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Marine Biodiversity ISSN 1867-1616 Mar BiodivDOI 10.1007/s12526-012-0121-8

The influence of productivity on abyssalforaminiferal biodiversity

Andrew J. Gooday, Brian J. Bett, DanielO. B. Jones & Hiroshi Kitazato

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REVIEW

The influence of productivity on abyssal foraminiferal biodiversity

Andrew J. Gooday & Brian J. Bett & Daniel O. B. Jones &

Hiroshi Kitazato

Received: 9 August 2010 /Revised: 8 February 2012 /Accepted: 20 May 2012# Senckenberg Gesellschaft für Naturforschung and Springer 2012

Abstract The quantity and quality of organic matter reachingthe deep-sea floor is believed to exert a strong control onbenthic foraminiferal assemblages, including the diversityand density of populations and the distribution patterns ofspecies. In addition, some species seem to be associated withstrong seasonality in primary productivity. We test relation-ships between diversity and mean annual productivity basedon carefully selected datasets (>63-μm sieve fraction includ-ing soft-shelled taxa) from the NE Atlantic, Weddell Sea, andEquatorial and North Pacific. We used (1) ‘live’ (Rose Bengalstained) foraminiferal density, (2) mean annual surface pro-ductivity and (3) estimated organic carbon flux to the seaflooras proxies for food supply to the benthos. A suite of speciesrichness, diversity and dominance measures all decreasedsignificantly with increasing density, whereas species densityshowed a significant increase. In contrast, none of the relation-ships between these measures and primary productivity or itsseasonality were significant. Only the Margalef and Brillouinindices exhibited a significant decrease with increasing values

of carbon flux to the sea floor. When sites from the NEAtlantic were treated separately, significant relationships(−ve) emerged between flux and all diversity measures, andbetween foraminiferal densities and most (8 of 9) diversitymeasures. For the equatorial Pacific, however, these relation-ships were mostly (16 of 18) not significant. Size fractioned(>150-μm and >63-μm fraction including phytodetritus) datafrom the NE Atlantic samples yielded significant correlations(−ve) between several diversity measures and foraminiferaldensities, but many fewer when related to estimated carbonflux to the seafloor. We also considered published datasetsfrom the Arctic (Wollenburg and Mackensen Mar Micropa-leontol 34: 153–185, 1998) and North Atlantic (Corliss et al.Deep-Sea Res 56: 835–841, 2009) Oceans. Diversity values(Fisher α index based on ‘live’ counts) from seasonally andpermanently ice-covered areas (depth range, 94–4,427 m) inthe Arctic were significantly correlated (+ve) with estimatedflux. Correlations were also significant for sites below perma-nent ice cover (1,051–4,427 m) and for those >4,000 m.Positive correlations between foraminiferal density and diver-sity were significant for the whole dataset and for sites withpermanent ice cover, but not for the deep sites. Analysis ofunstained calcareous foraminifera of Holocene age from the NAtlantic (2,118–4,673 m water depth) revealed significantrelationships between diversity and seasonality, but not withflux. Additional analyses of ‘seasonal’ and ‘non-seasonal’ NAtlantic sites with a comparable range of estimated flux values(2–4 g C m−2 year−1) revealed that diversity increased withincreasing flux and density in both cases, with significantlylower diversity at the seasonal compared to the non-seasonalsites. The contradictions between our data (−ve relationshipbetween food availability and diversity) and those ofWollenburg and Corliss (+ve relationship) are difficultto explain and underline the need for further studies

Electronic supplementary material The online version of this article(doi:10.1007/s12526-012-0121-8) contains supplementary material,which is available to authorized users.

A. J. Gooday (*) : B. J. Bett :D. O. B. JonesNational Oceanography Centre,Southampton, European Way,Southampton SO14 3ZH, UKe-mail: ang@noc.soton.ac.uk

H. KitazatoInstitute of Biogeosciences,Japan Agency for Marine-Earth Scienceand Technology (JAMSTEC),2-15 Natsushimacho,Yokosuka 237-0061, Japan

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employing consistent methods to analyse ‘entire live’assemblages across productivity gradients.

Keywords Phytodetritus . Organic carbon flux .

Seasonality . Diversity indices . Deep-sea benthos

Introduction

Foraminifera are a major component of the marine biotaacross a wide spectrum of size classes from the meiofaunato the megafauna. In the deep sea, they often account for>50 % of the meiofauna (Gooday 2001), and one group, thekomokiaceans, is reported to have a biovolume an order ofmagnitude greater than all metazoan macrofauna combinedin the central oceanic abyss (Tendal and Hessler 1977). Ingeneral, there is a decrease in the absolute and relativeabundance of calcareous foraminifera, and an increase inthe abundance of agglutinated taxa, as water depth increasesand the organic matter flux to the seafloor decreases(Jorissen et al. 1998; De Rijk et al. 1999; Gooday 2003;Cornelius and Gooday 2004). On the abyssal plains, fora-miniferal assemblages are dominated by agglutinated andorganic-walled species (e.g. Saidova 1975, 1981, 2000),including fragile monothalamous (single-chambered) forms(Bernstein et al. 1978; Nozawa et al. 2006) and komokiaceans(Tendal and Hessler 1977; Gooday et al. 2007, 2008). Wherepolymetallic (managanese) nodules are abundant, notably inthe Pacific Ocean, they provide an attachment substrate fornumerous species, many of them undescribed mat-like andtubular agglutinated forms (Veillette et al. 2007). Below theCarbonate Compensation Depth (CCD), virtually all benthicforaminifera belong to either agglutinated or organic-walledtaxa, many of them delicate and with virtually no fossilisationpotential.

Studies of deep-sea benthic foraminifera have tended tofocus on continental margins, which are more accessible,support higher foraminiferal standing stocks as well as amuch higher proportion of calcareous (fossilisable) speciesthan the abyssal plains (Gooday 2003; Gooday et al. 2008).Nevertheless, a fairly large body of faunal data from abyssalsites is available from the work of authors such as, amongmany others, Phleger et al. (1953), Streeter (1973), Lohmann(1978) and Mackensen et al. (1995) in the Atlantic Ocean,Corliss (1979) in the Indian Ocean, and Smith (1973) andSaidova (1975) in the Pacific Ocean. Here, we briefly reviewthe influence of productivity on deep-sea foraminiferal assem-blage characteristics, before presenting an analysis of selectedabyssal foraminiferal datasets. Our core dataset is derivedfrom a series of studies in the NE Atlantic by the senior authorand colleagues using a consistent methodology and including‘soft-shelled’ as well as the hard-shelled taxa (i.e. the ‘entirelive’ assemblage).

