Iterative evolution of digitate planktonic foraminifera

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Iterative evolution of digitate planktonic foraminifera

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Coxall, Helen K.; Wilson, Paul A.; Pearson, Paul N. and Sexton, Philip F. (2007). Iterative evolutionof digitate planktonic foraminifera. Paleobiology, 33(4) pp. 495–516.

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Paleobiology, 33(4), 2007, pp. 495–516

Iterative evolution of digitate planktonic foraminifera

Helen K. Coxall, Paul A. Wilson, Paul N. Pearson, and Philip F. Sexton

Abstract.—Digitate shell morphologies have evolved repeatedly in planktonic foraminiferathroughout the Cretaceous and Cenozoic. Digitate species are usually rare in fossil and modernassemblages but show increased abundance and diversity at times during the Cretaceous and mid-dle Eocene. In this paper we discuss the morphology and stratigraphic distribution of digitateplanktonic foraminifera and establish the isotopic depth ecology of fossil ones to draw parallelswith modern counterparts. �18O and �13C values of six extinct and two modern digitate species,from six time slices (Cenomanian, Turonian, Eocene, Miocene, Pleistocene and Holocene) have sim-ilar isotopic depth ecologies, consistently registering the most negative �13C and usually the mostpositive �18O compared to coexisting species. These results indicate a similar deep, subthermocline(�150 m) habitat, characterized by lower temperatures, reduced oxygen, and enrichment of dis-solved inorganic carbon. This is consistent with water-column plankton studies that provide in-sight into the depth preferences of the three modern digitate species; in over 70% of observationsdigitates occurred in nets below 150 m, and down to 2000 m. The correlation between digitatespecies and subsurface habitats across multiple epochs suggests that elongated chambers were ad-vantageous for survival in a deep mesopelagic habitat, where food is usually scarce. Increasedabundance and diversity of digitates in association with some early and mid-Cretaceous oceanicanoxic events, in middle Eocene regions of coastal and equatorial upwelling, and occasionally insome modern upwelling regions, suggests an additional link with episodes of enhanced ocean pro-ductivity associated with expansion of the oxygen minimum zone (OMZ). We suggest that the pri-mary function of digitate chambers was as a feeding specialization that increased effective shellsize and food gathering efficiency, for survival in a usually food-poor environment, close to theOMZ. Episodes of increased digitate abundance and diversity indicate expansion of the deep-waterecologic opportunity under conditions that were unfavorable to other planktonic species. Our re-sults provide evidence of iterative evolution reflecting common functional constraints on plank-tonic foraminifera shell morphology within similar subsurface habitats. They also highlight thepotential of digitate species to act as indicators of deep watermasses, especially where there wasexpansion of the OMZ.

Helen K. Coxall and P. N. Pearson.* School of Earth, Ocean and Planetary Sciences, Cardiff University,Main Building, Cardiff, CF10 3AT, United Kingdom. E-mail: [email protected]

P. A. Wilson and P. F. Sexton.* School of Ocean and Earth Science, National Oceanography Centre, South-ampton, European Way, Southampton, SO14 3ZH, United Kingdom

*Present address: Scripps Institution of Oceanography, University of California, San Diego, La Jolla, Cal-ifornia 92093-0244, and School of Earth, Ocean and Planetary Sciences, Cardiff University, Main Build-ing, Cardiff, CF10 3AT, United Kingdom

Accepted: 13 June 2007

Introduction

The fossil record of planktonic foraminiferareveals the repeated evolution of chambershapes and shell morphologies during inde-pendent Cretaceous and Cenozoic evolution-ary radiations (e.g., Berger 1969; Cifelli 1969;Frerichs 1971; Steineck and Fleischer 1978;Lipps 1979; Hart 1980; Caron and Homewood1983; Leckie 1989; Norris 1991; Pearson 1996;Moullade et al. 2002). Identifying biotic andabiotic factors that have played a role in selec-tion of morphologies across these radiations isa continuous goal for micropaleontologistsand an important area of research for pale-ontology in general. However, linking plank-

tonic ecology with shell morphology has beenproblematic, and isotopic data do not reveal aconsistent correlation with preferred depthhabitat among most common globular andcompressed shell morphologies (Berger 1969;Cifelli 1969; Frerichs 1971; Lipps 1979; Hart1980; Caron and Homewood 1983; reviews inCorfield and Cartlidge 1991, and Pearson1998).

A conspicuous but usually rare element ofplanktonic foraminifera assemblages through-out the Cretaceous and Cenozoic are ‘‘digitate’’planktonic foraminifera, i.e., forms that have oneor more chambers of the adult whorl radiallyelongated to form distinctive fingerlike exten-

496 HELEN K. COXALL ET AL.

sions. Little is known about the ecology of dig-itate species because of their scarcity and patchydistribution. Limited plankton-tow data (e.g.,Rhumbler 1911; Bradshaw 1959; Be 1977) havesuggested an unusually deep dwelling habitatfor modern digitates and a similar ecology hasbeen predicted for fossil species on the basis ofmorphological similarities (e.g., Berger 1969; Ci-felli 1969; Frerichs 1971; Steineck and Fleischer1978; Hart 1980; Caron and Homewood 1983;Leckie 1989; Norris 1991; Pearson 1996; Moul-lade et al. 2002). Several reports have also linkeddigitates from the Recent, Eocene, and Creta-ceous with enhanced surface ocean productivi-ty and/or low-oxygen conditions (e.g., Brad-shaw 1959; Magniez-Jannin 1998; Coccioni et al.2006; Coxall and Pearson 2006). These observa-tions suggest a correlation between digitateshell morphology and the environment but sup-porting data have been lacking. Here we test thehypothesis that digitate shell morphology is afunctional specialization to a deep-dwellingecology by comparing the isotopic paleodepthsignatures of digitate species from multiple timeslices. By integrating the geochemical data withstratigraphic and paleoenvironmental informa-tion, and with existing water-column planktonsampling data, we are able to explore parallelsbetween fossil and modern counterparts and as-sess the paleoceanographic significance of theseenigmatic forms.

Shell Function and Depth Ecology. Deter-mining the functional morphology of forami-nifera shells is a challenge because of theirsmall size (�1 mm), the difficulties in sustain-ing them under laboratory conditions, and thelimitation of their fossil remains and encasingsediment to provide environmental informa-tion. Oxygen and carbon stable isotopes (�13Cand �18O) measured on foraminiferal shell cal-cite can provide valuable insights into plank-tonic ecology that can be used to test aspectsof functional models for chamber design re-lated to depth habitat.

