benthic foraminiferal biogeography: controls on global...

MA04CH10-Gooday ARI 12 November 2011 11:51

Benthic ForaminiferalBiogeography: Controls onGlobal Distribution Patternsin Deep-Water SettingsAndrew J. Gooday1 and Frans J. Jorissen2

1National Oceanography Centre, University of Southampton, Southampton SO14 3ZH,United Kingdom; email: [email protected] of Recent and Fossil Bio-Indicators, University of Angers 2, 49045 Angers Cedex,France; Laboratoire d’Etude des Bio-Indicateurs Marins, Ker Chalon, 85350 Ile D’Yeu, France;email: [email protected]

Annu. Rev. Mar. Sci. 2012. 4:237–62

First published online as a Review in Advance onSeptember 19, 2011

The Annual Review of Marine Science is online atmarine.annualreviews.org

This article’s doi:10.1146/annurev-marine-120709-142737

Copyright c© 2012 by Annual Reviews.All rights reserved

1941-1405/12/0115-0237$20.00

Keywords

protist, abyssal, bathyal, biodiversity, endemic, cosmopolitan

Abstract

Benthic foraminifera, shell-bearing protists, are familiar from geologi-cal studies. Although many species are well known, undescribed single-chambered forms are common in the deep sea. Coastal and sublittoral speciesoften have restricted distributions, but wide ranges are more frequent amongdeep-water species, particularly at abyssal depths. This probably reflects thetransport of tiny propagules by currents across ocean basins that present fewinsurmountable barriers to dispersal, combined with slow rates of evolution.Undersampling of the vast deep-sea habitat, however, makes it very difficultto establish the ranges of less common foraminiferal species, and endemismmay be more prevalent than currently realized. On continental slopes, somespecies have restricted distributions, but wide-ranging bathyal species thatexhibit considerable morphological variation are more common. This maybe linked to the greater heterogeneity of continental slopes compared withoceans basins. Improved knowledge of deep-sea foraminiferal biogeogra-phy requires sound morphology-based taxonomy combined with moleculargenetic studies.

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1. INTRODUCTION

Foraminifera, heterotrophic protists classified within the protistan supergroup Rhizaria (Adl et al.2005), are ubiquitous organisms in marine (Murray 2006) as well as freshwater (Holzmann &Pawlowski 2002) and terrestrial (Lejzerowicz et al. 2010) environments. Although some marinespecies are important constituents of the plankton, most are benthic. Foraminifera have an out-standing fossil record, and much of the research on them has been conducted by geologists whohave described most of the known species. Estimates of the number of extant species range from∼4,100 (Murray 2007) to 10,000–12,000 (Boltovskoy & Wright 1976). Many of the describedbenthic species have robust shells (“tests”) composed of calcareous material and fossilize readily.Others have agglutinated tests composed of mineral or biogenic particles acquired from the sur-rounding sediment and are less likely to fossilize. In addition to these well-known taxa, recentstudies have revealed a profusion of species with flexible, single-chambered (monothalamous)tests composed of organic or agglutinated material and having very little fossilization potential(Gooday 2002, Habura et al. 2008). In contrast to the hard-shelled species, these soft-shelledmonothalamous foraminifera are poorly known and largely undescribed.

Because of their importance in reconstructing ancient marine environments, an enormousliterature exists on the relationship between modern foraminiferal species and environmentalparameters. However, their use as paleoenvironmental proxies is hampered by the complexity ofthese distributional controls (Murray 2001, Gooday 2003, Jorissen et al. 2007). In deep water, theorganic matter flux to the seafloor is believed to exert a particularly strong influence on benthicforaminiferal ecology. Altenbach et al. (1999) plotted the percentage abundance of some keydeep-sea species in samples from the Guinea Basin to the Arctic Ocean against flux estimates.All species were abundant only within certain limits, but they also occurred at lower densitiesacross a wide range of flux values. Thus, species that are considered typical of high productivityareas were also found in oligotrophic regions, and vice versa. As Mackensen et al. (1995) remark,“apparently similar assemblages correspond to very different environmental conditions in differentocean basins.” This represents a major obstacle for the development of transfer functions, aimingto quantitatively reconstruct single environmental parameters on the basis of faunal composition.

A comprehensive treatment of the mass of conflicting information regarding ecological controlson the distribution of modern benthic foraminiferal species is beyond the scope of this short review.Instead, we focus on the distribution and ecology of some key species from different environmentalsettings, incorporating molecular evidence when available. The study of foraminifera straddlesbiology and geology. In addition to being important proxies in paleoecological studies, theirhigh density and diversity in various settings make foraminifera ideally suited to address broaderquestions concerning the distribution of marine species (Buzas & Culver 1989). Among these isthe contentious issue of whether or not protists and small-sized animals exhibit biogeographicpatterns. One school of thought maintains that small organisms have ubiquitous distributions andoccur around the globe wherever the environmental conditions are suitable (e.g., Finlay & Fenchel2004). Another view is that some species are cosmopolitan but others exhibit distinct biogeographicpatterns that are not dependent on the existence of suitable habitats (the moderate endemicitymodel) ( Jenkins et al. 2007, Foissner 2008). Many foraminifera fall within the transition zone(0.1 to 10 mm) between large and small organisms where distributions switch from ubiquitous torestricted, according to Finlay & Fenchel (2004). Their patterns of distribution are therefore ofparticular interest in the context of this debate (Gooday 1999).

With these considerations in mind, we address the following questions:

1. Are there “typical” patterns of geographical distribution among deep-water foraminiferalspecies, and do they differ from those of foraminifera in shelf settings?

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Morphospecies: aspecies defined on thebasis of morphologicalfeatures; almost allforaminiferalmorphospecies arecharacterized byfeatures of their shells

Cryptic species:a morphospeciescontaining populationsthat are differentgenetically, but verysimilarmorphologically

Abyssal seafloor:deep seafloor situatedbetween 3,500 m and6,500 m water depth,much of it constitutingthe abyssal plains

Deep sea: the oceanfloor beyond the edgeof the continental shelf(the shelf break),generally located at adepth of 200–300 m

Endemic species: aspecies that is confinedto a particulargeographical area

2. What are the main factors influencing these distribution patterns, and do they differ indifferent settings (continental margins, ocean basins, hypoxic habitats)?

3. What is the degree of connectivity between populations in different regions and habitats?4. Are widely distributed foraminiferal morphospecies genetically coherent, or do they conceal

genetically distinct but morphologically very similar cryptic species?5. To what extent does imperfect taxonomy obscure biogeographic patterns?

We return to these questions in the Summary Points at the end of this review. Although ourmain focus is on modern deep-water foraminifera, for comparative purposes we also touch on thedistribution of those living in shelf and coastal settings.

2. PROBLEMS IN DETERMINING DISTRIBUTION PATTERNS

Many marine foraminifera are well known and widely reported, and their distributions are appar-ently well established (Murray 1991). However, the description of the same species under differentnames is a recurrent problem (Boltovskoy 1965); Murray (2007) estimates that 10% to 25% ofmodern species are synonyms. The opposite tendency, lumping different species under one name,also hampers the study of geographical ranges, especially in the case of agglutinated taxa. Somespecies names established early in the history of foraminiferal taxonomy have been applied tomorphotypes rather than to single species. For example, published images of Reophax scorpiurusde Montfort 1808, a species reported from coastal to abyssal sites around the world, show a widerange of test morphologies that must encompass a variety of different biological species. Anotherconcern is the existence of cryptic speciation among “species” in which the test morphology isfairly consistent (Tsuchiya et al. 2003, Hayward et al. 2004, Pawlowski et al. 2008). Althoughmost hard-shelled species have been described, a large proportion of monothalamous taxa remainundescribed (Habura et al. 2008), particularly in the deep sea where many species are rare andhave been recorded at only one site. The minute proportion [McClain (2007) gives a “very highestimate” of 0.5%] of this vast habitat that has ever been sampled makes it impossible to dis-tinguish genuinely endemic species distributions from restricted occurrences that are artifacts ofundersampling (Gooday et al. 2004, McClain & Mincks Hardy 2010, Tittensor et al. 2010).

