planktonic foraminifera - BioOne

Paleobiology, 27(2), 2001, pp. 311–326

Role of photosymbiosis and biogeography in the diversification of early Paleogene acarininids (planktonic foraminifera) Fre´de´ric Quille´ve´re´, Richard D. Norris, Issam Moussa, and William A. Berggren

Abstract.—Radiations are commonly believed to be linked to the evolutionary appearance of a novel morphology or ecology. Previous studies have demonstrated a close relationship between the evolutionary appearance of algal photosymbiosis in planktonic foraminifera and evolutionary diversification of Paleogene photosymbiotic clades. For example, the evolution of photosymbiosis was synchronous with the abrupt evolution of four major groups of Paleogene planktonic foraminifera including two clades within the genus Morozovella, as well as the genera Acarinina and Igorina. Our new isotopic and biogeographic data suggest that the acarininids evolved from a photosymbiotic ancestor (which we identify as Praemurica inconstans or early representatives of Praemurica uncinata), but also demonstrate that photosymbiosis did not trigger an immediate species-level radiation in this group. Instead, the acarininids remained a low-diversity taxon restricted to high latitudes for nearly 1.8 million years before radiating ecologically and taxonomically. The eventual radiation of the acarininids is tied to an expansion of their geographic range into the mid and low latitudes. Biogeographic analyses of modern plankton suggest that high-latitude environments may be less conducive to establishing radiations simply because there are fewer niches available to be filled than there are in the tropics. Accordingly, the acarininids may have initially failed to diversify because they started off in environments that presented few opportunities to sustain a large radiation. The high-latitude origin of the acarininids continued to retard their overall diversification until they were able to develop strategies that allowed them to expand into tropical environments and fully exploit their photosymbiotic ecology. Fre´de´ric Quille´ve´re´ and Issam Moussa. Institut des Sciences de l’Evolution, cc064, Universite´ Montpellier II, 34095 Montpellier cedex 05, France. E-mail: [email protected] Richard D. Norris and William A. Berggren. Department of Geology and Geophysics, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543. E-mail: [email protected] Accepted:

25 August 2000

Introduction Stable isotopic methods offer a powerful means of understanding major aspects of the ecology of extinct species of planktonic foraminifera. Many workers have shown that ratios of both oxygen and carbon isotopes denote gradients from surface to deep waters (Emiliani 1954; Boersma et al. 1979; Boersma and Premoli Silva 1983; Corfield and Cartlidge 1991; Schneider and Kennett 1996). It is well established that ␦18O composition in test carbonate is a function of the calcification temperature among other variables including salinity of the water (Epstein et al. 1953) and that ␦13C is controlled by the ratio of dissolved inorganic carbon in seawater and physiological processes such as respiration and symbiont photosynthesis (Spero et al. 1991). Trends in isotopic chemistry during ontogeny can also be reconstructed by analysis of different size fractions of discrete species. Several studies have shown that size can be used to approxi䉷 2001 The Paleontological Society. All rights reserved.

mate ontogenetic stage in planktonic foraminifera (Hemleben et al. 1989; Wei et al. 1992). Over the last few decades, many workers have documented correlations between test size and stable isotopic ratios in extant and fossil species (Berger et al. 1978; Shackleton et al. 1985; D’Hondt and Zachos 1993; Pearson et al. 1993; D’Hondt et al. 1994; Kelly et al. 1996; Norris 1996). Such information has considerable significance for identifying ontogenetic changes related to depth ecology, depths of reproduction and trophic strategy of the planktonic foraminifera. On the basis of analogies with extant taxa, Pearson et al. (1993), D’Hondt et al. (1994) and Norris (1996, 1998) have suggested that the relationships between test size and stable isotopic signal in Paleogene planktonic foraminifera may have resulted from a photosymbiotic effect. Photosymbiosis seems to be a common ecologic strategy among modern marine invertebrates as well as protists includ0094-8373/01/2702-0009/$1.00

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FRE´DE´RIC QUILLE´VE´RE´ ET AL.

ing foraminifera (Smith and Douglas 1987), and the incorporation of algal symbionts such as chrysophytes or dinoflagellates (Be´ 1982; Hemleben et al. 1989) in foraminifera is often cited as a pathway for the abrupt appearance of evolutionary novelty (Bermudes and Margulis 1987; Margulis and Fester 1991; Norris 1996). The isotopic signal of modern planktonic foraminifera believed to harbor photosymbionts displays characteristic patterns, distinct from those of nonsymbiotic taxa (Norris 1996; Berggren and Norris 1997). First, photosymbiotic taxa have the most negative ␦18O of any coexisting species, because they must grow in the upper part of the photic zone to maintain their symbionts. The warm water and perhaps disequilibrium fractionation associated with symbionts cause the test calcite to be depleted in ␦18O (Berger et al. 1978; Spero and Lea 1993). Second, as long as they grow in warm surface water during their life cycles, photosymbiotic species display modest size-related changes in ␦18O (Pearson et al. 1993; Norris 1996) that are affected only slightly by foraminiferal physiology (e.g., Spero 1992). Small differences in ␦18O, which eventually exist between coexisting symbiotic taxa, could reflect differences in depth habitat within the photic zone or variations in water temperature, depending upon the season of growth (Norris 1996, 1998). Culture experiments also show that such variations in foraminiferal ␦18O can be affected by the light intensities under which their symbionts are grown (Spero and Lea 1993). Third, photosymbiotic taxa have more positive ␦13C than nonsymbiotic taxa because photosynthetic symbionts preferentially take up 12C. If this 13C-enriched respiratory CO2 is used in foraminiferal calcification then the test calcite will have positive ␦13C (Spero et al. 1991, 1997). Fourth, photosymbiotic taxa show a trend toward increased ␦13C at larger test sizes. Trends toward increased ␦13C in larger test sizes probably reflect an increase in symbiont activity and density (Spero and Williams 1988; Spero 1992; Spero and Lea 1993). This relationship between test size and carbon isotopic composition observed in photosymbiotic taxa is absent or less marked in nonphotosymbiotic taxa. From these theoretical

