Palaeogeography, Palaeoclimatology, Palaeoecology 361-362 (2012) 94–103

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Palaeogeography, Palaeoclimatology, Palaeoecology

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Paleoceanographic significance of deep-sea benthic foraminiferal species diversity atsoutheastern Indian Ocean Hole 752A during the Neogene

Raj K. Singh ⁎, Anil K. Gupta 1, Moumita Das 2

Department of Geology and Geophysics, Indian Institute of Technology, Kharagpur‐721302, India

⁎ Corresponding author at: Wadia Institute of HimaDehradun‐248001, India. Tel.: +91 135 2525270; fax: +

E-mail address: rajkursingh@yahoo.com (R.K. Singh1 Present address: Wadia Institute of Himalayan Geol

248001, India.2 Present address: 5112 Adrian St, Rockville, MD 208

0031-0182/$ – see front matter © 2012 Elsevier B.V. Allhttp://dx.doi.org/10.1016/j.palaeo.2012.08.008

a b s t r a c t

a r t i c l e i n f o

Article history:Received 22 February 2012Received in revised form 20 July 2012Accepted 13 August 2012Available online 23 August 2012

Keywords:PaleoceanographyNeogeneBenthic foraminiferaDiversityIndian OceanOxygen Minimum Zone

Diversity parameters of Neogene deep-sea benthic foraminifera were measured at Ocean Drilling Program (ODP)Hole 752A, southeastern Indian Ocean (water depth of 1086.3 m) using Information Function (H), Equitability(E), number of species (S) and Sander's rarefaction values. These parameters combinedwith population abundanceof dominant benthic foraminifera (Bulimina macilenta, Nuttallides umbonifera, Cibicides wuellerstorfi, Cibicideslobatulus, Bolivina pusilla, Ehrenbergina carinata, Gavelinopsis lobatulus, Cassidulina laevigata, Globocassiulinasubglobosa) reveal significant paleoceanographic changes in the southeastern Indian Ocean during the Neogene.The values of all the diversity parameters show a decrease from 25 to 23 Ma and thereafter an increase with peakvalues at ~13.5 Ma. The Late Oligocene to Earliest Miocene was an interval of more unstable conditions at Hole752A dominated by species characteristic of low organic carbon, well-ventilated, carbonate corrosive high energyconditions. The highest values of diversity parameters coincide with the early Middle Miocene climatic optimum.All these parameters show a declining trend and gradual decrease from 13.5 to 4.5 Ma coinciding with the majorbuild up of ice sheets in the Antarctic region. Major increase in B. pusilla and E. carinata population during thistime suggests high nutrient levels and low oxygen conditions at Hole 752A. This interval corresponds with theso-called “biogenic bloom” and an intense Oxygen Minimum Zone as observed throughout the Indo-Pacific region.Deep waters were warmer from 4.5 to 3 Ma marked by an increase in species diversity values, coinciding with theearly middle Pliocene warmth. The species diversity values abruptly decreased in the younger interval, contempo-raneouswith themajorNorthernHemisphere glaciation. During this time species characteristics of high-energybot-tom currents and relatively cold deep water were dominant.

© 2012 Elsevier B.V. All rights reserved.

1. Introduction

Deep-sea faunal diversity fluctuated considerably across majorclimatic and oceanic turnovers throughout the Neogene (Thomasand Gooday, 1996; Gupta et al., 2001; Rai and Singh, 2001; Singhand Gupta, 2005; Rai and Maurya, 2009; Yasuhara et al., 2012).Numerous studies on faunal diversity indicate relationship betweenspecies diversity and latitude (e.g., Fischer, 1960; Valentine, 1966;Rex et al., 1993; Thomas and Gooday, 1996; Culver and Buzas, 2000;Corliss et al., 2009; Yasuhara et al., 2009; Powell et al., 2012) andalso with increasing depth in the marine environment (e.g., Gibson,1966; Buzas and Gibson, 1969; Gibson and Hill, 1992; Rex et al., 2006;Larkin and Gooday, 2009). Availability of nutrients, heterogeneity ofhabitat and predation are other important factors bringing changes indeep-sea species diversity patterns (Gooday, 1988; Rai and Singh,

layan Geology, 33 GMS Road,91 135 2625212.

).ogy, 33 GMS Road, Dehradun‐

53, USA.

rights reserved.

2001; Smart et al., 2007; Corliss et al., 2009; Gooday et al., 2010). Inthe northern Indian Ocean low species diversity values have beenobserved during intervals of environmental instability (Gupta andSrinivasan, 1992; Gupta et al., 2001).