Spatial and temporal patchiness create additional problems (Sen Gupta & Smith 2010). Sig-nificant small-scale spatial variability occurs at decametric to decimetric scales (e.g., Griveaudet al. 2010), perhaps reflecting concentrations of labile organic matter and highly localized nichesaround macrofaunal burrows. Seasonal and interannual studies (Ohga & Kitazato 1997, Fontanieret al. 2006, Langezaal et al. 2006, Gooday et al. 2010b) reveal a similar degree of faunal variabilityover time, partly attributable to inputs of labile organic matter that trigger bursts of reproduc-tion in opportunistic species. Because most distributional studies are based on single samples, thistemporal and spatial variability can strongly influence distributional pattern. Examination of dead(hard-shelled) tests, which represent a time-integrated view of the fauna at a particular locality,can help to alleviate this problem, as long as they have not been subject to significant postmortemtransport.

3. DISPERSAL IN FORAMINIFERA

The geographical ranges of species are related, at least in some taxa, to their dispersal ability(Gaston 2003). Information on dispersal in marine organisms is limited and biased toward low-dispersing metazoan species in low-latitude settings (Bradbury et al. 2008). Analyses of proxies fordispersal (e.g., genetic differentiation and duration of planktonic larval stages) suggest that marine

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metazoans exhibit a wide range of dispersive capabilities (Bradbury et al. 2008), although theseare not necessarily linked to species ranges (e.g., Emlet 1995).

Dispersal mechanisms in benthic foraminifera are reviewed by Alve (1999) and Murray (2006).The active movement of free-living species across the seafloor is too slow to account for wide-scaledispersal. Likewise, planktonic life stages, although a potentially efficient means of transport, arereported in only a few species. Most species, therefore, are probably passively entrained into thewater column and transported by currents, either as adults or juveniles or as tiny propagules. Smalladult and juvenile benthic foraminiferal tests have been caught in plankton-net and sediment-trapsamples obtained well above the seafloor (Alve 1999, Brunner & Biscaye 2003, Murray 2006). In aseries of elegant experiments, Alve & Goldstein (2010; also see their earlier papers) convincinglydemonstrated the transport of propagules small enough to pass through a 32-μm mesh sieve. Largenumbers of foraminifera belonging to coastal benthic species appeared and grew when the 32-μmfractions of sediments collected at 320-m water depth were exposed to simulated shallow-waterconditions in sealed containers on a window ledge. Similar results were obtained using sedimentthat had been kept in a dark cold-room for two years, suggesting that propagules can remain viablefor at least this period. If foraminiferal propagules have characteristics similar to those of metazoanlarvae (Bradbury et al. 2008), they are likely to survive longer at low temperatures, enhancing theirpotential for wide dispersal in the deep sea.

On geological timescales, benthic foraminifera seem to disperse instantaneously (Buzas &Culver 1991). Mediterranean sapropels provide good evidence of their rapid dispersal. Theserecurrent anoxic events have repeatedly wiped out benthic faunas across the entire easternMediterranean, at least below water depths of 500 to 1,000 m ( Jorissen 1999). Each lastedfor several thousands of years, after which the seafloor was rapidly repopulated by benthicforaminifera. These species must have either persisted in shallow-water refugia in the easternMediterranean or migrated from the western Mediterranean after reoxygenation of the watercolumn. Although recolonization was apparently very rapid (several decades to a few centuriesat most), it seems to have taken several millennia to fully restore biodiversity, suggesting thatrecolonization may be considerably slower for some taxa (Schmiedl et al. 2003).

In addition to natural mechanisms, species can be transported long distances in the ballasttanks of ships (Radziejewska et al. 2006). This mechanism may explain the disjunct distributionof one phylotype of the coastal genus Ammonia (Pawlowski & Holzmann 2008), the Japanesespecies Trochammina hadai in San Francisco Bay (McGann & Sloan, 1996), and the Europeanand North American species Haynesina germanica in an Argentinean estuary (Calvo-Marcilese &Langer 2010).

4. ENVIRONMENTAL PARAMETERS INFLUENCINGFORAMINIFERAL ASSEMBLAGES

Murray (2006) identified salinity, temperature, oxygen, tides and currents, substrate and food sup-ply, as well as competition and predation, as important factors influencing foraminiferal assem-blages (also see sidebar, Benthic Foraminifera as Paleoceanographic and Paleoecological Indica-tors). Additional factors on the shelf include coverage of the seafloor by seagrasses and macroalgae(e.g., Mateu-Vicens et al. 2010) and light penetration, the latter being crucial for symbiont-bearingspecies. Salinity plays a role mainly in marginal marine areas subject to freshwater discharges (e.g.,Baltic Sea, Black Sea) or to strong evaporation (e.g., Dead Sea, Red Sea). Although temperature isan important factor in coastal environments (Culver & Buzas 1999), it is relatively uniform in mostparts of the deep sea and therefore probably not a major parameter for foraminifera, at least inmodern oceans. Currents and particularly tides also mainly operate in shallow water, but elevated


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BENTHIC FORAMINIFERA AS PALEOCEANOGRAPHICAND PALEOECOLOGICAL INDICATORS

Foraminifera are by far the most abundant and widely distributed benthic organisms preserved in the fossil recordand are used widely to reconstruct conditions on ancient ocean floors (paleoceanography) as well as in near-shoresettings (paleoecology). Faunal characteristics (abundance, diversity, taxonomic composition) have been used toinfer, e.g., the food flux to the seafloor (and hence surface primary productivity), bottom-water oxygenation, currentactivity, and the depth of the carbonate compensation depth. This approach depends on an accurate knowledge ofthe distribution of species in relation to environmental parameters in modern oceans. Another approach dependson the chemical composition (stable isotope and elemental ratios) of foraminiferal carbonate shells. For instance,the Mg/Ca ratio is used to reconstruct temperature, and stable carbon isotope ratios reflect the organic-matterflux to the seafloor and ocean circulation. Once temperature is known, oxygen isotopes can be used to estimatepaleosalinity. In coastal settings, foraminifera have been used to reconstruct past sea levels. Efforts have been madeto develop quantitative proxies (transfer functions) for environmental variables on the basis of benthic foraminifera,but these are often fraught with difficulties. In recent years, benthic foraminifera have been used increasingly tomonitor the impact of anthropogenic activities in marine ecosystems.

flows are encountered in some deep-sea areas, where they are associated with distinctive epifau-nal assemblages (e.g., Schonfeld 1997). Sessile foraminiferal species depend on the availability offirm attachment surfaces. In the predominantly sediment-covered deep ocean, suitable substratesinclude rocky outcrops, glacial drop stones, manganese nodules, biogenic structures, and largersessile or even mobile animals. Carbonate dissolution is a major limiting factor for deep-sea calcare-ous foraminifera. Below the carbonate compensation depth, calcareous species disappear almostentirely and foraminiferal assemblages are composed of agglutinated and organic-walled forms(Saidova 1965). In areas such as oxygen minimum zones (OMZs), low bottom-water dissolvedoxygen (DO) concentrations eliminate hypoxia-sensitive species, leading to the formation of low-diversity, high-dominance faunas. However, DO is limiting only when concentrations decline tolow levels (∼0.5 ml per liter or less), at least where hypoxia is permanent, as in OMZs (Levin 2003).