The method relies on isotope fractionationprocesses occurring in the water column. Ox-ygen isotope fractionation between ambientseawater and foraminiferal calcite during cal-cification is temperature dependent. Thismeans that depth-stratified foraminiferal as-semblages from open-ocean sites can be ex-

pected to exhibit a trend of increasing fora-miniferal �18O with depth that parallels thetrend of decreasing temperature (Fairbanks etal. 1980, 1982). Species living in the warmestwaters closest to the surface, therefore, regis-ter more negative �18O than deeper dwellersand bottom living (benthic) species. In con-trast, foraminiferal �13C decreases with depthbecause of the preferential uptake of 12CO2

during photosynthesis in the surface euphoticzone and its subsequent remineralization backinto the �CO2 pool by respiration at depth. Asa result, dissolved inorganic carbon (DIC) inthe modern surface ocean may be 1‰ to 2‰more positive than the �13C of DIC in the deepocean (Kroopnick 1985) and the shells of sur-face dwelling forms would be expected tohave more positive �13C values than deeperdwellers. However, �18O and �13C values canbe offset from ‘‘equilibrium’’ with ambientseawater by the effect on isotope fractionationof environmental parameters such as [CO3

2�]and pH (Spero et al. 1997; Zeebe 1999) orphysiological processes such as symbiont pho-tosynthesis or foraminiferal respiration (Spe-ro and Williams 1989; Spero et al. 1991; Speroand Lea 1993, 1996; Ortiz et al. 1996). Despitethese complications, which tend to affect �13Cmore than �18O, the basic pattern of forami-niferal �18O and �13C variation with water-col-umn depth facilitates the reconstruction offossil foraminiferal depth habitats based onthe relative stable isotope offsets between spe-cies in an assemblage (see Spero 1998; Pearson1998; Pearson et al. 2001; Sexton et al. 2006).This method is used widely to identify fora-miniferal tracers of shallow and deep water-masses on multiple geological scales.

Previous stable isotope and environmentalinterpretations have suggested some function-al fits between various planktonic foraminif-era groups but there are plenty of non-ana-logues. For example, the Paleogene morozo-vellids and Cretaceous globotruncanids hadcomparable ornate keeled shells and their iso-topic signatures suggest they were both sur-face dwelling and symbiotic (Houston andHuber 1998; Norris 1996). The living speciesGloborotalia menardii, which has a keeled un-ornamented shell, and its Paleogene analogueGlobanomalina pseudomenardii are or were both

497DIGITATE FORAM ITERATIVE EVOLUTION

deep dwellers (Hemleben et al. 1989; Olsson etal. 1999). This is where the similarities end, be-cause the Eocene G. menardii-analogue Turbo-rotalia cunialensis was a surface mixed layerform (Pearson et al. 2006b), whereas counter-parts from the Cretaceous occurred in bothshallow (Planomalina buxtorfi) and deeper (Ro-talipora spp.) habitats (Wilson and Norris2001). Among the ‘‘globigerine’’ morphotypesthere are also differences in depth habitat. Forexample, modern Globigerinoides sacculifer andG. ruber live in shallow surface waters whereasPaleogene analogues in the genus Subbotinaroutinely register deep, probably thermoclineisotopic signatures (Olsson et al. 2006a). Smalltriserial forms on the other hand, which occurin modern oceans and throughout the Creta-ceous and Paleogene, are or were all surfacedwellers, specialized to continental marginupwelling environments and unstable marineconditions generally (Kroon and Nederbragt1990).

In many of these examples the functionalcomparisons are less than perfect becausethere are usually fine-scale differences in mor-phology beyond the general form (e.g., keelsmay be double or single, ornamentation maybe built of muricae or pustules), indicatingthat there have been various structural con-vergences that may not always have similarfunctions in detail. The correlation betweenmorphology and depth habitat is also far fromsimple, because, as in the case of the moderncompressed globorotaliids, some species mi-grate from the surface to deeper parts of thewater column during ontogeny. Digitate mor-phologies, however, which involve simpleelongations of individual chambers, are morelikely to be homologous structures and, wesuppose, are more likely to have a similarfunction.

Materials and Methods

The stratigraphic distribution of digitateplanktonic foraminifera from the Cretaceousand Cenozoic was recorded from new micro-paleontological observations in deep-sea corematerial and the literature. Morphologies areconsidered digitate if one or more adult cham-bers are radially elongated and have an aspectratio (chamber length divided by width at the

midpoint) of 1.5 or greater. This arrangementresults in widely separated chambers anddeeply incised sutures giving individuals adistinctly lobate outline. We include formswith bifurcating digitate chambers, as some-times occurs in the genus Leupoldina and inHastigerinella digitata but exclude Globigerinoi-des fistulosus, which has multiple protuberanc-es on individual chambers. By our definition,tubulospines, as occur in Hantkenina andSchackoina, do not alone constitute a digitateform because they are slender non-perforateprojections, whereas digitate chambers are ex-tended chambers with continuous wall tex-ture. The exceptions to this are the earliesthantkeninids and some schackoinids that havetubulospines (or prototubulospines, e.g.,Hantkenina singanoae [Coxall and Pearson2006]) emerging from elongated chambers.We regard tubulospines as a different struc-tural modification, although they may haveoriginally served a similar function (i.e., in in-creasing the effective size of the foraminifera).

Evidence for the distribution and ecology ofliving digitate species was synthesized fromthe literature and unpublished observationsfrom plankton surveys. A reconstruction ofthe geographic distribution of digitate specieswas produced for the middle Eocene, a time ofhigh digitate diversity that is well representedin deep-sea and continental margin sedi-ments. �13C and �18O analysis was used to in-vestigate the paleoecologies of digitate hom-eomorphs from six time-slices in seven mid-to low-latitude deep-sea sites in the Atlanticand Pacific Oceans (Table 1). Preservation offoraminiferal specimens varied between sites.Cenomanian, Turonian, and Pleistocene sam-ples show excellent (glassy) preservation (seeWilson and Norris 2001; Pearson et al. 2004;Sexton et al. 2006). Scanning electron micro-scope (SEM) examination reveals neomorphicrecrystallization of foraminiferal calcite at themicron scale (see Sexton et al. 2006) in theMiocene and Eocene material, suggesting thatthe primary isotopic signal has been partiallyaltered through diagenesis. The effect of dia-genetic alteration on planktonic foraminiferalcalcite close to the seafloor will be to increaseoxygen isotope values, and this effect will begreatest at low latitudes (where the vertical


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temperature gradient in the water column isgreatest and where sedimentation rates arelow; Schrag et al. 1995; Rudnicki et al. 2001).Previous studies have demonstrated, however,that interspecies offsets, which we assume re-flect original differences in depth habitat, aremaintained despite such minor alteration, al-though the absolute �18O values are likely tobe artificially increased and the multispeciesgradient compressed (Corfield et al. 1990;Pearson et al. 2001; Sexton et al. 2006).