The oceanic surface productivity and oxygenation of deep watershad significant impact on ocean's faunal regime during the Cenozoic(Dickens and Owen, 1999; Zachos et al., 2001; Sun et al., 2006;Corliss et al., 2009; Kender et al., 2009; Ifrim et al., 2011). Changesin thermocline and thermohaline circulation of ocean basin haveimpacted the surface and deep-sea biota as well as regional andglobal climates (Cane and Molnar, 2001; Karas et al., 2009). The pro-ductivity increased significantly in all the oceans since the late middleMiocene (~13 Ma) coinciding with a major increase in Antarctic glacia-tion (Kennett and Barker, 1990) and reached its peak during 10–8 Ma(Dickens and Owen, 1999; Hermoyian and Owen, 2001; Gupta et al.,2004) during which time the Asian monsoons intensified (Quade et al.,1989; Kroon et al., 1991; Gupta and Srinivasan, 1992; An et al., 2001).These productivity-related events are believed to have triggered theso-called “biogenic bloom” and expansion of Oxygen Minimum Zone(OMZ) to large parts of the intermediate Indian Ocean in the late middleMiocene at about 13 Ma (Pisias et al., 1995; Filippelli, 1997; Dickens andOwen, 1999; Hermoyian and Owen, 2001). The expansion of OMZ during

95R.K. Singh et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 361-362 (2012) 94–103

this time led to a decrease in species diversity (Kender et al., 2009;Gooday et al., 2010; Ifrim et al., 2011). Deep-sea benthic foraminiferahave good potential of adaptation and are able to survive in a widerange of marine environments. Several earlier and recent studiesprovide an insight into the factors controlling the distribution of benthicforaminifera (Streeter, 1973; Lohmann, 1978; Corliss, 1979a, 1979b;Schnitker, 1980, 1984; Lutze and Coulbourn, 1984; Thomas, 1986,1992; Hermelin and Shimmield, 1990; Gupta and Srinivasan, 1992;Smart et al., 1994, 2007; Jorissen et al., 1995; Gupta and Thomas, 1999,2003; Van der Zwaan et al., 1999; Gooday et al., 2000; De and Gupta,2010; Ortiz et al., 2011; Pérez-Asensio et al., 2012).

To understand the role of environmental parameter(s) in control-ling variations in species diversity, this study analyzed diversitytrends in deep-sea benthic foraminifera at Ocean Drilling Program(ODP) Hole 752A, southeastern Indian Ocean during the Late Oligoceneto theHolocene. Hole 752Amoved from43°S across the Late Oligocene–Miocene boundary (~23 Ma) to the present location of 30°S withoutany significant change in thewater depth throughout the studied inter-val (Peirce et al., 1989). A correlation between benthic foraminiferalspecies diversity and population abundances of dominant benthicforaminifera will help to understand ocean-driven diversification inthis faunal group in the southeastern Indian Ocean during the Neogene.

2. Oceanographic setting of the study area

Hole 752A is located near the crest of the Broken Ridge at a latitudeof 30°53.475′S, longitude of 93°34.652′E, and awater depth of 1086.3 min the southeastern Indian Ocean beneath the subtropical gyre (Fig. 1).The waters of the subtropical gyre have high salinity, low nutrientsand high dissolved oxygen. The West Wind Drift, the South EquatorialCurrent and the Subtropical Convergence largely control the surface-water circulation of the southeastern Indian Ocean in the area of Hole752A (Fig. 1; Okada and Wells, 1997). Besides, the Leeuwin Current,and South Indian Current are other components of the surface circula-tion off the coast of Western Australia near Hole 752A. At present, thishole is outside the influence of the Indian monsoon system.

India

80o 90o 100o 110o 120o E

10o

0o

10o

20o

30o752A

Sumatra

Java

Borneo

South C

hina S

ea

Indian Ocean

Mak

assa

r Str

ait

Lombok Strait

Au

stra

lia

SEC

LCSEC

SEC

N

WAC

SJC

Subtropical Convergence

Fig. 1. Location of Hole 752A with dotted arrow line showing different oceanic currentsaffecting this hole. SEC= South Equatorial Current, SJC= South Java Current, LC= LeeuwinCurrent, WAC=Western Australian Current (after Wijffels et al., 1996).

The strong westerly winds centered between the Subtropical andAntarctic Convergences in the Southern Ocean drive the West WindDrift current, whereas southeast tradewinds drive the South EquatorialCurrent of the tropics westward (Tchernia, 1980). Between these windsystems, major anticlockwise gyres are established in the Indian andPacific Oceans. The zone between 30°S and 10°S is located entirely inthe anticyclone belt to the south of the Southeast Trades where lowprecipitation and high evaporation is prevalent (Tchernia, 1980). TheSouth Equatorial Current and the cold saline South Indian Currentflowing west and north, respectively, make up the eastern wing of theanticlockwise gyre in the temperate-subtropical south Indian Ocean.This eastern wing flows equator-ward, while adjacent to it, along thewest coast of Australia, is the pole-ward flowingwarm Leeuwin Currentthat has low salinity. Parallel to the Leeuwin Current, there is thenorthward flowing eastern component of the South Indian OceanGyre known as the West Australian Current (Pearce, 1991).