In addition to these physical and chemical parameters, recent literature has placed considerableemphasis on food inputs derived from surface primary production as a major influence on thestructure and functioning of deep-sea communities in general (Smith et al. 2008), as well as onforaminiferal assemblage composition (e.g., Altenbach et al. 1999, Gooday 2003, Jorissen et al.2007), diversity (Wollenburg & Mackensen 1998), and faunal patterns with water depth (DeRijk et al. 2000). Distinctive assemblages are also associated with regions that have a pronouncedseasonality in the organic-matter flux to the seafloor (Loubere & Fariduddin 1999, Sun et al. 2006).

5. GEOGRAPHICAL DISTRIBUTIONS OF (MORPHO)SPECIESIN DIFFERENT HABITATS

5.1. Continental Shelf and Slope

Analyses of large data sets suggest that many foraminiferal species have restricted ranges oncontinental margins. Distributions around the North American continent (intertidal to abyssaldepths) have been examined in detail by Stephen Culver and Martin Buzas in a series of publications(e.g., Buzas & Culver 1991, Culver & Buzas 1998) based on literature sources combined with anextensive reexamination of museum material. Within this region, the majority (57%) of the 2,329


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species recognized were endemic, in the sense of being confined to one of five regions (Caribbean,Gulf of Mexico, Atlantic, Arctic, and Pacific); only 5% occurred in all regions. However, themajority of endemic species were rare. Similarly, Murray (2007) concluded that a high proportion(83%–90%) of species from marshes, lagoons/estuaries, and shelf seas were restricted to one ortwo of the six areas spanning either the three major oceans (marshes, lagoons/estuaries) or theeastern and western margins of the Atlantic Ocean (shelf seas). Mikhalevich (2004) estimates thatas many as 80% of shallow-shelf (2–50 m) foraminiferal species around the Antarctic continentare endemic.

A different view emerges from a comprehensive survey of foraminifera in the Gulf of Mexico(Sen Gupta & Smith 2010). This may reflect differences in the scale at which endemism andubiquity were evaluated, either around the North American continent (Buzas & Culver 1991,Culver & Buzas 1998) or globally (Sen Gupta & Smith 2010). Only 4% of the 987 species reportedfrom the Gulf of Mexico (0–3,850 m) are endemic to this region. Of the 557 species confined todepths <1,000 m, 29% are cosmopolitan (occurring in the three major oceans or in both polaroceans and two of the three major oceans), compared with 35% of the 48 species from depths>1,000 m and 47% of the 360 species that straddle this boundary. Evidence for wide speciesdistributions in the Gulf of Mexico also comes from a study of benthic foraminifera associatedwith hydrocarbon seeps, an important source of heterogeneity on this margin. Lobegeier & SenGupta (2008) recognized 183 species in 23 seep samples and 5 nonseep control samples (depthrange 245–2,918 m). Although no species was endemic to the seep habitats, some (e.g., Bolivinaspp.) were concentrated in seep samples, whereas others (Saccorhiza ramosa, Eponides turgidus,Nuttallides decorata) were more or less confined to nonseep samples. Other seep sites, notablyin Monterey Bay, California, are also reported to lack endemic species (Bernhard et al. 2001,Rathburn et al. 2003). Data from around New Zealand (0–5,000 m), compiled by Hayward et al.(2011), suggest that cosmopolitan distributions are more prevalent (69%) at depths >100 m thanat shallower sites (55%).

5.1.1. Species with wide distributions. Uvigerina peregrina, a species reported from all oceanbasins (Table 1), encompasses a plexus of morphotypes, mainly differing in their length-widthratio and test ornamentation, which varies from entirely costate to entirely spinose. Two differenttaxonomic concepts have been applied to this plexus. Some authors proposed new species namesfor different morphotypes, whereas the existence of many intermediate specimens has led othersto apply the name U. peregrina to the entire plexus; in the latter case the various morphotypes aredistinguished at a subspecies, variety, or informal level. Lutze (1986) distinguished six morphotypeswithin this complex on the basis of hundreds of samples from the eastern Atlantic continental slope(10◦–50◦ N). Typical U. peregrina, characterized by very sharp costae and no intervening spines,was found between 900-m and 2,000-m depth. In deeper water, U. peregrina was progressivelyreplaced by a morphotype with spines between the costae, and often an entirely spinose lastchamber (Uvigerina hollicki ). Below 3,000 m, completely spinose morphotypes, mostly identified(e.g., Van Leeuwen, 1986) as Uvigerina hispida, became increasingly dominant. Toward shallowerwater, the serrate costae of U. peregrina started to break up into irregular rows of spines. Uvigerinaparva, which is smaller than typical U. peregrina, occurred between 300-m and 1,100-m depths.Lutze (1986) found two other morphotypes on the upper slope off northeast Africa. Uvigerinabifurcata (300–450 m depth) has an elongated test with regular costae, whereas Uvigerina sp. 221( = Uvigerina celtica; Schonfeld 2006) resembles U. bifurcata but has numerous small spines betweenthe costae. Lutze (1986) found it between 100-m and 300-m depths.

Lutze (1986) described a complete bathymetric succession of these Uvigerina morphotypesbetween 10◦ N and 20◦ N in the eastern North Atlantic (Figure 1). Further north, U. hollicki and


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0

1,000

2,000

3,000

4,000

"celtica"

"bifurcata”"parva"

"peregrina”

"hollicki”

"hispida"

Wat

er d

epth

(m)

20° N

10° N

25° N

15° N

10° W20° W30° W5° N

Dakar

Atlantic Ocean

Africa

Sample location map

Collectionarea

Figure 1Bathymetric distribution (red lines) of Uvigerina morphotypes on the east Atlantic margin, 10◦–20◦ N. Thespecies names applied by some authors to these forms are given within quotation marks because there is noevidence that they represent distinct species. The map shows the area off northwest Africa within whichthese morphotypes form a bathymetric succession.

Bathyal seafloor:deep seafloor situatedbetween 300-m and3,500-m water depths;typically coincidingwith the continentalslope and continentalrise

U. bifurcata disappear, whereas others persist (Schonfeld, 2006). Unfortunately, only one geneticstudy partially elucidates the biological status of these various forms. Schweizer et al. (2005)studied small-subunit ribosomal DNA (SSU rDNA) sequences of U. peregrina from the Skagerrak.The divergence between the four recognized morphotypes, which belonged to U. hollicki and/orU. celtica, was rather minimal, leading to the conclusion that, despite substantial morphologicalvariability, the Uvigerina assemblages from the Skagerrak were genetically homogenous. Furthergenetic studies are needed to understand the relationships between the various morphotypes withinthe U. peregrina plexus.

The huge morphological variability encompassed by U. peregrina appears to be exceptional,although this may reflect the popularity of this very common species. Some other cosmopolitantaxa, such as the Gyroidina orbicularis/neosoldanii, Melonis barleeanum/zaandami, and Globobuliminaaffinis/pyrula groups as well as the biconvex Cibicoides (including C. pseudungerianus) (Table 1), alsoshow substantial morphological variability, which has yet to be examined genetically. In contrast,bathyal species with a wide geographical distribution and a consistent morphology appear tobe uncommon. Hoeglundina elegans is probably the best example (Table 1), although other lessfrequent but widely distributed taxa also have stable morphologies. Amphicoryna scalaris and severalmiliolids (Pyrgo subsphaerica, Pyrgo depressa, Sigmoilopsis schlumbergeri ) are good examples.

In summary, it appears that most common bathyal species with wide geographical ranges arecharacterized by substantial morphological variability. The number of genetic studies investigatingthese morphological complexes is still very limited, and at present, there is no positive evidencethat the various morphotypes represent different biological species.


