Deep-sea ostracode turnovers through the Paleocene–Eocene thermal maximum in DSDP Site 401, Bay of Biscay, North Atlantic

Marine Micropaleontology 86–87 (2012) 32–44

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Deep-sea ostracode turnovers through the Paleocene–Eocene thermal maximum in DSDP Site 401, Bay of Biscay, North Atlantic Tatsuhiko Yamaguchi a, b,⁎, Richard D. Norris b a b

Postdoctoral Fellow for Research Abroad, Japan Society for the Promotion of Science, Japan Scripps Institution of Oceanography, University of California, San Diego, United States

a r t i c l e

i n f o

Article history: Received 24 December 2010 Received in revised form 4 January 2012 Accepted 12 February 2012 Keywords: Deep sea DSDP Site 401 Extinction Ostracoda Paleocene–Eocene thermal maximum

a b s t r a c t Previous low resolution studies suggest that ostracodes, in contrast with deep sea foraminifera, largely survived the massive environmental changes of the Paleocene–Eocene thermal maximum (PETM). In a new high-resolution study from the continental slope (~1800 m paleodepth) NE Atlantic, we also find extensive survivorship of ostracode faunas, but this is accompanied by a temporary drop in species diversity and ecological diversity during the PETM. There are 12 common ostracode species before the PETM that are reduced to only two species at the same time as the benthic foraminiferal extinction event. All but three species reappear in the later parts of the PETM and statistical analysis suggests that most of the apparent “Lazarus” species might be found with sufficient sampling of PETM faunas. We find no evidence for an excursion fauna of ostracodes as has been detected in calcareous nannofossils, planktic foraminifera, and benthic foraminifera. However, the ostracode assemblages changed from a relatively diverse ecological assemblage before and after the PETM to one dominated by infaunal species typical of low oxygen conditions during the PETM. The absence of major extinction and the temporary nature of species disappearances are comparable to turnovers in shallow marine ostracodes and stands in sharp contrast to the ~ 50% species-level extinction in benthic foraminifers. © 2012 Elsevier B.V. All rights reserved.

1. Introduction The Paleocene–Eocene thermal maximum (PETM) is an extreme climate event ~ 56 Ma associated with abrupt ocean warming (e.g., Zachos et al., 2003, 2005; Tripati and Elderfield, 2005; Hilgen et al., 2010), a marked shoaling of the carbonate compensation depth, and a shift in ocean circulation (e.g., Bains et al., 1999, 2000; Zachos et al., 2003; Nunes and Norris, 2006). These environmental changes are known to have precipitated major changes in both surface ocean taxa and deep sea biota, including extinctions, geographic range extensions, and changes in assemblage composition. For example, deep sea benthic foraminifers experienced an extinction of 35–50% of cosmopolitan taxa (Thomas and Shackleton, 1996) while most planktonic groups saw temporary geographic shifts in population but little extinction (e.g., dinoflagellate cysts: Crouch et al., 2003; planktonic foraminifers: Kelly, 2002; calcareous nannofossils: Gibbs et al., 2006; radiolaria: Hollis, 2006). Previous studies of ostracode turnover during the PETM (Steineck and Thomas, 1996; Speijer and Morsi, 2002; Webb et al., 2009) reveal a contrasting pattern of moderate levels of extinction and origination in shallow marine Tethyan

⁎ Corresponding author at: Scripps Institution of Oceanography, University of California, San Diego. Tel.: + 1 858 822 2783; fax: + 1 858 534 3310. E-mail address: [email protected] (T. Yamaguchi). 0377-8398/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.marmicro.2012.02.003

sections, as well as temporary disappearance and replacement by a novel assemblage in the deep Southern Ocean. In other cases, ostracodes show no replacement of species across the PETM in a deep sea Tethyan section (Caravaca, Spain) and the deep western North Atlantic (Blake Nose, US East Coast) (Guernet and Molina, 1997; Guernet and Belliner, 2000). Abrupt shifts in the ecological structure of oceanic species are typically attributed to changes in food supplies, hypoxia, and ocean acidification (e.g., Thomas, 1998, 2003; Takeda and Kaiho, 2007). In this paper we study ostracode assemblages because – as multicellular species – they may have different physiological limits to growth and persistence through the PETM than unicellular foraminifera, nannoplankton, and radiolarians. Ostracode assemblages may be more sensitive to environmental changes than benthic foraminifers, because although ostracodes share habitats with the epifaunal and shallow-infaunal benthic foraminifers, they also have lower productivity and dispersal capability as well as higher oxygen demands than neighboring protists. For instance, ostracodes directly develop and settle in places where they are born (e.g., Cohen and Morin, 1990), whereas benthic foraminifers may drift in sea water as propagules before settling (e.g., Alve and Goldstein, 2003). In addition, ostracodes live only in oxic surface sediments, which suggests that they may be particularly sensitive to reductions in sea floor oxygen content, as proposed for the PETM in many deep sea locations (Kaiho, 1988; Thomas, 1998). Finally, ostracodes may also show

T. Yamaguchi, R.D. Norris / Marine Micropaleontology 86–87 (2012) 32–44

greater physiologic homeostasis than protists which may help ostracodes resist changes in ocean chemistry. Here we analyzed the late Paleocene–early Eocene ostracode species from Deep Sea Drilling Project (DSDP) Site 401 (47°25.650′N, 8°46.618′ W, 2495 m water depth; Fig. 1) in the Bay of Biscay, North Atlantic. Planktonic foraminifer and calcareous nannofossil biostratigraphy

60°W

30°W

0°

33

has been described for this site (Pardo et al., 1997; Tremolada and Bralower, 2004), as well as the extinction of benthic foraminifers that marks the base of the PETM (Pak and Miller, 1992; Thomas, 1998). Our samples were previously used to construct a benthic foraminiferal (Nuttallides truempyi) stable isotope record (Nunes and Norris, 2006) and we have used this record to delineate ostracode faunal changes in response to environmental changes through the PETM.

30°E

90°N

2. Paleocene–Eocene stratigraphy and stable isotope records of DSDP Site 401 We examined a ~500 kyr interval of DSDP Site 401, that includes the 150–220 kyr long PETM (Röhl et al., 2007; Murphy et al., 2010). This interval consists of nannofossil chalk (Montadert and Roberts, 1979) that shifts from yellowish gray to light reddish brown near 202.70 mbsf. The interval is assigned to the planktonic foraminiferal Zone P5 (Pardo et al., 1997) of Blow (1979)'s zonation scheme. Biostratigraphic markers for calcareous nannofossil Zone NP10 of Martini (1971)'s scheme have been identified at and above 202.14 mbsf (Müller, 1979). Pak and Miller (1992) identified the benthic foraminifer extinction event (BEE) between 202.60 and 202.40 mbsf (Fig. 2). Nunes and Norris (2006) located the PETM carbon isotope excursion (CIE) interval between 202.72 and 200.83 mbsf (Fig. 2) with the Paleocene/Eocene boundary (defined by the base of the PETM, 55.8 Ma; Luterbacher et al., 2004) occurring at 202.72 mbsf. In the CIE zone, the minimum value of δ 13C is at 202.02 mbsf (Nunes and Norris, 2006) and is correlated with the tie point C of Röhl et al. (2007) as well as the re-appearance of N. truempyi after a short interval of its absence from the record. For the purposes of this paper, we place the base of the PETM at 202.50 mbsf corresponding to both the approximate location of the BEE and the most rapid decrease in δ 13C. DSDP Site 401 was recovered from a present sea floor water depth of 2495 m. Pak and Miller (1992) estimated the Paleocene–Eocene water depth at Site 401 to be 1800 m, using the backtracking method. Ducasse and Peypouquet (1979) studied Cenozoic ostracodes from Site 401 and inferred a paleowater depth of 2000 m.