The physico-chemical properties of deep and bottom water circula-tion in the Indian Ocean is different than the other ocean basins as it islandlocked in the north. The GEOSECS (1983) data together with thestudies by Tchernia (1980) and Warren (1981) show that AntarcticBottom Water (AABW) flows northward in the Indian Ocean below3800 m, which is formed in the Weddell Sea and penetrates the IndianSector near 62°E between the Crozet Islands and Kerguelen Plateau.Antarctic Intermediate Water flows at 1200 m in the Indian Ocean.Thus location of Hole 752A is influenced by Antarctic IntermediateWater in the present day ocean. Geochemical data from GEOSECSstation 436 (lat. 29°15′S; long. 109°58′E) shows deep ocean waterclose to Hole 752A has a temperature of 3.8 °C, PO4 content of0.051 ml/l and NO3 content of 0.74 ml/l (Fig. 2a). The dissolved oxygenconcentration of the overlying water is ~3.36 ml/l (Fig. 2a and b). Theoxygen minimum zone exists as a wedge shaped lens extending upto 5000 km southeast from the Arabian coast and between waterdepths of 200 and 2000 m (Wyrtki, 1971; Slater and Kroopnick, 1984;Dickens and Owen, 1994, 1999). The present day depth of Hole 752Ahas lowest value of dissolved oxygen in comparison to the water lyingabove and below this zone (Fig. 2b).

This hole has been under the influence of southern componentdeep water during the entire Neogene and has remained almost atits present water depth over the studied interval with extremelylow sedimentation rate of b0.61 cm/kyr (Peirce et al., 1989). Thesedimentation rate has remained nearly constant over the entireNeogene period (Fig. 3).

3. Materials and methods

We analyzed 142 samples of 10 cm3 volume, whichwere processedusing the standard methods as given in Gupta and Thomas (1999). Wegenerated benthic foraminiferal census data from an aliquot of ~300specimens from 125 μm+ size fraction. Interpolated ages for eachsample are based on the age model of Peirce et al. (1989) and revisedaccording to Berggren et al. (1995) (Fig. 3). The average time resolutionper sample is ~170 kyr based on the interpolated ages. The dominantbenthic foraminiferal species were selected on the basis of theirpresence with more than 20% in at least two samples (Table 1).

We calculated the species diversity in terms of Information Function(H), Equitability (E) and Sander's rarefaction number (Fig. 4). Thenumbers of species (S) were also counted from each sample. TheInformation Function (H) was calculated using the Shannon-WienerDiversity index (Shannon and Wiener, 1949) given by the formula:

H ¼ −XS

i¼1

pi ln pi

where, S is the number of species in a given sample, pi is the proportionof the ith species in the sample and ln is the natural logarithm. To

0 5 10 15 20 25

3 3.5 4 4.5 5 5.5

0

1000

2000

3000

4000

5000

6000

-0.2 0 0.2 0.4 0.6 0.8

GEOSECS 436

0.01 0.02 0.03 0.04 0.05 0.060.00

Oxygen ml/l

NO3 ml/l

PO4ml/l

Dep

th (

m)

a)

PO ml/l4

NO ml/l3

2500

2000

1500

1000

500

0

920 930 940 950 960

Hole 752A

Longitude (E)

Wat

er D

epth

(m

)

30 53.475 S transect0 ’

5.19

4.52

3.70

3.50

DOml/L

3.36

SICW

AAIW

NIDW

b)TemperatureoC

Fig. 2. (a) Vertical profiles of hydrological properties of GEOSECS 436 station located near ODP Hole 752A. (b) Vertical profiles of dissolved oxygen content along the east–westtransect at 30°53.475′S. NIDW=North Indian DeepWater, AAIW= Antarctic Intermediate Water, and SICW= South Indian Central Water (from Murgese and De Deckker, 2005).(a) and (b) Source: GEOSECS data (1983).

96 R.K. Singh et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 361-362 (2012) 94–103

calculate the equitability, we used the mathematical expression givenby Buzas and Gibson (1969) as below:

E ¼ eH= S:

Sander's values were calculated by rarefying against 100 individuals(Sanders, 1968). These values were also used in the studies of deep-seafaunal diversity (Rex et al., 1997; Gupta et al., 2001; Singh and Gupta,2005).

0

20

40

60

80

1000 5 10 15 20 25

Age (Ma)

Dep

th (

m)

Fig. 3. Depth versus age plot of Holes 752A based on nannofossil data (Peirce et al., 1989)and updated to the timescale of Berggren et al. (1995).

The δ18O and δ13C data of benthic foraminifer Cibicidoides sp. arefrom Rea et al. (1991) and plotted with diversity values against thenumerical ages (Fig. 4). The diversity functions are linearly correlatedwith each other showing high positive correlation (Fig. 5). Thedominant species are plotted with Information Function (H) againstthe numerical ages (Fig. 6).