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Tab

le1

Dis

trib

utio

nof

sele

cted

bent

hic

fora

min

ifera

indi

ffer

ent

ocea

ns∗

Atl

anti

cO

cean

Indi

anO

cean

Pac

ific

Oce

anM

edit

erra

nean

Nor

thSo

uth

Gul

fof

Mex

ico

Nor

thSo

uth

Red Sea

Nor

thSo

uth

Sout

hern

Oce

anA

rcti

cO

cean

Wes

tE

asta

Agg

luti

nate

dsp

ecie

sC

ribr

osto

moi

dess

ubgl

obos

a19

,26,

3929

,34

22,3

323

1919

12,1

3,15

19,4

114

,36

3,11

,12

Cyc

lam

min

aca

ncel

lata

8,25

88,

29,3

433

72,

176,

13,1

536

3E

gger

ella

brad

yi32

,39

3129

22,3

34,

277,

9,16

,32

12,1

76,

1510

Hor

mos

ina

glob

ulife

ra2,

82

2922

7,9,

162,

1212

,13,

1536

Hyp

eram

min

asu

bnod

osa

2,8

22

2,12

178

8,40

363

Rha

bdam

min

aab

ysso

rum

2,8

28

27,

9,16

2,12

2,12

,15

2,12

36R

eoph

axde

ntal

inifo

rmis

2534

3316

1715

14Sp

irop

lect

amm

ina

bifo

rmis

816

2,17

10,1

312

,40,

41C

alca

reou

ssp

ecie

sC

assid

ulin

ala

evig

ata/

cari

nata

b2,

25,2

62,

3128

22,3

327

2,30

2,38

2,17

2,13

2,12

353,

20

Chi

losto

mel

laoo

lina

2,5,

2531

2922

,33

2,38

2,17

14C

ibici

doid

esps

eudu

nger

ianu

s39

3129

1715

3,36

3,20

Cib

icido

ides

wue

llers

torfi

2624

,31

2933

4,27

307,

9,16

1212

,15

12,1

8,40

,41

21

Epi

stom

inel

laex

igua

12,2

5,26

3112

22,3

34,

2712

12,1

76,

1340

,41

11

Glo

bobu

limin

aaf

finis

529

2217

1c

Glo

boca

ssidu

lina

subg

lobo

sa2,

3924

,31

3433

4,27

302

2,6,

13,

1536

3,20

Gyr

oidi

naor

bicu

lari

s/ne

osol

dani

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5.1.2. Species with restricted distributions. As indicated above, there is conflicting evidenceregarding the distribution of foraminiferal species on continental margins (Buzas & Culver 1991,Culver & Buzas 1998, Sen Gupta & Smith 2010). However, there do appear to be relativelyfew common species with restricted distributions living on bathyal continental slopes not subjectto oxygen minima. One example is Uvigerina mediterranea, which strongly dominates Mediter-ranean faunas (>125-μm size fraction) and occurs in the eastern Atlantic between 15◦ N and 50◦

N (Lutze 1986), but apparently not in the western Atlantic or in other ocean basins. Planulinaariminensis appears to have a very similar distribution, whereas Uvigerina elongatastriata is foundexclusively in the eastern Atlantic. The deep-water miliolid Articulina tubulosa is known only fromthe eastern Mediterranean, where it has adapted to the extremely oligotrophic conditions of thedeep Levantine Basin. These endemic species, restricted to the Mediterranean and east Atlantic,support the concept of the Mediterranean as a hot spot for benthic foraminiferal evolution dueto repeated anoxic episodes, at least since the beginning of the Pliocene (Verhallen 1991). Ac-cording to Mikhalevich (2004), endemism among bathyal foraminiferal faunas in the SouthernOcean is “significant,” as it is for many metazoan taxa (Brandt et al. 2007). Species with apparentlyrestricted geographical distributions also occur at depths between 200 and 2,000 m around NewZealand. Hayward et al. (2011) record 41 such species within this depth range. These include 3species of Notorotalia, a genus restricted to the Southern Hemisphere that probably originated andradiated in the New Zealand region. Of the 41 bathyal (200–2,000 m) endemic species recognizedby Hayward et al. (2011), 10 extend below 2,000 m.

5.2. Abyssal Seafloor

Much of the ocean floor is situated at abyssal depths (Smith et al. 2008). In their recent review,McClain & Mincks Hardy (2010) concluded that “many taxa appear broadly distributed across thedeep-sea floor.” By contrast, Vinogradova (1997) argued for a high degree of endemism amongmacro- and mega-faunal animals confined to abyssal depths. In the case of foraminifera, the generalperception (e.g., Douglas & Woodruff 1981, Murray 2006) is that many morphospecies occupyingthis vast habitat are cosmopolitan, a view supported by literature records from different oceans(Table 1). As noted above, however, inconsistencies in the identification of species mean thatsuch records should not be accepted without reference to published photographs, or preferably tooriginal material. Nevertheless, specimens of organic-walled, agglutinated, and calcareous speciesfrom widely separated oceanic areas are often remarkably similar in terms of the general appearanceand structure of their tests (Figure 2). The existence of cosmopolitan deep-sea foraminiferalspecies is also indicated by ultradeep sequencing of short, highly variable regions of the SSUrDNA gene in sediment samples from deep-sea sites in the Arctic, North Atlantic, Southern,and Pacific Oceans and the Caribbean Sea (Lecroq et al. 2011). However, most of the operationaltaxonomic units recognized were confined to one or two sites, and replicates from the same stationyielded similar species compositions, suggesting that some species may have restricted distributions( J. Pawlowski, written communication).

5.2.1. Species with wide distributions. We focus on four well-known, predominantly abyssalspecies, all belonging to the order Rotaliida, for which molecular data are available.

Epistominella exigua is reported from all oceans (Table 1) and from depths between 500 m and7,500 m (Murray 1991). However, it is a predominately abyssal species, and the shallower recordsare questionable. This epifaunal/shallow infaunal species occurs across a wide range of organic-matter flux rates (Altenbach et al. 1999). It appears to feed on algal cells embedded within lumpsof phytodetritus derived from surface production. In the northeast Atlantic, E. exigua exhibits an


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a b

c d

e f

g h

i j

Figure 2Similar foraminiferal morphospecies from different oceans. Purple outline indicates specimens from theNorth Atlantic: Porcupine Abyssal Plain, 48◦59.4′ N, 16◦30′ W, 4,840-m water depth (a,c,e,g) and 57◦5.3′ N,12◦24.3′ W, 1,980-m water depth (i ). Blue outline indicates a specimen from the North Pacific: 48◦59.4′ N,176◦55.06′ W, 5,289-m water depth. Red outline indicates specimens from the central Pacific: 9◦14′ N,146◦15′ W, 5,300-m water depth (d ) and ∼151◦ N, ∼119◦ W, ∼4,100-m water depth ( f,h). Green outlineindicates specimens from the Weddell Sea: 65◦20.09′ S, 54◦14.72′ W, 1,108-m water depth. Speciesidentifications are as follows: (a,b) Conicotheca sp.; (c,d ) Nodellum-like form 2; (e,f ) Lagenammina sp.;( g,h) Adercotryma glomerata; (i,j) Epistominella arctica.


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opportunistic, population-level response to pulsed inputs of phytodetritus (Gooday 1988).Cibicidoides wuellerstorfi is also reported from all the main oceans. It is often attached to substratessuch as stones, sponges, and other biogenic structures and is considered to be a suspension feederthat intercepts fresh phytodetrital aggregates just above the seafloor (Lutze & Thiel 1989).Oridorsalis umbonatus is another widely distributed species. Epistominella arctica is a tiny speciesdescribed from the deep Arctic Ocean and subsequently reported from the North Atlantic andSouthern Oceans (Figure 2).