60°N

DSDP 401 Caravaca Tethys Sea

30°N

Gebel Duwi Atlantic Ocean Gebel Aweina 0°

30°S

3. Material and methods

ODP 690 ODP 689

60°S

Southern Ocean

90°S 30°W

60°N

0°

DSDP 403 DSDP 405 DSDP 404 DSDP 406 DSDP 549 DSDP 550 DSDP 400

Hampshire Basin Paris Basin

Aquitaine Basin DSDP 402 DSDP 401

Basque Basin Caravaca 30°N Fig. 1. Paleogeography in 56 Ma (Ocean Drilling Stratigraphic Network: http://www. odsn.de/odsn/services/paleomap/paleomap.html) and locations of study (star), discussion (circle) sites.

Sediment samples with a volume of ~10 cm 3 were taken at 1 to 20-cm intervals in Cores 14–4 to 14–1 through the PETM interval and were analyzed by Nunes and Norris (2006). They were allowed to dry overnight at 50 °C before being washed with deionized water through a 38-μm sieve. Ostracodes were picked up from the >115-μm fraction, resulting in samples with an average of 70% juvenile valves (Fig. 2). Our methods differ somewhat from previous studies that typically use a sieve with a 200-μm opening (Danielpol et al., 2002). To identify species, we used a binocular microscope and a scanning electron microscope (SEM) Philips Quanta 600 at the Analytical Facility, Scripps Institution of Oceanography. We also sketched the inner structure of ostracode valves with a digital camera attached to a binocular microscope. We counted as individuals the sum of the number of both adult and juvenile valves and carapaces for a given species, assuming that the valves in the samples are not paired. Species diversity was estimated for each sample using the Shannon Index, H and by calculating a rarefaction curve at a sample size of 15 individuals, E(S15). For the calculation of the species diversity indexes and statistical tests, we used the free software GNU R (http://www.r-project.org/) and its software package, vegan (Oksanen et al., 2010). Ostracode habitats (epifauna/infauna) were identified from the modern ecology of related genera (Elofson, 1941; Maddocks, 1969a,b; Majoran and Agrenius, 1995). To analyze data with statistically valid sample sizes, we binned samples in each 30 cm interval from 202.75 mbsf. We did not bin

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T. Yamaguchi, R.D. Norris / Marine Micropaleontology 86–87 (2012) 32–44

Geological age (Ma)

Lithology mbsf

LAD of Morozovella velascoensis

198.5

Early Eocene

199.0

199.5

200.0

Tie point (ky) End of CIE (~170)

200.5

55.63 201.0

201.5

55.80

202.0

C (42.38)

202.5

BEE Onset of CIE (0)

Late Paleocene

203.0

203.5

204.0

204.5 −1.5

1.0

δ18O vs PDB (‰)

−1.0

0

1.5

δ13C vs PDB (‰)

50

Individuals Raw sample

0

350 0

Individuals Binned sample

1.0

Juvenile/total valves ratio

Fig. 2. Lithology, oxygen (δ18O) and carbon (δ13C) stable isotope records of Nuttallides truempyi (Nunes and Norris, 2006) and abundance of ostracode individuals. Datum events are shown for the benthic foraminiferal extinct event (BEE; Pak and Miller, 1992) and planktonic foraminifer biostratigraphy (Pardo et al., 1997). Also shown (in parentheses) are the elapsed times after the onset of the CIE (Röhl et al., 2007). Gray shading denotes the CIE zone (Nunes and Norris, 2006). The gray dashed and dotted lines indicate the horizons of the minimum of δ13C and BEE, respectively.

the interval of 198.25–198.55 mbsf, because it contains only one sample (Appendix). Ostracode assemblages were identified by cluster analysis using Horn's overlapped index (Horn, 1966) as a measure of similarity and the unweighted pair-group average as a linkage method. Our analysis used the free software PAST (Hammer et al., 2001). We calculated the Shannon index and rarefaction at a cutoff of 30 individuals, E(S30). We estimated the statistical range limits of the highest occurrences of extinct taxa using the methods of Roberts and Solow (2003). To identify “Lazarus taxa”, we calculated the upper limits of the highest occurrences of species near the onset of the PETM and the lower limits of the first occurrences above the highest ones. True “Lazarus taxa” were assumed to have non-overlapping highest and lowest ranges in the interval represented by their presumed migration to some other habitat. The method is non-parametric and appropriate for our data, because a Shapiro-Wilk test indicated that

stratigraphic distribution is not normally distributed in Bythoceratina sp., Cardobairdia sp., and Poseidonamicus sp. For example, the test for Poseidonamicus sp. rejected the normality of its distribution at 95% confidence (W = 0.9274, p = 3.727 × 10 − 2). The calculation of range limits is effective for species found in at least five horizons (Solow, 2005). We calculated the potential range limits for observed first and last occurrences, and the number of fossiliferous horizons using a 95% confidence limit. 4. Taxonomic notes We identified 20 species in 90 samples (Figs. 3 and 4; Appendix). Two of the species were already described, while the other species stand in open nomenclature. We consider 18 species to be new, referring to studies of Paleocene deep-sea ostracodes (Benson, 1977; Ducasse and Peypouquet, 1979; Coles and Whatley, 1989; Guernet

Fig. 3. SEM images of ostracodes from DSDP Site 401. All the specimens are adult forms. Scale bars = 100 μm. The arrow points anterior direction. 1. Abyssobairdia sp., right external view of carapace, 14–2, 8–10 cm. 2. Argilloecia sp., 14–1, 148–150 cm, external view of left valve. 3. Bythoceratina sp., 14–4, 24–25 cm, external view of left valve. 4. Cardobairdia sp., 14–4, 90–91 cm, external view of left valve. 5. Cytherella sp.1, 14–3, 112–114 cm, external view of left valve. 6–7. Cytherella sp.2, 14–1, 148–150 cm, left valve, 6. external view. 7. dorsal view. 8. Cytheropteron sp.1, 14–4, 85–86 cm, external view of left valve. 9. Cytheropteron sp.2, 14–4, 37–38 cm, external view of left valve. 10. Eucythere sp., 14–4, 28–29 cm, external view of left valve, 11. Krithe crassicaudata van den Bold, 1946, 14–1, 14–47 cm, external view of left valve. 12. Krithe sp.1, 14–2, 129–131 cm, external view of left valve. 13. Krithe sp.2, 14–2, 129–131 cm, external view of left valve. 14–15. Neonesidea cymbula (Deltel, 1964), 14–1, 148–150 cm, left valve. 14. external view. 15. internal view. 16. Paleoabyssocythere sp., 14–4, 26–27 cm, external view of left valve. 17. Phacorhabdotus sp., 14–1, 128–130 cm, external view of left valve. 18–19. Platyleberis sp., 14–4, 80–81 cm, right valve. 18. external view, 19. internal view. 20. Poseidonamicus sp., 14–3, 143–145 cm, external view of left valve. 21. Trachyleberidea sp., 14–2, 8–10 cm, external view of left valve.

