Geology

doi: 10.1130/0091-7613(2000)28<87:HDAAEL>2.0.CO;2 2000;28;87-90Geology

 Helen K. Coxall, Paul N. Pearson, Nicholas J. Shackleton and Mike A. Hall Hantkeninid depth adaptation: An evolving life strategy in a changing ocean  

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INTRODUCTIONDuring the Eocene (54.7–33.7 Ma), the Earth’s

climate and patterns of ocean circulation changeddramatically (Zachos et al. 1994). The generallywarm “greenhouse” world that had prevailedthrough the Cretaceous to early Eocene graduallygave way to cooler conditions that ultimately led topolar glaciation. Pronounced high-latitude coolingevents in the early middle Eocene and near themiddle-late Eocene boundary were associatedwith evolutionary turnover in many biologicalgroups on the continents and in the oceans(Prothero, 1994). Surface-ocean circulation pat-terns changed progressively in response to open-ing of high-latitude and closing of low-latitude tec-tonic gateways. Deep waters cooled, resulting inreorganization of the vertical thermal structure ofthe water column and changes in biological pro-ductivity in many places (Keller, 1983; Boersmaet al., 1987; Premoli Silva and Boersma, 1988;Zachos et al., 1994; Diester-Haas and Zahn, 1996).

Low-latitude planktonic foraminifera peakedin diversity and morphological disparity in thewarm early middle Eocene, but toward the end ofthe middle Eocene they underwent significant ex-tinctions. The dominant surface dwellers in theearly Paleogene were the “muricate” forms(Morozovella,Acarinina, and Igorina), which arethought to have lived in association with photo-synthetic algae (Pearson et al., 1993; D’Hontet al., 1994). These near-surface taxa were elimi-nated by the end of the middle Eocene, leading tothe suggestion that their extinction was linked toglobal cooling (Keller, 1983; Boersma andPremoli Silva, 1991; Keller et al., 1992; Pearson,1996). At the same time, cold-tolerant deeper-dwelling species increased in abundance anddiversity (Keller et al., 1992).

One of the most distinctive groups of planktonicforaminifera of the Eocene were the hantkeninids,which are characterized by planispiral coiling andhollow, slender extensions of each chamberknown as tubulospines (Fig. 1). The ancestor ofthe hantkeninids had radially extended chambersbut no tubulospines (genus Clavigerinella). Thehantkeninid morphology first appeared about 49Ma, and the clade underwent substantial morpho-

Geology;January 2000; v. 28; no. 1; p. 87–90; 4 figures. 87

Hantkeninid depth adaptation: An evolving life strategy in a changing oceanHelen K. CoxallPaul N. Pearson

Department of Earth Sciences, University of Bristol, Wills Memorial Building, Queens Road, Bristol BS8 1RJ, UK

Nicholas J. Shackleton Godwin Laboratory, Department of Earth Sciences, University of Cambridge, Cambridge CB2 3RS, UKMike A. Hall

ABSTRACTThe interplay between evolution, paleoecology, and environmental change is examined in a

geochemical study of a group of Eocene planktonic foraminifera. The hantkeninids, which arewell-known biostratigraphic index fossils, underwent spectacular long-term evolution in themiddle and upper Eocene (49.0–33.7 Ma), a time when major global climate and oceanicchanges were occurring. We use oxygen and carbon isotope analysis of their shell calcite toinvestigate how their habitat changed as they evolved. The hantkeninids originated in a deep-water oxygen-minimum environment, but migrated into fully oxygenated near-surface watersas global temperatures decreased and water-column stratification declined. This change indepth ecology coincided with pronounced morphological evolution, involving changes inchamber shape and degree of inflation, and modification of the primary aperture. These devel-opments are considered to be adaptations to a near-surface habitat.

Keywords: planktonic, foraminifera, evolution, stable isotopes, Eocene, depth-ecology.

Figure 1. Scanning elec-tron microscope photo-graph of middle Eocenedeep-water dwelling plank-tonic foraminifera Hant-kenina mexicana . Radial,open-ended tubulospinesare believed to have an-chored food-gathering rhi-zopods.

Figure 2. Stratigraphic ranges and suggestedevolutionary relationships of hantkeninidspecies. Future morphometric studies may re-veal that these stratigraphically useful divi-sions are merely morphospecies within one ormore continuously evolving lineages.