4. Results

The species diversity, H, E, S and Sander's values at Hole 752Ashow significant variability (Fig. 4). The E and H, S and H, and Sander's

Table 1Dominant species of benthic foraminifera (species with >20% abundance in at leasttwo samples) at Hole 752A, their environment preferences and age of dominance.

Species Micro-habitat Environmentalpreferences

Age of dominance

Buliminamacilenta

Shallowinfaunal

Intermediate oxygen,intermediate foodsupply

25 and 20.5 Ma

Nuttallidesumbonifera

Epifaunal Low temperature, highoxygen, low foodsupply, corrosivebottom water

22.5 to 19.5 Ma andagain during 15 to14 Ma

Cibicideswuellerstorfi

Epifaunal Intermediate to hightemperature, highoxygen, intermediatepulsed food supply

20–19 Ma, and asignificant increasefrom 14 to 4.5 Ma andduring the last 1 Ma

Cibicideslobatulus

Epifaunal Low to intermediatetemperature, highoxygen, intermediatefood supply

2 to 1 Ma

Bolivinapusilla

Deepinfaunal

High temperature, lowoxygen and high foodsupply

13.5 to 4.5 Ma

Ehrenberginacarinata

Shallowinfaunal

High temperature, lowoxygen and high foodsupply

7.5 to 4.5 Ma

Gavelinopsislobatulus

Epifaunal Intermediate oxygen,pulsed food supply

9.5–9 Ma, 7–6 Ma and4.5–1.6 Ma

Cassidulinalaevigata

Shallow todeep infaunal

Low to intermediatetemperature, highoxygen, intermediatefood supply

After 1 Ma

Globocassidulinasubglobosa

Shallowinfaunal

High temperature,high oxygen, low tointermediate, pulsedfood supply

Throughout Neogene,continuous decreaseuntil ~2 Ma; thereafterit shows a majorincrease

Age (Ma)

15

20

25

30

35

40

45

0 5 10 15 20 25

0.2

0.3

0.4

0.5

0.6

0.722.22.42.62.8

33.23.43.6 25

30

35

40

45

50

55

0

1

2

3

0

1

2S

ande

r ’s

val

uera

refie

d to

100

indi

vidu

als

Equ

atib

ility

(E

)

Info

rmat

ion

Fun

ctio

n (H

)

No.

of S

peci

es (

S)

LateOligocene

EarlyMiocene

MiddleMiocene

LateMiocene

EarlyPliocene

Pleist-ocene

LatePliocene

Cib

icid

oide

s sp

. δ18

O (

‰) Cib

icid

oide

s sp

. δ13

C (

‰)

Fig. 4. Species diversity values atODPHole 752AofH, S, E and Sander's rarefied values andCibicidoides sp. δ18O and δ13C values are plotted against numerical ages ofHole 752A (Rea et al., 1991).

97R.K. Singh et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 361-362 (2012) 94–103

values and H show a high positive correlation, while H and δ18Ovalues of Cibicidoides sp. (Rea et al., 1991) show a weak, inversecorrelation (Fig. 5). However in an earlier study, Singh and Gupta(2005) observed a strong inverse relation between δ18O values ofUvigerina sp. and H at intermediate depth ODP Site 757 (waterdepth 1652 m), which is located on the Ninetyeast Ridge north ofHole 752A. The E, H, S and Sander's values were low from ca 25 to20.5 Ma and thereafter show an increase up to ~13.5 Ma. All theseparameters show a gradual decrease from ~13.5 to 4.5 Ma coincidingwith the major build up of ice sheets in the Antarctic region (Kennettand Barker, 1990). The E, H, S and Sander's values show an increase

for a brief period from ~4.5 to 3 Ma (Fig. 4), followed by an abruptdecrease in the younger interval, coinciding with major northernHemisphere Glaciation (NHG). The isotope values show a broadparallelism with the diversity values. The δ18O values of Cibicidoidessp. show a gradual increase whereas δ13C values show a decreasesince ~14 Ma (Fig. 4).

4.1. Environmental preferences of benthic foraminifera

Numerous studies suggest that distribution patterns of benthicforaminifera are closely tied to organic carbon flux as well as organic

Information Function (H) Information Function (H)

Information Function (H) Information Function (H)

R=0.31,RR=0.77, R

2=0.600

R=0.87,R2 =0.767R=0.88,R

2= 0.779

0.2

0.3

0.4

0.5

0.6

0.7

2 2.2 2.4 2.6 2.8 3 3.2 3.4 3.615

20

25

30

35

40

45

2 2.2 2.4 2.6 2.8 3 3.2 3.4 3.6

25

30

35

40

45

50

55

2 2.2 2.4 2.6 2.8 3 3.2 3.4 3.6

2=0.096

0

0.5

1

1.5

2

2.5

3

2 2.2 2.4 2.6 2.8 3 3.2 3.4 3.6

No.

of S

peci

es(S

)E

quat

ibili

ty (

E)

San

der’s

val

ue r

are

fied

to 1

00 in

divi

dual

sC

ibic

idoi

des

sp. δ

18O

(‰

)

Fig. 5. Linear correlation between different indices of species diversity and δ18O values of Cibicidoides sp. at Hole 752A. The values show good positive correlation as can be seenfrom coefficients of correlation (r) and coefficients of determination (r2). However, δ18O values of Cibicidoides sp. and Information Function (H) show a weak inverse correlation.