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AD1 AD2 AD3 AD4

Stratigraphic range: Upper Paleocene–Lower Eocene. Bythoceratina sp. Fig. 3.3 Remarks: this species is similar to Monoceratina umbonatoides Kaye, 1964 in lateral outline and the blunt oblique muri on the antero-ventral area. M. umbonatatoides is found in Coniacian–Campanian deposits in England (Kaye, 1964; Neale, 1978). Bythoceratina is distinguished from Monoceratina by the hingement (Benson et al., 1961). However this species is distinguished from M. umbonatoides by its larger carapace and lack of reticulation on the anterior area. Stratigraphic range: Upper Paleocene.

1 AD4 ARPC1 ARPC2

2 AD1 AD4

3 Fig. 4. Sketches of the inner part of ostracode valves from DSDP Site 401. All the specimens are adult forms. Scale bars = 100 μm. 1. Krithe crassicaudata van den Bold, 1946, 14–1, 14–47 cm, left valve, the same specimen as Fig. 3.11. 2. Krithe sp.1, 14–3, 52–54 cm, right valve. 3. Krithe sp.2, 14–2, 100–102 cm, left valve. The codes AD1–4 and ARPC were designed by Coles et al. (1994).

and Galburn, 1992; Boomer and Whatley, 1995; Rodriguez-Lazaro and Garcia-Zaraga, 1996; Guernet and Molina, 1997; Guernet and Belliner, 2000; Majoran and Dingle, 2002; Guernet and Danelian, 2006; Aumond et al., 2009). However, to maintain the focus of this paper on faunal changes and comparisons between ostracode and foraminifera turnover patterns we do not describe the new species here, but merely provide a brief comment on the major species. For taxonomy, we use the terminology of Coles et al. (1994) and Horne et al. (2002). The terminology contains codes of five anterodorsal radial pore canals, AD1–5, and anterior radial pore canals, ARPC in Krithe. Argilloecia sp. Fig. 3.2 Remarks: This species is similar to Argilloecia sp.A of Boomer (1999) in lateral outline. Argilloecia sp.A is found in the latest Cretaceous– Miocene sediments of DSDP Site 463, central Pacific. However, this species is distinguished from Argilloecia sp.A by having a carapace with a longer upper part of the anterior margin and a shorter upper part of the posterior margin.

Cardobairdia sp. Fig. 3.4 Remarks: The species is similar to Cardobairdia sp.1 of Guernet and Belliner (1997) in lateral outline and size, but has a gentler arch than Cardobairdia sp.1. in dorsal outline. It is different from Cardobairdia sp.2 of the middle Eocene sediments at DSDP Site 401 (Ducasse and Peypouquet, 1979) in having a larger and elongated carapace. The left valve of Cardobairdia sp. in Fig. 3.4 is 0.59 mm long, whereas that of Cardobairdia sp.2 is 0.34 mm long. Stratigraphic range: Upper Paleocene. Cytherella sp.1 Fig. 3.5 Remarks: Cytherella sp.2 differs from Cytherella sp.1 by having straight dorsal and ventral margins and a slightly depressed dorsal area. Stratigraphic range: Upper Paleocene–Lower Eocene. Cytherella sp. 2 Fig. 3.6 and 3.7 Cytherella consueta Deltel. Ducasse and Peypouquet, 1979, pl. 1, Fig. 1. Cytherella transversa Speyer. Ducasse and Peypouquet, 1979, pl. 1, Fig. 2. Remarks: having a smooth surface and straight dorsal margin parallel to the ventral margin, the C. consueta and C. transversa of Ducasse and Peypouquet (1979) belong to Cytherella sp.2. C. consueta Deltel, 1964 is different from Cytherella sp.2 in the position of the maximum width of the carapace. The maximum width of C. consueta is across the middle of its carapace, while that of Cytherella sp.2 is through the posterior area (Fig. 3.7). C. transversa Speyer, 1863 differs from Cytherella sp.2 by having the surface covered with punctation and a sinuous ventral margin. Stratigraphic range: Upper Paleocene–Lower Eocene. Krithe crassicaudata van den Bold Figs. 3.11 and 4.1 Krithe crassicaudata van den Bold, 1946, p. 78, pl. 7, Fig. 2. Krithe crassicaudata van den Bold. Coles et al., 1994, p. 91–94, pl. 3, Fig. 6–10, text-Fig. 4. Remarks: Having a subovate lateral outline and Y-shaped anterior vestibulum with the elongated AD4, we identified these specimens as Krithe crassicaudata. Stratigraphic range: Upper Paleocene–Lower Oligocene (Coles et al., 1994; This study). Krithe sp.1 Figs. 3.12 and 4.2 Remarks: This species resembles Krithe morkhoveni morkhoveni van den Bold, 1960 and Krithe praemorkhoveni Coles et al., 1994 in