�13C and �18O was measured on monospe-cific samples of digitate morphotypes plusthree or more additional taxa and a benthicspecies (where possible) from each assem-blage representing a range of mixed-layer anddeeper-water ecologies. Samples were com-posed of 2–25 specimens, depending on spe-cies size and abundance (Appendix). Analyseswere performed at the National Oceanogra-phy Centre in the United Kingdom, using aEuropa Geo 20–20 mass spectrometerequipped with a ‘‘CAPS’’ automatic carbonatepreparation system and at Cardiff Universityon a MAT252 gas source mass spectrometerwith an automated KIEL device. Results arereported relative to Vienna Pee Dee Belemnitestandard (VPDB). Standard analytical preci-sion is better than 0.1‰ for �18O and �13C forall data.

Results

Digitate Species in the Cretaceous and Cenozo-ic. We recognize a minimum of 27 digitatespecies in 13 genera (Fig. 1), each havingchamber aspect ratios of 1.5 or greater in oneor more of the adult chambers (Table 2). Thenumber of chambers in the final whorl is con-sistent within species but varies from 3.5 to 7between taxa. The distal ends of the chambersalso vary between species, ranging from sim-ple and rounded (e.g., ‘‘Hedbergella’’ simplex,Clavigerinella eocanica, and Clavatorella bermu-dezi), to bulb-like (e.g., Leupoldina spp., Clavi-hedbergella watersi, Clavigerinella akersi) orpointed (Clavihedbergella alexanderi, Clavigeri-nella caucasica, and Globigerinella adamsi). Coil-ing is mostly low trochospiral or planispiralexcept in Beella digitata and Hastigerinella digi-tata, which tend to show more irregular coil-ing patterns. SEM imaging reveals differences


FIGURE 1. The stratigraphic distribution of living and fossil planktonic foraminifera with digitate morphologies,highlighting the iterative evolution of this morphology in successive evolutionary radiations. Foraminiferal diver-sity trends (right) from Norris (1991) and Leckie et al. (2002). Ranges are approximate because occurrences aresporadic. Note: The Pliocene to Holocene timescale is exaggerated. Data sources—Cretaceous: Longoria 1974; Mag-niez-Jannin 1998; Premoli Silva and Sliter 1999; Verga and Premoli Silva 2002; Coccioni et al. 2006; Mesozoic Plank-tonic Foraminifera Working Group. Paleogene: Coxall and Pearson 2006; Quilty 1976; de Klasz et al. 1987; Cicha etal. 1998. Neogene–Quaternary: Cicha et al. 1998; Kennett and Srinivasan 1983; Pearson 1995; Saito et al. 1976; Sri-nivasan and Kennett 1975. Generic abbreviations: B. Beella, C. Clavihedbergella, Cl. Clavigerinella, Clt. Cla-vatorella, E. Eohastigerinella, G. Globigerinella, Gn. Globigerinelloides, H. Hedbergella, Ha. Hastigerinella,Hastigerin. Hastigerinoides, Hk. Hantkenina, L. Leupoldina, P. Parasubbotina. Arrows on the right identifyCretaceous oceanic anoxic events (OAEs) of the Mediterranean Tethys (after Coccioni et al. 2006). W Weissert, F Faraoni. Ages of stage boundaries (left) are from Gradstein and Ogg (2004) for the Cretaceous and from Berggrenet al. (1995) for the Cenozoic.


TABLE 2. Aspect ratios of forms with elongated chambers measured in mm from Figure 1. Species marked with *are not considered ‘‘digitate’’ because their adult chamber aspect ratios are less than 1.5.

Species

Finalchamber

height

Finalchamber

width

Finalchamber

aspect ratio

Penultimatechamber

height

Penultimatechamber

width

Penultimatechamber

aspect ratio

Hastigerinella digitata 27.0 6.0 4.5 25.0 6.0 4.2Globigerinella adamsi 28.0 6.0 4.7 26.0 7.0 3.7Beella digitata 20.0 7.5 2.7 18.0 11.0 1.6Protentella spp. 21.0 9.0 2.3 11.0 5.0 2.2Clavatorella bermudezi 19.0 10.0 1.9 13.0 5.0 2.6‘‘Clavigerinella’’ nazcaensis 18.0 7.0 2.6 14.0 6.0 2.3Clavigerinella eocanica 17.0 9.0 1.9 11.0 6.0 1.8Parasubbotina paleocenica 17.5 12.0 1.5 13.0 8.0 1.6Clavigerinella akersi 16.0 6.0 2.7 16.0 6.0 2.7Clavigerinella jarvisi 26.0 7.0 3.7 17.0 6.0 2.8Clavigerinella colombiana 18.0 7.0 2.6 17.0 7.0 2.4Clavigerinella caucasica 26.0 7.0 3.7 16.0 7.0 2.3Hantkenina mexicana 17.0 10.0 1.7 12.0 7.0 1.7Clavihedbergella subcretacea 15.0 7.0 2.1 15.0 7.0 2.1Eohastigerinella watersi 23.0 6.0 3.8 15.0 5.0 3.0Hedbergella alexanderi 30.0 5.0 6.0 21.0 4.0 5.3Eohastigerinella subdigitata 15.0 6.0 2.5 11.0 7.0 1.6‘‘Globigerinelloides’’ clavata 14.0 9.0 1.6 10.0 9.0 1.1Hastigerinoides sp. 24.0 7.0 3.4 10.0 9.0 1.1Schackoina multispinata 15.0 6.0 2.5 10.0 5.0 2.0Clavihedbergella moremani 21.0 7.0 3.0 11.0 6.0 1.8Clavihedbergella sp. 19.0 6.0 3.2 11.0 7.0 1.6Leupoldina reicheli 15.0 5.0 3.0 14.0 7.0 2.0Leupoldina cabri 22.0 3.0 7.3 18.0 3.0 6.0Leupoldina pustulans 12.0 3.5 3.4 12.0 3.0 4.0Hedbergella bizonae 17.0 8.0 2.1 10.0 8.0 1.3‘‘Hedbergella’’ simplex 15.0 7.0 2.1 11.0 7.0 1.6Globigerinelloides saundersi* 12.0 9.0 1.3 11.0 8.0 1.4Hedbergella roblesae* 12.0 13.0 0.9 14.5 11.5 1.3Hastigerinella semielongata* 17.0 12.0 1.4 15.0 11.5 1.3