Background

Influence of productivity on the distribution and ecologyof foraminiferal species

Early studies emphasised water depth as a major control onforaminiferal distribution patterns (Phleger 1960). Later, itwas realised that the depth ranges of species varied geo-graphically, leading to the idea, particularly prevalent in the1970s and 1980s, that distributions were linked to bottomwater masses (Streeter 1973; Schnitker 1974, 1980; Douglasand Woodruff 1981). Although some water-mass attributes,e.g. current flow (Corliss 1983; Schőnfeld 2002) and thedegree of carbonate undersaturation (Bremer and Lohmann1982), strongly influence foraminiferal assemblage compo-sition (Mackensen et al., 1995; Murray 2006), small differ-ences in physico-chemical characteristics between bottomwater masses are unlikely to have much effect (Corliss et al.1984). Since the 1980s, increasing attention has focusedinstead on regional variations in surface productivity andthe resulting flux of labile organic matter (‘food’) to theseafloor (reviewed by Loubere and Fariduddin 1999;Gooday 2003). For example, on the NW African margin,Lutze (1980), Lutze and Coulbourn (1984) and Altenbach(1985) observed that Uvigerina peregrina is concentratedon an area of the continental slope south of Cap Blanc thatreceives a high flux of organic carbon to the seafloor linkedto upwelling. Subsequent studies have demonstrated linksbetween organic carbon fluxes and foraminiferal accumula-tion rates (Herguera and Berger 1991) and assemblage com-position on regional scales (Loubere and Fariduddin 1999and papers cited therein), as well as with the abundance (e.g.Altenbach et al. 1999), bathymetric distribution (De Rijk etal. 2000) and microhabitat occupancy (Corliss and Chen1988; Corliss and Emerson 1990; Jorissen et al. 1995;Jorissen 1999) of particular foraminiferal species.

In addition to its quantity, the seasonal variability andquality (lability) of organic matter reaching the deep-seafloor are believed to influence foraminiferal assemblagecomposition. In their review of the relationship betweenbenthic foraminifera and organic carbon fluxes to the seafloor, Loubere and Fariduddin (1999) conclude that theeffects of seasonality are particularly apparent where aver-age annual productivity is higher. Species linked to highseasonality include the so-called ‘phytodetritus species’,Alabaminella weddellensis and Epistominella exigua, whichrespond to seasonally-pulsed inputs of labile organic matterwith rapid growth and reproduction (Gooday 1988, 1993).Based on their analysis of core-top samples of Holocene agecollected between 2,178 and 4,673 m water depth in theNorth Atlantic, Sun et al. (2006) recognized an assemblagedominated by these two epifaunal/shallow infaunal speciesin areas characterised by a highly seasonal organic carbon

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flux. A Globocassidulina subglobosa–Epistominella umbo-nifera assemblage, on the other hand, was negatively corre-lated with seasonality in primary production. We considerthis study further in a later section. There also appears to be alink between some species and more degraded organic matter,an idea first suggested by Caralp (1989) based on faunal andbiochemical analyses of glacial and post-glacial sediments in acore from theMauritanianmargin. In the modern ocean, densepopulations of intermediate (Melonis barleeanum) and deep-infaunal (Chilostomella oolina and Globobulimina affinis)species are associated with accumulations of degraded organicmatter, for example in submarine canyons (e.g. Schmiedl et al.2000; Fontanier et al. 2005). These authors defined the degreeof degradation of organic matter by the ratio of phaeopigmentsto glucids (Caralp 1989) and the ratio of enzymaticallyhydrolysable amino acids to total hydrolysable amino acids(Fontanier et al. 2005).

Regional patterns in the quantity, quality and seasonalityof food supply are likely to be particularly important eco-logical drivers in the abyssal deep sea, where the physico-chemical conditions (temperature, salinity) are uniform andecosystems are food limited (Levin et al. 2001). In athoughtful article, Smith et al. (2008) argue that ‘manyaspects of ecosystem structure and function in the abyssare strongly modulated by the rate and nature of food fluxto the seafloor’. This conclusion is particularly relevant toforaminifera, many species of which feed at a low trophiclevel (Lipps and Valentine 1970; Gooday et al. 1992, 2008).

Patterns of deep-sea foraminiferal diversity in modernoceans

General characteristics

Gooday et al. (1998) reviewed the earlier literature on deep-sea foraminiferal diversity. Much of the published datarelate to ‘total’ (live+dead, but mainly dead) assemblagesthat have not been stained with Rose Bengal. Because thedead component has been averaged over centennial to mil-lennial time scales and subjected to taphonomic alteration(Wollenburg and Kuhnt 2000), total and dead assemblagesmay not reflect modern conditions (Murray 2000). In ageneral sense, however, they suggest that deep-sea forami-niferal assemblages typically exhibit high species richnessand relatively low dominance, with a long ‘tail’ of rarespecies. The relatively sparse data for stained assemblagesreveal that ‘live’ faunas have similar characteristics (Gooday1986); for example, 66–100 species were recognized insyringe subsamples (6.6 cm2 surface area) from the KaplanEast site (4,100 m water depth) in the eastern Pacific(Nozawa et al. 2006). Dominance is usually no more thana few percent, but increases to >10 % in cores where thesediment surface is overlain by a phytodetritus deposit

inhabited by opportunistic species (Gooday 1996; Goodayet al. 1998, 2010; Sun et al. 2006). Murray (2006: fig. 7.11therein) compiled data for benthic foraminifera (a mixture ofstained and unstained faunas) from various deep-sea regionsand concluded that diversity is not universally high in thedeep sea. This is certainly the case at bathyal depths oncontinental margins overlain by oxygen minimum zones(OMZs <0.5 ml l−1). Here, foraminiferal densities are oftenvery high but the assemblages exhibit low species richnessand high dominance by a few species that normally occupydeep-infaunal microhabitats (Phleger and Soutar 1973;Gooday et al. 2000, 2009). These assemblages appear toreflect a combination of low bottom-water oxygen concen-trations, which eliminate many species, and a high organic-matter input, which allows those species that can toleratelow oxygen concentrations to flourish (Levin and Gage1998; Gooday 2003; Levin 2003). Similar low diversity,high dominance assemblages occur in organically-enrichedsediments where oxygen disappears close to the sediment/water interface, although the bottom water is well oxygen-ated (e.g. Sen Gupta et al. 1981; Gooday et al. 2001).

Regional diversity trends

Species diversity in relation to bathymetric gradients has beena topic of interest since the advent of modern deep-sea biologyin the 1960s (e.g. Hessler and Sanders 1967; Buzas andGibson 1969). Early studies explained these patterns in termsof productivity (food availability), combined with predationand competition (e.g. Rex 1973, 1981, 1983). The data accu-mulated subsequently have tended to support this interpreta-tion, while also pointing to the modulating effects of factorssuch as physical disturbance and sediment grain-size diversity(Rex and Etter 2010; Leduc et al. 2011).

