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Selectivity of Foraminiferal Extinction in the Late Eocene Author(s): Amit Banerjee and George E. Boyajian Source: Paleobiology, Vol. 23, No. 3 (Summer, 1997), pp. 347-357 Published by: Paleontological Society Stable URL: http://www.jstor.org/stable/2401108 . Accessed: 21/08/2011 12:52
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Paleobiology,23(3), 1997, pp. 347-357

Selectivity of foraminiferal extinction in the late Eocene

Amit Banerjee and George E. Boyajian
Abstract.-Late Eocene foraminiferal extinction shows diverse patterns of selective morphologic and latitudinal extinction. Taxa with discoidal shape, calcareous tests, and narrow and low-latitudinal ranges are at significantly greater risk of extinction. Elevated extinction intensities in calcareous tests are mainly due to the presence of larger benthic foraminifera that evolved in late Paleocene and diversified through the lower to middle Eocene. Selectivity of late Eocene foraminiferal extinction indicates that this extinction event was not a globally uniform event. Although this result does not verify an extraterrestrial impact or any other proposed cause of extinction, it does constrain the causes of late Eocene extinction. Furthermore, the geography of late Eocene foraminiferal extinction, and previously studied Cenomanian/Turonian extinction, demonstrates that mass extinctions exhibit different patterns of selectivity. Amit Banerjee.Geology Department, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6316 George E. Boyajian. Principal, Science & Technology,Roundtable Partners Incorporated,1400 Mill Creek Road, Gladwyne, Pennsylvania 19035 Accepted: 21 April 1997

Introduction Large-scale extinctions over geologic time are one of the primary indicators of global climatic events that affect the biosphere. Mass extinction events are episodes of accelerated extinction of variable magnitude that affect widespread taxa and cause at least temporary decline in their diversity (Sepkoski 1986; see also McLaren 1996). Selective killing of fauna with common biological and ecological characteristics is believed to provide clues to the proximate cause of mass extinctions (Bretsky 1973; Jablonski 1986a,b,c, 1991; Raup and Sepkoski 1986; Talent 1988; Copper 1989; Westrop 1991; Norris 1991, 1992; Kauffman and Fagerstrom 1993; Jablonski and Raup 1995). Marked selective removal of agglutinated foraminifera in the late Cenomanian (C / T), calcareous tests in the late Eocene (E / 0), and lack of selective extinction at the Cretaceous / Tertiary (K / T) boundary over the last 150 m.y., suggest a different proximate cause for each extinction (Banerjee and Boyajian 1996). We examine the selectivity of extinction of foraminiferal genera across the E /0 boundary, demonstrating the different patterns of selective killing documented in the fossil record. It is clear from earlier studies that an examination at lower taxonomic levels of the ecologies of the victims and survivors can reveal extensive patterns of selectivity of mass extinctions, although it is difficult to demonstrate taxonomic selectivity
C?1997 The Paleontological Society. All rights reserved.

at the class or phylum level (McKinney 1987; Raup and Boyajian 1988). Selectivity of the E/O extinction supports the idea that biological traits played a very significant role in foraminiferal extinction. Our study indicates that latitudinal range, morphology, and test composition are correlated with the survival of foraminiferal taxa at the E /0 boundary. Moreover, comparison of geography of the E / 0 and C / T foraminiferal extinction reveals different patterns of selectivity for these two large extinctions. Database and Method The late Eocene extinction appears to have been a prolonged global environmental perturbation that affected marine organisms (Sepkoski 1986; Brasier 1988); however, some have questioned the magnitude and abruptness of the E / 0 event (Snyder et al. 1984; Van Valen 1984). Overall, approximately 16% of all marine genera disappeared during the late Eocene compared with the average background level of 5-9% during the other Cenozoic stages (Sepkoski 1986). Taxa with particularly heavy extinction rates include planktonic dinoflagellates, coccolithophorids, ebridians, silicoflagellates, foraminifers, echinoids, gastropods, bryozoans, and malacostracans (Lipps 1970; Tappan and Loeblich 1971; Sepkoski 1986). Three data sets have been used to investigate the selectivity of late Eocene foraminif0094-8373 / 97/ 2303-0005 / $1.00