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lateral outline and the vestibulum shape with four ADs (AD1–4). These species are found in Paleocene–Pliocene sediments from deep-sea cores. However, this species differs from the described species in having more pores in the posterodorsal area and the vestibulum with the unbranched AD4 and ARPC2 that diverges from ARPC1. K.morkhoveni morkhoveni has the vestbulim with the AD, that bifurcated into AD4 and AD5. K. praemorkhoveni has a vestibulum with ARPC2, that diverges not from ARPC1, but from the vestibulum. Stratigraphic range: Upper Paleocene–Lower Eocene. Krithe sp.2 Figs. 3.13 and 4.3 Remarks: this species resembles Krithe sp.4 of Coles et al. (1994) in having two ADs and the mushroom-shaped anterior vestibulum. Krithe sp. 4 is found in the lower Eocene of DSDP Site 550, North Atlantic. However this species is different from Krithe sp.4 by its subrectangle lateral outline and a broader anterior vestibulum. Stratigraphic range: Upper Paleocene–Lower Eocene. Neonesidea cymbula (Deltel) Figs. 3.14 and 3.15 Bairdia cymbula Deltel, 1964, p. 139–140, pl.2, Figs. 21, 22. Bairdia cymbula Deltel. Ducasse and Peypouquet, 1979, pl. 1, Figs. 8, 9. Bairdia cf. cymbula Deltel. Guernet and Molina, 1997, p.34, Figs. 3.7, 3.10–3.12. Remarks: this species has an adont-type hinge and a distinct tapering in the posterior margin (Fig. 3.14 and 3.15). These features indicate that the species is best placed in Neonesidea Maddocks, 1969a. N. cymbula is similar to Bairdoppilata cassida (van den Bold, 1946) in lateral outline. B. cf. cassida was reported from the Paleocene sediments of DSDP Sites 549 and 550 (Whatley and Coles, 1991). N. cymbula is different from B. cassida in having a smaller carapace with a flattened anterior area. N. cymbula is 1.10–1.27 mm long in specimens from DSDP Site 401 (number of specimen: n = 27) and 1.30 mm long in the holotype (Deltel, 1964). On the other hand, B. cassida is 1.50 mm long in the holotype (van den Bold, 1946). Stratigraphic range: Lower Paleocene–Upper Eocene (Ducasse and Peypouquet, 1979; Ducasse et al., 1985). Platyleberis sp. Figs. 3.18 and 3.19 Platyleberis chamela (van den Bold). Rodriguez-Lazaro and GarciaZaraga, 1996, pl. 1, Fig. 8. Remarks: the species has a triangular lateral outline and flattened ventral surface, suggesting it belongs to Platyleberis Bonaduce and Danielopol, 1988 (Figs. 3.18 and 3.19). Rodriguez-Lazaro and GarciaZaraga (1996) reported the species from the Paleocene–Eocene deposits in the Basque Basin, Spain. This species is distinguished from Platyleberis chamela (van den Bold, 1960) by having a carapace with a wider antero-dorsal angle and a sharper curve in the posterior margin. Xestoleberis sp. of Guernet and Molina (1997) is similar to this species in lateral outline, but differs from it by having a larger carapace (0.50 mm long) and more tapered apex in the posterior margin. This species is 0.40 mm long (Figs. 3.18 and 3.19). Stratigraphic range: Upper Paleocene–Middle Eocene (RodriguezLazaro and Garcia-Zaraga, 1996). Poseidonamicus sp. Fig. 3.20 Remarks: this species is similar to Poseidonamicus dinglei Boomer, 1999 and Poseidonamicus rudis Whatley et al., 1986 in lateral outline, reticulation with blunt muri, and small round fossae on the anterior area. P. dinglei and P.rudis were originally described from

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Maastrichtian sediments of DSDP Site 463, central Pacific and Miocene sediments of DSDP Site 207, southwestern Pacific, respectively. However this species is distinguished from the described species by having finer reticulation with blunter muri on the central area, smaller fossae inside the anterior rim, and a blunter ventrolateral carina. Stratigraphic range: Upper Paleocene. Trachyleberidea sp. Fig. 3.21 Remarks: this species is similar to Trachyleberidea pisinensis (Kollmann, 1962) and Trachyleberidea marginata Guernet and Molina, 1997 in lateral outline and distribution of reticulation on the valves. T. pisinensis and T. marginata were found in Paleocene–Eocene sediments of DSDP Sites 549 and 550 (Whatley and Coles, 1991) and Caravaca in Spain (Guernet and Molina, 1997), respectively. T. pisinensis is distinguished from this species by having a smaller carapace with reticulation with fewer fossae. T. pisinensis is 0.58 mm long in the holotype (Zorn, 2010), while this species is 0.71–0.81 mm long (n= 17). T. marginata differs from this species by having a larger carapace with finer reticulation and a distinct subcentral tubercle. T. marginata is 0.83–0.86 mm long (n= 6: Guernet and Molina, 1997). Stratigraphic range: Upper Paleocene–Lower Eocene. 5. Results: ostracode assemblages Krithe crassicaudata dominates most of the samples. Identifications of Cytherella sp.2 and Neonesidea cymbula were based on illustrations in Ducasse and Peypouquet (1979). N. cymbula was identified based on illustrations of specimens found in the Paleocene–Eocene Jorquera Formation of Caravaca, Spain (Guernet and Molina, 1997). These two species occur in the epibathyal lithofacies (500–1000 m depth) (Ortiz, 1995). Platyleberis sp. was also recognized from illustrations of ostracodes in the Paleocene–Eocene deep-sea deposits of the Basque Basin, Spain (P. chamela cited in Rodriguez-Lazaro and Garcia-Zaraga, 1996). Thus, some of the ostracodes observed here have already been recorded from deep-sea sediments near the Bay of Biscay. The other species have never been reported in deep-sea sites close to DSDP Site 401 (DSDP Sites 400–406: Ducasse and Peypouquet, 1979; DSDP Sites 549 and 550: Whatley and Coles, 1991; Basque Basin: Rodriguez-Lazaro and Garcia-Zaraga, 1996; Fig. 1). The cluster analysis of binned samples suggests that we can recognize three assemblages spanning the PETM at 0.85 similarity (Fig. 5). Krithe crassicaudata–Poseidonamicus Assemblage. —This assemblage ranges up to the lowermost PETM from 204.55 to 202.45 mbsf and is characterized by Bythoceratina sp., Poseidonamicus sp., and Cardobairdia sp. It shares Cytherella sp.1, Cytherella sp.2, and Trachyleberidea sp. with the K. crassicaudata-Cytherella Assemblage. Species diversity in the K. crassicaudata-Poseidonamicus Assemblage is the highest of all the assemblages. Richness ranges from 7 to 16 species with an H of 1.56–2.29, and E(S30) between 7.18 and 10.42. Krithe crassicaudata Assemblage. —This assemblage occurs during and after the PETM. It is found in intervals of 202.45–200.95, 200.05–199.75, and 199.15–198.25 mbsf and is dominated by infaunal Krithe sp.1, Krithe sp.2, and Argilloecia sp., which are also found in the other assemblages. Neonesidea cymbula and Trachyleberidea sp. are present in this assemblage. All of these species, save Neonesidea and Trachyleberidea are dwarfed compared to the same taxa before and after the PETM. Species diversity is the lowest of all the assemblages with a richness is 2–4, H of 0.40–1.65, and E(S30) of 2.53–7.64. Species with ornamentedvalves, such as Bythoceratina sp. and Poseidonamicus sp are absent.

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Horn’s ovelapped index

38

0.75 0.85 0.8 0.9 0.95

Abyssobairdia sp. Gen. et sp. indet.2 Phacorhabdotus sp. Krithe sp.2 Cytherella sp.2 Paleoabyssocythere sp. Bythoceratina sp.

Species

Platyleberis sp. Cytheropteron sp.1 Poseidonamicus sp. Eucythere sp. Cytherella sp.1 Cardobairdia sp. Trachyleberidea sp. Neonesidea cymbula Krithe crassicaudata Krithe sp.1 Argilloecia sp.