In the case of foraminiferal diversity, studies conductedin different regions have yielded contrasting trends withwater depth (Rex and Etter 2010: fig. 3.15 therein). In thewestern North Atlantic, the diversity (species per sampleand Shannon-Wiener index) of both ‘total’ and ‘live’assemblages increases in a non-linear fashion with depthto reach maximum values below 2,500 m (Buzas and Gib-son 1969; Gibson and Buzas 1973). Likewise, off NWAfrica, the numbers of ‘live’ species (per 100 specimens)increases down to >3,000 m (Lutze 1980). Possible reasonsfor the high foraminiferal diversity at abyssal depths includereduced metazoan predation and competition for food, andtheir ability to reproduce asexually (Rex and Etter 2010). Inthe Gulf of Mexico, species richness shows different pat-terns with depth in different regions. In the less productivewestern part, species numbers decline below the shelf, in thecentral part, they are strongly depressed at upper bathyaldepths off the Mississippi Delta before rising at lower bathyaldepths, and in the more productive eastern part, they exhibit a

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parabolic pattern, peaking at mid-slope depths (Rex and Etter2010: fig. 3.15 therein, based on data from Gibson and Buzas1973). Mediterranean assemblages likewise exhibit a broadpeak in species richness between 200 and 1,000 m, belowwhich values decrease down to 2,000–3,000 m (De Rijk et al.1999). In the Arctic Ocean, the species richness and diversityof ‘total’ (Lagoe 1976) and ‘live’ (Wollenburg and Kuhnt2000) faunas decreases with depth below 600 m. A similarpattern is evident in the Norwegian Sea (Rex and Etter 2010).A number of other studies, e.g. Timm (1992; ‘live’ faunas)and Cutter et al. (1994; ‘total’ faunas), revealed no particularbathymetric trends. These contrasting results probably reflectdifferences in the oceanographic characteristics of these dif-ferent regions, for example, the oligotrophic character of theArctic.

In more recent years, latitudinal trends in diversity to thenorth and south of the equator have been described in anumber of metazoan macrofaunal taxa (e.g. Rex et al. 1993;Stuart et al. 2003; Rex et al. 2000, 2005; Rex and Etter2010) as well as in benthic foraminifera. Thomas andGooday (1996) reported that a latitudinal gradient in deep-sea foraminiferal diversity developed in the Southern Hemi-sphere about 36 million years ago as a result of an increasedphytodetrital flux leading to an increased abundance ofopportunistic species. Based on an analysis of publisheddata, Culver and Buzas (2000) suggest that this gradientpersists in the modern ocean. They detected a decrease inthe species richness and diversity (α) of ‘total’ assemblages(∼2,000–4,000 m depth) with increasing latitude in bothHemispheres. Culver and Buzas also conclude that diversityis generally lower in the Northern than in the SouthernHemisphere. Based on an analysis of ‘total’ calcareousforaminiferal assemblages of presumed Holocene age,Corliss et al. (2009) found that species richness, Shannon–Wiener diversity, and evenness were fairly constant betweenthe equator and 40ºN in the North Atlantic, but weredepressed at higher latitudes (45–60ºN). The diversitymetrics showed no significant correlations with primaryproductivity but were more or less strongly related tothe degree of seasonality in primary production. Theseresults are consistent with previous evidence that theseasonal delivery of phytodetritus to the seafloor influ-ences the diversity of metazoans (e.g. Rex et al. 1993,2005) and foraminifera (Gooday et al. 1998).

Diversity responses in the palaeo-record

Analyses of Quaternary records have led to divergent hypoth-eses regarding the main controls on the diversity of deep-seaforaminifera over geological time scales. Theoretical studies(e.g. Allen et al. 2002) suggest that environmental temperaturecan influence species diversity through its effect on metabolicrates. Hunt et al. (2005) tested this ‘species-energy hypothesis’

by analysing the relationship between foraminiferal speciesrichness and temperature and productivity (inferred fromproxies) over the last 130,000 years in 10 cores from theAtlantic (24.7ºS to 58.9ºN; 1,685–3,547 m water depth) andPacific (47.8ºS to 34.2ºN; 2,169–2,664 m depth) Oceans. Theoverall relationship with temperature was positive and signif-icant whereas the overall relationship between productivityand species richness was negative and not significant. Theyattributed the relatively strong relationship with temperature tochanges in species distributions caused by species-level differ-ences in physiological tolerances or metabolic rates. Unfortu-nately, it was not possible to test whether the weaker linkbetween productivity and species richness resulted from thehump-shaped relationship (positive in oligotrophic, negativein eutrophic settings) between these two parameters (Levin etal. 2001). A recent comparison of changes in ostracod andforaminiferal diversity over the last 250,000 years on theShatsky Rise (North Pacific) concluded that temperature wasweakly and positively related to foraminiferal diversity andstrongly related to foraminiferal faunal composition (Yasuharaet al. 2012). The authors acknowledged the possible influenceof seasonality in productivity on foraminiferal diversity, butdid not include this factor in their models.

Wollenburg et al. (2007) came to somewhat differentconclusions based on benthic foraminifera in cores takenat 1,000–2,500 m water depth to the west and north ofSvalbard. Over the last 24,000 years, diversity was higherduring warmer periods (interstadial and interglacials) thanduring colder periods (stadial and glacials). Wollenburg etal. (2007) considered that abyssal benthic foraminiferal di-versity in the Arctic is related to North Atlantic sea surfaceclimate, which in turn impacts thermohaline circulation.More specifically, they conclude that variations in diversityare mainly a result of changes in food availability related tothe duration of minimum sea-ice cover. They acknowledgethe possible influence of temperature, but conclude that,because primary production is enhanced by warmer temper-atures, it is impossible to disentangle the influences of thetwo parameters. These studies suggest that the relationshipbetween foraminiferal diversity and productivity is com-plex, particularly in the Arctic Ocean, where it involves aninterplay between temperature and temperature-sensitivemetabolic functions, thermohaline circulation, seasonal icecover and primary production, with the latter possibly beingthe proximal factor (Wollenburg et al. 2007).