Pawlowski et al. (2007b) explored genetic differentiation between Arctic and Antarctic popula-tions of E. exigua, C. wuellerstorfi, and O. umbonatus separated by a distance of 17,000 miles. Analysesof a fragment of the SSU rDNA gene from specimens collected west and north of Svalbard (ArcticOcean) and in the Weddell Sea (Southern Ocean) revealed no differences between populations ofC. wuellerstorfi and only minor differences in the case of E. exigua. The degree of differentiationwas higher in O. umbonatus, which exhibited a maximum sequence divergence of 2.9% as well asa substantial degree of genetic polymorphism within an individual. Lecroq et al. (2009) reporteda similar lack of differentiation between Arctic and Antarctic populations of E. arctica. Analyses ofthe highly variable internal transcribed spacer (ITS) region of the rDNA gene from the northernand southern polar sites likewise yielded very similar sequences in all three species, with meandivergencies of <1% (Pawlowski et al. 2007b). Some differences were observed between Antarcticand Arctic populations of O. umbonatus when ITS sequences were analyzed, but there was noevidence for differentiation in the other two species. However, a population-genetics approachinvolving an analysis of molecular variance indicated that a deep abyssal (4,650–4,975 m) Antarcticpopulation of E. exigua was genetically distinct from shallower abyssal Antarctic (2,600–4,600 m)and bathyal northern (1,352–2,784 m) populations of this species. Arctic and Antarctic populationsof O. umbonatus were also significantly differentiated, whereas those of C. wuellerstorfi were not.

Subsequent analyses by Lecroq et al. (2009) of SSU rDNA sequences of E. exigua from deepwater off the coast of Japan revealed a striking degree of genetic similarity between these westernPacific populations and those from the Antarctic, Atlantic, and Arctic studied by Pawlowski et al.(2007b). A population-genetics analysis based on ITS rDNA sequences also failed to demonstrateany evidence for cryptic speciation within this species. Instead, much of the genetic variation wasattributable to differences between specimens within, rather than between, populations (Lecroqet al. 2009). These results echo those for other protistan taxa, such as heterotrophic flagellates,which include marine species with cosmopolitan distributions (e.g., Scheckenbach et al. 2005).

5.2.2. Species with restricted distributions. The dual problems of rarity and undersampling areparticularly acute in deep-ocean basins, making it difficult to establish the existence of endemism.In the abyssal equatorial Pacific, there are some obvious faunal differences between the KaplanEast (Nozawa et al. 2006) and Kaplan Central (N. Ohkawara & A.J. Gooday, unpublished results)sites. In particular, Saccammina minimus, the overwhelmingly dominant species at the Centralsite (5,042-m water depth) (Ohkawara et al. 2009), is absent at the shallower (4,100 m) East site.However, because this minute species has an extremely patchy distribution at small spatial scalesand is easily overlooked, no conclusions can be drawn about its wider distribution.

At regional and global scales, some deep-sea foraminifera appear to be restricted to particularbasins or oceans. Despite close faunal links between the Southern Ocean and North Atlanticabyssal faunas (Cornelius & Gooday 2004), certain species may be confined to deep Antarcticwaters. These include a distinctive form of the cosmopolitan deep-sea genus Vanhoeffenella,characterized by a broad agglutinated rim and a three-dimensional morphology. Another possibleexample is Haplophragmoides umbilicatum, a species known only from the abyssal Southern Ocean(N. Cornelius, personal communication). There are also faunal differences between the Pacific


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and Atlantic Oceans. Among large and distinctive foraminifera that are unlikely to be overlooked,stannomid xenophyophores and the tubular species Jugimurammina stellaperuta are largely orentirely confined to the Pacific (Gooday et al. 2004). Conversely, the discoidal miliolid Discospirinatenuissima is currently reported only from the Atlantic and Indian Oceans. Similar examples prob-ably exist among the smaller foraminifera. Given the different geological ages and environmentalcharacteristics (bottom-water oxygenation and corrosivity, sediment types, sedimentary processes,timing and magnitude of primary production) of the Pacific and Atlantic Oceans (Levin & Gooday2003), it seems highly unlikely that all deep-water foraminiferal species occur in both oceans.

5.3. Hypoxic Environments

Deep-water hypoxia (O2 <0.5 ml per liter) has persisted over millennial-scale time periods atbathyal depths in stratified basins and OMZs, where it is associated with upwelling combined withreduced circulation, water column stratification, and oxygen-depleted source waters (Levin 2003).OMZs are developed intensely in the eastern Pacific and in the northern Indian Ocean (ArabianSea and Bay of Bengal), and somewhat less so in the eastern Atlantic (Diaz & Rosenberg 1995,Levin 2003, Helly & Levin 2004). Where they impinge on the seafloor, OMZs create strongbottom-water oxygen gradients. In addition to oxygen depletion, these regions are characterizedby high sediment organic carbon content, lowered pH, and soft, unconsolidated sediments with ahigh water content (Gooday et al. 2010a).

Bathyal hypoxic environments are usually inhabited by low-diversity, high-dominance assem-blages of foraminiferal species. Despite the depressed pH, calcareous taxa typically dominate thesefaunas. Many species exhibit at least some morphological, physiological, or ultrastructural adap-tations to hypoxia (Bernhard & Sen Gupta 1999). These include an ability to accumulate andrespire nitrate, as demonstrated initially in Globobulimina (Risgaard-Petersen et al. 2006) and sub-sequently in numerous other taxa (Pina-Ochoa et al. 2010). Deep-infaunal species, which occupyhabitats deeper in the sediment in well-oxygenated benthic environments, replace species that areless resistant to hypoxia in low-oxygen settings. Specialized shallow-infaunal taxa may also appear.Whereas the deep-infaunal taxa are mostly cosmopolitan, the hypoxia-resistant surface dwellersoften show more regional distributions. OMZs undoubtedly limit species ranges by excludinghypoxia-sensitive species (Gooday 2003). They may also act as a strong barrier to the spread ofspecies between upper and lower slope environments (Rogers 2000).

There is mounting evidence that the extent and thickness of OMZs in tropical and subtropicalregions of the oceans have increased since the 1960s (Stramma et al. 2008, 2010). Continuedexpansion of OMZs (Hofmann & Schellnhuber 2009) is likely to have profound consequences formarine life (Stramma et al. 2010, Gruber 2011). These effects will probably include an increaseddominance of carbon processing by hypoxia-tolerant foraminiferal species (Woulds et al. 2007)and an expansion of their geographical ranges.

5.3.1. Species with wide distributions. The best example is Virgulinella fragilis, reported atdepths between 16 m and >100 m from off west Africa, the eastern Arabian Sea, the Japaneseislands, the Australian and New Zealand margins, the Peru margin, the Gulf of Mexico, and theVenezuelan shelf (Tsuchiya et al. 2008, Leiter & Altenbach 2010). This species appears to be ahabitat endemic (Anderson 1994) that is confined to sulfidic/hypoxic environments; it occupiesa deep-infaunal microhabitat where the bottom-water oxygen content is <0.3 ml per liter (Leiter& Altenbach 2010). Molecular analyses of individuals from three widely separated and isolatedpopulations off Japan, New Zealand, and Namibia demonstrated a remarkable degree of genetichomogeneity with no hint of cryptic speciation (Tsuchiya et al. 2008). Because gene flow between


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Cosmopolitanspecies: a widelydistributed species thatis found in many partsof the world

the populations and recent dispersal are very unlikely, Tsuchiya et al. (2008) suggested thatV. fragilis exhibits evolutionary stasis (both genetic and morphological), perhaps enhanced bypersistent asexual reproduction.