98 R.K. Singh et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 361-362 (2012) 94–103

carbon content of sediments (e.g., Miller and Lohmann, 1982; Gooday,1988, 1993; Altenbach and Sarnthein, 1989; Schmiedl et al., 1997;De Stigter et al., 1998; Gooday et al., 2000, 2010; Diester-Haass et al.,2004, 2005; Brandt et al., 2007; Ingels et al., 2012). Other studiesemphasized on sensitivity of benthic foraminifera to oxygen levels ofthe bottom water and pore-water oxygenation (Corliss, 1985; SenGupta and Machain-Castillo, 1993; Gooday, 1994; Loubere, 1996;Jannink et al., 1998; Levin, 2003; Gooday et al., 2009, 2010; Levinet al., 2009). Benthic foraminifera occupy perched epibenthic todeep infaunal microhabitats and utilize diverse trophic mecha-nisms (Corliss, 1985; De Stigter et al., 1998; Gooday et al., 2010;Duros et al., 2011; Contreras-Rosales et al., 2012). Their goodfossilization potential and often considerable population makethem useful tool in paleoceanographic and paleoclimatic studies.

Little is knownabout environmental preferences ofBuliminamacilentawhich has been reported from the eastern Indian Ocean with rare andsporadic occurrences. This species has been found in association with anassemblage indicative of low organic carbon flux, well-ventilated envi-ronment in the eastern Indian Ocean (Gupta et al., 2004). B. macilentawas originally described from the Eocene rocks of California, USA andlater on from the Late Eocene–Oligocene of Barbados (Wood et al.,1985). Berggren and Aubert (1976) earlier noted this species withwidespread occurrences fromUpper Cretaceous throughOligocene levels.This species is more regularly presented at shallower sites (Tjalsma andLohmann, 1983). The first appearance of this species at Site 752 was

reported from the lowermost Eocene sample with time equivalence asobserved by Tjalsma and Lohmann (1983). At Hole 752A, this species isfound with highest abundances between 25 and 20.5 Ma (Fig. 6, Table 1).

Nuttallides umbonifera is an epifaunal species occurring in diverseenvironments, quite often in association with AABW (Streeter, 1973;Lohmann, 1978; Bremer and Lohmann, 1982; Mackensen et al.,1995). This species has been interpreted as an indicator of low foodsupply (Gooday, 1994; Loubere and Fariduddin, 1999), carbonatecorrosiveness and intensity of AABW circulation (Corliss, 1979b;Gupta, 1997; Smart et al., 2007). N. umbonifera has a stronger relationwith carbonate corrosivity than any other environmental factor(Singh, 2009). Singh and Gupta (2010) observed a relation betweenN. umbonifera and cold, corrosive, oligotrophic, oxygenated deepwater from the Pacific Ocean during 11.5 Ma at ODP Site 757. Thisspecies is dominant from 22.5 to 19.5 Ma and again during 15 to14 Ma at Hole 752A (Fig. 6, Table 1).

Cibicides wuellerstorfi has been found throughout the Neogeneinterval, showing a major peak during 20–19 Ma, and a significantincrease from 13.5 to 4.5 Ma and during the last 1 Ma (Fig. 6,Table 1). This species is considered as a raised epibenthic speciesthat prefers to live in high energy environments (Lutze and Thiel,1989; Linke and Lutze, 1993; Mackensen et al., 1995). C. wuellerstorfireflects scarcity of food particles in the sediment of Arctic Basin andNorwegian–Greenland Sea (Linke and Lutze, 1993). As a suspensionfeeder and elevated epibiont, C. wuellerstorfi can survive on low

99R.K. Singh et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 361-362 (2012) 94–103

organic carbon levels and can withstand strong bottom currents(Linke and Lutze, 1993). This species has also been considered as anindicator of high seasonal food supply under oligotrophic conditions

Ag

LateMiocene

EarlyPliocene

Pleist-ocene

LatePliocene

G. s

ubgl

obos

aC

. lae

viga

taC

. lob

atul

usG

. lob

atul

usE

. car

inat

aB

. pus

illa

C.w

uelle

rsto

rfi

N. u

mbo

nife

raB

.mac

ilent

aI.