in wall texture between homeomorphs, vary-ing from smooth or weakly cancellate andprobably sparsely spinose (Clavigerinella [Cox-all and Pearson 2006]) to honeycomb-spinose(Globigerinella, Beella), monolamellar, triradi-ate-spinose (Hastigerinella) (Saito et al. 1976;Hemleben et al. 1989), microperforate (Leupol-dina [Verga and Premoli Silva 2002]), andsmooth pustulose (Hedbergella, Globigerinelloi-des, and Clavihedbergella [BouDagher-Fadel etal. 1997; Wilson et al. 2002; Mesozoic Plank-tonic Foraminifera Working Group 2006]).These wall textures define independent phy-logenetic groups that evolved during succes-sive evolutionary radiations (e.g., Olsson et al.1999; BouDagher-Fadel et al. 1997; Moulladeet al. 2002) and highlight the convergence onthe digitate form. In B. digitata, only one ortwo chambers are elongated and the degree ofelongation varies significantly between speci-mens.

Digitate morphologies first appeared mid-way through the Early Cretaceous (Barremi-an–Aptian) and occur throughout the remain-der of the Cretaceous and Cenozoic with threespecies living today (Fig. 1). None survivedthe K/T extinction or late Eocene turnoverthat define the bases of the major epoch-span-ning evolutionary radiations. They were mostdiverse in the Aptian (eight species), the Tu-ronian to Santonian (eight species) and the lat-est early middle Eocene (six species). Theywere less diverse in the Paleocene, late Eoceneto early Oligocene, and most of the Neogene.This may reflect lack of study or climaticallydriven changes in pelagic environments overtime that influence the occurrence of digitatespecies. The list of taxa presented in Figure 1may not be exhaustive by some workers’ stan-dards because of the different taxonomicschemes currently in use. Cretaceous taxono-my, especially, is less stable than that of the


Cenozoic (see BouDagher-Fadel et al. 1997;Moullade 2002) but most workers accept thegeneric classification of Loeblich and Tappan(1988), separating planispiral clavate (Eohas-tigerinella), planispiral tapering (Hastigerinoi-des), and trochospiral clavate (Clavihedbergella)(B. Huber personal communication 2007), andFigure 1 has been constructed to reflect thisscheme. Despite differences in taxonomicopinion, we believe that the list is largely rep-resentative of the generic and specific diver-sity across epochs and should therefore cap-ture the essence of the stratigraphic distribu-tion of taxa exhibiting digitate morphologies.Moreover, our definition of digitate form (i.e.,elongate chamber(s) with an aspect ratiogreater than 1.5) will exclude some taxa thatother workers may consider digitate (e.g., Hed-bergella bollii, Claviblowiella sigali) (Table 2).There are also other genera, e.g., Protentella,that may meet our criteria for being digitatebut whose specific diversity is still unre-solved.

Ecology of Living Digitate Species. There arethree digitate species living today, Globigeri-nella adamsi (Banner and Blow 1959), Beella dig-itata (Brady 1879), and Hastigerinella digitata(Rhumbler 1911). None have been observedalive in the laboratory and only limited infor-mation is available on their ecology and en-vironmental preferences. All three species arerestricted to the low and mid latitudes (Table3) and are typically rare in open-ocean water-masses and underlying sediments. Beella dig-itata is more common than G. adamsi and H.digitata and occurs throughout the Atlanticand Mediterranean (Gross 2001; Hemleben etal. 1989), whereas the latter two species arethought to be mostly restricted to the Indianand Pacific Oceans (Bradshaw 1959; Be andTolderlund 1971). Because of its delicate mon-olamellar shell wall, H. digitata has an ex-tremely low preservation potential and is rare-ly seen in sediments (Hilbrecht 1996). Thereare several records, however, of modern digi-tate species occurring at unusually high abun-dance levels (5–10% of assemblage), e.g.,abundant G. adamsi in the South Pacific region(Brady 1884), west-central Equatorial Pacific,and off Japan (Bradshaw 1959). In addition,numerous H. digitata have been recorded on

video film by a remotely operated submers-ible vehicle (ROV) in Monterey Bay, California(S. Haddock, MBARI, unpublished), a regionthat is known for the strong seasonal upwell-ing and pronounced oxygen minimum con-ditions. None of these unusual occurrences,however, have been systematically studiedand presently they provide little informationabout the environmental preferences of mod-ern digitate species.

Rare observations of digitate species inplankton studies reveal deep habitats, usuallybelow 200 m; in over 70% of observations dig-itates occurred in nets below 150 m, and some-times as deep as 2000 m (Table 3). The Mon-terey Bay ROV observations also support adeep habitat for H. digitata, with concentra-tions observed at depths of approximately 200m, i.e., below the base of the seasonal ther-mocline (S. Haddock personal communication2002). Examination of ingested material inrare captured specimens suggests that H. dig-itata, like its close relative H. pelagica, is strictlycarnivorous (Rhumbler 1911; C. Hemlebenpersonal communication 2005), whereas B.digitata and G. adamsi are thought to be om-nivorous (C. Hemleben personal communica-tion 2005). Symbionts have not been observedin H. digitata or B. digitata (M. Kucera personalcommunication 2007). No information is avail-able on symbiotic associations of G. adamsi.

Although usually restricted to the low andmid latitudes, B. digitata has been reported inPleistocene sediments from the Rockall Chan-nel, 60�N (northeast Atlantic) (Holmes1984), together with a second species of Beella,B. megastoma Earland. However, the specimensof B. digitata illustrated by Holmes (1984: p.102, Pl. 1, Figs. 6, 7) do not possess the radiallyelongate chambers characteristic of B. digitatasensu stricto (i.e., with adult-chamber aspectratios of 1.5 or greater), suggesting that thesehigh-latitude forms represent morpho- andecotypes different from the extreme digitateforms found at lower latitudes. Interestingly,abundance spikes of B. megastoma in the Nor-wegian-Greenland Sea have been correlatedwith meltwater pulses associated with latePleistocene glacial terminations (Bauch 1994).Although these northerly occurrences of Beellaspp. are clearly of paleoceanographic interest,


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we suggest they are unrelated to the distri-butional patterns of B. digitata s.s. and do notconsider them further in this paper.