0

K. crassicaudataPoseidonamicus Ass.

K. crassicaudataCytherella Ass.

201.85-202.15

202.15-202.45

198.85-199.15

198.55-198.85

201.55-201.85

200.95-201.25

201.25-201.55

199.75-200.05

200.65-200.95

200.35-200.65

199.45-199.75

200.05-200.35

199.15-199.45

204.25-204.55

203.65-203.95

203.35-203.65

203.05-203.35

202.75-203.05

203.95-204.25

Interval

Relative abudance (%)

Gen. et sp. indet.1 100

202.45-202.75

Cytheropteron sp.2

Krithe crassicaudata Ass.

Fig. 5. A cluster analysis of binned ostracode assemblage data relative to stratigraphic depth at DSDP Site 401. Gray shading indicates relative abundance of each species. Depth intervals in meters below sea floor.

Krithe crassicaudata–Cytherella Assemblage. —Found after the PETM, the K. crassicaudata-Cytherella Assemblage occurs in the intervals of 200.95–200.05 and 199.75–199.15 mbsf and is dominated by Cytherella sp.1 and Cytherella sp.2. This assemblage lacks three common species characteristic of the K. crassicaudata–Poseidonamicus Assemblage. Four other species (Cytheropteron sp.2, Eucythere sp., Paleoabyssocythere sp., and gen. et sp. indet. 2) that were rare in the K. crassicaudata–Poseidonamicus Assemblage are also absent, but whether this reflects extinction, a failure of repopulation, or a sampling artifact cannot be determined. Taxonomic diversity is lower than the K. crassicaudata–Poseidonamicus Assemblage and three species unknown from the earlier part of the record are also present as rare individuals in the K. crassicaudata–Cytherella Assemblage.

Population metrics for this assemblage include a richness of 7–9, H of 1.65–2.03 and E(S30) index of 7.64–8.23.

6. Discussion 6.1. Benthic ecological patterns in the deep Bay of Biscay The ostracodes are considered as autochthonous thanatocoenoses in low-energy environments, because they include adult specimens and show high juvenile/adult ratios (>0.5 in most of the samples; Fig. 2; Boomer et al., 2003). The ostracode assemblages reflect the taxonomic composition of census assemblages.

T. Yamaguchi, R.D. Norris / Marine Micropaleontology 86–87 (2012) 32–44

39

Geological mbsf age (Ma) 198.5

K

55.63

199.5

K-C

200.0

K

200.5

K-C

Early Eocene

199.0

201.0 201.5

K

202.0

55.80

203.0

K-P

Late Paleocene

202.5

203.5 204.0

Assemblage

Gen et sp. indet.1

Abyssobairdia sp.

Gen et sp. indet.2

*Cytheropteron sp.2

Paleoabyssocythere sp.

+Eucythere sp.

Cardobairdia sp.

Bythoceratina sp.

Platyleberis sp.

Poseidonamicus sp.

*Cytheropteron sp.1

Phacorhabdotus sp.

+Cytherella sp.2

Trachyleberidea sp.

+Cytherella sp.1

*Neonesidea cymbula

+Krithe sp.2

+Argilloecia sp.

+Krithe sp.1

Species

+Krithe crassicaudata

204.5

Fig. 6. Stratigraphic distribution of ostracode species. Filled circles indicate the presence of a species. Plus and asterisk superscripts indicate infaunal and epifaunal live habitats, respectively. Other symbols as in Fig. 2. Bars are the calculated 95% upper and lower confidence bounds, which were calculated with the method of Roberts and Solow (2003). Abbreviation: K–P = Krithe crassicaudata–Poseidonamicus Assemblage, K = Krithe crassicaudata Assemblage, and K–C = Krithe crassicaudata–Cytherella Assemblage.

The Paleocene–Eocene ostracodes at DSDP Site 401 represent entirely extinct species, but many of the genera are still extant. Nonetheless, the patterns of diversity relative to environmental changes are significantly different between the Paleogene and today. We find that Paleogene species diversity (as represented by E(S15)) positively correlates with δ 18O (Spearman's rank correlation coefficient ρ = 0.6175, p = 5.802 × 10− 3, n = 19) whereas the Quaternary data of Yasuhara et al. (2009) show that E(S50) negatively correlates with δ18O (ρ = −0.4278, p = 3.585 × 10 − 5, n = 87). Apparently, bottom water temperatures had an inverse effect on the Paleocene–Eocene and Quaternary ostracode diversity. Prior to the PETM, the generic composition of the K. cassicaudata– Poseidonamicus Assemblage suggests relatively stable conditions on the continental slope. Ostracode assemblages shift to the near total dominance of Krithe during the initial phase of the PETM – a low diversity – high dominance community consistent with strong environmental stress. Currently, Krithe is known as a generalist and tolerant of changes in temperature (Didié and Bauch, 2000). This taxon is distributed worldwide and abundantly occurs in both glacial and interglacial sediments of Quaternary deep-sea cores (e.g., Didié and Bauch, 2000; Yasuhara et al., 2008; Alvarez Zarikain et al., 2009). Today, Krithe is also tolerant of low oxygen conditions on the sea floor (e.g., Whatley and Zhao, 1993).

The composition of the K. crassicaudata Assemblage and the abundance of ostracodes at DSDP Site 401 both suggest that seafloor oxygen content did not dip much below 1 ml/l. This is in general agreement with the benthic foraminifer assemblage – composed mostly of Nuttallides truempyi and buliminids – that indicates depleted oxygen contents and/or higher organic matter during the PETM at DSDP Site 401 (Thomas, 1998). The abundance of ostracode valves throughout the DSDP Site 401 record agrees with studies of modern deep-sea ostracodes that are completely absent or rare from the modern oxygen minimum zone when O2 falls below 1 ml/l of oxygen (Zhou and Ikeya, 1992; Ozawa, 2004). Furthermore, experiments show that the mortality of ostracodes exceeds 20% and abruptly increases as O2 drops to less than 1 ml/l at 10 °C (Newrkla, 1985). We believe that oxygen and temperature, rather than organic matter flux, is likely the controlling Table 1 Lazurus taxa in ostracode assemblages after the “core” phase of the CIE zone. Site

Lazarus taxon

Reference

ODP Site 689

Dutoitella Oertiella Pelecocythere Cytherella sp.2

Steineck and Thomas (1996)