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AMIT BANERTEEAND GEORGE E. BOYAJIAN

eral extinction. First, the list of fossil marine foraminiferal genera and their stratigraphic ranges by Sepkoski (personal communication 1994), primarily based on the work of Loeblich and Tappan (1988), was used to determine which genera survived and which became extinct in the late Eocene. Foraminiferal genera show 14% extinction for this interval. Foraminifera are an ideal group for a global study because they are abundant, well skeletonized, found in diverse marine environments, and have a generally stable taxonomy. Also, the Cenozoic foraminiferal record is largely continuous as a result of the availability of Deep Sea Drilling Project (DSDP) and Ocean Drilling Project (ODP) data. Approximately 50 studied localities are from DSDP and ODP sites. Second, a database of global continental reconstructions was used to place the localities into their paleogeographic coordinates. For this study the localities are rotated back to their paleoposition using PaleoGeographic Information System (PGIS) software developed by Ross (1992). This software provides paleocoordinates of longitude and latitude, given the map coordinates for the present continental configuration and the time in millions of years before the present. Reconstruction of late Eocene continental configurations are well known due to the amount of sea floor available for study and its associated magnetic signatures (Ross 1992). Finally, a literature search (GEOREF)for articles containing information about late Eocene foraminifera reveals upwards of 400 peer-reviewed papers, of which 250 papers record the genus and species name of foraminifera, their stratigraphic interval, and locality name. These data provide a global view of foraminiferal diversity for the late Eocene. The database compiled from the 250 peer-reviewed sources contains late Eocene foraminiferal genera from 212 different localities containing 4226 occurrences of 222 genera (Fig. 1). An occurrence is defined as the presence of a genus at a locality, separated by >1? latitude or longitude. In our database, 14% (31 / 222) of foraminiferal genera were killed during the late Eocene. Both planktonic and benthic foraminifera are included in these es-

timates, with planktonic and larger benthic foraminifera constituting only 7% and 12% of the taxa, respectively. Invalid genera and junior synonyms were eliminated from the analysis.

Estimates of the duration of the late Eocene average approximately four million years (Harland et al. 1990). Despite the highly resolved nature of late Eocene biostratigraphy, the late Eocene has not been subdivided in this study for two reasons. First, on a global scale there are difficulties in correlation and chronostratigraphy. Second, sample size would have become too small for meaningful statistical analyses. Raup and Jablonski (1993) encountered similar problems in their study of K / T marine bivalve extinctions. Furthermore, the geographic range of genera before extinction is the focus of this paper. Foraminiferal genera, rather than species, are analyzed to eliminate peculiarities of sampling, preservational bias, and local species taxonomies. Conducting the analysis at the genus level provides the greatest signal-to-noise ratio and has the greatest resolving power. Raup and Jablonski (1993) have demonstrated the feasibility of using this compilation method, analysis, and level of taxonomy. In this study paraphyly is not as crucial a problem as it is in other analyses because the data are collected and analyzed at the generic level. Recently, in an analysis of modeled monophyletic and paraphyletic taxa, Sepkoski and Kendrick (1993) showed that paraphyletic taxa provide an accurate representation of extinction patterns and intensity (especially at low levels of sampling). Moreover, higher taxa are extensively used in studying patterns of past and present-day ecological and biodiversity changes (see Roy et al. 1996; Lee 1997). Although foraminifera are often identified as different taxa on the basis of their morphotypes (Loeblich and Tappan 1988), the disappearance of distinctive morphologies (or of a collection of species within a genus) is of no less significance than the loss of taxa that are defined on the basis of shared-derived characters. In either case, the disappearance from the fossil record of a group with a specific ecology or geographic distribution may pro-

SELECTIVITY OF FORAMINIFERAL EXTINCTION

349

'

V D

Late Eocene 36.6 m.y.

,~<,

rnap tlae ? l. T FICIJRE ocation of 21 localities. x~~~~~~~~~~~~~~ -x x~~~~~~~~~~~~~~~

-500

km at Equator

FIGURE

1.