This collection of observations providesonly limited insights into the ecology and dis-tribution of modern digitate species. However,the available evidence suggests a consistentlydeep dwelling habitat (�200 m) below thethermocline, for all living digitate species dur-ing some stage of the life cycle.

Stable Isotope Paleoecologies. Figure 2 shows�18O and �13C values of fossil digitate speciescompared to other planktonic and benthicspecies (unadjusted) in the same sample fromsix time slices at seven different deep-sea sites.Interspecies offsets are assumed to reflectoriginal differences in depth habitat, with thedeep dwellers registering higher �18O andlower �13C than surface dwellers. The differ-ences in absolute and relative �18O reflect re-gional differences in surface-water (plankton-ics) and deep-sea (benthics) temperature, de-gree of thermal stratification, and depth of thethermocline (Berger et al. 1978; Arthur andNatland 1979; Bralower et al. 1995). Minor dia-genetic alteration may also contribute to in-creased absolute �18O values and an artificiallycompressed multispecies gradient in materialfrom ODP Sites 865 and 872 and Kane-9 PistonCore. �13C differences reflect patterns of globalcarbon storage, local productivity, and deep-water circulation.

Despite site-to-site isotopic differences, therelative depth ranking of digitate species an-alyzed is very similar in each time slice. Cre-taceous, Eocene, Miocene, Pleistocene, andHolocene digitate forms consistently registerthe highest or close to the highest �18O values(implying the coolest calcification tempera-tures) and usually the lowest �13C of all plank-tonic foraminifera. This finding is consistentwith limited isotopic data from previous in-vestigations into Eocene and Miocene digitatespecies (Pearson et al. 1993; Coxall et al. 2000,2003 on Clavigerinella; Pearson and Shackleton1995 on Clavatorella bermudezi) that suggest adeep-dwelling habitat.

Distribution of Eocene Digitate Forms. Themiddle Eocene was a time of increased digi-tate diversity, with up to six species of Clavi-gerinella and several species of Hantkenina with


FIGURE 2. Multispecies stable isotope arrays from six time slices (seven sites) showing the relative isotopic depth-ranking of digitate homeomorphs (black and gray diamonds) compared with co-occurring planktonic and benthicspecies (where possible). A, DSDP Site 137-12-5, 4–6 cm. B, DSDP 144A-6R-1, 141–142.5 cm, data from Wilson etal. (2002). C, ODP 865C-8H-3, 70–110 cm. D, Kane-9 Core-42, 470 cm. E. ODP 872C-9H-3, 95–97 cm. F, Box ERDC-92-5, 22–23 cm, data from Berger et al. (1978) except G. adamsi, which are new. Note: Variation in �18O and �13Cbetween sites reflect inter-basin and temporal differences in seawater isotopic composition. Generic abbreviations:A. Acarinina,* B. Beella, C. Clavihedbergella, Cb. Cibicidoides, Cl. Clavigerinella, Clt. Clavatorella, G. Globigerinella, Gd. Globigerinoides,* Gl. Globorotalia, Glm. Globanomalina, Glq. Globoquadrina, Gn. Globi-gerinelloides, Gu. Guembelitrioides, H. Hedbergella,* Het. Heterohelix,* M. Morozovella,* N. Neogloboquadrina,P. Parasubbutina, Pr. Praeglobotruncana, Pu. Pulleniatina, R Rotalipora, S Subbotina. *Inferred or known surfacedwellers (Wilson et al. 2002; Boersma et al. 1987; Pearson 1998; Berger et al. 1978; Hemleben et al. 1989). Data arepresented in Appendix 1.


FIGURE 3. Distribution of Clavigerinella spp. during the middle Eocene (46 Ma base map). The map was constructedusing the method outlined by Ziegler et al. (1985). Stippled fill indicates records where Clavigerinella spp. were foundat unusually high abundance levels (�10% of assemblage). The sediments in other Clavigerinella localities are fo-raminiferal oozes with higher species diversity more typical of the low latitudes. Questions marks identify recordswhere other microfossil and host sediment characteristics are unknown. Clavigerinella-rich samples typically containonly a few other species of planktonic foraminifera (e.g., Parasubbotina spp.) but are usually rich in radiolaria. SeeTable 4 for key to localities and data sources.

elongate chambers recognized. This time in-terval is relatively well represented in deep-sea and land sections and we have been ableto produce a paleogeographic reconstructionof Clavigerinella spp. in order to explore thepossible environmental controls on its distri-bution. The reconstruction was produced us-ing 29 records compiled from new observa-tions and the literature (Fig. 3). Paleo-coordi-nates of the Eocene localities are presented inTable 4. The reconstruction shows that Clavi-gerinella spp., comprising C. eocanica, C. akersi,C. jarvisi, C. caucasica, and C. colombiana, is re-stricted to the mid and low latitudes. Recordsare concentrated along segments of continen-tal margin (mostly western boundaries) andthe equatorial Pacific, with fewer occurrencesin fully open ocean regions. In 12 localitiesClavigerinella sp. was recorded as being unusu-ally abundant (�10% planktonic assemblage)and occurred in association with radiolarian-rich sediments, suggesting high surface-waternutrient availability. Today these regions arecharacterized by high productivity due to up-welling; an atmospheric general circulationmodel suggests similar high-productivityconditions prevailed during Eocene time(Huber and Sloan 2000).

Discussion

Depth Ecology. Our �18O and �13C data sug-gest that all the fossil digitate species investi-gated calcified their shells in a relatively coolwatermass with high DIC content, as occursbelow the surface mixed layer. The occurrenceof modern digitates in deep-towed planktonnets supports this interpretation. The deepchlorophyll maximum, situated within or justbelow the thermocline, represents a possiblehabitat for digitate species that provides foodat depth. Deep chlorophyll maxima, however,are widespread features in much of theworld’s oceans and should support largerpopulations of digitates than are observed.Therefore, we suggest that digitate specieshave more-specialized deep water ecologiesdefined by physio-biological structures unfa-vorable to most planktonic foraminifera spe-cies. The typical scarcity of digitates in deep-sea records is consistent with this hypothesisbecause fewer pelagic organisms live belowthe mixed layer outside of chlorophyll maxi-ma, and even fewer in the mesopelagic zone(200–2000 m), where food is usually scarcecompared to the epipelagic zone (0–200 m)(Gage and Tyler 1991; Wishner et al. 1995;Gowing and Wishner 1998).