Some other deep-infaunal, hypoxia-tolerant species have wide distributions. Chilostomellaovoidea/oolina (the names are probably synonyms) is a particularly interesting example (Table 1).An analysis of partial SSU rDNA sequences of specimens from disjunct, bathyal (611–1,449 m),moderately hypoxic sites in the Pacific and Atlantic Oceans and Mediterranean Sea yielded threedistinct genetic types that could not be distinguished morphologically. These types, which weresupported by ITS data, occurred in (a) the Bay of Biscay and Mediterranean (AtlMed), (b) SagamiBay ( Japan) and the Oregon slope (NPac), and (c) Sagami Bay and the Costa Rica slope (CPac)(Grimm et al. 2007). The NPac and CPac types occurred on both sides of the Pacific Ocean,probably reflecting recent or ongoing genetic exchange across the Pacific mediated by the passivedispersal of propagules (Grimm et al. 2007). Globobulimina is another important deep-infaunalgenus that is widely distributed in hypoxic settings. It includes a number of species with onlyminor and rather subtle morphological differences, in some cases supported by molecular data(Ertan et al. 2004). One such species, Globobulimina affinis, is reported from the Atlantic, Indian,and Pacific Oceans as well as the Sea of Marmara (Table 1).

5.3.2. Species with restricted distributions. Different species are found at different localitieswithin the same general area, such as the California borderland (e.g., Bernhard & Sen Gupta 1999).Different oxygen concentrations probably explain much of this variation (Bernhard et al. 1997), butit could also reflect restricted distributions. In the Arabian Sea, Uvigerina ex gr. U. semiornata andBolivina aff. B. dilatata dominate the core region of the Pakistan margin OMZ, where bottom-wateroxygen levels drop to ∼0.1 ml per liter (Schumacher et al. 2007, Larkin & Gooday 2009). Similarforms occur on the Oman margin (Gooday et al. 2000). Following an exhaustive effort to identifythem, Schumacher et al. (2007) concluded that both were undescribed species confined to theArabian Sea. They contrasted the endemic character of foraminiferal species inhabiting the OMZcore with assemblages of more cosmopolitan species (e.g., Globobulimina spp. and Chilostomellaspp.) found in the lower part of the zone.

6. CRYPTIC SPECIATION

There is good evidence among planktonic foraminiferal species for cryptic speciation, associ-ated with slight morphological as well as biological, ecological, and physiological differences (e.g.,Huber et al. 1997, de Vargas et al. 2002, Darling et al. 2004). However, cryptic speciation is less ev-ident among benthic foraminifera, which evolve at a slower rate than their planktonic counterparts(Pawlowski et al. 1997). The best evidence comes from shallow-water taxa. Analyses of ITS rDNAsequences in Planoglabratella opercularis (Tsuchiya et al. 2003) from intertidal locations aroundJapan demonstrates the existence of two cryptic species, Type A and Type B, the sequences ofwhich diverge by 7.0% to 8.5%. Type B is genetically closer (3.9% to 4.8% divergence) to anotherspecies, P. nakamurai, than it is to Type A. Careful examination revealed subtle morphological dif-ferences between the two phylotypes of P. opercularis, with Type B exhibiting some test features incommon with P. nakamurai. Cryptic speciation has also been described within Ammonia, a highlyvariable coastal genus often regarded as comprising a few species with many different ecopheno-types (Hayward et al. 2004, Pawlowski & Holzmann 2008). Partial, large-subunit rDNA sequencesrevealed 13 phylotypes (T1 to T13), each sufficiently distinct to be regarded as a species and ex-hibiting a variety of biogeographic patterns. Phylotype T1 is distributed around the world in bothhemispheres, T2 and T5 occur on either side of the North Atlantic and South Pacific, respectively,


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whereas T3 is widely distributed around European coastlines. T6 has been found in Japanese andEuropean waters and may be an invasive species dispersed by shipping. The other 8 phylotypeshave restricted distributions. Some shallow-water morphospecies with bipolar distributions alsoencompass cryptic species (Mikhalevich 2004, Brandt et al. 2007, Pawlowski et al. 2008).

Although genetic studies have revealed complexes of cryptic species among some animal groupsin the deep sea (e.g., isopods; Raupach et al. 2007), there is currently little unequivocal evidencefor cryptic speciation among bathyal or abyssal benthic foraminifera. The only real example isConqueria laevis, a monothalamous species of which Arctic and Antarctic individuals were genet-ically distinct (Brandt et al. 2007). The three genetic types of Chilostomella mentioned above areless differentiated than the five planktonic forms of Neogloboquadrina pachyderma recognized byDarling et al. (2004) and apparently lack any clear morphological expression, leaving their tax-onomic status uncertain (Grimm et al. 2007). Likewise, the genetic differences observed amongArctic and Antarctic populations of O. umbonatus, and to a lesser extent in E. exigua, do not amountto cryptic speciation (Pawlowski et al. 2007b). Some species (e.g., Adercotryma glomerata) are re-ported from shelf to abyssal depths (Murray 1991); inaccurate taxonomy is possibly responsiblefor these vast bathymetric ranges, but cryptic species occupying progressively deeper depth zonescould also be involved. Although this latter suggestion is purely speculative, it would be consis-tent with the considerable degree of depth-related genetic differentiation observed among someanimal morphospecies (e.g., Zardus et al. 2006). By contrast, there is good molecular evidencethat the monothalamous species Bathyallogromia weddellensis is genetically coherent across a depthrange of 1,100–6,300 m in the Southern Ocean (Gooday et al. 2004). Populations of the calcareousspecies Epistominella vitrea from 15 to 30 m in McMurdo Sound and bathyal depths (>1,000 m) inthe Weddell Sea on the opposite side of the Antarctic continent are genetically almost identical(Pawlowski et al. 2007a). These wide bathymetric ranges are possibly related to the essentiallyisothermal water column around Antarctica.

7. CONTROLS ON DISTRIBUTION PATTERNS

7.1. Evolutionary Factors

Coastal and shelf environments have been subject to repeated modification, for example, as aresult of sea-level changes, leading to the continual destruction and reformation of shallow-watermarine habitats. Geological and oceanographic fluctuations have also impacted bathyal continentalmargins, particularly at upper-slope depths. Environmental instability of this sort is likely toenhance genetic differentiation (Katz et al. 2005) as well as create barriers to gene flow, resultingin a greater degree of endemism compared with deeper-water settings, which have been generallymore stable over geological timescales (Buzas & Culver 1984, 1989; Rogers 2000).

Caron (2009) suggested that different modes of reproduction (sexual versus asexual) mayinfluence distribution patterns in protists. Foraminifera can reproduce sexually or asexually. Mostof the species that have been studied undergo an alternation of generations. However, becausepopulation densities are generally lower in the deep sea, asexual reproduction is more likelyto occur here than in shelf settings (Murray 1991, p. 301). If this is true, then rates of geneticdifferentiation and speciation are also likely to be slower, promoting the development of largergeographical ranges, particularly at abyssal depths (Pawlowski et al. 2007b). A slower rate ofevolution would be consistent with the greater geological longevity that seems to be typical ofdeep-water species (Buzas & Culver 1984). As mentioned above, evolutionary stasis, rather thangene flow, is one possible explanation for the remarkable genetic homogeneity between widelyseparated and isolated populations of the hypoxia-tolerant species Virgulinella fragilis.