FIGURE 1. Model for recognition of photosymbiosis from oxygen/carbon isotopic variation in foraminifera, from Norris 1996.

arguments and observations made on modern taxa, Norris (1996, 1998) has presented a model for recognition of photosymbiosis and nonphotosymbiosis in planktonic foraminifera from their stable isotopic features (Fig. 1). In this broad context, and to provide a better understanding of the role that the symbiotic ecology may have played in the morphological diversification of planktonic foraminifera, we have chosen to investigate the Paleogene radiation of the genus Acarinina. The acarininids are considered a sister group to the Morozovella clade and both contain members that were photosymbiotic (Berggren and Norris 1997; Olsson et al. 1999). Norris (1996) and Kelly et al. (1996) have shown that photosymbiosis initially appeared in the rootstocks of the morozovellids within the genus Praemurica, but they were unable to determine whether the earliest representatives of Acarinina were also photosymbiotic or acquired the symbiotic ecology later in their history. Although the major evolutionary patterns of the Paleogene planktonic foraminifera were established shortly after the Cretaceous/Paleogene extinction (Berggren and Norris 1997), the acarininids did not arise until the middle Paleocene (Selandian) with the evolution of their common ancestor Ac. strabocella. Olsson (1970) suggested that Globorotalia stra-

ACARININA: ECOLOGY AND BIOGEOGRAPHY

FIGURE 2. Phylogeny and ecological evolution for the acarininid clade and other muricates (Igorina and Morozovella) based upon cladogram of Berggren and Norris (1997). Heavy lines indicate the presence of photosymbiosis based upon results of D’Hondt et al. (1994), Norris (1996), and this paper. Species of Globanomalina lived primarily in the thermocline and lacked photosymbiosis in contrast to the surface ocean habitat and symbiotic ecology of the muricate species and the youngest representatives of Praemurica (Berggren and Norris 1997). Pr. ⫽ Praemurica, Ac.⫽ Acarinina, M. ⫽ Morozovella.

bocella was the first acarininid and it evolved from ‘‘Globorotalia’’ inconstans. On the basis of studies of wall texture, Olsson and Hemleben (in Olsson et al. 1999) recently altered their position and argued that the muricate clades (Morozovella, Acarinina, and Igorina) are derived from the finely perforate Globanomalina clade. However, numerous other morphological, cladistic, and stable isotopic analyses strongly support the traditional view that the muricate groups are derived from the genus Praemurica (which includes ‘‘Globorotalia’’ inconstans [e.g., Kelly et al. 1996; Norris 1996; Berggren and Norris 1997]). For example, Berggren and Norris (1997) showed that the muricate clades and praemuricates were surface-water groups in contrast to the globanomalinids, which exhibit a distinct thermocline ecology. These authors also conducted a cladistic analysis and found that the muricate and praemuricate groups form a distinctive clade separated from globanomalinids by numerous synapomorphies (Fig. 2). Finally, re-

313

cent isotopic studies of morozovellids (Kelly et al. 1996; Norris 1996) and acarininids (this study) demonstrate that these groups are united with Praemurica by the common presence of photosymbiosis, whereas globanomalinids were asymbiotic (e.g., Berggren and Norris 1997). The phylogenetic relationships between the Paleocene species of the genus Acarinina are well established (Norris 1996; Berggren and Norris 1997; Quille´ve´re´ et al. 2000). The ancestor Ac. strabocella gave rise to two lineages, the first one corresponding to the very divergent Ac. subsphaerica, which did not produce any late Paleocene descendants, and the second one containing Ac. nitida and its descendant Ac. mckannai. In turn, Ac. nitida appears to have evolved into Ac. coalingensis and Ac. mckannai into Ac. soldadoensis (Berggren and Norris 1997), and both groups led to a series of large radiations in the Eocene. Recent studies (Berggren and Norris 1997; Quille´ve´re´ et al. 2000) have provided evidence that the genus originated in high latitudes during early–middle Paleocene (early Selandian) and that the initial radiation of this group (small-size Ac. nitida, Ac. subsphaerica and Ac. mckannai), denoting the P3b/P4a biochronal boundary (around 59.2 Ma), resulted from a migration event from high to low latitudes. However, the second Paleocene radiation (First Appearance Datum [FAD sensu Aubry 1995] of Ac. soldadoensis and Ac. coalingensis), denoting the P4b/P4c biochronal boundary (at 56.5 Ma), occurred in low-latitude, oligotrophic water masses. The Paleocene and Eocene species of the acarininid group that have been isotopically analyzed, including Ac. nitida (D’Hondt et al. 1994), Ac. mckannai (Shackleton et al. 1985; Norris 1996), Ac. soldadoensis (Shackleton et al. 1985), and Ac. matthewsae, Ac. pseudotopilensis, and Ac. aff. triplex (Pearson et al. 1993), have a carbon and oxygen isotopic composition indicative of photosymbiosis. The isotopic signature of the earliest representative of the genus Acarinina (Ac. strabocella) has not been studied prior to this investigation owing to problems associated with its taxonomic identity, its small size, and its general rarity. Hence, Norris (1996) mentioned that there was


314

FIGURE 3.

Location map of ODP Sites 750 and 761.