Location map of the 212 localities.

vide evidence necessary to deduce the cause of the extinction. Ranges of foraminiferal genera are grouped in 150 latitudinal belts (Table 1). Ranges were measured as maximum latitudinal extent. Analyses were conducted both with and without planktonic and larger benthic foraminiferal genera, as well as the 24 benthic genera that occurred in only one or two localities (for method see Banerjee and Boyajian 1996). FurTABLE

1. Latitudinal distribution of 4226 occurrences of genera. Data were gathered from more than 245 peerreviewed articles and reduced to 212 localities.
Latitude Localities Occurences

ther, taxa with at least five and ten occurrences, representing 76% and 52% of our database, were analyzed to check for possible bias in latitudinal range data. Neither treatment showed any significant change in the results. Moreover, all the genera having at least five occurrences were found not only at broadly separated localities within a latitudinal belt, but also in different latitudinal belts. The genera in the database are divided into five morphotypes for the morphological analysis: serial, globular, discoidal, plano-convex, and biconvex forms (see Haynes 1981; Banerjee and Boyajian 1996). Selectivity of Extinction Latitudinal Selectivity of Late Eocene Extinction.-Foraminiferal genera restricted to narrow and low-latitudinal belts were more severely affected than high-latitude (>600) and cosmopolitan genera. Extinction rates of foraminiferal genera with calcareous and agglu-

45N-60N 30N-45N 15N-30N 0-15N 15S-0 30S-15S 45S-30S 60S-45S

20 65 39 23 11 17 16 21

512 1468 489 487 284 380 377 229

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AMIT BANERJEE AND GEORGE E. BOYAJIAN

(A)
Latitude
45N-60N 30N-45N 15N-30N 0-15N 15S-0 30S-15S 45S-30S 6.S-45S
X 20 40 X 20 40 X 20 40 X 20 40 X 20 40 X 20 40

All groups

Agglutinated

Calcareous

Globular

Discoidal

Serial

extinction percentages (B) Latitude 45N-60N 30N-45N 15N-30N 0-15N 15S-0 30S-15S 458-308 608-458
X 20 40 X20 40 X 20 40 X20 40 X20 40 X 20 40

All groups

Agglutinated

Calcareous

Globular

Discoidal

Serial

extinction percentages
2. Latitudinal variation in extinction percentages of late Eocene foraminifera. A, All foraminifera. B, Excluding larger calcareous benthic foraminifera. X's indicate those groups that have extinction rates significantly higher than the average (x 14%) for the stage (G-test p < 0.05).
FIGURE

tinated tests show elevated extinction in low (Banerjee and Boyajian 1996), and the endlatitudes, as do each of the five morphotypes. Cretaceous (Hallock 1982; Kauffman 1984). Extinction levels for the latitudinal belts of 15? Extinction levels for 15? latitudinal belts are given in Figure 2 for the late Eocene. Ele- show disproportionate rates of extinction in vated low-latitude extinction has been report- the low latitudes, a result consistent with preed for various taxonomic groups from the end- vious observations (Raup and Jablonski 1993; Ordovician (Berry 1979; Sheehan 1979), Late Huber et al. 1994; Banerjee and Boyajian 1996). Devonian (Copper 1977), the end-Permian Raup and Jablonski (1993), however, found no (Bretsky 1973; Valentine and Moores 1973; latitudinal patterns once rudists were excludWaterhouse 1973; Erwin 1989, 1993), the Late ed from their Cretaceous bivalve database. In Triassic (Hallam 1981), the late Cenomanian contrast, when analyzed without 27 (12 ex-

SELECTIVITY OF FORAMINIFERAL EXTINCTION

351

(A) TEST COMPOSITION AGGLUTINATED

20 30

CALCAREOUS
calcareous (withlarger enhc foramninifera) 30 calcareous larger (excluding benthic foramninifera)