Fun

ctio

n (H

) 3.6

3.2

2.8

2.4

2.0

20

10

0

20

10

0

20

10

0

20

10

0

20

10

0

30

20

10

0

30

20

10

0

30

20

10

0

30

40

0

5

10

15

20

0 5 10

Fig. 6. Dominant benthic foraminiferal species (present >20% in at least two sampl

(Loubere and Fariduddin, 1999). In the Indian Ocean, C. wuellerstorfiand N. umbonifera have been found associated with AABW (Corliss,1979b; Bremer and Lohmann, 1982), whereas in the Atlantic and

e (Ma)

LateOligocene

EarlyMiocene

MiddleMiocene

15 20 25

e) along with the Information Function (H) are plotted against numerical ages.

100 R.K. Singh et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 361-362 (2012) 94–103

Southern Oceans, C. wuellerstorfi has been associated with young,well oxygenated water masses like North Atlantic Deep Water(Weston and Murray, 1984; Mackensen et al., 1995; Schmiedl andMackensen, 1997; Gooday, 2003). Thus, C. wuellerstorfi can toleratelow organic carbon levels (Linke and Lutze, 1993). In the IndianOcean, Gupta (1997) related this species with the oxygenated, strongbottom currents and strongly pulsed food supply.

Bolivina pusilla has a well-established infaunal microhabitat andhave preference to low oxygen and high food levels (Thomas andGooday, 1996; Gupta and Satapathy, 2000). This species has signifi-cant dominance from 13.5 to 4.5 Ma at Hole 752A (Fig. 6, Table 1),coinciding with the Indo-Pacific biogenic bloom (Dickens andOwen, 1999; Gupta and Thomas, 1999; Hermoyian and Owen,2001). B. pusilla together with Ehrenbergina carinata suggest highflux of organic matter in the equatorial Indian Ocean (Sarkar andGupta, 2009). Bolivinids, in general, have a preference for low oxygenand high food environments (Gupta and Satapathy, 2000; Gooday,2003). They flourish in relatively warm water of the OMZ (Nigamet al., 2007; Sarkar and Gupta, 2009). Species of Bolivina are rareand observed at a wide range of depths throughout the IndianOcean (Gupta, 1994). High abundances of Bolivinids in the Bay ofBiscay (Poag and Low, 1985) and the North Central Indian Ocean(Boersma andMikkelsen, 1990) during the Neogene have been attrib-uted to increased primary productivity, increased organic flux anddevelopment of an OMZ.

Ehrenbergina carinata has a shallow infaunal micro habitat andthrives in conditions with high temperature, low oxygen and high nu-trient levels (Nomura, 1991; Gupta and Satapathy, 2000). Gupta et al.(2006, 2008) suggested that E. carinata is indicative of intermediateto high and sustained flux of organic matter and low oxygen condi-tion in the central Indian Ocean. This species has high abundancesfrom 7.5 to 4.5 Ma at Hole 752A (Fig. 6, Table 1).

Gavelinopsis lobatulus is an epifaunal species that feeds on freshphytodetritus (Gooday, 1993) and is suggestive of highly variableand overall oligotrophic environmental conditions (Gupta and Das,2007). This species has been found associated with an assemblagereflecting intermediate oxygen levels, a pulsed food supply, andoligotrophic conditions in the northwestern Indian Ocean (Guptaand Thomas, 1999). Gupta et al. (2008) found this species to beassociated with assemblage characteristics of low to intermediateorganic carbon flux and high seasonality. This species shows peakabundances during ~9.5–9 Ma, 7–6 Ma and 4.5–1.6 Ma at Hole752A (Fig. 6, Table 1).

Cibicides lobatulus is an epibenthic species living on elevated objectsin high energy conditions (Schönfeld, 2002) with intermediate to highfood supply (Gupta and Das, 2007). In the Arctic, C. lobatulus has beenreported in high-energy environments with strong bottom-watercurrents and coarse sediments in recent assemblages (Haynes, 1973;Hald and Korsun, 1997; Murray, 2006). At Hole 752A, this species isdominant from 2 to 1 Ma (Fig. 6, Table 1).

Cassidulina laevigata is abundant in areas with high seasonal fluxes(Schmiedl and Mackensen, 1997; Loubere and Fariduddin, 1999) andglacial intervals of the northeastern Atlantic (Schnitker, 1984). Thisspecies is a typical of shelf assemblage (Ubaldo and Otero, 1978;Murray, 1991) and has been correlated to relatively cold waters(Fontanier et al., 2003). C. laevigata is found living in the upper0.5 cm of sediment in an experimental setup (Alve and Bernhard,1995) and in the sediment of Tagus Prodelta (Jónsdóttir et al.,2006). This species shows peak abundance after 1 Ma at Hole 752A(Fig. 6, Table 1).