TABLE 4. Reconstructed middle Eocene coordinates of the Clavigerinella-localities mapped in Figure 3.

ID Locality Palaeolat.Palaeo-

long. Source

1 ODP Site 865, Alison Guyot 4 �143 This study2 ODP Site 1218, Equatorial Pacific 0 �107 Lyle et al. 20023 DSDP Site 42, Equatorial Pacific �3 �106 McManus et al. 19704 Oregon Southern Coast Range, Elkton/upper Tyee Fm. 49 �98 McKeel & Lipps 19755 Oregon Coast Range Tyee, Yamhill & Nestucca Fms. 42 �104 McKeel & Lipps 19726 Mount Diablo, California 35 �104 Church 1931; Clark & Camp-

bell 19427 Santa Cruz Mts., California, San Lorenzo Fm. 20 �94 Poore & Brabb 19778 Veracruz, Mexico, Aragon Fm. 20 �76 Nuttall 19309 Arroyo San Carlos, Carmen de Bolivar Pste., Colom-

bia, Chengue Fm.0 �74 This study

10 Guayaquil, Ecuador �13 �64 Stainforth et al. 194811 San Cristobal, Peru, Talara & Sechura Fms. �13 �66 Cruzado Castaneda 198512 Parinas, Peru, Talara & Sechura Fms. �13 �68 Cruzado Castaneda 198513 El Alto, Lobitos, Peru �15 �65 Cruzado Castaneda 198514 ODP Site 683, Peru Continental margin �18 �64 Suess et al. 198815 Basal Salina, Peru, Chacra & Talara Fms. �21 �61 Cruzado Castaneda 198516 DSDP Site 390, Blake Nose 24 �61 Benson et al. 197817 DSDP Site 150, Aruba Gap, Venezuela 3 �60 Premoli Silva & Bolli 197318 Dept. of Bolivar, Colombia �1 �60 Petters 195419 San Fernando, Trinidad 4 �49 Bolli 195720 ODP Site 1258, Demerara Rise �1 �40 Erbacher et al. 200421 Kane-9 Piston Core, Endeavor Seamount 21 �19 This study22 DSDP Site 21, Rio Grande Rise �31 �9 Saito et al. 197623 DSDP Site 523, S. Atlantic �33 �2 Hsu et al. 198424 ODP Site 960, Cote d’lvoire �1 �3 Mascle et al. 199625 Alicante, S. Spain 31 3 Cremedes Campos 197826 Mattsee, Austria, Helveticum Section 47 8 Gorbandt 1967; this study27 Northern Caucasus Mts., Russia 48 36 Subbotina 195828 Kilwa, Masoko, Tanzania �12 40 Pearson et al. 200429 Khasi Hills, Assam, S. India 7 91 Samanta 1973

Upwelling and Oxygen Minimum Conditions.Increased abundance and diversity of digitatespecies in the Cretaceous and middle Eocene,and in restricted regions today, indicate thatthe digitate ecologic opportunity can be ex-panded at times. Examination of these concen-trations of digitates should provide further in-sight into their ecology.

Cretaceous digitate species occurred inwarm epicontinental sea localities as well as inthe deep sea (e.g., Eicher and Worstell 1970;Longoria 1974; Masters 1977; Premoli Silva etal. 1999) (Fig. 1). Unusually diverse assem-blages have been found in association with or-ganic-rich sediments preserved on continentalmargins that are the hallmark of Cretaceousoceanic anoxic events (OAEs) (e.g., Magniez-Jannin 1998; Aguado et al. 1999; Cobianchi etal. 1999; Premoli Silva et al. 1999; Luciani et al.2001; Leckie et al. 2002; Verga and Premoli Sil-va 2002; Coccioni and Luciani 2004, 2005; Coc-cioni et al. 2006). OAEs involved severe per-

turbations to the marine carbon system andpelagic ecosystems and in some cases were ac-companied by extinction of many surface-liv-ing planktonic foraminifera (Leckie et al. 2002;Coccioni et al. 2006). Their cause is widely de-bated. One theory is that tectonic events andwidespread transgressions led to stagnationof deep waters and creation of a large numberof salinity-stratified marginal basins (Erbach-er et al. 2001). Another is that bottom-waterand water-column dysoxia resulted from in-tensified surface productivity related to activesubmarine volcanism (e.g., Schlanger and Jen-kyns 1976; Premoli Silva et al. 1999; Leckie etal. 2002; Jenkyns 2003). The most widespreadOAEs—the Faraoni, OA1a, and OA2—arethought to have involved extensive eutrophi-cation (Leckie et al. 2002; Coccioni et al. 2006).These are also the times when digitate specieswere most abundant and diverse (Coccioni etal. 2006). The association has led to the sug-gestion that digitate species were specialists of


low-oxygen environments (e.g., BouDagher-Fadel et al. 1997; Magniez-Jannin 1998; Agua-do et al. 1999; Cobianchi et al. 1999; PremoliSilva et al. 1999; Luciani et al. 2001; Coccioniand Luciani 2004, 2005; Coccioni et al. 2006).

Digitates were also unusually diverse in themiddle Eocene (six species). There were nosedimentary equivalents to the CretaceousOAEs during this time but Clavigerinella spp.occurrence shows a correlation with increasedmarine productivity in regions of coastal andequatorial upwelling (Fig. 3). There is no di-rect evidence for intensified oxygen-minimumconditions preserved in these regions (i.e., inthe form of increased sedimentary organiccarbon), but pronounced OMZs may havebeen features of these environments, as theyare in modern upwelling regions (e.g., Wish-ner et al. 1995), even if there is no record insediments. It seems logical that usually raredeep-dwelling digitate species would prolif-erate during times of high productivity be-cause of increased food sinking out of the sur-face layer. However, surface productivity can-not be the principal control on digitate distri-bution because, besides the Cretaceous,middle Eocene, and Monterey Bay occurrenc-es, digitate species have not been reportedwidely in typical modern or early Neogeneupwelling systems (e.g., Arabian Sea and Ben-guela Current) (Prell and Curry 1981; Sum-merhayes et al. 1992; Little et al. 1997; Reichartet al. 1998). Therefore, specialization to OMZconditions, which may be a consequence of in-creased surface productivity, and whichwould be unfavorable to most planktonic spe-cies, seems plausible. A closer look at the anat-omy of OMZs reveals the hostilities faced bypelagic organisms and provides clues to theirpotential attraction.