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7.2. Barriers to Dispersal

Grassle & Morse-Porteous (1987) noted the “lack of barriers to dispersal over very large areas” asone of the main influences on deep-sea benthic community structure. Certainly, the generally opennature of abyssal plains is consistent with the widespread distribution of many abyssal foraminiferalspecies. Nevertheless, barriers to dispersal do exist in the deep sea. Hydrographic features, suchas strong current systems, create barriers that potentially limit the ranges of deep-sea animals(e.g., Won et al. 2003). However, the most obvious are topographic features such as major ridges(Vinogradova 1997). Preliminary analysis of foraminiferal assemblages on either side of the Mid-Atlantic Ridge (49◦–54◦ N, 2,500-m depth) did not reveal any clear faunal differences (N. Rothe& A.J. Gooday, unpublished data). Similar abyssal foraminiferal assemblages occupy areas to thenorth and south of the Walvis Ridge, a feature that rises 4,000 m above the adjacent basins(Schmiedl et al. 1997). The bathymetric distributions of many deep-sea foraminiferal species, andpresumably of their propagules, are sufficiently broad to span these kinds of topographic obstacles(Pawlowski et al. 2007b). Given the ability for propagules to survive inhospitable conditions forperiods of years (Alve & Goldstein 2010), the potential for the wide dispersal of foraminifera bycurrents at abyssal depths is considerable. Passive transport by bottom currents across topographicbarriers has been invoked to explain the cosmopolitan distributions of abyssal harpacticoid copepodspecies in the genus Mesocletodes (Menzel et al. 2011).

Additional topographic barriers exist on continental margins, which are generally much moreheterogeneous than the abyssal plains (Levin & Dayton 2009). This heterogeneity has been im-plicated in the greater degree of morphological (Etter & Rex 1990) and genetic (Etter et al. 2005)variability on bathyal continental slopes compared with abyssal plains. Submarine canyons, fea-tures that often extend from near the coastline to abyssal depths, constitute one obvious sourceof heterogeneity. Distinctive foraminiferal species are sometimes common within canyons butare not present on adjacent slopes (Hess & Jorissen 2009). However, these species appear to beadapted to special conditions inside the canyons, such as sediment instability and/or organic mat-ter focusing. There is no evidence that canyons, or other physical obstacles, limit the geographicaldistribution of any species at bathyal depths on continental margins.

Shallow sills create major barriers to the influx of species into partially land-locked basins. Themost obvious example is the Mediterranean, where the Straits of Gibraltar has limited the exchangeof species with the North Atlantic since the basin refilled following the Late Miocene Messiniansalinity crisis. As a result, the deep fauna is impoverished compared with that in the Atlantic (Murray1991). However, the low diversity of these faunas, especially in the eastern Mediterranean, mayalso reflect the extreme oligotrophy of the deep Levantine basin (De Rijk et al. 2000). As explainedabove, several species (e.g., Articulina tubulosa, Rotamorphina involuta) appear to be limited to theMediterranean, whereas others (e.g., U. mediterranea, Planulina ariminensis, Paranomalina coronata)may have evolved in the Mediterranean and then invaded the eastern Atlantic.

7.3. Environmental Parameters

Irrespective of the overall geographical range of a particular species, environmental factors willdetermine where that species actually occurs (Finlay & Fenchel 2004, Tsuchiya et al. 2008). Asindicated above, the abundance, diversity, and composition of foraminiferal assemblages in coastaland sublittoral environments are controlled largely by a combination of physical and chemicalparameters (temperature, salinity, currents, substrate, vegetation cover), food resources, and bioticinteractions (Culver & Buzas 1999, Murray 2006). In deep water, early studies related the oc-currence of foraminiferal species to the physical and chemical properties of bottom-water masses(Schnitker 1980). These ideas are no longer considered tenable ( Jorissen et al. 2007), although


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some water-mass properties, notably current flow (Schonfeld 1997) and bottom-water corrosive-ness (Schmiedl et al. 1997), may be important. Levin et al. (2001) concluded that food inputs,bottom flow, bottom-water oxygenation, sediment heterogeneity, and ecological disturbance arethe five main influences on deep-sea diversity patterns. Mackensen et al. (1995) identified a similarset of parameters that they considered to underlie the distribution of foraminiferal assemblagesin the South Atlantic Ocean. Jorissen et al. (2007) reformulated these as follows: (a) organicmatter exported to the seafloor and organic carbon content of the sediment, (b) bottom-waterhydrodynamics and related sediment grain-size properties, (c) bottom-water oxygenation, and(d ) bottom-water carbonate saturation. Hayward et al. (2011) reached similar conclusions basedon their analysis of foraminiferal assemblages around New Zealand. Organic-matter flux andcarbonate dissolution are probably the dominant ecological parameters across the vast abyssalareas, particularly in the Pacific Ocean (Saidova 2000), whereas hydrodynamics, oxygen, andsediment grain size are more influential at bathyal depths. Carbonate dissolution, together withsediment characteristics, is believed to exert an important influence on foraminiferal distributionsdown to abyssal depths around the Antarctic continent (e.g., Echols 1971, Anderson 1975).

Particularly in oligotrophic abyssal settings, the supply of organic matter to the seafloor, whichis related to phytoplankton primary production, profoundly influences the structure, composi-tion, and functioning of deep-sea benthic communities (Smith et al. 2008). The scale of the flux(Altenbach et al. 1999) and its seasonality (Gooday 1988, Loubere & Fariduddin 1999, Sun et al.2006) are both important for foraminifera. In the North Atlantic (2,178–4,673-m water depth),an assemblage dominated by two phytodetritus species (Alabaminella weddellensis and Epistominellaexigua) is associated with a highly seasonal organic carbon flux, whereas a Globocassidulina subglobosa–Nuttallides umbonifera assemblage is negatively correlated with a seasonal flux (Sun et al. 2006). Thesurface-ocean biogeochemical provinces recognized by Longhurst (1998) provide a comprehensiveoverview of the contrasting productivity regimes that undoubtedly underlie global macroecologi-cal patterns among benthic foraminifera. However, the main impact of food availability is likely tobe on the ability of some species to outcompete others, as indicated by increases in their absoluteand relative abundance (e.g., Koho et al. 2009). Whether fluxes of labile organic matter to theseafloor also limit species ranges is debatable. In contrast, physical and chemical parameters suchas temperature, salinity, and oxygen concentrations act as limiting factors where they approach thetolerance level of the species under consideration (Murray 2001, 2006). At lower levels, variationsin the magnitude of these parameters probably have no effect on species distribution patterns.Thus, given sufficient ability to disperse, species will probably occur everywhere, at higher orlower densities according to available food resources, except in areas where physical and chemicalparameters (e.g., temperature, salinity, DO concentrations) place them under intolerable stress.

8. CONCLUSIONS

Like those of other organisms, biogeographic studies of deep-sea benthic foraminifera are ham-pered by imperfect taxonomy, the relative rarity of many species, and undersampling of the vastocean-floor environment. Nevertheless, there is more information about foraminifera than manyother deep-sea taxa. In contrast to the apparent prevalence of endemic distributions among coastaland sublittoral species, many common, well-characterized hard-shelled species appear to be dis-tributed widely at bathyal and abyssal depths. This is consistent with the pattern of moderatecosmopolitanism and low endemism among species in the Gulf of Mexico (Sen Gupta & Smith2010). However, this generalization must be tempered with some important caveats. Broad rangesare supported by genetic data in only a few cases, and widespread bathyal species often exhibitconsiderable morphological variation. It is possible that endemism is more prevalent among rare


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species than currently realized, although conclusive evidence for restricted distributions will bedifficult to obtain.

SUMMARY POINTS

Here, we return to the questions posed in the Introduction (see section above).1. Do deep-water foraminiferal species have typical distribution patterns? Many common

bathyal and abyssal morphospecies appear to have broad ranges (in few cases, supportedby genetic analyses), while relatively few have restricted distributions. This contrasts withthe frequency of apparent endemic distributions among shallow-water species. However,many deep-sea foraminiferal species are rare, often undescribed in the case of monothal-amous taxa, and known only from one or a few samples. This makes it impossible to drawsensible conclusions about their geographical ranges.