Globocassidulina subglobosa is a cosmopolitan infaunal speciesoccurring over a wide range of bathymetry and in association with anumber of different water masses, feeding on phytodetritus (Gooday,1994). This species is associated with the NADW in the AtlanticOcean and categorized as a low-productivity taxon (Faridduddin andLoubere, 1997). The high abundances of Globocassidulina subglobosa

are reported within the depth range of Circumpolar Deep Water andin oligotrophic areas at higher elevations of ridges and submarinehills, in the South Atlantic (Schnitker, 1980; Mackensen et al., 1995).In the South China Sea, G. subglobosa was observed tolerating warmwaters (Miao and Thunell, 1993), and in the southeastern IndianOcean, G. subglobosa has been found associated with the AABW(Corliss, 1979b). This species indicates pulsed food supply to theseafloor in the northeastern Indian Ocean (Gupta and Thomas, 2003).Singh and Gupta (2004) suggested that this species reflects welloxygenated deep waters having strongly pulsed food supply and goodcarbonate preservation in commonly oligotrophic environments inthe southeastern Indian Ocean. This species is found throughoutthe Neogene at Hole 752A with a continuous decrease until ~2 Ma;thereafter it shows a major increase (Fig. 6, Table 1).

5. Discussion

Deep-sea benthic species diversity combined with faunal abundancesat Hole 752A shows significant variations coincidental with changes inglobal ice volume, ocean productivity as well as ocean circulation. Thespecies diversity values show a decreasing trend from Late Oligocene toEarly Miocene. The stable carbon isotopic values also indicate graduallyincreasing productivity in the Early Miocene (low δ13C values, Fig. 4).The successive peaks of B. macilenta and N. umbonifera indicate a changein environment from low organic flux, well ventilated to dominance ofcarbonate corrosive AABW up to 20.5 Ma. The decrease in the diversityparameters during 25–20.5 Ma suggests that conditions were unstableduring this time. From 20.5 to 13.5 Ma the deep-sea environmentgradually changed and conditions becamemore stable (increased speciesdiversity values) coinciding with a decrease in productivity (increasingδ13C values, Fig. 4). This was an interval of climatic optimum and/ordecreased ice volume (low δ18O values, Fig. 4) in Antarctica (Rea et al.,1991; Zachos et al., 2001; Barker and Thomas, 2004; Singh and Gupta,2005). The sharp increase in the δ18O values of Cibicidoides sp. at19.5 Ma indicates cooling of the deep sea causing drop in sea level. Thisevent corresponds to the hiatus NH1 of Keller and Barron (1983) and ismarked by high population of C. wuellerstorfi and decrease in the numberof species as well as species diversity parameters. From 18.5 to 13.5 Madeep sea conditions were well oxygenated with strongly pulsed foodsupply (high G. subglobosa). The species diversity values were increasingand infaunal species dominated over the epifaunal species during thisinterval. This was an interval of Miocene Climatic Optimum havinglow mean δ18O and high mean δ13C values, and burial of organicallypreferred 12C rich carbon (Vincent et al., 1985 and Zachos et al., 2001).

The intensification of OMZ during 13.5–4.5 Ma, marked by thedominance of classic low oxygen foraminiferal taxa B. pusilla andE. carinata, indicate high nutrient levels and low oxygen conditionsat Hole 752A leading to a decrease in the species diversity parametersduring this time interval (Fig. 6). Kender et al. (2009) also observeddecrease in species diversity during intervals of high abundancesof low oxygen species in the offshore West Africa during theMiddle Miocene. This interval corresponds to the so-called “biogenicbloom” and an intense OMZ as observed throughout the Indo-Pacificregion (Pisias et al., 1995; Filippelli, 1997; Dickens and Owen, 1999;Gupta and Thomas, 1999; Hermoyian and Owen, 2001). The causeof this biogenic bloom is not yet known because this coincides withthe intensification of the Indian monsoon and major increase ofAntarctic ice volume. Hole 752A has been outside the influence ofthe Indian Monsoon system and its proximity to the Antarctic regionallows us to argue that the biogenic bloom was an outcome of globalcooling when wind intensities were stronger that led to widespreadsurface ocean productivity.

During the Late Miocene, OMZ intensified and expanded to largeparts of the Indian Ocean at intermediate depths coinciding withincreased strength of the Indian monsoon (Dickens and Owen, 1999;Gupta and Thomas, 1999) as well as trade winds (Gupta et al., 2004).

101R.K. Singh et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 361-362 (2012) 94–103

Productivity increased throughout the Indo-Pacific region and theIndian monsoon intensified during this time (Filippelli, 1997; Dickensand Owen, 1999; Gupta and Thomas, 1999). The increase in productiv-itywasmarked by low δ13C values ofCibicidoides sp. (Fig. 4). The speciesdiversity continued to decrease and low oxygen infaunal foraminiferaB. pusilla and E. carinata continued to dominate the deep sea environ-ment except for some small durations when low to intermediateorganic carbon flux and high seasonality species (e.g., G. lobatulus)were common. The seasonal changes and organic carbon flux signifi-cantly impact the biodiversity of the deep sea (Corliss et al., 2009)and species diversity increased when G. lobatulus dominated the deepsea environment.