no certitude that the earliest acarininids hosted photosymbionts and that there was a possibility that the acarininids acquired photosymbiosis independently of the morozovellids, their photosymbiotic sister group (Norris 1996; Berggren and Norris 1997). Moreover, analyses of different size fractions were not available for numerous Paleocene acarininids, such as Ac. subsphaerica and Ac. coalingensis, and previous data were inadequate to determine whether such taxa carried algal symbionts. Comparison of our isotopic results with previous studies allows us to answer such questions, test the possibility that acarininids acquired photosymbiosis by a convergent process, and examine the evolutionary significance of the photosymbionts in the Paleocene radiation of the genus Acarinina. Material The material was collected in deep-sea sediments recovered at ODP (Ocean Drilling Program) Hole 761B (16⬚44.23⬘S,115⬚32.10⬘E; 2466 m water depth) on the Wombat Plateau (eastern Indian ocean) and ODP Hole 750A (57⬚35.54⬘S,81⬚14.42⬘E; 2030.5 m water depth) on Kerguelen Plateau (southern Indian ocean) (Fig. 3). Stable isotopic analysis is focused on middle Paleocene (Selandian) and upper Paleocene (Thanetian) samples from cores 16X to 19X at Site 761 and core 11R at Site 750. We have concentrated our efforts on these parts of the sections in which the initial radiation of the acarininids occurred. These sites have sev-

eral advantages for such a study. First, the preservation of the planktonic foraminifera is particularly good and acarininids are abundant. Second, the sites are located in different paleoceanographic settings and provide a means of comparing the trophic strategy of early representatives of the genus, which first appeared in high latitudes (Quille´ve´re´ et al. 2000), and their low-latitude descendants. The age determinations for the different samples are based on the temporal interpretation of the Paleocene section recovered at each site following the methodology established by Aubry (1995). The temporal interpretation at ODP Hole 761B was based on integrated bioand magnetostratigraphy (Galbrun 1992; Siesser and Bralower 1992; Quille´ve´re´ et al. 1998), calibrated to the magnetobiochronology of Berggren et al. (1995), recently revised by Berggren et al. (2000). The samples selected for this study are listed in Table 1. At ODP Hole 750A, age determination of the sample we selected is based on a biostratigraphy proposed by Berggren in the Initial Reports of the ODP Leg 120 (Schlich, Wise et al. 1989) and revised in this work. The biostratigraphic setting of the sections and stratigraphic ranges of the species studied in this paper are presented in Figure 4A for ODP Hole 761B and Figure 4B for ODP Hole 750A. Methods To assess whether Paleocene acarininids from both high and low latitudes were already photosymbiotic, we analyzed all the species involved in their initial radiation: Acarinina strabocella (Loeblich and Tappan), Ac. nitida (Martin), Ac. subsphaerica (Subbotina), Ac. mckannai (White), Ac. soldadoensis (Bro¨nniman), and Ac. coalingensis (Cushman and Hanna). As a control and point of comparison, specimens of Morozovella praeangulata (Blow), M. angulata (White), M. velascoensis (Cushman), Subbotina triloculinoides (Plummer), and S. triangularis (White) were also picked and analyzed. Morozovella angulata and M. velascoensis are believed to have been photosymbiotic since they present a clear pattern of increasing slope in the ␦13C/size relationship (Shackleton et al. 1985; Kelly et al. 1996; Norris 1996). Subbotina triloculinoides and S. tri-

315


TABLE 1. Selected samples, age estimates, and planktonic foraminiferal species analyzed in this paper.

Sample

Depth (mbsf)

Age (Ma)

761B, 16 ⫻ 2, 110–112 cm

125.3

56.2

761B, 17 ⫻ 4, 10–12 cm

136.8

57.9

761B, 18 ⫻ 2, 10–12 cm

143.3

58.4

761B, 18 ⫻ 5, 10–12 cm

147.8

59.0

761B, 19 ⫻ 1, 10–12 cm

151.3

59.4

750A, 11R2, 50–52 cm

309.5

60.9

angularis are believed to have been nonphotosymbiotic since they apparently grew deeper in the water column (Douglas and Savin 1978; Boersma et al. 1979) and do not display large size-related variation in ␦13C (Pearson et al. 1993; D’Hondt et al. 1994; Norris 1996). The isotopic signature of M. praeangulata is poorly known owing to the rarity of this taxon. Anal-

FIGURE 4.

Foraminiferal species analyzed S. triangularis M. velascoensis Ac. soldadoensis Ac. coalingensis S. triloculinoides M. velascoensis Ac. nitida Ac. subsphaerica Ac. mckannai S. triloculinoides Ac. strabocella Ac. nitida Ac. subsphaerica S. triloculinoides M. velascoensis Ac. strabocella S. triloculinoides M. angulata Ac. strabocella S. triloculinoides M. praeangulata Ac. strabocella

ysis of a few samples from DSDP Site 577 by Shackleton et al. (1985) did not lead to definitive conclusions on the trophic strategy of M. praeangulata. However, the abundance of M. praeangulata in the same stratigraphic levels as the more primitive acarininids at ODP Hole 750A has allowed us to determine whether these early representatives of the genus Mo-

Biostratigraphic setting of the sections from ODP Holes 761B (A) and 750A (B) mentioned in this paper.

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rozovella in high latitudes were clearly photosymbiotic. To determine intraspecific relationships between isotopic signals and test sizes, multiple specimens of each taxon were picked from 1/4-phi sieve fraction including 125, 150, 180, 212, 250, 300, and 355 ␮m. Sieve fractions smaller than 125 ␮m were avoided because kinetic fractionation and the effects of growth rate on the foraminifer isotopic signature are maximized among the smallest individuals (Norris 1996). Individuals were ultrasonically cleaned in distilled water, weighed and analyzed with (1) a Finnigan MAT 252 mass spectrometer and associated ‘‘Kiel’’ carbonate preparation system at the Woods Hole Oceanographic Institution for samples 761B-18X2, 10–12 cm and 761B-19X2, 10–12 cm and (2) with an OPTIMA AC117 Multiprep mass spectrometer at the University of Montpellier for samples 761B16X2, 103–105 cm; 761B-17X4, 10–12 cm; 761B-18X4, 10–12 cm; and 750A-11R2, 50–52 cm. The number of specimens necessary to supply sufficient calcium carbonate and to limit the effect of individual variation on our isotopic results ranged from approximately 3 for the larger size fraction to 40 for the smallest size fraction. Repeated analysis of in-house standards (Atlantis-II, Carrara Marble, and B1 marine planktonic carbonate) and NBS (National Bureau of Standards) 19 suggested that the standard machine error for oxygen and carbon isotopic measurements was respectively 0.07‰ and 0.03‰ at the Woods Hole Oceanographic Institution and 0.1‰ and 0.05‰ at the University of Montpellier. Recrystallization or dissolution of foraminiferal calcite can alter stable isotopic values (Killingley 1983; Wu and Berger 1989). These factors do not seem to have significantly af-