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logical evolution before its extinction at 33.7 Ma(Fig. 2). This extinction event is used to correlatethe Eocene-Oligocene boundary worldwide(Berggren et al., 1995). In this study we use stableisotope analysis to investigate how evolutionarychanges in the hantkeninids were related to eco-logical and environmental changes in the Eocene.

ISOTOPE ANALYSIS ANDPALEOECOLOGY

Studies of living and fossil planktonic forami-nifera have revealed that they occupy a range ofhydrographically and latitudinally restrictedpelagic habitats and exhibit diverse morphologiesthat are believed to reflect ecological specializa-tions (Hemleben et al., 1989). Oxygen and car-bon stable isotope analysis of test calcite providesa well-established tool for investigating forami-niferal paleoecology (see Spero, 1998; Pearson,1998, for review). Isotopic data show that like liv-ing planktonic foraminifera, fossil assemblages

were depth stratified in the water column duringlife. Differences in the δ18O values from speciesin the same sample are believed to primarilyreflect depth-related or seasonal temperaturedifferences (Mulitza et al., 1997; Pearson, 1998).Surface-dwelling species, which live in thewarmest water mass (the shallow mixed layer),tend to register lighter oxygen isotope values thancool-water forms that live at greater depthswithin or below the thermocline. Additionalinformation about depth habitat is provided bycarbon isotope values, because surface waters aredepleted in 12C as a result of algal photosynthesisin the euphotic zone. Near-surface species there-fore tend to yield heavier carbon isotope ratiosthan deep dwellers, although biological isotopicfractionation effects can influence the geochemi-cal signal (see Spero, 1998).

Various authors have used isotopic evidence tospeculate that microevolutionary patterns inplanktonic foraminifer lineages were related to

oceanographic or habitat changes (Hodell andVayavananda, 1993; Norris et al., 1993, 1994;Schneider and Kennett, 1996; Pearson et al.,1997). Hantkeninids were relatively rare through-out most of their evolution and consequentlyhave not been widely used in stable isotopestudies, although occasional analyses have beenpublished (Boersma et al., 1987; Pearson et al.,1993; van Eijden, 1995). The objective of thisstudy is to use stable isotope analysis in order toinvestigate the life habit of the hantkeninids.

STUDY SITES AND SAMPLESSamples were selected from pelagic sediments

cores recovered from three deep-sea drill sites.Ocean Drilling Program (ODP) Site 865 (midPacific, lat 18°26.425′N, long 179°33.339′W;Eocene paleolatitude: 2°N–6°N), provides themost complete section. Bralower et al. (1995)produced stable isotope records for the Paleoceneand Eocene from Hole 865C, but they did not

88 GEOLOGY, January 2000

Figure 3. Oxygen and car-bon stable isotope stratig-raphy for hantkeninids andvarious benthic and plank-tonic foraminiferal speciesfrom Site 865 (A and D), DeepSea Drilling Project (DSDP)Site 94 (B and E), and DSDPSite 549 (C and F). Paleomag-netically calibrated plank-tonic foraminiferal and nan-nofossil datum levels wereused to develop age modelsfor each site. Sample age as-signments follow time scaleof Berggren et al. (1995).Isotopic paleodepth signa-tures of three taxa are high-lighted for comparison withhantkeninids; Acarinina (shal-low), Subbotina (thermocline),and Cibicides (benthic). Ana-lytical accuracy is better than0.08‰ for oxygen and betterthan 0.06‰ for carbon. PDB isPeedee belemnite.

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analyze hantkeninids. Middle and late Eoceneforaminifera from this site are excellently pre-served owing to shallow burial depths (13–66 mbelow sea floor). We have been careful to avoidreworked shells by analyzing short-rangingspecies and by avoiding stained specimens. Oneto two samples per core section (one every0.75 m to 1.5 m) were selected for isotopic analy-sis from Hole 865C. Further samples were ana-lyzed from Deep Sea Drilling Program (DSDP)Site 94 (Gulf of Mexico, lat 24°31.64′N, long88°28.16′W) and Site 549 (northeast Atlantic; lat49°05.28′N, long 13°05.88′W). In each case, wemeasured the shell isotopic ratios of hantkeninidsand a number of other reference species from thesame sample, including benthic and deep- andshallow-dwelling planktonic forms.