The response of the Late Miocene productivity event has beenobserved across the Indian, Atlantic, and Pacific Oceans (Kroon et al.,1991; Dickens and Owen, 1999; Hermoyian and Owen, 2001; Guptaet al., 2004) aswell as the South China Sea (Chen et al., 2003). Sedimen-tation andmass accumulation rates of biogenic CaCO3 increased rapidlythroughout the Indian Ocean (Peterson et al., 1992; Rea, 1992), in theArabian Sea, and at southeastern Indian Ocean sites. The widespreadgeological, geochemical, and biological expressions of this event indi-cate that the region of increased biogenic productivity reached as farsouth as latitude 30°S in the Indian and Atlantic Oceans, throughoutthe tropical Pacific (Dickens and Owen, 1999; Hermoyian and Owen,2001), and into the South China Sea (Chen et al., 2003). Gupta et al.(2004) linked the Late Miocene productivity increase to strengthenedwind regimes and partly to the intense Indian monsoon. These authorssuggested that the increased glaciations onAntarcticamay have strength-ened wind regimes, causing widespread open-ocean as well as coastalupwelling over a large part of the Atlantic, Indian and Pacific oceansduring the Late Miocene. This increased upwelling could have triggeredthe widespread increase in biological productivity. The other changeslike formation of the North Atlantic Deep Water at that time (Roth et al.,2000) and changes in the ocean–atmosphere system may also haveplayed a role. The local factors like northward shift of subtropical conver-gence zone during the glacial interval may have also contributed toincreased productivity at Hole 752A (Gupta and Das, 2007).

The increase in species diversity from 4.5 to 2.5 Ma was associatedwith the decrease in productivity (high δ13C, Fig. 4), coincidingwith the Early Pliocene warmth (Crowley, 1996; Raymo et al., 1996;Kim and Crowley, 2000; Draut et al., 2003). The little decrease inδ18O is observed globally (Zachos et al., 2001). However, this isnot prominent at Hole 752A due to low resolution of the samplesanalyzed (Fig. 4). In this interval G. lobatulus, characteristic of low tointermediate organic carbon flux and high seasonality, was highwhereas low oxygen forminifera B. pusilla and E. carinata were low.

The increasing Northern Hemisphere glaciations and expansion ofwest Antarctica Ice sheet at ~3 Ma (Zachos et al., 2001; Mudelsee andRaymo, 2005) strengthened the wind regimes causing upwelling andincreased surface productivity (increased δ18O, decrease δ13C, Fig. 4;Gupta et al., 2004; Singh and Gupta, 2005). The increased productivityduring the glacial interval decreased the species diversity parameters.This study agrees with Herguera (1992, 2000) and Herguera andBerger (1991)who found increased productivity during glacial intervalsin the western and eastern equatorial Pacific Ocean. The dominanceof both epifaunal and infaunal species (G. lobatulus, C. lobatulus,C. laevigata, G. subglobosa, and C. wuellerstorfi) suggests high-energyenvironments with relatively cold strong bottom-water currents,strongly pulsed food supply and high seasonality during this period.The high seasonality in food supply perhaps further amplified thedecreasing trend of species diversity during this period as observedby Corliss et al. (2009).

6. Conclusions

Diversity parameters of Neogene benthic foraminiferal species suchas H, E, S and Sander's value combined with population abundance of

dominant benthic foraminifera at Hole 752A are correlated with theincreased glaciations on Antarctica and related oceanwide productivity.Species diversity decreased during the glacial and increased duringinterglacial intervals in the southeastern Indian Ocean. The decreasein the species diversity parameters of the southeastern Indian Oceanis also related with the occurrences of low oxygen species and highseasonality as observed in the offshore ofWest Africa andNorthAtlantic(Corliss et al., 2009; Kender et al., 2009). The increase in the speciesdiversity was observed during the Middle Miocene Climatic Optimumand Early Pliocene climatic warmth. The low values of species diversityamplified by high seasonality and relatively cold, strong bottom-watercurrents after ~3 Ma correspond to the substantial build up of theNorthern Hemisphere glaciation and West Antarctic Ice Sheets.

Acknowledgments

Ocean Drilling Program is thankfully acknowledged for providingcore samples to AKG for the present study (ODP Request 13626). Weare grateful to the Editor Thierry Corrège for editorial comments, andreviewer Matias Reolid and an anonymous reviewer for thoughtfulreviews. The Council of Scientific and Industrial Research (CSIR), NewDelhi provided the financial support (No. 24(0256)/02/EMR-II) and anindependent Junior Research Fellowship to RKS.

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