fected either the oxygen or carbon stable isotopic signals in our foraminiferal samples. The specimens we picked and studied were free of carbonate infilling, visible dissolution, or significant surficial overgrowth (Fig. 5). Their interspecies variation in both oxygen and carbon signals is consistent with that of other well-preserved upper Paleocene sequences (Shackleton et al. 1985; Norris 1996). Results and Discussion High-Latitude Origin for Acarininids. Previous studies of acarininids have repeatedly found the earliest members of the group to appear above the Danian/Selandian boundary in the lower part of Planktic Foraminifer Biozone P3a (⬃60.5 Ma) (e.g., Berggren and Norris 1997; Olsson et al. 1999). Most of these records of the FAD of Ac. strabocella come from low- to mid-latitude sites and are followed near the P3b/P4 biochronal boundary (⬃59.2 Ma) by the FADs of several other acarininid species. Indeed, we find a similar or slightly younger FAD for Ac. strabocella in ODP Hole 761B (⬃16⬚S) where the species makes its appearance near the Biozone P3a/P3b boundary (⬃60 Ma) (Fig. 4A). In contrast, at ODP Hole 750A (57⬚S), we have found acarininids at about 61–61.2 Ma just below the P2 biochronal boundary (Fig. 4B). This age determination is based on the presence of numerous specimens that were found in the same stratigraphic levels as Morozovella praeangulata morphotypes, which are commonly identified in biozones P2 and lower P3a (Berggren and Norris 1997; Olsson et al. 1999). The overlapping ranges of M. praeangulata and Ac. strabocella and the occurrence of Ac. strabocella below the FAD of M. angulata (marker for the base of Biozone P3a) suggest that ODP Site 750 contains the oldest record of acarininids presently known from →

FIGURE 5. Scanning electron photomicrographs of representative Paleocene taxa we studied (scale bar, 100 ␮m). 1: Umbilical view of Ac. strabocella from 750A-11H2, 50–52 cm. 2, 3: Umbilical and spiral views of Ac. strabocella from 761B-18X2, 10–12 cm. 4, 5: Umbilical and spiral views of Ac. nitida from 761B-18X2, 10–12 cm. 6, 7, 8: Umbilical, edge and spiral views of Ac. subsphaerica from 761B-17X4, 10–12 cm. 9, 10: Umbilical and spiral views of Ac. mckannai from 761B-17X4, 10–12 cm. 11, 12: Umbilical and spiral views of Ac. soldadoensis from 761B-16X2, 10–12 cm. 13, 14: Umbilical and spiral views of Ac. coalingensis from 761B-16X2, 10–12 cm. 15: Umbilical view of S. triloculinoides from 761B-18X2, 10–12 cm. 16: Umbilical view of S. triangularis from 761B-16X2, 10–12 cm. 17, 18: Umbilical and edge views of M. praeangulata from 750A-11H2, 50–52 cm. 19: Umbilical view of M. angulata from 761B-19X2, 10–12 cm. 20: Umbilical view of M. velascoensis from 761B-17X4, 10–12 cm.


317

318


FIGURE 6. Stratigraphic range and ecological evolution of Paleocene acarininids. Biostratigraphy from ODP Hole 750A suggests the initial appearance of the group in high latitudes followed by their subsequent appearance in low latitudes as mostly small populations. Diversification of the acarininid clade occurred ⬃ 59.2 Ma and resulted in the appearance of large populations in many mid-and low-latitude sites as well as the dominance of acarininids in the surface waters at many highlatitude sites. Thick bars indicate frequent occurrence of large numbers of individuals, thin bars rare occurrence of individuals. The initial latitude of the acarininid diversification at 59.2 Ma is unknown since the acarininids quickly become cosmopolitan.

the deep sea. We suggest that the biochronology for ODP Site 750 supports inferences that the acarininids first appeared in temperate or high-latitude sites and subsequently expanded their range into mid- and low-latitude regions. We acknowledge that mid- and high-latitude records are poor around the Danian/Selandian boundary, inhibiting further testing of a high-latitude origin for acarininids. Furthermore, the morozovellids used to construct the chronology for ODP 750 are typical low- and mid-latitude species whose ranges may be diachronous in the high latitudes. However, barring diachrony in the range of M. angulata, the data presently available are compatible with a high-latitude FAD for the acarininids about 61–61.2 Ma followed by the diversification of the whole group throughout the oceans by ⬃59.2 Ma (Fig. 6). Carbon Isotopic Composition. At each strati-

graphic level, species of the Paleocene planktonic foraminiferal genus Acarinina have a tendency for the carbon isotopic composition to show size dependency, similar to that of the genus Morozovella, with the larger specimens consistently having heavier values (Table 2). All six species of Acarinina and three species of Morozovella we analyzed exhibit this strong positive ␦13C relationship (Fig. 7). At 60.9 Ma, Ac. strabocella increases by 0.56‰ and M. praeangulata by 0.60‰ over a 125-␮m to 250␮m mean test size range (Fig. 7A). At 59.4 Ma, the ␦13C of Ac. strabocella and M. angulata increases respectively by 1.28‰ and 1.22‰ over a 125-␮m to 300-␮m test size range (Fig. 7B). Over the same size range, at 59.0 Ma, this ␦13C relationship is about 0.88‰ and 0.90‰ for Ac. strabocella and M. velascoensis, respectively (Fig. 7C). At 58.4 Ma, the ␦13C of Ac. strabocella, Ac. nitida, and Ac. subsphaerica increases respectively by 0.67‰, 0.56‰, and 0.43‰ over a 125-␮m to 250-␮m range (Fig. 7D). At 57.9 Ma, the ␦13C of Ac. nitida, Ac. subsphaerica, Ac. mckannai, and M. velascoensis increases by 0.86‰, 0.87‰, 0.73‰, and 0.90‰ over a 125␮m to 250-␮m size range (Fig. 7E). Finally, in the latest Paleocene (56.2 Ma), Ac. soldadoensis, Ac. coalingensis, and M. velascoensis display a ␦13C increase respectively by 0.57‰, 0.72‰, and 0.89‰ over a 125-␮m to 250-␮m size range (Fig. 7F). In comparison, S. triloculinoides and S. triangularis do not exhibit any clear and significant ␦13C increase over the similar size ranges in the Paleocene samples we selected (Fig. 7A–F). Our results show that acarininids and morozovellids display considerably heavier carbon isotopic composition in comparison with size series of subbotinids. The magnitude of the ␦13C difference between these groups is about an average of 0.5–0.7‰ for smaller test sizes and 1.1–1.4‰ for test sizes of 212–250 ␮m. The difference is maximum (respectively 0.76‰ and 1.47‰) at 60.9 Ma (ODP Hole 750A) for the 125–150-␮m sieve fraction (Fig. 7A) and at 59.4 Ma (ODP Hole 761B) for the 212–250-␮m sieve fraction (Fig. 7B). But remarkably, this magnitude appears to be very constant over geologic age in all the samples we selected from both deep-sea sites. The magnitude of the ␦13C difference is also con-