OMZs are ubiquitous and persistent fea-tures of midwater depths in much of theworld’s ocean but they may become expandedthrough heightened marine productivity orreduced water-column ventilation (Wishner etal. 1995). Although plankton biomass and di-versity are dramatically reduced withinOMZs because of the limitations on aerobicrespiration, plankton may become abundantat the ‘‘redoxcline,’’ the level at the base of theOMZ (400 to 1100 m) where oxygen levels be-

gin to increase. High concentrations of organicparticles and bacteria at the redoxcline pro-vide an abundant food source to deep-dwell-ing plankton (Wishner and Gowing 1992;Wishner et al. 1995; Gowing and Wishner1998). Although no records of planktonic fo-raminifera have been obtained so far, it is pos-sible that deep-dwelling species, such as thedigitates, can survive in these environments,feeding directly on bacteria and organic par-ticles or preying on the primary consumers ofmicrobes, e.g., copepods. This hypothesis isconsistent with distribution patterns of digi-tates associated with Cretaceous OAEs; digi-tate species were absent from the core of theOAEs where minimum oxygen levels wouldhave prevented aerobic respiration, but theydiversified during the recovery phase (Coc-cioni et al. 2006), perhaps as oxygen levels be-gan to increase but food availability remainedhigh. Digitates may have been able to respondquickly to this expanding deep-water ecolog-ical opportunity because of their existing tol-erance of hostile deep-water conditions.

The unusually low shell �13C values seen insome digitate species, e.g., Clavigerinella spp.G. adamsi, and B. digitata, which are alwayslower than in other planktonic species andsometimes lower than in co-occurring benth-ics, are consistent with this hypothesis be-cause water-column �13C values reach a mini-mum within the OMZ (Fig. 4). However, giventhat foraminiferal shell carbon isotope valuesusually reflect a mixed signal of seawater �13Cand physiological fractionation effects (e.g.,Zeebe 1999; Ortiz et al. 1996; Norris 1998; Spe-ro 1998), it is possible that the depleted �13Cvalues are the result of a vital effect. One wayof enriching 12C is incorporation of metabolicCO2 into test calcite, although this effect haspreviously been recorded only in surfaceforms such as Globigerina bulloides and Globi-gerinella siphonifera, which tend to have unusu-ally high feeding rates (e.g., Spero and Lea1996; Bijma et al. 1998). Shell calcite isotopicdepletion might also be achieved by feedingon an isotopically ‘‘light’’ food source, e.g.,bacteria; it is possible that, as has been dem-onstrated for other mesopelagic microplank-ton (Wishner et al. 1995; Gowing and Wishner1998), a large part of the forams’ diet at these


FIGURE 4. A, Typical vertical profile of seawater dis-solved inorganic carbon (�CO2), �13C, and dissolved O2

from the North Pacific (Kroopnick 1985) to aid interpre-tation of carbon isotopes. OMZ, oxygen minimum zone.

depths was derived from bacteria-dependentfood chains, whose biosynthetic pathways re-sult in 13C-depleted organic matter (e.g.,Hayes 2001). Because it is difficult to imaginethat 13C depletion through physiological frac-tionation effects would occur to a similar ex-tent in multiple independently evolved digi-tate homeomorphs, we suggest that the �13C isprimarily an environmental signal.

These various strands of evidence support aconnection between digitate species and oxy-gen minimum zones but this cannot be the fullstory because not all OMZ environments areassociated with digitate species. A possibleexplanation for why H. digitata is common inMonterey Bay but not other upwelling regionsis that the low-oxygen watermass off Califor-nia and the eastern Pacific is more or less per-manent, whereas the low-oxygen conditionsin the Arabian Sea and Benguela systems arehighly seasonal. If digitate species were slowin maturing, low population densities mighthave prevented their persistence where theOMZ is seasonal. The lack of evidence for dig-itate evolution during episodes of increasedorganic-matter accumulation associated withPlio-Pleistocene sapropels (e.g., Rohling 1994;

Rohling et al. 2004) may reflect differences inthe causal mechanisms of the oceanic dysoxiaand its effect on deep-dwelling plankton as-sociated with the late Neogene events as com-pared to the Cretaceous OAEs.

Data are lacking for the Oligocene and Mio-cene but available records suggest that digi-tate species were less common from the lateEocene onward and they have never been asabundant or diverse as they were during theearly Aptian, Albian, and late Cenomanian(Coccioni et al. 2006). This may be because pe-riods of sustained and expanded OMZ con-ditions, which occurred more frequently un-der greenhouse climates because of reducedwater-column stratification and increased vol-canic input of biologically limiting nutrients(Leckie et al. 2002), became less frequent ascrustal production slowed and thermal anddensity stratification of the surface ocean in-creased under the evolving icehouse climatesystem.

Functional Significance of Digitate Chambers.Our results suggest that digitate morpholo-gies were maintained in planktonic foraminif-era populations exposed to similar environ-mental constraints. One possibility is thatelongation of individual chambers is efficientfor survival in persistently low-oxygen envi-ronments by increasing shell surface area forimproved gas transport, as has been proposedfor Cretaceous species of the OAEs (e.g.,BouDagher-Fadel et al. 1997; Magniez-Jannin1998; Aguado et al. 1999; Cobianchi et al. 1999;Luciani et al. 2001; Coccioni and Luciani 2004,2005; Coccioni et al. 2006). The problem withthis hypothesis is that there is almost no ex-perimental evidence to support the idea thatgas exchange occurs across the shell surface,aside from the observation that pores are as-sociated with concentrations of mitochondria,which in turn are associated with gas trans-port. In addition, if gas transport is the issue,flattened discoidal shells might be expected toprovide a geometrically more efficient bodyplan. Moreover, not all digitate species showassociations with low-oxygen environments.Even among the Cretaceous species associatedwith OAEs, digitates are absent from the coreof the events and diversify in parallel withsome non-digitate species, suggesting that ad-


ditional factors control their distribution be-sides oxygen availability (Coccioni et al. 2006).