Methods

Sample collection and processing

We analysed datasets obtained using consistent methods byour research group from abyssal sites in the North Atlantic

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Ocean (Porcupine, Madeira, Cape Verde Abyssal Plains)(Gooday 1996), the North Pacific Ocean (Hori 2001; Todo2003), Equatorial Pacific Ocean (Nozawa et al. 2006;Ohkawara 2006), and the Southern Ocean (Weddell Sea)(Cornelius and Gooday 2004) (see Supplementary Materialfor complete dataset). All samples were collected using ahydraulically damped multiple corer that obtained coreswith a cross-sectional area of 25.5 cm2 (Atlantic, SouthernOcean) or 52.8 cm2 (Pacific). At the Pacific stations (2/3, 6a,15, 64), the top 3 cm of the entire core was subdivided into0.5-cm-thick layers (Gooday et al. 2004), although only thetop 1 cm of sediment was analysed. Each layer was fixedand stored in buffered 4 % formaldehyde solution (10 %formalin). In the laboratory, the upper 1 cm layer of wetsediment was split separately with a plankton splitter into 1/4 splits. One of these splits was then sieved into the follow-ing size fractions: >500, 250–500, 125–250, 63–125, and32–63 μm (Station 64) or >63 and 32–63 μm (Stations 2/3,6b, 15). The Atlantic cores were dealt with in a similarfashion, except that the 0–1 cm layer was not split andwas sieved into the following size fractions: >500, 150–500, 125–150, and 63–125 μm (Gooday 1996). In theWeddell Sea, 2–3 replicate subcores (surface area3.45 cm2) were taken from intact multicores using a cut-off 20-ml syringe. The upper 1 cm layer was wet-sieved into>300, 150–300, 125–150, and 63–125 μm fractions(Cornelius and Gooday 2004). The sieve residues werestained overnight with Rose Bengal to identify foraminiferaltests that were alive when captured, and wet sorted under astereo-microscope. All stained foraminifera, including soft-shelled monothalamous species, were included in the anal-yses. We base our analyses on the >63-μm fraction (i.e. allsize fractions>63 μm added together) of the 0–1 cm sedi-ment layer. The number of specimens per sample rangedfrom 85 (in a 3.45-cm2 subcore) to 2,250 (in a 25.5-cm2

core). Please see supplementary material for all originaldata.

In addition to data originating from our working group,we explored two published datasets that report values fordiversity indices together with mean annual productivityand other environmental information.

Diversity estimates and statistics

No single value index can simultaneously represent the fullcomplexity of biological diversity. We have therefore calcu-lated a range of diversity indices to examine the richness,heterogeneity and dominance aspects of diversity. The useof multiple indices also facilitates comparison with otherinvestigations. We follow Magurran (2004) for nomencla-ture and notation. The following indices were calculated, inmost cases using the PRIMER 6 software package (PRIM-ER-E): Margalef (DMg), Pielou (J´), Brillouin (HB), Fisher

(α), rarefaction (ES85, ES30), Shannon (H´2), and Simpson(1-λ´). Two other diversity measures, species density (S10 cm−2) and Berger-Parker (d), were derived by simplespreadsheet manipulation. In analysing diversity and otherparameters, we have employed Spearman’s rank correlation(see, e.g., Siegel and Castellan 1988), simple linear regres-sion and analysis of covariance (see, e.g., Steel and Torrie1981). All statistical operations were carried out using theMinitab 15 software package.

We present tabulations of multiple diversity indicescorrelated with multiple environmental factors. Somecaution is required when interpreting the significancelevels resulting from simultaneous testing of this kind.For example, adjusted p values are often employedusing the Bonferroni method (see, e.g., Sokal and Rohlf1995). Instead of this approach, we have directlyassessed the underlying sampling distribution using arandomization procedure (see, e.g., Manly 1997). Thenine diversity indices employed with our field data (33sites) were correlated with 100 sets of randomly gener-ated environmental factors, yielding 900 Spearman’srank correlation values. The frequency distribution ofthese values was then compared with that of the stan-dard two-tailed significance levels tabulated for Spear-man’s rank correlation. Our randomized values layinside the tabulated values, i.e. the standard tabulatedvalues produced conservative significance levels for thesimultaneous comparisons of our field diversity values.This result likely reflects the high degree of correlationbetween the various diversity indices (i.e. they are notindependent variables). For simplicity and repeatability,we report our results using significance levels from thestandard tabulation of Spearman’s rank correlation (i.e. aconservative interpretation in the present case).

Surface productivity and estimated organic matter fluxto the seafloor

To derive primary production values for our abyssal studysites, we extracted data from the Vertically Generalised Pro-duction Model (VGPM) of Behrenfeld and Falkowski (1997).The model was based on climatological monthly mean (1998–2007) level-3 SeaWiFS chlorophyll-a concentration, photosyn-thetically available radiation and Advanced Very High Reso-lution Radiometer sea surface temperature data downloadedfrom http://oceancolour.gsfc.nasa.gov and http://pathfinder.nodc.noaa.gov/. The VGPM dataset comprised global meanmonthly surface primary production (mg Cm−2 day−1) values,spatially averaged to a nominal 1º grid. The coefficient ofvariation was employed as a measure of seasonality in primaryproduction. Monthly average primary production values alongwith measured sea floor depths were used to predict flux ofcarbon to the seafloor with the Lutz et al (2007) algorithm. At

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four of the Antarctic sites (AND133, AND132, AND131 andAND134) seasonal ice cover resulted in missing values fromthe global 10-year monthly-average dataset (missing valuesoccurred if any data over the 10-year timespan were missing).For the Antarctic samples only, monthly VGPM primary pro-duction time-series data were extracted from 2002 until 2010.From these, monthly averages were calculated from the avail-able data (ignoring the months where ice or cloud coverresulted in no estimate of primary production). These monthlyaverages were then used in subsequent calculation of flux tothe seafloor.

‘Live’ foraminiferal density as a proxy for flux

Because estimates of surface primary productivity and theresulting flux of organic matter to the deep oceanfloorinvolve many uncertainties (Corliss et al. 2009), we alsouse the density of ‘live’ (stained) benthic foraminifera as aproxy for food availability. Biomass could be considered amore reliable proxy for food availability than density(Altenbach and Struck 2001). In order to test the relation-ship between density and biomass, we assembled literaturedatasets reporting both these parameters for deep-sea fora-minifera. There is a good correlation (log-log linear regres-sion r2072.3-95.7 %, ANOVA p<<0.001; rank correlation

p<0.002) for the three different size fractions examined(>37, >125, >250 μm) (Fig. 1).