~20
-10

~20

zlo zl_0

0 s ! o1 C0

Latitudinal Ranges

Latitudinal Ranges

Latitudinal Ranges

(B) MORPHOTYPE
20 20 20

GLOBULAR

SERIAL

DISCOIDAL

~~~~~0

z
tO\

Latitudinal Ranges
FIGURE

Latitudinal Ranges

Latitudinal Ranges

3. Histograms showing latitudinal ranges of foraminifera with different test compositions and morphotypes. A, Calcareous and agglutinated foraminifera show similar latitudinal distribution when larger calcareous benthic foraminifera showing significantly narrower latitudinal ranges are excluded. B, The frequency distributions of different morphotypes show narrower latitudinal range for discoidal taxa compared with globular and serial shapes.

tinct taxa) larger calcareous benthic foraminiferal genera, principally represented by miliolid alveolines and rotaliid nummulites, the latitudinal pattern of foraminiferal extinction does not go away entirely, but does become considerably weaker and statistically insignificant (Fig. 2B). The latitudinal gradient in extinction intensity is partly due to the larger calcareous benthic foraminifers showing significantly narrow latitudinal range (Fig. 3A). The larger calcareous benthic foraminiferal taxa of the upper Eocene were probably restricted to low-latitude shelf environments within the photic zone, as observed in their present-day distribution (Hallock 1979; Haynes 1981). Further, they have a very narrow range of thermal tolerance (Wei and Kennett 1983, 1986). Nevertheless, the raw extinction values of 27% among foraminifera with latitude range of <60 and 5% among those

with >60? of latitude suggest that taxa restricted to narrow latitudinal ranges are more severely affected. The greatest concentration of localities containing victims is restricted between 30?S and 30?N latitude, despite the presence of 33% of our localities between 30?N and 45?N latitude (Table 1). The largest number of sampled localities lie in northwestern Europe, and they constitute some of the most extensive and best-studied late Eocene deposits. Morphotype Selectivity of Late Eocene Extinction.-Discoidal morphotypes, irrespective of their test composition, show 29% extinction for the late Eocene. This is significantly higher than the serial, globular, plano-convex, and biconvex morphotypes (Fig. 4B). They also demonstrate disproportionate extinction in the low latitudes. The elevated extinction of discoidal morphotypes does not change the re-

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AMIT BANERJEE AND GEORGE E. BOYAJIAN

ALL LATITUDINALRANGES
140 (A)

calcareous* 70. (B) globular discoidal*

serial

agglutinated
70 35

0~~~~~~~~~~~

<60 DEGREES
(C) 70 40 - (D)

calcareous* globular

discoidal*
serial

~ ~ ~ ~~~~~2

35 agglutinated

L
FIGURE4.

victims

survivors

significantlyhigherextinction

Histograms showing selectivity of extinction for late Eocene foraminiferal genera. A, Foraminifera with calcareous tests show significantly higher extinction rates than foraminifera with agglutinated tests for genera with latitudinal ranges from <15' to a maximum of 120? latitude. B, Foraminifera with discoidal tests show significantly higher extinction rates than foraminifera with other shell morphologies for genera with latitudinal ranges from <15' to a maximum of 120? latitude. In C and D, selectivity is still pronounced for foraminifera with smaller geographic ranges. C, Foraminifera with calcareous tests show significantly higher extinction rates than those with agglutinated tests for genera with ranges 60?. D, Foraminifera with discoidal tests show significantly higher extinction rates than foraminifera with other shell morphologies for genera with ranges 60? (t-test p < 0.05).

sults significantly when analyzed without the larger calcareous benthic foraminiferal group composed of nine discoidal taxa, of which seven were killed. Among all the foraminiferal genera with latitudinal ranges <60?, foraminifera with discoidal tests show significantly higher extinction rates (Fig. 4D). Modern and fossil foraminiferal genera are ecologically dependent on sunlight, temperature, dissolved

oxygen levels, and organic carbon flux (Douglas 1981; Sen Gupta et al. 1981; Caralp 1984; Bernhard 1986; Corliss and Chen 1988; Niensted and Arnold 1988; Sjoerdsma and Van der Zwann 1992). The higher extinction rates of discoidal taxa are quite intriguing as present-day flattened taxa are known to provide a more favorable geometry for oxygen diffusion than that provided by inflated tests

SELECTIVITY OF FORAMINIFERAL EXTINCTION