sistent with isotopic values published on different Paleocene species by Shackleton et al. (1985) at DSDP Site 577 (North Pacific), D’Hondt et al. (1994) at ODP Site 758 (Indian Ocean), and Norris (1996) at DSDP Site 384 (North Atlantic). These results and our data show that relationships between carbon isotope composition and test size of both acarininid and morozovellid species appear to be relatively constant from site to site and age to age. This consistency implies that over a large range of latitude (from 40⬚N at DSDP 384 to 57⬚S at ODP 750), planktonic foraminifera acquired similar ecologic strategies. Oxygen Isotopic Composition. Among living planktonic foraminifera from a given location, a wide range in oxygen isotopic composition has been observed. These results for living species are known to be due to large differences in calcification temperature (Emiliani 1954; Be´ 1982) that are related to changes in depth habitat during growth. In contrast with observations made on modern planktonic foraminifera, the oxygen isotopic composition of the Paleocene species analyzed here shows no significant trend to variation over the size range (Table 2, Fig. 8). Apparently, these Paleocene taxa usually did not change their depth habitat in the water column during their life cycle. The oldest sample we studied from ODP Hole 761B (59.4 Ma) seems to represent an exception to the rule. Indeed, the ␦18O of Ac. strabocella and M. angulata decreases respectively by 0.59‰ and 0.54‰ over a 125-␮m to 300-␮m size range (Fig. 8B). The sample from 57.9 Ma also shows a pronounced negative ␦18O/size relationship in M. velascoensis. The negative ␦18O/size relationship may be due to changes in surface ocean hydrography rather than evolution of depth habitats since these isotopic trends are not observed in our other samples. The oxygen isotopic compositions of Paleocene planktonic foraminifera we have studied show that acarininids and morozovellids display considerably lighter oxygen isotopic composition at a given size than do subbotinids, in agreement with previous studies (Douglas and Savin 1978; Boersma et al. 1979; Corfield and Cartlidge 1991; Pearson et al. 1993; Berggren and Norris 1997). The isotopic

319

evidence for a deep-water habitat of subbotinids is also supported by this work: in each sample, S. triloculinoides and S. triangularis have an oxygen isotopic composition approximately 0.5‰ more positive than that of coexisting acarininids and morozovellids (Fig. 8), which is consistent with a difference in calcification temperature of 2.0–2.5⬚C cooler than coexisting surface-water taxa (Norris 1996). Our results support previous isotopic studies at low latitudes, which suggested that morozovellids and acarininids were surface mixedlayer groups and that subbotinids inhabited relatively deep and colder waters, within or below the thermocline (Boersma et al. 1979; Boersma and Premoli Silva 1983; Berggren and Norris 1997). Measurements of ␦18O in morozovellids and acarininids suggest that there were at most minor differences in their depth habitats. In most samples Acarinina has more positive ␦18O values than coexisting Morozovella, which could be interpreted as indicative of occupation by acarininids of cooler and deeper waters than by morozovellids. The oxygen isotopic gradient between subbotinids and surface-water taxa is very small in comparison with that of DSDP Hole 384 (Berggren and Norris 1997). The waters over ODP Site 761 probably had a deep mixed layer in which surface waters and thermocline waters were nearly the same temperature, whereas a stronger temperature gradient existed in the upper ocean over DSDP Site 384. Hence, the isotopic record at ODP Hole 761B did not record the differences in depth habitat as sensitively as DSDP Hole 384. Berggren and Norris (1997) have shown that the earliest representatives of Ac. nitida and Ac. subsphaerica from DSDP Hole 384 had very positive oxygen isotopic values similar to that of coexisting deep-water taxa, suggesting that the earliest species of the genus may have grown in deeper environments than subsequent taxa. The samples these authors analyzed were dated at 58.4 Ma for Ac. nitida and 57.4 Ma for Ac. subsphaerica. Remarkably, Ac. subsphaerica from DSDP Hole 384 showed a dramatic decrease in ␦18O (approximately 0.7‰) over a short period of time (0.6 Myr). Our data do not present such a pattern. Anal-


320

TABLE 2. Sample horizons and isotopic data in ODP Holes 750A and 761B used in this study. ODP 761B, 16 ⫻ 2, 110–112 cm, 56.2 Ma Sieve size (␮m)

␦13C

␦18O

␦13C

␦18O

␦13C

␦18O

␦13C

␦18O

355 300 250 212 180 150 125

2.26 2.23 2.25 2.27 2.21 2.23 2.29

⫺0.54 ⫺0.48 ⫺0.57 ⫺0.57 ⫺0.61 ⫺0.45 ⫺0.55

3.87 3.82 3.68 3.12 3.11 2.88 2.79

⫺1.14 ⫺1.16 ⫺1.14 ⫺1.45 ⫺1.24 ⫺1.23 ⫺1.22

3.81 3.22 3.10 2.91 2.66 2.65

⫺1.48 ⫺1.10 ⫺1.10 ⫺0.97 ⫺1.30 ⫺1.04

4.03 3.44 3.24 3.26 2.92 2.72

⫺1.14 ⫺1.20 ⫺1.07 ⫺1.15 ⫺1.10 ⫺1.02

S. triangularis

M. velascoensis

Ac. soldadoensis

Ac. coalingensis

ODP 761B, 17 ⫻ 4, 10–12 cm, 57.9 Ma Sieve size (␮m)