A more likely explanation is that radialchamber elongation was efficient for feedingin a subsurface habitat where the food supplywas sparse and/or irregular. Elongate cham-bers may function as ‘‘fishing rods,’’ support-ing long food-gathering rhizopods (strands ofcytoplasm) that increase the effective shellsize and volume of water that could besearched for food at minimum metabolic cost(R. D. Norris personal communication 2001).Radial elongation allows digitate species to at-tain unusually large shell sizes; the sizes ofClavigerinella spp. and Clavatorella bermudezi,commonly 500 mm, and of H. digitata, up to2 mm, are consistent with this hypothesis. Ef-fective shell size is further increased in somedigitate species by the presence of fine calciticspines; e.g., H. digitata has spines emergingfrom the tips of individual chambers, creatinga radiating net that more than triples the ra-dius. The purpose of these spines is very likelyto provide additional support for rhizopodsand to help secure large prey items. Beella dig-itata and G. adamsi are also spinose and mayhave had similar arrangements of spines, al-though live specimens have not been ob-served. Spines were absent in Cretaceous andpossibly most Paleogene digitate forms. Gasexchange efficiency under low-oxygen condi-tions may also have been improved as a con-sequence of having digitate chambers.

Although digitate species appear to be ex-clusively deep dwelling, digitate form is not aprerequisite for subsurface living becausethere are a number of other species with ob-served or inferred deep dwelling habitats thatdo not have elongated chambers e.g., Paleo-gene and Neogene Globorotaloides spp., includ-ing living G. hexagona (Ortiz et al. 1996), andPaleogene Parasubbotina spp. (Olsson et al.2006b). However, the evolution of some digi-tate species may have occurred within a sub-surface habitat in response to changing phys-ical chemical and nutrient structures. This hy-pothesis is consistent with phylogenetic re-constructions that suggest that acquisition ofdigitate chambers in some groups involvedparapatric speciation, with digitate speciesevolving from existing deep dwellers (e.g., C.

bermudezi from Globorotaloides hexagona (Fleish-er 1974) and C. eocanica from Parasubbotinaeoclava (Coxall et al. 2003)). Moreover, loss ofelongated chambers in the tubulospinose ge-nus Hantkenina was paralleled by a shift froma deep- to a shallow-water habitat (Coxall etal. 2000), although modified extensions of thechambers, in the form of narrow non-perfo-rate tubulospines, were retained in youngersurface-dwelling forms. Modern digitate spe-cies, on the other hand, appear to be moreclosely related to surface and intermediate-depth dwellers (e.g., H. pelagica and Globigeri-nella spp. [Hemleben et al. 1989; M. Kucerapersonal communication 2007]), suggestingthat different selection pressures were respon-sible for evolution of digitate morphologies inthe late Neogene.

The isotopic data and distribution patternspresented here provide an environmental cor-relate with digitate morphologies—life indeep, DIC-enriched, and possibly regularlyoxygen-depleted watermasses associated withincreased marine production. This iterativeevolution very likely reflects common func-tional constraints that could be regarded asrepresenting an adaptive process, eventhough we might not know their exact func-tion or be able to demonstrate the pathway ofspeciation. By this we mean that digitatechambers, arising through natural variation,are efficient for survival under certain envi-ronmental conditions and, therefore, are‘‘maintained’’ or ‘‘selected for’’ when theseconditions occur, while ineffective charactersare eliminated. This is a remarkable findingbecause few other structural convergencesamong planktonic foraminifera have beenfound to correlate with similar ecologies be-tween independently evolved genera andacross multiple epochs.

Summary and Conclusions

Digitate planktonic foraminifera morphol-ogies have evolved multiple times over thepast 130 million years. Previous studies havehinted that some digitate homeomorphs hadsimilar depth habitats, but our stable isotoperesults provide the first evidence of a clearcorrelation between this morphology and asubsurface habitat over multiple epochs.


These findings are consistent with planktontow data that suggest that all modern digitatespecies spend part of their life cycle living atmesopelagic or bathypelagic habitats. Geolog-ical and modern evidence also links some dig-itate species with increased marine productiv-ity and low-oxygen environments, but theyappear to like strong, quasi-permanent OMZconditions such as those that developed on theeastern sides of the major ocean basins and inequatorial upwelling systems. The need forthese persistent OMZ conditions may explainwhy these species do not occur in the temper-ate and high latitudes today but were commonduring Cretaceous OAEs. However, digitatespecies are not always associated with regionsand episodes of eutrophication and low oxy-gen concentration, suggesting there are addi-tional physio-chemical and biological controlson their distribution, such as temperature, sa-linity, nutrients, type of food, and trace ele-ments. We suggest that the function of elon-gate chambers is primarily a feeding adapta-tion that allows the foraminifera to search alarger volume of water for food at minimummetabolic cost in a usually food-poor meso-pelagic environment. There also appears to bean element of opportunism in the ecology ofdigitate species, allowing them to proliferateand diversify under certain environmentalconditions that are unfavorable to many otherplanktonic species. As has been suggested forCretaceous OAE digitates (Coccioni et al.2006), relative abundance of digitate speciesmay be proportional to the strength of the en-vironmental perturbation related to the OAEs.

Our findings suggest that digitate plank-tonic foraminifera may be used as a proxy forintervals of expansion of the OMZ, especiallyduring Mesozoic and early Cenozoic green-house climates when thermal and densitystratification may have been weaker and epi-sodes of widespread eutrophication weremore frequent. Further insight into digitateecologies and environmental preferences canbe obtained by studying the ecology of mod-ern digitate taxa, starting with the systematicassessment of Hastigerinella digitata distribu-tion in Monterey Bay, and building an ex-panded database on the isotopic paleoecolo-

gies and biogeographic distribution of digi-tate species over time.

Acknowledgments

We thank G. Miller and A. Henderson forloan of material from the Natural History Mu-seum London BP collection and S. Haddockfor information on Monterey Bay foraminif-era. Thanks to P. Markwick of Robinson Re-search for mapping Clavigerinella paleogeog-raphies. Thanks also to M. Bolshaw, M. Coo-per, and J. Becker for laboratory assistance, B.Huber, M. Hart, C. Hemleben, N. Norris, andan anonymous reviewer for constructive re-views of earlier manuscripts; and M. Leckiefor discussions on Cretaceous taxonomy. Weare also grateful to I. Hall for providing Ho-locene material, M. Kucera for sharing his wa-ter-column plankton-sampling data, and B.Huber for his data on Cretaceous taxonomythat were incorporated during the review pro-cess. This work was supported by the RoyalCommission for the Exhibition of 1851 UKODP, the Natural Environment ResearchCouncil and the Royal Society. Samples wereprovided by the Ocean Drilling Program (U.S.National Science Foundation under the man-agement of the Joint Oceanographic Institu-tions).

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8

Iterative evolution of digitate planktonic foraminifera

Documents