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found in more oxic shallow marine environments (Bernhard 1986; Corliss and Chen 1988; Corliss and Emerson 1990; Koutsoukos et al. 1990; Corliss 1991; Sen Gupta and MachainCastillo 1993; Kaiho 1994). In the present study, however, it is these flattened forms that suffer the greatest extinction and also display significantly smaller latitudinal ranges when compared with globular and serial morphotypes (Fig. 3B). On the contrary, planktonic foraminifera suffered extinction with the elimination of long-ranging, specialized, morphologically diverse, and deeper-dwelling low-trochospired forms irrespective of their latitudinal range. Surviving genera are simple, globular, and surface dwelling (see also Toumarkine and Luterbacher 1985). In the present-day oceans, the planktonic foraminifera species are primarily present in the upper 200 meters of the water column (Haynes 1981: pp. 328330). Although isotopically inferred depth habitat for the Mesozoic and Tertiary planktonic foraminifera is poorly understood, modern species with complex morphologies usually dwell in the relatively deeper waters, while morphologically simple globular species tend to be surface dwellers (Van Eijden 1995). Moreover, discoidal taxa show narrow and low-latitudinal range in the shallow marine shelf environment. This pattern of selective killing demonstrates that sharing of habitat by planktonic foraminifera and foraminifera with discoidal shape in the late Eocene regulated extinction susceptibility or else resulted from different proximate causes, but a common ultimate cause. Calcareous assemblages show a higher extinction rate (20%) when compared with that of their agglutinated counterparts (7%) (Fig. 4A). Even among those genera with latitudinal ranges of <60?, calcareous foraminifera continue to show significantly higher extinction rates when compared with agglutinated taxa (Fig. 4C). When analyzed without the 27 larger calcareous benthic foraminifera, the extinction rate of calcareous taxa (5%) falls below the rate of the agglutinated assemblage. Though there may be bias in the number of workers studying calcareous and agglutinated forms, high rates of extinction in the late Eo-

TABLE

2. Selectivity of foraminiferal extinction during late Eocene and late Cenomanian.

Late Cenomanian Late Eocene

Geographic selectivity Latitudinal range Morphotype selectivity Test shape Test composition

low latitude narrow discoidal agglutinated

low latitude narrow discoidal calcareous

cene indicates preferential survival of genera with agglutinated tests. Comparison of the extinction rates of foraminiferal genera with agglutinated tests and those with calcareous tests reveals different patterns of selective extinction for late Eocene and late Cenomanian extinctions (Banerjee and Boyajian 1996): the late Eocene extinction shows an exaggeration of the background pattern, with calcareous taxa suffering a significantly larger extinction than foraminifera with agglutinated shells, as compared with selective extinction of agglutinated taxa in the late Cenomanian. Results The appearance of a latitudinal gradient in the E/O foraminiferal mass extinction was caused by the narrow and low-latitudinal habitat range of discoidal morphotypes; when 27 larger calcareous benthic foraminifera are excluded, the extinction intensity shows a very weak, statistically insignificant latitudinal gradient. This suggests that the late Eocene extinction is controlled primarily by shell morphology and partly by the presence of larger calcareous benthic foraminifera that evolved in the late Paleocene and diversified in the early and middle Eocene (Brasier 1988). Nevertheless, shell morphology, test composition, and latitudinal range play a significant role in the selectivity of E / 0 extinction. Table 2 illustrates the similarities and differences in the selectivity of foraminiferal extinction during E / 0 and C / T boundaries (for C/T extinction selectivity see Banerjee and Boyajian 1996). Discoidal foraminifera during both extinction events were restricted to narrow and low-latitudinal belts. Moreover, they were killed at a higher rate in comparison with other morphologies and with those oc-

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AMIT BANERJEE AND GEORGE E. BOYAJIAN