␦13C

␦18O

␦13C

␦18O

␦13C

␦18O

␦13C

␦18O

␦13C

␦18O

355 300 250 212 180 150 125

2.25 2.50 2.47 2.49 2.52 2.45 2.28

⫺0.22 ⫺0.10 ⫺0.11 ⫺0.28 ⫺0.17 ⫺0.18 ⫺0.19

4.37 4.06 3.79 3.72 3.65 3.34 2.89

⫺0.88 ⫺0.80 ⫺0.80 ⫺0.69 ⫺0.59 ⫺0.61 ⫺0.63

3.65 3.59 3.41 3.27 2.80

⫺0.70 ⫺0.69 ⫺0.61 ⫺0.88 ⫺0.80

3.72 3.53 3.26 3.08 2.85

⫺0.78 ⫺0.55 ⫺0.58 ⫺0.60 ⫺0.59

3.65 3.71 3.33 3.33 2.93

⫺0.92 ⫺0.76 ⫺0.86 ⫺0.68 ⫺0.62

S. triloculinoides

M. velascoensis

Ac. nitida

Ac. subsphaerica

Ac. mckannai


␦13C

␦18O

␦13C

␦18O

␦13C

␦18O

␦13C

␦18O

300 250 212 180 150 125

2.56 2.51 2.53 2.50 2.43 2.43

0.07 0.07 0.04 0.04 0.02 0.12

3.71 3.47 3.32 3.15 3.03

⫺0.55 ⫺0.42 ⫺0.35 ⫺0.31 ⫺0.31

3.65 3.34 3.30 3.21 3.08

⫺0.31 ⫺0.33 ⫺0.29 ⫺0.39 ⫺0.28

3.43 3.31 3.28 3.09 3.01

⫺0.34 ⫺0.25 ⫺0.22 ⫺0.21 ⫺0.23

S. triloculinoides

Ac. strabocella

Ac. nitida

Ac. subsphaerica


␦13C

␦18O

␦13C

␦18O

␦13C

␦18O

300 250 212 180 150 125

2.43 2.41 2.34 2.26 2.17 2.13

⫺0.38 ⫺0.37 ⫺0.45 ⫺0.30 ⫺0.61 ⫺0.43

3.65 3.64 3.27 3.13 2.97 2.75

⫺1.00 ⫺0.99 ⫺0.92 ⫺0.89 ⫺0.91 ⫺0.69

3.64 3.52 3.33 3.13 2.93 2.77

⫺0.76 ⫺0.79 ⫺1.06 ⫺0.67 ⫺0.77 ⫺0.80

S. triloculinoides

M. velascoensis

Ac. strabocella


␦13C

␦18O

␦13C

␦18O

␦13C

␦18O

300 250 212 180 150 125

2.27 2.23 2.21 2.26 2.13 2.13

3.03 ⫺0.15 ⫺0.08 0.05 ⫺0.01 0.01

3.92 3.51 3.44 3.10 2.89 2.70

⫺0.79 ⫺0.67 ⫺0.71 ⫺0.42 ⫺0.37 ⫺0.25

3.93 3.82 3.25 3.20 2.83 2.65

⫺0.81 ⫺0.74 ⫺0.45 ⫺0.31 ⫺0.22 ⫺0.22

S. triloculinoides

M. angulata

Ac. strabocella

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TABLE 2. Continued. ODP 750A, 11R2, 50–52 cm, 60.9 Ma Sieve size (␮m)

␦13C

␦18O

␦13C

␦18O

␦13C

␦18O

300 250 212 180 150 125

1.95 1.97 2.24 2.00 2.11 1.99

0.41 0.47 0.39 0.24 0.10 0.09

3.27 3.66 3.13 3.05 2.67

⫺0.37 ⫺0.40 ⫺0.66 ⫺0.64 ⫺0.65

3.38 3.47 3.22 3.03 2.82

⫺0.47 ⫺0.46 ⫺0.58 ⫺0.54 ⫺1.96

S. triloculinoides

M. praeangulata

yses made on samples from ODP Hole 761B and dated at 58.4 Ma (Fig. 8D) show that the oxygen isotopic composition of early representatives of Ac. nitida and Ac. subsphaerica is consistent with a surface mixed-layer habitat. It is probable that DSDP Hole 384 was able to capture ecological differences that are not obvious at ODP Hole 761B. Photosymbiosis in Acarininids. Acarininids display considerably lighter oxygen isotopic and heavier carbon isotopic composition in comparison of size series of the selected subbotinids. The ontogenetic pattern of carbon isotopic composition is very similar between

Ac. strabocella

acarininids and coexisting morozovellids. By analogy with extant taxa, Norris (1996) suggested that the isotopic pattern of morozovellids probably reflected the occurrence of photosymbionts. Other explanations for this pattern, such as kinetic fractionation and variations in depth habitat, were investigated and rejected by D’Hondt et al. (1994). Indeed, our data confirm that acarininids did not migrate during ontogeny through a wide range of water depths and isotopic paleoequilibria, since the ␦18O of their shells never approached that of coexisting subbotinids. On the basis of the model established by

FIGURE 7. Variation in carbon isotopic composition compared with test size, with solid symbols for acarininid species and open symbols for subbotinid and morozovellid species. Taxa include Subbotina triloculinoides (large open squares), Morozovella praeangulata (open diamonds), Acarinina strabocella (black diamonds), M. angulata (large open circles), Ac. nitida (gray squares), Ac. subsphaerica (black upward-pointing triangles), M. velascoensis (small open circles), Ac. mckannai (black right-pointing triangles), Ac. soldadoensis (gray downward-pointing triangles), Ac. coalingensis (black circles), and S. triangularis (small open squares). Sample A from ODP Hole 750A; all others from ODP Hole 761B. Sizes are standard sieve fractions.