OXYGEN ISOTOPESAccording to the oxygen isotope data (Fig. 3,

A–C), the relative depth ordering of most speciesremained stable throughout the Eocene, despite ageneral trend toward increased δ18O values. Hant-keninid δ18O values, however, show a significantshift through time, which is best seen in the recordfrom Site 865 (Fig. 3A). The δ18O signatures ofClavigerinella(the ancestral form) from biozoneP10 and the earliest hantkeninids (H. mexicana)from lower biozone P11 are more positive thanthe thermocline-dwelling subbotinids. From themiddle of biozone P11 to about the middle of P12,the δ18O data are similar to the subbotinids. Therewas a cooling of bottom waters ca. 42 Ma that isindicated by a shift toward more positive δ18Ovalues in the benthic foraminifera. Following thisevent the δ18O values of thermocline and mixed-layer dwelling reference taxa converge. Hant-keninid δ18O values from the upper part of Bio-zone P12 and stratigraphically higher are all morenegative than the subbotinids and similar to thoseof mixed-layer-dwelling reference taxa such asAcarininaand Morozovella. Following the extinc-tion of these mixed-layer species, the hant-keninids consistently yield among the lightestδ18O values of the planktonic foraminiferal assem-blages. The four δ18O data points for the lateEocene genus Cribrohantkenina are similar to,but slightly more positive than,Hantkenina spp.

Oxygen isotope records at key intervals fromother sites support this pattern. Samples ofH. liebusifrom middle Eocene biozones P11 andP12 of Site 94 (Fig. 3B), and biozone P11 of Site549 (Fig. 3C), have δ18O values similar to thoseof the subbotinids. However, upper Eocene H.alabamensisfrom biozone P15 of Site 94 is morenegative than the cooccurring subbotinids andamong the most negative of the assemblage.Other data in the literature also conform to thispattern (Boersma et al., 1987; Pearson et al.,1993; van Eijden, 1995).

CARBON ISOTOPESThe carbon isotope species ordering also

changes through the Eocene (Fig. 3, D–F).

Benthic and planktonic δ13C signatures are con-sistently offset, shallow-dwelling symbioticforms (Morozovellaand Acarinina) registeringthe most positive values. At Site 865 Clavigeri-nella and the hantkeninids from biozones P10and P11 register δ13C values that are more nega-tive than those of the subbotinids. In biozonesP12 and P13, hantkeninid δ13C values are indis-tinguishable from subbotinid δ13C values, but inP15 and above,Hantkeninaand Cribrohant-keninaconsistently give relatively enriched δ13Cvalues. At no stage do the hantkeninid valuesapproach the very positive δ13C values of about3‰ that are characteristic of the symbioticmixed-layer-dwelling reference taxa (Morozo-vellaand Acarinina).

DEPTH ECOLOGY ANDMORHPOLOGICAL EVOLUTION

We interpret the shift in hantkeninid stableisotope ratios as reflecting a two-stage change inpreferred depth habitat. Isotopes indicate that theancestral form,Clavigerinella, was deep-dwell-ing, inhabiting the cold, oxygen-starved watersbelow the thermocline. As has been suggested

for some morphologically similar Cretaceousspecies (Premoli Silva et al., 1998), the radiallyextended, perforate chambers of Clavigerinellamay have been an adaptation to facilitate oxygenuptake in a relatively dysaerobic environment.The evolution of tubulospines, by which the earli-est hantkeninids are recognized, also occurred indeep water. The tubulospines probably func-tioned as anchors to large radial rhizopods, en-abling the foraminifera to graze a larger volumeof water at minimal metabolic cost. It is possiblethat the rhizopods passed detrital food particlesdirectly into the shell through the small apertureat the apex of the tubulospine.

Isotopes indicate that the hantkeninids shiftedto a shallower depth habitat ca. 43.5 Ma andoccupied a thermocline environment similar tothe subbotinids. At this time, laterally com-pressed Hantkenina mexicana morphotypes werereplaced by less stellate forms with slender-based tubulospines and more rounded peripheraloutlines (Hantkenina liebusiand Hantkeninadumblei). The less clavate chamber shape mayhave evolved as selective pressures to exchangeoxygen over a large surface area were reduced.