Analysis of abyssal datasets

PAP, MAP, CVAP, North and Equatorial Pacific, WeddellSea

For these sites in the North Atlantic, Southern, andPacific Oceans (Fig. 2), we first took the density of‘live’ (stained) foraminifera as a proxy for organic mat-ter flux to the seafloor. When the entire dataset (33samples, >63 μm fraction) was analysed, rarefied spe-cies richness, different indices of species diversity[Shannon–Wiener (H'log2), Margalef, Brillouin, Fisherα, Simpson], evenness (Pielou index) and dominance(Berger–Parker) all showed a significant overall de-crease with increasing density (indicating increasingflux), whereas species density showed a significant in-crease (Table 1; Fig. 3). However, no diversity measureshowed a significant relationship with estimated primaryproduction or its seasonality. Estimated organic carbonflux to the seafloor was only significantly correlated(−ve) with two of the nine diversity measures tested(Margalef, Brillouin; Table 1).

Although they employed consistent methods, the analy-ses summarised above combined data from different oceansand from samples sorted by different people. They alsoinclude regions where the structure and dynamics of thephytoplankton communities are different, with potentialconsequences for the quality of organic matter sinking tothe sea floor. In order to test whether the rather heteroge-neous nature of this dataset obscured underlying diversity–productivity relationships, we conducted separate analyses(>63 μm fraction, including phytodetritus) of sites located inthe NE Atlantic and Equatorial Pacific (Table 2). The numb-ers of samples (n05) available from the Northern Pacificand Weddell Sea were too small to analyse separately. Forthe NE Atlantic (BIOTRANS, PAP, MAP, CVAP sites),there were significant relationships (−ve) between estimatedcarbon flux to the seafloor and all diversity measures, andbetween foraminiferal densities and all diversity measuresexcept the Margalef index. For the equatorial Pacific, rela-tionships were only significant between foraminiferal den-sity and species density (p<0.05) and between the estimatedflux and the Pielou index (p<0.005) (Table 2). Compared tothe >63-μm fraction (including phytodetritus), analysesbased on the >150-μm fraction of the NE Atlantic samplesyielded a similar number of significant correlations betweendiversity measures and foraminiferal densities, but fewercorrelations when flux estimates were used as proxies forfood availability (Table 3).

Fig. 1 Log–log plots and regressions of deep-sea foraminiferal bio-mass on density for three sieve-mesh size classes: >37 μm, log(B)0−0.2897+0.8290 log(D), ANOVA p<0.001, r2 89 % (data from Shir-ayama 1984, assuming a 50 % conversion of Ash-Free Dry Weight toorganic carbon; see Gerlach et al. 1985). >125 μm, log(B)0−0.1668+1.050 log(D), ANOVA p<0.001, r2 96 % (data from Kurbjeweit et al.2000). >250 μm, log(B)0−7,248+0.9515 log(D), ANOVA p<0.001,r2 72 % (data from Altenbach and Struck 2001)

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Other published datasets

We focus on two datasets, one from the Arctic and one fromthe North Atlantic. Other abyssal datasets (e.g. Mackensenet al. 1993; Harloff and Mackensen 1997; Schmiedl et al.1997; Kurbjeweit et al. 2000) either do not include enoughsampling points or do not encompass a sufficient range ofproductivity values to yield useful insights into productivity-

diversity relationships and therefore are not consideredfurther.

Arctic Ocean

Wollenburg and Kunht (2000), incorporating data fromWollenburg and Mackensen 1998), report diversity values(based on ‘live’ counts) from seasonally and permanently

Fig. 2 Locations of sampling sites from which data on ‘entire live’foraminiferal assemblages (i.e. Rose Bengal stained and including‘soft-shelled’ as well as hard-shelled species) have been obtained usingmore or less consistent methods. PAP Porcupine Abyssal Plain; BIOT

BIOTRANS site; MAP Madeira Abyssal Plain; CVAP Cape VerdeAbyssal Plain; AND ANDEEP Project sites; KAP KAPLAN Projectsites; PAC other Pacific sites

Table 1 Spearman’s rank cor-relations between environmentalparameters and diversity meas-ures for the complete >63 μm‘entire live’ data set (Atlantic,Pacific and Weddell Sea sam-ples, n 033)

Flux to seafloor calculated usingLutz et al. (2007) algorithm.Only significant (p<0.05) corre-lation coefficients are shown

CV coefficient of variation; nsnot significant; a0p<0.05;b0p<0.01; c0p<0.005;d0p<0.001

Depth(m)

Density(indiv.10 cm−2)

Primaryproduction(mg C m−2 day−1)

Flux toseafloor(mg Cm−2 day−1)

Seasonality(CV)

Species density(S 10 cm−2)

ns 0.812 d ns ns ns

Margalef (DMg) ns −0.409 a ns −0.435 a ns

Pielou (J´) ns −0.432 a ns ns ns

Brillouin (HB) ns −0.578 d ns −0.402 a ns

Fisher (α) ns −0.494 c ns ns ns

Rarefaction (ES85) ns −0.579 d ns ns ns

Shannon (H´2) ns −0.599 d ns ns ns

Simpson (1-λ´) ns −0.522 c ns ns ns

Berger-Parker (d) ns 0.437 a ns ns ns

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ice-covered areas of the Arctic Ocean (around Svalbard, theNansen and Amundsen Basins, and the Lapdev Sea).Wollenburg and Mackensen (1998) report flux to seafloordata to two decimal places. We have recalculated thesevalues using the same method (Suess 1980) to a higher

precision to avoid a high proportion of tied-ranks in thecorrelation analysis. When the entire depth range (94–4,427 m) is considered, diversity values (Fisher α) aresignificantly (p<0.001) correlated (+ve) with our recalcu-lated values for the organic flux to the seafloor, as well as

Fig. 3 Relationships betweenforaminiferal density andselected diversity measures forcomplete >63 μm dataset (n033). All four relationships arestatistically significant(p<0.005; see Table 1)

Table 2 Spearman’s rank cor-relations between diversitymeasures, foraminiferal densityand organic matter flux to theseafloor for NE Atlantic andEquatorial Pacific sites from the>63 μm ‘entire live’ data set

Flux to seafloor calculatedusing Lutz algorithm. Onlysignificant (p <0.05) correlationcoefficients are shown.

ns not significant; a0p<0.05;b0p<0.01; c0p<0.005;d0p<0.001

NE Atlantic (n011) Equatorial Pacific (n012)

Density(indiv.10 cm−2)

Flux to seafloor(mg C m−2 day−1)

Density(indiv.10 cm−2)

Flux to seafloor(mg C m−2 day−1)

Species density (S10 cm−2)

0.891 c 0.758 b 0.720 a ns

Margalef (DMg) ns −0.680 a ns ns

Pielou (J´) −0.909 d −0.922 d ns 0.821 c

Brillouin (HB) −0.745 a −0.877 c ns ns

Fisher (α) −0.700 a −0.817 c ns ns

Rarefaction (ES85) −0.845 c −0.918 d ns ns

Shannon (H´2) −0.764 b −0.849 c ns ns

Simpson (1-λ´) −0.855 c −0.941 d ns ns

Berger-Parker (d) 0.827 c 0.890 c ns ns

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negatively with water depth (Table 4; Fig. 4). Correlationsare also significant when only sites below permanent icecover (1,051–4,427 m; n035) (p<0.001) and those deeperthan 4,000 m (n015) (p<0.05) are included. Correlations(+ve) between live foraminiferal density and diversity aresignificant for the whole dataset (p<0.001) and for siteswith permanent ice cover (p<0.005), but not for the deepsites (Table 4; Fig. 4).