322


FIGURE 8. Variation in oxygen isotopic composition compared with test size. Taxa include Subbotina triloculinoides (large open squares), Morozovella praeangulata (open diamonds), Acarinina strabocella (black diamonds), M. angulata (large open circles), Ac. nitida (gray squares), Ac. subsphaerica (black upward-pointing triangles), M. velascoensis (small open circles), Ac. mckannai (black right-pointing triangles), Ac. soldadoensis (gray downward-pointing triangles), Ac. coalingensis (black circles) and S. triangularis (small open squares). Sample A from ODP Hole 750A; all others from ODP Hole 761B. Sizes are standard sieve fractions.

Norris (1996) for oxygen/carbon isotopic variation in symbiotic and asymbiotic modern planktonic foraminifera, we have separated each Paleocene planktonic foraminiferal population in two distinctive groups (Fig. 9). One group, composed by acarininids and morozovellids, shows a large range of ␦13C with size and a small range of ␦18O, which is consistent with the effects of photosymbiosis. All the Paleocene species of the genus Acarinina perfectly overlap the oxygen and carbon isotopic composition of coexisting Morozovella, suggesting that they harbored algal photosymbionts. The other group, composed of subbotinids, probably did not use this trophic strategy, since the isotopic composition of their shells has a very small range of ␦13C, similar to those of modern nonsymbiotic taxa. Our results show that early representatives of the ancestor Ac. strabocella, analyzed at ODP Hole 750A and dated around 61 Ma (or slightly older), appear to have harbored photosymbionts. The variability of carbon isotope com-

position is higher in acarininids than in coexisting subbotinids, and both the acarininids and morozovellids show a strong ␦13C/size dependency observed in other photosymbiotic taxa (Fig. 7A). For this reason, we reject the possibility that acarininids acquired photosymbiosis independently of the morozovellid group and suggest that acarininids inherited photosymbionts from the common ancestor they shared with morozovellids. Hence, we support the hypothesis of Norris (1996), that both Morozovella and Acarinina derived from a photosymbiotic common ancestor, close to Praemurica inconstans or Pr. uncinata. By analyzing Danian (early Paleocene) samples taken from near the highest occurrence of Pr. inconstans and the lowest occurrence of Pr. uncinata, Kelly et al. (1996) and Norris (1996) found a pattern of a size-dependent carbon isotopic increase during the evolutionary transition between these species. Moreover, as Pr. uncinata is believed to be absent from high latitudes (Olsson et al. 1999), and as the acar-


323

FIGURE 9. Oxygen isotopic composition plotted against carbon isotopic composition for the same samples as depicted in Figures 7 and 8. Taxa include Subbotina triloculinoides (large open squares), Morozovella praeangulata (open diamonds), Acarinina strabocella (black diamonds), M. angulata (large open circles), Ac. nitida (gray squares), Ac. subsphaerica (black upward-pointing triangles), M. velascoensis (small open circles), Ac. mckannai (black right-pointing triangles), Ac. soldadoensis (gray downward-pointing triangles), Ac. coalingensis (black circles) and S. triangularis (small open squares).

ininids evolved first in these areas, it would appear parsimonious to consider the youngest representatives of Pr. inconstans, believed to have harbored the first algal symbionts, as the most likely ancestor of the genus Acarinina. The isotopic signature of photosymbiosis is well developed in all the Paleocene species of Acarinina, including the high-latitude representatives of Ac. strabocella and their low-latitude descendants. Carbon isotopic analyses of middle Paleocene (Selandian) and late Paleocene (Thanetian) representatives of Ac. strabocella show that it retained a ␦13C size dependency in all the samples we studied (Fig. 7B–D). Acarinina strabocella almost perfectly overlaps the oxygen and carbon isotopic composition of coexisting morozovellids (M. angulata and M. velascoensis) at the same ontogenetic stages (Fig. 9B–D), suggesting that this taxon harbored photosymbionts throughout its geologic range. Analyses of the descendants Ac. nitida, Ac. subsphaerica (Fig. 9D,E) and Ac. mckannai (Fig. 9E)

suggest, moreover, that these taxa also harbored photosymbionts they inherited from Ac. strabocella. Finally, the latest Paleocene (late Thanetian) species Ac. soldadoensis and Ac. coalingensis present a similar ␦13C/size dependency, consistent with a photosynthetic trophic strategy (Fig. 7F). As indicated by Pearson et al. (1993), the early and middle Eocene species Ac. matthewsae, Ac. pseudotopilensis, and Ac. aff. triplex all exhibited isotopic evidence for photosymbionts. Hence we conclude that many, if not all, the Paleocene and Eocene species of Acarinina were photosymbiotic. Evolutionary Consequences of Photosymbiosis on the Paleocene Radiation of Acarininids. The acquisition of algal symbionts has been cited as a pathway for the appearance of evolutionary novelty (Bermudes and Margulis 1987; Margulis and Fester 1991). This may have played a significant role in the morphologic diversification of a taxonomic group such as

324


the acarininids. It is well documented that photosymbiosis expanded the ecologic niche of the planktonic foraminifera and allowed them to maintain reproduction in low-nutrient water masses (Norris 1996, 1998). Therefore, this ecologic strategy could have opened opportunities for speciation within oligotrophic environments in subtropical areas during the Paleocene. In this context, the establishment of photosymbiosis within Pr. inconstans appears to have given rise to morphologic diversification of acarininids and morozovellids as these groups expanded into new habitats. Just as the taxonomic diversity within the genus Morozovella increased rapidly after the evolution of photosymbiosis (Norris 1996), so too did the acarininids undergo a distinct radiation in the late Paleocene and early Eocene. However, this acarininid radiation was delayed relative to that of the morozovellids. From the first appearance of Ac. strabocella (around 61 Ma) to the first appearance of Ac. nitida, Ac. subsphaerica and Ac. mckannai (around 59.2 Ma), 1.8 million years of history occurred before the genus began its morphologic diversification. Therefore, the acquisition of photosymbionts and the initial radiation of acarininids did not occur simultaneously. The long geologic range of Ac. strabocella suggests that speciation events in the initial radiation of acarininids were not a direct response to the photosymbiotic ecology. It is notable that the earliest acarininids are considerably smaller (Fig. 10) and less ornate than their later representatives and are more typical of high-latitude regions than the cosmopolitan species that ultimately replaced them. The first representatives of Ac. strabocella, Ac. nitida and Ac. subsphaerica have maximum shell diameters that are a fraction of the size of later acarininid species and are also typically smaller than their immediate ancestors in the genus Praemurica. The increase in shell size that accompanied the diversification of acarininids into the low- and mid-latitude oceans further suggests that the early members of the genus differed ecologically from the later, more cosmopolitan taxa. Today, photosymbiotic taxa occur in a wide variety of surface-water environments from the polar seas to the equator and from up-