cupying broad latitudinal ranges and temperate to boreal latitudes. Foraminifera with calcareous tests show relatively higher extinction rates in the late Eocene, in contrast to agglutinated taxa in the late Cenomanian, although this is primarily due to larger calcareous benthic foraminifera. Mass extinctions play an important role in shaping the world's biota, but the driving mechanisms are still poorly understood. Although microtektites provide evidence for an extraterrestrial impact (O'Keefe 1980; Alvarez et al. 1982; Ganapathy 1982; Glass 1982), the exact role of a late Eocene impact in the extinction is unclear and problematic (Corliss et al. 1984; Miller et al. 1991). At least three microtektite horizons are known from the late Eocene and none appears to correspond exactly to significant marine or terrestrial extinction (e.g., Keller et al. 1983; Jablonski 1986b; Byerly et al. 1988; Hazel 1989; Poag et al. 1992). Furthermore, microinvertebrates display a stepwise extinction pattern that corresponds with episodes of cooling, rather than an abrupt mass extinction at the end of the Eocene (Keller 1983; Snyder et al. 1984; Wei 1991; Thomas 1992). The time-transgressive nature of the late Eocene event (Douglas and Woodruff 1981; Kennett 1983; Corliss et al. 1984; Snyder et al. 1984; Brasier 1988) and the selectivity of foraminiferal extinction do not point to a globally uniform and sudden catastrophic extinction, as might be caused by a bolide impact; rather they suggest the combined action of different physical phenomena. Changes in plate tectonic configurations and deep-sea circulation patterns in the late Eocene have been used to explain the observed climatic changes and faunal turnovers (Keigwin 1980; Burns and Nelson 1981; Cavelier et al. 1981; Corliss 1981; Haq 1981, 1982; Van Couvering et al. 1981; Norris 1982; Crowley 1983; Kennett 1983; Snyder et al. 1984). Similarly, tectonically induced eustatic changes are thought to be the most likely cause for changes in the composition of larger foraminiferal faunas during the Cenozoic (Adams 1983). Adams (1983) failed to find any correlation between climate and diversity change in the larger benthic foraminiferal family of Miliolidae, Miogypsinidae,

and Lepidocyclinidae. Nonetheless, an appreciable drop in temperature and an increase in meridional temperature gradients between polar and tropical regions (Saunders 1985; Jenkins 1986; Wei 1991; Mackensen and Ehrmann 1992; Barrera and Huber 1991; Prothero and Berggren 1992; Miller et al. 1992; Molina et al. 1993; Zachos et al. 1994) are plausible agents for the late Eocene extinction, given the smaller latitudinal range of discoidal forms, the narrow thermal tolerance of larger calcareous benthic foraminifera, the deeper habitat of specialized planktonic forms, and the effect of climate on oceanic circulation (see also Wei and Kennett 1983, 1986). Furthermore, the sharp fall in late Eocene sea level (Vail et al. 1977), associated with global cooling, may have destroyed the habitat of larger calcareous benthic foraminifers of "reefal" habitat (Brasier 1988). Conclusions We conclude that the latitudinal gradient of the late Eocene foraminiferal extinction is principally controlled by the discoidal morphotype. When the larger calcareous benthic foraminifera are excluded from the database, extinction intensities in the low latitudes are indistinguishable from those of the high-latitude values. Similarly, the high extinction rate of calcareous tests compared with agglutinated taxa is mainly due to larger calcareous benthic foraminifera. Marked selectivity of extinction with the demise of discoidal morphotypes, larger calcareous benthic foraminifera, and long-ranging, specialized, morphologically diverse, and deeper-dwelling low-trochospired planktonic forms reflect disruption of habitat, rather than true latitudinal gradient. This extinction pattern is probably due to the combined effect of destruction of watermass configuration, change in thermocline, and decreased productivity. When analyzed together, our analyses indicate that late Eocene extinction was not a globally uniform event. Although this result does not verify extraterrestrial impact or any other proposed cause of the extinction, it does constrain the causes of late Eocene extinction.

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Acknowledgments We thank J. J. Sepkoski Jr.for use of his data on stratigraphic ranges of foraminiferal genera; R. Bambach, B. Le Page, R. Norris, H. W Pfefferkorn, K. Roy, K. Yemane, and an anonymous reviewer for criticism and advice on earlier versions of this manuscript; Inter Library Loan Office, Van Pelt Library, University of Pennsylvania for procuring numerous articles: and Gary Hughes for data management. Literature Cited
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