GEOLOGY, January 2000 89

Figure 4. Variation in car-bon isotope ratio withplanktonic foraminifereralshell size. High rates of in-creasing δ13C values withincreasing shell size (opensymbols) are characteris-tic of species that areknown (modern Globigeri-noides sacculifer ,A),or be-lieved (Eocene Acarininamatthewsae , C) to pos-sess dinoflagellate ecto-symbiotionts. Conversely,species with low rates ofincreasing δ13C values withincreasing shell size (filledsymbols) are known or be-lieved to be asymbiotic(Globorotalia inflata ,B,andSubbotina cf. linaperta ,D, respectively). Ontoge-netic δ13C signals of twohantkeninid species (Eand F) do not show anysignificant δ13C enrich-ment trend.Additional datafor Holocene are fromRavelo and Fairbanks(1995); for Eocene arefrom Pearson et al. (1993).DSDP is Deep Sea DrillingProject; ODP is OceanDrilling Program.

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Following a brief warming of surface watersin biozone P12, there was a reduction in water-column stratification at Site 865 associated withnear-surface and deep-water cooling. Isotopicratios indicate that shortly after this, the hant-keninids changed their depth habitat again(ca. 41.2 Ma). At the same time hantkeninidsbecame increasingly rounded, and the tubulo-spines shifted to an anterior position on eachchamber. From biozone P14 to the end of theEocene,Hantkenina alabamensisand Cribro-hantkenina inflata appear to have lived in thewarm surface mixed-layer.

The shift into near-surface waters occurred intandem with further developments to the test,including pronounced chamber inflation, whichmay be viewed as a morphological response tothe move into warmer, less dense water (globularshapes are believed to retard sinking). Unlikemodern shallow-dwelling species, the hant-keninids did not acquire numerous acicularspines, although retention and evolution of thehollow tubulospines imply that these structurescontinued to serve some useful function, such asanchoring rhizopods to facilitate prey capture oraiding in flotation. The final major morphologi-cal development to the test occurred in biochronP15 and involved modification of the primaryaperture into a system of multiple openings in thechamber wall (genus Cribrohantkenina). Thesesubcircular openings were often numerous (asmany as 16) and symmetrically arranged.

Isotope data also show that, unlike many of theolder tropical and equatorial shallow-dwellingspecies that were eliminated during the middleEocene evolutionary turnover (including Morozo-vella and Acarinina), the hantkeninids never hadhigh δ13C values (>2.3‰; Fig. 3, D–F). Further-more, they do not exhibit a size-related δ13Cenrichment trend (Fig. 4, E and F), which is con-sidered to be the isotopic signature of paleosym-biosis (Pearson et al., 1993; D’Hondt et al., 1994;Norris, 1996, 1998). These results suggest that thehantkeninids did not possess dinoflagellate ecto-symbionts like G. sacculiferand A. matthewsae,despite their shallow depth habitat. Alternatively,they may have had a type of symbiont ecologythat does not produce a δ13C enrichment trend. Inthis case, it is possible that the additional aperturesmay have functioned as windows, providing lightto endosymbiotic algae in a self-maintainedgreenhouse, as in some benthic foraminifera (seereview by Lipps, 1983).

SUMMARYThe evolution of the hantkeninids and their

changing ecological specializations occurredagainst a backdrop of climatic cooling andoceanographic reorganization. The combinedapproach used in this case study, linking morpho-logical change, depth ecology, and stable iso-tope composition of hantkeninid foraminifera,demonstrates long-term relationships betweenevolution and environmental change in the

Eocene, which are usually difficult to identify inpaleontological studies.

ACKNOWLEDGMENTSThis project was supported by United Kingdom

Natural Environment Research Council grant GT4/96/31/E. We thank Richard D. Norris, Isabella PremoliSilva, and two anonymous reviewers for their construc-tive suggestions on earlier drafts of the manuscript andBrian T. Huber for helpful comments and discussion.

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Manuscript received May 13, 1999Revised manuscript received September 9, 1999Manuscript accepted October 1, 1999

90 Printed in U.S.A. GEOLOGY, January 2000

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