FIGURE 10. Maximum shell size ( ␮m) versus geologic age for the late Paleocene acarininids from low latitudes analyzed in this paper (Acarinina strabocella, Ac. nitida, Ac. subsphaerica, Ac. mckannai, Ac. soldadoensis, and Ac. coalingensis). Symbols as in Figures 7, 8, and 9. Note that the maximum shell size of the acarininids increased during the late Paleocene.

welling cells to the centers of the strongly oligotrophic subtropical gyres. Photosymbiotic species are represented in modern subpolar planktonic foraminifera assemblages primarily by one species, Turborotalita quinqueloba. As with Acarinina strabocella in the Paleocene, T. quinqueloba is most abundant in high-latitude waters although it also ranges into mid- and low latitudes. Throughout its range, T. quinqueloba is most common within seasonally mesotrophic environments like the Mediterranean and the Arabian Sea (Brummer and Kroon 1988). We speculate that Ac. strabocella may also have favored relatively mesotrophic environments but did not found the acarininid radiation until diversifying into more oligotrophic or less seasonal environments characteristic of the low latitudes. We suggest that the ecological deployment of the early acarininids within relatively mesotrophic settings may account for their later radiation relative to the morozovellids, which began their radiation in oligotrophic water masses. Why did the acarininids fail to diversify when they were initially established in highlatitude water masses? We suspect the answer


has to do with geographic variations in the number of niches that control latitudinal species diversity. There is much debate about the causes of latitudinal gradients in species diversity, with opinions ranging from differences in solar energy, geography, and geographic ranges of species to differences in water column structure (Roy et al. 1998; Rutherford et al. 1999). Recently, Rutherford et al. (1999) have shown a close correlation between planktonic foraminifer species diversity and sea surface temperature. They propose that cool, high-latitude waters have relatively few niches within them owing to the weak vertical thermal gradients of subpolar water masses whereas low-latitude oceans tend to be better stratified and provide more opportunities for niche subdivision in the upper ocean. Hence, there is a reason to believe that high-latitude environments may be less conducive to establishing radiations simply because there are fewer niches available to be filled by diversification. Accordingly, the acarininids may have initially failed to diversify because they started of in environments that presented few opportunities to sustain a large radiation. In effect, the initial appearance of acarininids in high-latitude oceans may have initially stifled their radiation, which began in earnest only with the subsequent evolution of low- and mid-latitude species. Conclusions Operating on the assumption that size is an adequate measure of the ontogenetic age in planktonic foraminifera, we found a small range of variation of ␦18O and large range of variation of ␦13C during ontogeny in our isotopic study of the Paleocene species of Acarinina. Our results show that acarininids have an isotopic size dependency similar to that of coexisting Morozovella. We also found an absence of size-related trends in ␦13C within Subbotina. The relationships between isotopic composition and ontogeny appear to be remarkably constant from high (ODP Hole 750A) to low latitudes (ODP Hole 761B) during the Paleocene. We suggest that the isotopic pattern of acarininids probably reflects the occurrence of algal photosymbionts and it can be used to trace the evolution of this trophic

325

strategy among this group during the Paleocene. The early morphotypes of the common ancestor Ac. strabocella, dated around 61 Ma, appear to have already harbored photosymbionts. However, we reject the possibility that the group acquired photosymbiosis by parallel evolution and suggest that it inherited the symbionts from the common ancestor it shared with morozovellids, believed to be close to the early Paleocene (late Danian) species Praemurica inconstans. The isotopic signature of photosymbiosis is present in all Paleocene species of Acarinina, all of which have a broadly similar depth habitat to that of Morozovella, even in the case of the early representatives of the group. Our results are consistent with previous isotopic studies that argued that the Paleogene morozovellids and acarininids were surface mixed-layer planktonic foraminifera and that subbotinids inhabited deeper and colder waters, within or below the thermocline, at low latitudes. Acknowledgments M.-P. Aubry (Institut des Sciences de l’Evolution de Montpellier) made useful comments on an early version of this manuscript. We gratefully acknowledge the reviews by B. Huber and M. Leckie, which substantially improved this work. We also thank D. Ostermann and L. P. Zou (Woods Hole Oceanographic Institution) for assistance with the mass spectrometer. Stable isotope mass spectrometry at WHOI was supported by grants from the Geology and Paleontology Program of the National Science Foundation (to R. D. N.). This is publication ISEM No. 2000-043, contribution UMR 5554 of Centre National de la Recherche Scientifique (CNRS), and WHOI contribution No. 10369. Literature Cited Aubry, M.-P. 1995. From chronology to stratigraphy: interpreting the lower and middle Eocene stratigraphic record in the Atlantic Ocean. Pp. 213–274 in W. A. Berggren, D. V. Kent, M.P. Aubry, and J. Hardenbol, eds. Geochronology, time scales and global stratigraphic correlations. SEPM (Society for Sedimentary Geology), Tulsa, Okla. Be´ , A. W. H. 1982. Biology of planktonic foraminifera. Pp. 51– 89 in M. A. Buzas, B. K. Sen Gupta, and T. W. Broadhead, eds. Foraminifera—notes for a short course. University of Tennessee, Knoxville. Berger, W. H., J. S. Killingly, and E. Vincent. 1978. Stable iso-

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