DSDP Site 401

This study

40

T. Yamaguchi, R.D. Norris / Marine Micropaleontology 86–87 (2012) 32–44

of small sample size. In the end, only one species, Cytherella sp.2 , has a statistically-supported gap in its range (Fig. 6; Table 1). We infer that Cytherella sp.2 (and possibly other species) must have either been displaced along the depth gradient or geographically along the European slope. This pattern of spatial displacement is also inferred in Tethyan shelf and slope sections in Egypt and the Southern Ocean (Table 1); however, without statistical tests, it is difficult to determine how common the “Lazarus” phenomenon really is in these settings (Morsi and Speijer, 2003; Morsi and Scheibner, 2009; Morsi et al., 2011). This pattern of migration during times of environmental stress is also seen in depth migrations in response to the Quaternary glacial/interglacial climate changes (e.g., Cronin et al., 1999; Yasuhara et al., 2009). Ostracode communities may also be responding to changes in substrate or the corrosiveness of sea water during the PETM. Schmitz et al. (2001) note that the PETM sediments are commonly clay-rich in the Basque Basin, including the Zumaya section, which they considered to reflect increasing of continental erosion during warming associated with the hyperthermal. Alegret et al. (2009b) agree that erosion rates increased during the PETM, but they further suggest, along with Zili et al. (2009), that the Calcite Compensation Depth (CCD) shoaled in the CIE zone and reached 500–1000 m depth in northern Spain (Zumaya), based upon an interval of clay-rich and carbonate-depleted sediments between the BEE horizon and the end of the CIE. We find little evidence of extensive carbonate dissolution at Site 401, where samples of the CIE zone yield ostracodes as abundant as the pre- and post-CIE zones (Fig. 2) and planktonic

factor for the Paleogene ostracode assemblage because Argilloecia (an indicator of organic-rich sediments; Alvarez Zarikain et al., 2009) does not increase during the PETM interval. The K. crassicaudata–Cytherella Assemblage has higher taxonomic diversity than the K. crassicaudata Assemblage, suggesting a decline in environmental stress. The assemblage correlates with a return to relatively positive benthic δ 18O, which indicates cooling (Figs. 2, 6 and 7) and, according to Nunes and Norris (2006), a gradual return to a southern-sourced water mass in the Bay of Biscay similar to pre-PETM conditions. After the PETM interval, ostracode assemblages repeatedly oscillate between the K. crassicaudata-Cytherella and the K. crassicaudata Assemblage. This suggests that there was a long period of environmental change following the PETM in which fluctuations in oxygen often occurred. Both δ18O and δ13 C are relatively stable during these oscillations in ostracode assemblages, suggesting that the ostracode communities are not responding to the direct changes in temperature and carbon cycle processes initiated by the PETM. A number of ostracode species disappear during the PETM only to reappear during the waning phases of the hyperthermal event. Species that temporarily disappear, presumably reflecting migration, are called “Lazarus taxa” and have been documented from periods of mass extinction elsewhere in the geologic record (Jablonski, 1986). In DSDP Site 401, most species that are not recorded during the PETM cannot be shown, unequivocally, to be true Lazarus species since a statistical evaluation suggests that the apparent gap in their ranges could be an artifact

Geological age (Ma)

mbsf 198.5

K

199.5

K-C

200.0

K K-C

Early Eocene

199.0

200.5

55.63

202.0 202.5

Late Paleocene

203.0 203.5 204.0 204.5

E(S15)

0 18 Species richness

0

2.5

H

0

E(S30)

12 Rarefaction

0

100 Relative abundance (%)

Assemblage

55.80

K

K-P

201.5

Krithe crassicaudata

Poseidonamicus sp. Cytherella sp.2 Cytherella sp.1

201.0

Fig. 7. Stratigraphic changes of species richness, Shannon index, H, and rarefaction, E(S15) and E(S30), and the relative abundance of the key taxa. Closed circles reflect data from the raw samples, while diamonds indicate data of the binned samples. The relative abundances were calculated, using the binned dataset. Other symbols and abbreviations as in Figs. 2 and 6, respectively.

T. Yamaguchi, R.D. Norris / Marine Micropaleontology 86–87 (2012) 32–44

2002; Morsi and Speijer, 2003; Webb et al., 2009; Figs. 1, 8). Because of uncertainty about the samples, abundance of specimens, and geochronology, we excluded previously published data from DSDP Sites 549, 550, and 762, ODP Sites 865 and 1051, the Sindh Province of Pakistan, the Basque Basin and Caravaca of Spain, the Jaisalmer Basin of India, the Southern Galala Plateau of Egypt, and the Sidi Nasseur– Wadi Mezaz area of Tunisia (Whatley and Coles, 1991; Brouwers and Fatmi, 1992a,b; Guernet and Galburn, 1992; Boomer and Whatley, 1995; Rodriguez-Lazaro and Garcia-Zaraga, 1996; Guernet and Molina, 1997; Guernet and Belliner, 2000; Bhandari, 2008; Morsi and Scheibner, 2009; Morsi et al., 2011). One of the most striking aspects of ecological changes during the PETM is the 35–50% extinction of deep sea benthic foraminifera (e.g., Thomas and Shackleton, 1996). The PETM records a drastic increase in species dominance and temporarily disappearances of species that later repopulate the sea floor. In addition, a unique fauna of benthic foraminifera temporarily appeared during the PETM. This so-called disaster and/or opportunistic fauna, consists of Nuttallides truempyi and buliminid species as dominant taxa (e.g., Takeda and

foraminifera are usually well preserved. We do observe a rapid shift in the clay content from ~ 60–70% carbonate below the BEE to about 40% carbonate with the onset of the PETM. Our observations indicate that the PETM sediments were above the CCD and that claydominated sediments likely reflect terrestrial weathering as inferred by Schmitz et al. (2001). High clay content and dark colored sediments persist through the PETM and for several hundred thousand years afterward at Site 401 suggesting that climate changes associated with the PETM were persistent long after the climate forcing of the hyperthermal event.

6.2. Global patterns of ecosystem change during the PETM To assign changes in ostracode faunas across the PETM on the global spatial scale, we compared our data with the late Paleocene– early Eocene data from five DSDP and Ocean Drilling Program (ODP) sites and shallow-marine strata of Egypt and Spain (Steineck and Thomas, 1996; Guernet and Molina, 1997; Speijer and Morsi,

Tethys Sea Southern Ocean Gebel Aweina, Egypt Gebel Duwi, Egypt ODP Site 689 ODP Site 690 Paleodepth 100–300 m Paleodepth <100 m Paleodepth 1100 m Paleodepth 1900 m mbsf mbsf Horizon (cm) Horizon (cm)

North Atlantic DSDP Site 401 Paleodepth 1800 m

Taxonomic diversity

mbsf 198.5

350 300

350

200

150

200.5 100

201.5

50

0

202.5

-50

203.5

-100

-150

204.5

-200

-250

10

0

20

Species richness

10

2

Species richness 350

202.5

0

-50

203.5

-100

-150 -250

212 213

250 200 150

200.5 100

201.5

204.5

50

-200 0

0

350

Abundance

Abundance 350 300

198.5 199.5

Kr cra ithe ss ica u

200.5

ta

350

150

100

50 -50

204.5

-200 0

100

Relative abundance (%)

Alocopocythere ramalia

Reticulina -150 sangalkamensis

-100

203.5

Paracosta kefensis

250

0

202.5

-250 0

168 169 170 171 172 173 10

100

Relat. abundance (%)