2. What are the main factors influencing distribution patterns? Foraminiferal species dis-tributions are influenced by their evolutionary history and environmental controls. Inshallow-water settings, species ranges are limited by temperature and salinity close tothe shore as well as by sediment characteristics, vegetation cover, and light penetrationon the shelf. On the continental slope, distributions are influenced by food quantityand quality, sediment characteristics, topographic features (e.g., canyons), and, in places,bottom-water DO concentrations and current flow. On the environmentally more uni-form abyssal plains, the main factors are the quantity and quality of organic matterreaching the seafloor, its seasonality, and the carbonate corrosion of the bottom water.

3. What is the degree of connectivity between populations? Most foraminifera appear tohave excellent dispersive capabilities, mediated mainly by microbe-sized propagules,which can remain viable for several years. Transport of propagules by thermohalineand other currents has the potential to link distant populations genetically, either di-rectly or via intermediate populations. However, slow evolution may also account for alack of genetic differentiation, as is likely in the case of isolated populations of Virgulinellafragilis, a species confined to hypoxic/sulfidic habitats.

4. Are widely distributed benthic foraminiferal morphospecies genetically coherent or dothey conceal cryptic species? There is good evidence for cryptic speciation (combinedwith slight morphological differences) in a few coastal benthic foraminifera as well asin planktonic species. Distant populations of certain bathyal and abyssal species havediverged genetically but probably not enough to regard them as cryptic species. Somemorphologically simple monothalamous species, which possess few taxonomically usefulcharacters, may encompass cryptic species. It is also possible that morphospecies withwide bathymetric ranges are genetically differentiated, although evidence is lacking.

5. To what extent does imperfect taxonomy obscure biogeographic patterns? Establishingspecies ranges depends crucially on the consistent use of species names. Synonyms appearto be quite prevalent among shelf-dwelling species and may lead to the inappropriatesplitting of widely distributed species (pseudoendemism). The opposite problem, that ofincluding disparate forms within one species name, seems to be quite common in somemonothalamous and agglutinated taxa. This can artificially inflate species ranges.


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FUTURE ISSUES

1. Taxonomy: Determining biogeographic patterns among foraminifera requires accuratetaxonomy. A major effort is needed to revise difficult species groups (e.g., Uvigerina andGlobobulimina spp.) and to describe novel species, particularly those belonging to themonothalamous taxa that abound in deep-sea sediments.

2. Endemism: How can endemic distributions be recognized, given the difficulty in estab-lishing the presence of rare species in a particular area? The problem of undersampling isparticularly acute in the deep sea, where only a tiny proportion of the vast benthic habitathas ever been sampled and the proportion of rare species, many of them undescribed, isparticularly high.

3. Cosmopolitanism: Conversely, claims for ubiquitous species distributions based on lit-erature sources from different regions depend crucially on the assumption that the speciesare accurately identified. Imperfect taxonomy means that, unless species are clearly il-lustrated, or the original material reexamined, reliance on faunal lists for distributionalrecords is risky.

4. Molecular genetics: Only a handful of deep-sea species has been studied genetically.More analyses based on the SSU and ITS regions of the rDNA gene would reveal thedegree of genetic differentiation between geographically and bathymetrically dispersedpopulations of the same morphospecies, as well as the possible existence of cryptic species.New generation sequencing will provide a rapid way to identify species in sedimentsamples as well as reveal species that cannot easily be detected visually.

5. Climate change: The consequences of ocean warming will create multiple challengesfor benthic foraminifera. Many species feed at the base of the food chain on detritalmaterial and will be impacted by warming-related changes in the quantity and qualityof surface-derived organic matter reaching the seafloor. This is likely to lead to shiftsin the diversity and dominance of foraminiferal assemblages, as well as species ranges,particularly at abyssal depths. In bathyal settings, hypoxia-tolerant species will becomemore widely distributed as OMZs expand and intensify.

6. Reproduction: Foraminifera can reproduce both sexually and asexually. Species thatreproduce asexually may evolve more slowly and hence establish wider geographicalranges. Very little is known about which mode is typical for deep-sea foraminifera, al-though asexual reproduction seems more likely in the case of rare species, particularlyat abyssal depths. This question could be investigated by studying the prevalence ofmicrospheric and megalospheric forms in deep-sea samples.

DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

We thank Jan Pawlowski for his comments on an earlier draft of this paper. This paper is a contri-bution to the Oceans 2025 Project funded by the Natural Environment Research Council, United


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Kingdom, and the Collaborative Project HERMIONE funded under the European Commission’sFramework 7 program.

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MA04-FrontMatter ARI 16 November 2011 9:36

Annual Review ofMarine Science

Volume 4, 2012 Contents

A Conversation with Karl K. TurekianKarl K. Turekian and J. Kirk Cochran � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Climate Change Impacts on Marine EcosystemsScott C. Doney, Mary Ruckelshaus, J. Emmett Duffy, James P. Barry, Francis Chan,

Chad A. English, Heather M. Galindo, Jacqueline M. Grebmeier, Anne B. Hollowed,Nancy Knowlton, Jeffrey Polovina, Nancy N. Rabalais, William J. Sydeman,and Lynne D. Talley � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �11

The Physiology of Global Change: Linking Patterns to MechanismsGeorge N. Somero � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �39

Shifting Patterns of Life in the Pacific Arctic and Sub-Arctic SeasJacqueline M. Grebmeier � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �63

Understanding Continental Margin Biodiversity: A New ImperativeLisa A. Levin and Myriam Sibuet � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �79

Nutrient Ratios as a Tracer and Driver of Ocean BiogeochemistryCurtis Deutsch and Thomas Weber � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 113

Progress in Understanding Harmful Algal Blooms: Paradigm Shiftsand New Technologies for Research, Monitoring, and ManagementDonald M. Anderson, Allan D. Cembella, and Gustaaf M. Hallegraeff � � � � � � � � � � � � � � � � 143

Thin Phytoplankton Layers: Characteristics, Mechanisms,and ConsequencesWilliam M. Durham and Roman Stocker � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 177

Jellyfish and Ctenophore Blooms Coincide with Human Proliferationsand Environmental PerturbationsJennifer E. Purcell � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 209

Benthic Foraminiferal Biogeography: Controls on Global DistributionPatterns in Deep-Water SettingsAndrew J. Gooday and Frans J. Jorissen � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 237

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MA04-FrontMatter ARI 16 November 2011 9:36

Plankton and Particle Size and Packaging: From Determining OpticalProperties to Driving the Biological PumpL. Stemmann and E. Boss � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 263

Overturning in the North AtlanticM. Susan Lozier � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 291

The Wind- and Wave-Driven Inner-Shelf CirculationSteven J. Lentz and Melanie R. Fewings � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 317

Serpentinite Mud Volcanism: Observations, Processes,and ImplicationsPatricia Fryer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 345

Marine MicrogelsPedro Verdugo � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 375

The Fate of Terrestrial Organic Carbon in the Marine EnvironmentNeal E. Blair and Robert C. Aller � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 401

Marine Viruses: Truth or DareMya Breitbart � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 425

The Rare Bacterial BiosphereCarlos Pedros-Alio � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 449

Marine Protistan DiversityDavid A. Caron, Peter D. Countway, Adriane C. Jones, Diane Y. Kim,

and Astrid Schnetzer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 467

Marine Fungi: Their Ecology and Molecular DiversityThomas A. Richards, Meredith D.M. Jones, Guy Leonard, and David Bass � � � � � � � � � � � � 495

Genomic Insights into Bacterial DMSP TransformationsMary Ann Moran, Chris R. Reisch, Ronald P. Kiene, and William B. Whitman � � � � � � 523

Errata

An online log of corrections to Annual Review of Marine Science articles may be found athttp://marine.annualreviews.org/errata.shtml

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benthic foraminiferal biogeography: controls on global...

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