North Atlantic Ocean

Corliss et al. (2009) analysed unstained (live plus dead) cal-careous benthic foraminifera in 41 multicore, box core, andtrigger core samples from the North Atlantic (equator to 60ºN;2,118–4,673 m water depth). As discussed below, it could beargued that this study is compromised by the fact that the

foraminifera were extracted from samples that span the Holo-cene (the last 10,000 years). Nevertheless, it is one of the fewregional-scale studies that relates foraminiferal diversity tomean annual surface productivity in a central oceanic area,and is therefore worth examining. Based on the data presentedin Table 1 of Corliss et al. (2009), we compared the Shannon–Wiener index (H'loge), Sheldon’s Evenness (E; Sheldon 1969)and species numbers per sample against the seasonality indexof Sun et al. (2006) (also plotted by Corliss et al. in their fig. 3)and against flux rates to the seafloor calculated by applyingthe Suess (1980) formula to the primary production data inCorliss et al. (2009). There were no significant relationshipsbetween diversity parameters and flux (Fig. 5a). On the otherhand, as already reported by Corliss et al. (2009), H'loge, Eand species numbers showed significant correlations (−ve)with seasonality (Fig. 5b).

Table 3 Spearman’s rank cor-relations between environmentalparameters and diversity meas-ures for the >150-μm and>63-μm sieve-mesh fraction(including phytodetritus, P)(n08)

Flux to seafloor calculated usingLutz et al. (2007) algorithm.Only significant (p<0.05) corre-lation coefficients are shown

ns not significant; a0p<0.05;b0p<0.01; c0p<0.005

Density (indiv.10 cm−2) Flux to seafloor (mg C m−2 day−1)

>150 μm >63 μm + P >150 μm >63 μm + P

Species density (S 10 cm−2) ns 0.905 c ns 0.880 a

Margalef (DMg) −0.786 a ns ns ns

Pielou (J´) ns −0.881 b ns ns

Brillouin (HB) −0.786 a ns ns ns

Fisher (α) −0.762 a −0.762 a −0.762 a ns

Rarefaction (ES30) −0.810 a −0.810 a ns ns

Shannon (H´2) −0.762 a −0.762 a −0.762 a ns

Simpson (1-λ´) −0.810 a −0.810 a −0.786 a ns

Berger-Parker (d) ns 0.833 a 0.857 a 0.738 a

Table 4 Spearman’s rank correlations between environmental parameters and Fisher’s alpha diversity for Arctic Ocean datasets derived fromWollenburg and Mackensen (1998) and Wollenberg and Kuhnt (2000)

Depth (m) Flux to seafloor(g C m−2 year−1)

Density(indiv.10 cm−2)

Complete dataset (n089) Flux to seafloor (g C m−2 year−1) −0.920 d

Density (indiv.10 cm−2) −0.723 d 0.724 d

Fisher (α) −0.784 d 0.824 d 0.709 d

Sites below permanent ice cover only (n035) Flux to seafloor (g C m−2 year−1) −1.000 d

Density (indiv.10 cm−2) −0.746 d 0.746 d

Fisher (α) −0.690 d 0.690 d 0.478 c

Deep (>4,000 m) sites only (n015) Flux to seafloor (g C m−2 year−1) −1.000 d

Density (indiv.10 cm−2) ns ns

Fisher (α) −0.560 a 0.560 a ns

Flux to seafloor estimated from the authors’ depth and primary production data using the Suess (1980) equation. Only significant (p<0.05)correlation coefficients are shown

ns not significant; a0p<0.05; b0p<0.01; c0p<0.005; d0p<0.001

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Additional analyses of this dataset were carried out usingonly sites with a comparable range of estimated flux values(2–4 g C m−2 year−1) but including sites that could becategorized as more (seasonality index >0.5) or less (sea-sonality index <0.5) seasonal (Fig. 5c). This division corre-sponds with a N–S split of the sites at approximately43ºN, close to the region (34–41ºN) identified by

Merrett (1987) as a zone of faunal change in abyssaldemersal fish assemblages. It is also close to the bound-ary between two of the biogeographical provinces ofLonghurst (2006)-the North Atlantic Drift Province(NADR) and the eastern North Atlantic SubtropicalGyral Province [NAST(E)]. Variations in diversity(Shannon index, loge) were explored by analysis of

Fig. 4 Relationships betweenFisher’s alpha diversity, flux tothe seafloor and foraminiferaldensity for Arctic Oceandatasets derived fromWollenburg and Mackensen(1998) and Wollenburg andKuhnt (2000). a, b completedataset (94–4,427 m waterdepth; n089 samples); c, d sitesbelow permanent ice cover only(1,051–4,427 m; n035); e, fdeep-water sites only(>4,000 m; n015). Relation-ships (a–e) are statistically sig-nificant (p<0.05; see Table 4)

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covariance (ANCOVA; see, e.g., Steel and Torrie 1981)with more/less seasonal as a treatment and estimated

flux as a covariate. Within this subset of samples,diversity increases significantly (p<0.005) with flux for

Fig. 5 Relationships between Shannon diversity, primary productionseasonality index and flux to the seafloor for North Atlantic dataderived from Corliss et al. (2009). For the total dataset, the relation-ships with b seasonality index is statistically significant (p<0.001), butthat with a flux is not (p>0.05). When assessed for only those sites

with a common range of flux values (2–4 g C m−2 year−1) in more(index >4.5) and less (index <4.5) seasonal regions, flux has a signif-icant influence on diversity (p<0.005) as well as seasonality (p<0.001)when assessed using analysis of covariance (ANCOVA)

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both the seasonal and the non-seasonal sites, and overallis significantly (p<0.001) lower at the more seasonalsites compared to the less seasonal sites.

