximum but increased sharply in absoluteand relative abundance during the period of degla-ciation 15 00016 000 years ago (Figure 9). At thesame time there was a decrease in the abundance ofNeogloboquadrina pachyderma, a planktonic fora-minifer found in polar regions, and an increase in theabundance of Globigerina bulloides, a planktonicspecies characteristic of warmer water. These chan-ges were interpreted as follows. Surface primaryproductivity was low at high latitudes in the glacialNorth Atlantic, but was much higher to the south of

the Polar Front. At the end of the glacial period, theice sheet shrank and the Polar Front retreatednorthwards. The 511N site was now overlain bymore productive surface water characterized by astrong spring bloom and a seasonal flux of phyto-detritus to the seafloor. This episodic food sourcefavored opportunistic species, particularly E. exiguaand A. weddellensis, which became much moreabundant both in absolute terms and as a proportionof the entire foraminiferal assemblage.

Conclusions

Benthic foraminifera are a major component of deep-sea communities, play an important role in ecosystemfunctioning and biogeochemical cycling, and are

enormously diverse in terms of species numbers andtest morphology. These testate (shell-bearing) protistsare also the most abundant benthic organisms pre-served in the deep-sea fossil record and providepowerful tools for making paleo-oceanographic re-constructions. Our understanding of their biology hasadvanced considerably during the last two decades,although much remains to be learnt.

See also

Abrupt Climate Change. Anthropogenic Trace

Elements in the Ocean. Benthic Organisms

Overview. Cenozoic Oceans Carbon Cycle

Models. Deep-Sea Fauna. Floc Layers.

Macrobenthos. Meiobenthos. Microphytobenthos.

Ocean Carbon System, Modeling of. Phytoplankton

Blooms. Primary Production Processes.

Radiocarbon. Stable Carbon Isotope Variations in

the Ocean. Tracers of Ocean Productivity.

Further Reading

Fischer G and Wefer G (1999) Use of Proxies inPaleoceanography: Examples from the South Atlantic.Berlin: Springer-Verlag.

Gooday AJ, Levin LA, Linke P, and Heeger T (1992) Therole of benthic foraminifera in deep-sea food webs andcarbon cycling. In: Rowe GT and Pariente V (eds.)Deep-Sea Food Chains and the Global Carbon Cycle ,pp. 63--91. Dordrecht: Kluwer Academic.

Jones RW (1994) The Challenger Foraminifera. Oxford:Oxford University Press.

Loeblich AR and Tappan H (1987) Foraminiferal Generaand their Classification, vols 1, 2. New York: VanNostrand Reinhold.

Murray JW (1991) Ecology and Palaeoecology of BenthicForaminifera. New York: Wiley; Harlow: LongmanScientific and Technical.

SenGupta BK (ed.) (1999) Modern Foraminifera.Dordrecht: Kluwer Academic.

Tendal OS and Hessler RR (1977) An introduction to thebiology and systematics of Komokiacea. GalatheaReport 14: 165--194, plates 926.

Van der Zwan GJ, Duijnstee IAP, den Dulk M, et al. (1999)Benthic foraminifers:: proxies or problems? A review ofpaleoecological concepts. Earth Sciences Reviews 46:213--236.


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