0

50

10

168 169 170 171 172 173 0

2000

0

Abundance 203 204 205 206 207 208 209 210

Propo

100

300

Abundance

ntocy

pris

N/A Krithe

211 212 213

Relat. abundance (%)

25

Species richness 167

Abundance

Cytherella aegyptopunctata

200

da

201.5

600

0

150

167

Genus richness 203 204 205 206 207 208 209 210 211

199.5

Abundance

10

Species richness

350 300

198.5

Dominant taxon

203 204 205 206 207 208 209 210 211 212 213

250

199.5

0

41

0

60

Relat. abundance (%)

Fig. 8. Comparison of species or generic richness, abundance of ostracodes, and the dominant taxa through the PETM at DSDP Site 401 and previous studies. Gray areas and black dash lines indicate the CIE zone and the horizon or sample with the minimum δ13C, respectively. The black thick line means unconformity in Gebel Aweina. In the relative abundance of the dominant taxa, solid lines connect points at samples with more than 24 individuals. Ostracode data derived from the: ODP Site 689, Steineck and Thomas (1996); ODP Site 690, Webb et al. (2009); Gebel Duwi and Gebel Aweina, Morsi and Speijer (2003). δ13 C data were used to identify the CIE zone and are derived from the following studies: ODP Site 689, Thomas and Shackleton (1996); ODP Site 690, Bains et al. (1999); Gebel Duwi and Gebel Aweina, Schmitz et al. (1996). Paleodepth data derived from: ODP Sites 689, 690, Thomas (1998); Gebel Duwi and Gebel Aweina, Morsi and Speijer (2003). The data of DSDP Site 401 are from the binned samples. N/A means no applicability. Localities of these sites are shown in Fig. 1.

42

T. Yamaguchi, R.D. Norris / Marine Micropaleontology 86–87 (2012) 32–44

Kaiho, 2007; Alegret et al., 2009a,b). The extinctions and ecological shifts in benthic foraminifera stand in marked contrast to the situation in planktonic protists such as planktonic foraminifera, calcareous nannoplankton, dinoflagellates, and radiolarians. These pelagic groups show ecological disruption, geographic range changes and, sometimes, short-lived appearances of species restricted to the PETM interval – so called “excursion taxa” – but very little extinction. Ostracodes, in contrast, display a fairly simple history that involves the local demise of a host of species that were common in the late Paleocene, which then repopulate the seafloor in the waning phases of the PETM. There is a fairly abrupt local extinction of ostracode species associated with the benthic foraminiferal extinction horizon but few species are involved. Only three species (Cytheropteron sp.1, Bythoceratina sp., and Poseidonamicus sp.) can be demonstrated to have failed to repopulate in the Bay of Biscay (Fig. 6). Bythoceratina sp. and Poseidonamicus sp. disappeared coincidently with the BEE while Cardobairdia sp. was extinct before the CIE zone. Eucythere sp. and Paleoabyssocythere sp. might have vanished before the CIE but we have too few records to determine precise ranges. These five species were not reported from deposits after the Paleocene at DSDP Site 401 and its neighboring sites (DSDP Sites 400–406: Ducasse and Peypouquet, 1979; DSDP Sites 549 and 550: Whatley and Coles, 1991; Basque Basin: Rodriguez-Lazaro and Garcia-Zaraga, 1996; Fig. 1). Hence, the disappearance of these species is considered to be due to at least a regional extinction, but whether this reflects global extinction or a local signal is presently unclear. The PETM ostracode fauna does not possess “excursion” taxa that are widely distributed across many sites in the way that is seen in other groups of marine plankton and benthos. For example, ‘excursion’ biota are found in benthic foraminifera (the Nuttallides truempyi or buliminid taxa-dominated benthic foraminiferal assemblage; e.g., Thomas, 1998), dinoflagellates (Apectodinium floods into PETM dinoflagellate assemblages; e.g., Couch et al., 2003), nannoplankton (e.g. Rhomboaster dominated nannoplankton; e.g., Kahn and Aubry, 2004), and planktonic foraminifera (such as Acarinina africana and Acarinina sibaiyaensis; e.g., Kelly, 2002). Indeed, in most sites, the ostracode assemblages during the PETM do not include opportunistic taxa, known only from the core of the PETM. In the Southern Ocean and Tethyan shallow-marine sections, dominant taxa change during the PETM whereas in DSDP Site 401, Krithe crassicaudata ranges throughout the PETM (Steineck and Thomas, 1996; Morsi and Speijer, 2003; Fig. 8). The closest we come to an ostracode excursion fauna is the record of Propontocypris in the Southern Ocean which makes an appearance late in the PETM before becoming rare again in post PETM sediments (Steineck and Thomas, 1996) (Fig. 8). In DSDP Site 401, epifaunal, morphologically-varied species (Cytherella) are removed entirely during the core of the PETM leaving a low diversity assemblage (K. crassicaudata Assemblage) characterized by unornamented, infaunal taxa (Argilloecia and Krithe). Species dominance increases as species richness declines above the BEE and then gradually falls off again as species typical of the late Paleocene repopulate the slope environment. The pattern of ostracode turnover in the Bay of Biscay resembles a previously documented ostracode turnover during the PETM in Egypt and Spain — then located on the shelf and slope of the Tethys seaway, respectively (Guernet and Molina, 1997; Morsi and Speijer, 2003). In the Tethys, shallow marine ostracodes display a marked turnover, losing seven species out of a standing stock of 18 abundant taxa at or just before the onset of the PETM in Gebel Duwi, Egypt. Of the species that disappear in the deep Bay of Biscay at the PETM, Cytherella sp.2 is a “Lazarus taxon” that subsequently reappears after the “core” phase of the PETM (Table 1). The main difference between the records on the Tethyan shelf and the deep Bay of Biscay is that the post-PETM appearance of two species (Abyssobairdia sp. and gen. et sp. indet. 1) is not recorded below the PETM in the shelf setting around the Bay of Biscay (Hampshire Basin: Keen, 1978; Aquitaine and Paris Basins:

Ducasse et al., 1985; Fig. 1). These species may have been introduced from the other deep-sea basins. However, this apparent difference may reflect sampling differences, since the number of study sites, the sample sizes, and total numbers of valves studied was generally lower in the Bay of Biscay and its adjacent regions than in the Tethyan sections. The only other extensive studies of deep-sea ostracodes through the PETM are from the Southern Ocean (ODP Sites 689 and 690) — two mid water sites with paleodepths of ~1900 m and 2900 m, respectively. No census data have been published for either site, but assemblage reconstructions for the shallow site identify a short-lived, “disaster fauna” during the PETM composed of infaunal, smoothwalled species associated with warm, suboxic waters (Steineck and Thomas, 1996). In ODP Site 690, ostracode diversity clearly drops coincidently with the decrease of δ13C at the beginning of the PETM (Webb et al., 2009). In ODP Site 689, ostracode assemblages from the later stages of the recovery from the PETM and afterward have unusually high generic richness, a high percentage of infaunal species, and high overall abundance compared to assemblages from before the PETM or the initial phases of the CIE. Hence, it appears that there was a crash in ostracode diversity in the Southern Ocean sites as is also observed at DSDP Site 401. The PETM diversity loss probably occurred in the Tethys Sea as well (Fig. 8). In Gebel Duwi, the ostracodes show diversity loss during the PETM. However, the ostracode taxonomic diversity increases in Gebel Aweina. Since the Gebel Aweina section lacks the early part of the PETM (Morsi and Speijer, 2003), the diversity increase appears during the “recovery” phase (the tie point E to the end of the PETM; Röhl et al., 2007). Therefore we suggest that deep-sea ostracodes underwent their diversity loss during the “core” phase of the PETM. Data for the Southern Ocean and North Atlantic sites suggest that the ostracode assemblage developed lower dominance during the later stage of the PETM while displaying slightly lower generic richness than seen in the pre-PETM assemblages. However, the Southern Ocean sites did not show the spike in species dominance seen at the North Atlantic sites. Benthic foraminifers also show the diversity loss during the core of the PETM and the diversity rebounds during the recovery phase (e.g., Speijer et al., 1997; Thomas, 2007; Alegret et al., 2009a,b). Southern Ocean ostracode assemblages were dominated by small, thin-walled species during the later stage of the PETM. Steineck and Thomas (1996) inferred that PETM faunas may have been exposed to low pH waters that restricted the ability of the ostracode fauna to calcify robust valves. In contrast, ostracodes at Site 401 maintain robustly calcified valves throughout the record. By the reasoning of Steineck and Thomas (1996), our data would be consistent with exposure of ostracodes to less acidified waters in the North Atlantic than in the Southern Ocean. However, we regard the extent of valve calcification as a poor indicator of acidification. We note that freshwater ostracodes exposed to acid rain do not vary significantly in calcification compared to the same species grown in normal conditions. Indeed, in a study of ostracode geochemistry, Wansard et al. (1998) presented data that show no correlation between pH and valve weight in the freshwater species, Candona. The over-riding conclusion from all these studies is that the PETM was not a major extinction horizon for ostracodes. Instead, species evidently found refugia during the core of the PETM, either by migrating latitudinally or shifting the core of their depth distribution. While some distinctive species appear in the Southern Ocean during the PETM, at the northern sites, the PETM assemblage is characterized more by the temporary loss of formerly common taxa than by range extensions of previously unusual species. 7. Conclusions Both ostracode assemblages and benthic foraminifers experienced significant turnover during the PETM including: 1) turnover coinciding with the start of the PETM, 2) both species geographic range shifts

T. Yamaguchi, R.D. Norris / Marine Micropaleontology 86–87 (2012) 32–44

and species extinction; 3) a drop in taxonomic diversity and often an increase in species dominance within the benthic community; 4) a switch from a mixed epifaunal and infaunal life assemblage to one dominated by infauna; and 5) a rebound after the PETM in which taxonomic diversity increased and species dominance dropped. These ecological patterns stand in contrast with those in planktonic phytoplankton and zooplankton which diversified and show often large, but usually temporary biogeography ranges and little extinction (e.g., Kelly, 2002, Gibbs et al., 2006; Hollis, 2006). However the ostracode assemblages at Site 401 show different characters from benthic foraminifers of Site 401 including: 1) abundant endemic ostracode species before the PETM; 2) no ostracode “excursion fauna” during the PETM; 3) few extinct species at the start of the event, and 4) a single well supported case of a “Lazarus” species. Although there have been relatively few studies of PETM ostracodes to date, comparison of faunal patterns in the Southern Ocean, Egyptian shelf and Bay of Biscay, show that in Northern Hemisphere sites, ostracodes experience a low level of species extinction associated with temporary migrations and subsequent repopulation. PETM faunas in the Bay of Biscay may have been reduced in diversity by a drop in seafloor O2, but oxygen levels do not appear to have dropped below ~ 1 ml/l by analogy with the oxygen tolerances of living faunas. The decline in ostracode diversity in the Bay of Biscay is probably not due to ocean acidification since the preservation of foraminifera and ostracodes is generally excellent throughout the PETM and those species that survived and are thick-walled despite the persistent increase in clay content of the PETM and post-PETM sediments. Acknowledgements We are grateful to Akihisa Kitamura (Shizuoka Univ., Japan) for his valuable suggestion on identifying extinction events at the 10th International Paleoceanography Congress, Johnnie A. Lyman (Scripps Institution of Oceanography: SIO) for preparing sediment samples, Jill S. Leonard-Pingel (SIO) for useful discussion on benthic paleoecology, Aruni Suwarnasarn (SIO) for her help with the SEM, and David J. Horne (Univ. London) for his help in collecting references. We are also grateful to Robert P. Speijer (K.U. Leuven) and an anonymous reviewer for their critical comments and Richard Jordan (Yamagata Univ., Japan) for his helpful comments during editing of the manuscript. Funding for this research was provided by the Japan Society for the Promotion of Science to TY and the National Science Foundation and the US Science Support Program to RDN. Appendix. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.marmicro.2012.02.003. References Alegret, L., Ortiz, S., Molina, E., 2009a. Extinction and recovery of benthic foraminifera across the Paleocene–Eocene Thermal Maximum at the Alamedilla section (Southern Spain). Palaeogeography, Palaeoclimatology, Palaeoecology 279, 186–200. Alegret, L., Ortiz, S., Orue-Etxebarria, X., Bernaola, G., Baceta, J.I., Monechi, S., Apellaniz, E., Pujalte, V., 2009b. The Paleocene–Eocene thermal maximum: new data on microfossil turnover at the Zumaia section, Spain. Palaios 24, 318–328. Alvarez Zarikain, C.A., Stepanova, A.Y., Grützner, J., 2009. Glacial–interglacial variability in deep sea ostracod assemblage composition at IODP Site U1314 in the subpolar North Atlantic. Marine Geology 258, 69–87. Alve, E., Goldstein, S.T., 2003. Propagule transport as a key method of dispersal in benthic foraminifera. Limnology and Oceanography 48, 2163–2170. Aumond, G.N., Kochhann, K.G.D., Florisbal, L.S., Fauth, S.B., Bergue, C.T., Fauth, G., 2009. Maastrichian-Early Danian radiolarians and ostracodes from ODP Site 1001B, Caribbean Sea. Revista Brasileira de Paleontologia 12, 195–210. Bains, S., Corfield, R.M., Norris, R.D., 1999. Mechanisms of climate warming at the end of the Paleocene. Science 285, 724–727. Bains, S., Norris, R.D., Corfield, R.M., Faul, K.L., 2000. Termination of global warmth at the Paleocene/Eocene boundary through productivity feedbacks. Nature 407, 171–174.

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