Discussion

Limitations of study

We analysed stained foraminiferal assemblages only in thetop 1 cm layer of sediment. However, foraminifera live todepths down to 10 cm or more in deep-sea sediments(Corliss 1985; Jorissen 1999) and we therefore underesti-mated diversity by confining ourselves to this upper layer.More complete diversity data are available in the case of twocores from the PAP and one from the MAP site that weresorted down to 10 cm depth (data in Gooday et al. 1998).Around two-thirds (∼66 % at PAP, 68 % at MAP) of allspecies were present in the 0–1 cm layer, and the values ofdiversity indices were depressed correspondingly. More-over, because a larger proportion of foraminifera live nearthe sediment surface in oligotrophic settings, the effect ofanalysing the top 1 cm is likely to change along a produc-tivity gradient. Nevertheless, sorting samples for soft-shelled as well as hard-shelled foraminifera is extremelytime consuming, making examination of deeper layers dif-ficult to achieve within a realistic time scale. The approachwe adopted did enable us to analyse replicate samples aswell as the finer sediment fractions (63–125 µm) that yieldsmall, shallow-infaunal species likely to respond to inputs oflabile organic matter.

Controls on abyssal foraminiferal diversity

Despite the geological evidence referred to above, tempera-ture does not appear to have much influence on the diversityof deep-sea metazoans and foraminifera in modern oceans.On the Scottish margin of the NE Atlantic, a strong corre-lation exists between macrofaunal diversity and temperaturevariation (range), although not with temperature itself (Bett2001). The diversity of benthic foraminifera in the modernArctic Ocean exhibits no obvious relationship to bottom-water temperature (Wollenburg and Kuhnt, 2000). Rex andEtter (2010) consider it ‘unlikely that temperature directlyaffects present-day bathymetric patterns of diversity’, al-though they do not rule out an effect at regional scales.Any such effect is likely to be minimal at abyssal depths,where there is little variation in bottom-water temperatures.

The links between productivity and regional and bathymet-ric patterns of diversity are reviewed by Levin et al. (2001)and Rex and Etter (2010), respectively. The latter authorsconclude that productivity levels at abyssal sites are not highenough to depress diversity (except perhaps locally, e.g.

around whale falls), and therefore diversity should increasealong a gradient of increasing productivity, as reported byGlover et al. (2002) for polychaetes in the equatorial Pacific.Foraminiferal diversity trends along deep-sea productivitygradients (e.g. bathymetric transects) suggests that they alsorespond in a unimodal fashion to increased organic loading(Rex and Etter 2010). At abyssal depths, providing there isenough food, diversity may remain high because of reducedcompetition and predation frommetazoans. In fact, foraminif-eral diversity is probably underestimated in most studies ofabyssal regions where soft-shelled, monothalamous andkomokiacean foraminifera, usually ignored in geological stud-ies, dominate benthic assemblages (Tendal and Hessler 1977;Bernstein et al. 1978; Nozawa et al. 2006). The inclusion ofthese delicate taxa may be one reason why our dataset revealsa negative relationship between productivity and abyssal fo-raminiferal diversity, whereas the Corliss et al. (2009) study,based on dead hard-shelled assemblages, indicates a positiverelationship. However, Wollenburg and Mackensen (1998)also report a positive relationship, despite the fact that theyinclude some delicate species (e.g.Hippocrepina flexilis, Hip-pocrepinella hirudinea).

Unfortunately, few data are available to explore thesecontradictions further. Moreover, our analysis of Atlantic,Southern Ocean and Pacific data obtained using the samemethodologies also yielded somewhat ambiguous results.When data from different oceans were combined and ana-lysed together, there were no significant relationships be-tween different diversity measures and either primaryproduction or the estimated organic carbon flux to the sea-floor. On the other hand, all diversity measures were relatedsignificantly (−ve) to the density of ‘live’ foraminifera.When data from the NE Atlantic were analysed separately,significant correlations emerged between all diversity meas-ures and flux values, as well as between most diversitymeasures and foraminiferal densities (Table 2). However,for the Equatorial Pacific sites, there was only one signifi-cant correlation, probably because the area covered by thesampling sites was much larger and therefore encompasseda greater range of complicating factors.

We draw two conclusions from these results. First, it ismore helpful to analyse diversity data obtained using consis-tent methods along a single productivity gradient spanningone ocean basin, or a series of adjacent basins, than fromwidely scattered and environmentally dissimilar regions ofthe World Ocean. This may reflect the fact that phytoplanktoncommunity structure and dynamics, and hence the quality ofsedimented organic matter, vary regionally in the ocean(Smith et al. 2008). Consequently, when comparisons aremade across regions and ocean basins, it cannot be assumedthat a particular level of organic carbon flux represents thesame food availability. Second, ‘live’ foraminiferal densitiesprovide a more accurate proxy of food availability than either

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mean annual surface productivity or the estimated flux oforganic carbon to the seafloor. Global models of flux to theseafloor derived from mean annual surface productivity can-not accurately reflect local to regional scale variations, letalone the food available to meiofauna-sized organisms livingwithin an area of the abyssal seabed measuring a few 10s ofcm2. Moreover, as discussed by Corliss et al. (2009), the mostextensive studies of organic carbon fluxes to the seafloor(Dunne et al. 2007; Lutz et al. 2007) failed to yield consistentestimates. Given these uncertainties, the densities of ‘live’foraminifera in single samples are likely to provide morerealistic estimates of the food available within small patchesof seafloor. This is particularly important in areas where thefood (e.g. phytodetritus) has a very patchy distribution bothspatially and over intra- and inter-annual time scales.

Live versus dead assemblages

One way to avoid the problems created by the spatial andtemporal patchiness of foraminiferal populations is to ana-lyse dead assemblages. These represent a time-averaged,and spatially-integrated view of species composition anddiversity, rather than the ‘snapshot’ provided by the ‘live’assemblage. Dead assemblages are usually dominated bycalcareous species, most of the agglutinated taxa havingbeen eliminated by taphonomic processes (e.g. Mackensenet al. 1990, 1993; Gooday 2003) that are likely to be partic-ularly intense at abyssal depths. Gooday and Hughes (2002)report that assemblages of dead calcareous foraminifera inthe 0–1 cm layer of multiple corer samples from a bathyal(1,920 m depth) site on the Scottish margin included morespecies than assemblages of stained calcareous foraminiferafrom the same cores. Moreover, the fact that the relativeabundance of dead species was very similar in foursamples, two from May 1998, before the spring bloom,and two from July 1998, after the spring bloom whenphytodetritus was present on the sea floor, suggests thatthe dead assemblage was well mixed. In contrast, therelative abundance of stained foraminifera showed con-siderable variation between cores with and without aphytodetritus layer.

In the North Atlantic studies referred to above, Sun et al.(2006) and Corliss et al. (2009) analysed ‘total’ (mainlydead) calcareous assemblages. They concluded that, al-though mean annual primary production was not significant-ly correlated with various diversity and equitabilitymeasures, these parameters were inversely correlated withseasonality of productivity. One problem with this approachis that bioturbation ensures that surficial deep-sea sedimentscontain a mixture of dead foraminiferal tests of differentages. This is likely to be particularly important in well-oxygenated abyssal sediment with low sedimentation rates.The samples studied by Sun et al. (2006) and Corliss et al.

(2009) were obtained from multicores, box cores, and trig-ger cores, but most were trigger-core tops, which presum-ably had suffered some loss of surficial material. Theauthors acknowledged these problems and made a thoroughassessment of the ages of their core tops based on δC13

records (Sun et al. 2006; Corliss et al. 2009). They elimi-nated those that yielded glacial ages and only included coreswith ages from the present to 10,000 years BP (theHolocene). Although relatively stable compared to thePleistocene, this period has been subject to some cli-matic oscillations (Bond et al. 1997) and it cannot beassumed that productivity patterns during the earlier partwere the same as those prevailing in the modern ocean.In the Sun et al and Corliss et al. studies, the problemof sediment mixing was probably exacerbated by theloss of some surface sediment. Although mixing is unavoid-able, such problems can be minimised by analysing surficialsamples obtained using a hydraulically-dampened multiplecorer or a similar device that obtains cores in which thesediment surface is more of less undisturbed.

Seasonality

The impact of seasonally-pulsed resources on benthic diver-sity is poorly understood. In both terrestrial and marinesystems, pulsed resource inputs, including food resources,can increase diversity when combined with non-linear pop-ulation responses (Chesson 2000; Snelgrove and Smith2002; Chesson et al. 2004). On the other hand, food pulsescan depress diversity in marine birds (Procellariiformes)because feeding is confined to periods of the year whenfood is abundant (Chown and Gaston 1999). For deep-seaforaminifera, seasonal deposits of food (phytodetritus) rep-resent the most important temporally variable resource.Aggregates of phytodetritus are often inhabited by forami-nifera, most of them belonging to a few opportunistic spe-cies. Combining these with the much more diverseassemblages occupying the underlying sediment increasesspecies richness slightly, but also increases dominance,thereby slightly depressing diversity (Gooday et al. 1998).This mechanism was invoked by Thomas and Gooday(1996) to explain a decrease after the late Eocene in fossilforaminiferal diversity at high latitudes. The analyses ofCorliss et al. (2009), referred to above, support the idea thatforaminiferal diversity is different in seasonal and non-seasonal areas of the North Atlantic.

Possible effects of climate change on abyssal foraminiferalfaunas

Smith et al. (2008) predict that rising levels of atmo-spheric CO2 and associated climatic changes will lead toa shift from pelagic ecosystems dominated by diatoms

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and large zooplankton to systems dominated by pico-plankton and microzooplankton. This transformation inthe nature of pelagic ecosystems would lead to a reduc-tion in overall primary production and the efficiencywith which organic carbon is exported from the eupho-tic zone, and hence a decrease in the amount andquality of the food available to the deep-sea benthos.The consequences of these changes for abyssal benthicforaminiferal faunas are likely to be considerable. Adecrease in the quantity and quality of available foodwill probably result in a reduction of foraminiferal bio-mass and, above the Carbonate Compensation Depth(CCD), an increase in the relative abundance of komo-kiaceans and other monothalamous taxa at the expenseof calcareous species. It has been suggested that thesestercomata-bearing foraminifera feed on bacteria anddegraded organic matter and have a slower metabolicrate than the more ‘advanced’ calcareous foraminifera(Gooday et al. 2008). A shift to dominance by theseforms is likely to have consequences for ecosystemfunctioning, notably the processing of labile organiccarbon. Such changes will probably be particularly ev-ident in the more eutrophic parts of the Atlantic Ocean,where the CCD is deeper than in the Pacific and cal-careous foraminifera are presently common at abyssaldepths. As Corliss et al. (2009) suggest, climaticchanges may also alter the extent of areas that experi-ence seasonal surface production. However, they con-clude that would have only a minor impact of benthicforaminifera species richness, diversity and dominance.

Future goals

1. Studies of abyssal foraminifera that include diversitydata are sparse and few span pronounced productivitygradients. There are also considerable inconsistencies inthe methods (e.g. different sampling gears, sieve sizefractions and sediment layers examined, inclusion orotherwise of delicate taxa, dry vs. wet sorting) used toanalyse deep-sea foraminiferal assemblages. Theseissues underline the need for a focussed research effortemploying consistent methods to characterise assemb-lages across productivity gradients or at sites of con-trasting productivity. Ideally, such studies should bebased on high-quality multiple corer samples in whichthe surficial flocculent sediment is retained and includethe deeper (>1 cm) sediment layers not analysed in thepresent paper. Among the possible target areas are twoabyssal sites, located at similar depths near the CrozetIslands (southern Indian Ocean), but characterised bydifferent levels of mean annual surface productivity(Wolff et al. 2011), and the equatorial Pacific, where a

productivity gradient is known to influence nematode(Lambshead et al., 2002) and polychaete (Glover et al.2002) diversity.

2. Abyssal foraminiferal assemblages, particularly thoselocated below the CCD across vast swathes of thePacific Ocean, are dominated by agglutinated andorganic-walled taxa, including those encrusting manga-nese nodules. It is important to incorporate these largelyundescribed taxa into diversity estimates, although thefragmentation of their fragile tests (Bernstein et al. 1978;Nozawa et al. 2006) and the sparse cytoplasm, whichoften makes it difficult to distinguish between ‘live’ anddead individuals, make this a challenging task.

3. Studies that combine an analysis of ‘live’ assemblages,which give a snapshot of diversity at a particular mo-ment in time, with dead assemblages, which provide aview of foraminiferal communities integrated over aperiod of decades or centuries, may be particularlyinformative.

4. Next Generation Sequencing approaches, which havealready proved applicable to deep-sea foraminifera(Pawlowski and Lecroq 2010; Lecroq et al. 2011), couldusefully be applied to assess diversity at abyssal sites.

Acknowledgements We thank Prof. Craig Smith for inviting one ofus (A.J.G.) to participate in the CeDAMar Synthesis Workshop onImpacts of Productivity Gradients on Biodiversity and EcosystemFunction in the Abyss (Friday Harbor, 11–15 May 2009). We aregrateful to our colleagues Dr Stephanie Henson, Dr Veerle Huvenneand Ms Elizabeth Ross for implementing the VGPM primary produc-tion model and allowing us to access its output. We thank threeanonymous reviewers, and Craig Smith, for many helpful commentsand suggestions that substantially improved the paper. This paper is acontribution to the Oceans 2025 project of the UK Natural Environ-ment Research Council.

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