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Southern turnover in response to stepwise cooling over the past 15 million years

James S. Cramptona,b,1, Rosie D. Codya,c,2, Richard Levya, David Harwoodd, Robert McKayc, and Tim R. Naishc

aGNS Science, Lower Hutt 5040, New Zealand; bSchool of Geography, Environment and Sciences, University of Wellington, Wellington 6140, New Zealand; cAntarctic Research Centre, Victoria University of Wellington, Wellington 6140, New Zealand; and dDepartment of Earth and Atmospheric Sciences, University of Nebraska–Lincoln, Lincoln, NE 68588

Edited by James P. Kennett, University of California, Santa Barbara, CA, and approved May 4, 2016 (received for review January 7, 2016) It is not clear how Southern Ocean phytoplankton communities, . Marine-based ice, grounded on bedrock below which form the base of the marine food web and are a crucial level in West and East , continued to expand and element of the carbon cycle, respond to major environmental contract through variable of the late Miocene and into disturbance. Here, we use a new model ensemble reconstruction the Pliocene (14–3 Ma) (12, 13), driving global sea-level fluctu- of speciation and extinction rates to examine phytoplank- ations of between 20- to 30-m amplitude and up to 20 m above ton response to change in the southern high over the present-day level (14). These marine ice sheets then stabi- the past 15 My. We identify five major episodes of species turnover lized as global climate cooled again in the late Pliocene and early (origination rate plus extinction rate) that were coincident with Pleistocene (3–2.5 Ma) and perennial became a “per- times of cooling in southern high- climate, Antarctic ice manent” feature in the Southern Ocean (15). sheet growth across the continental shelves, and associated sea- The response of Southern Ocean to these major sonal sea-ice expansion across the Southern Ocean. We infer that changes has been, until now, poorly resolved. To realize the po- past turnover occurred when a warmer-than-present cli- tential of their rich microfossil record, it is first necessary to mit- mate was terminated by a major period of glaciation that resulted in igate pervasive biases that are inherent to paleontological records loss of open-ocean habitat south of the polar front, driving non-ice (Supporting Information). To achieve this, we used a quantitative adapted diatoms to regional or global extinction. These findings biostratigraphic method, constrained optimization [CONOP (16)] suggest, therefore, that Southern Ocean phytoplankton communi- (Materials and Methods and Supporting Information), applied to a ties tolerate “baseline” variability on glacial–interglacial timescales regional database of fossil species occurrences in the Southern but are sensitive to large-scale changes in mean climate state driven Ocean and Antarctic margin that was drawn from 34 drill cores by a combination of long-period variations in orbital forcing and (17) (Fig. 1 and Table S1). Data were restricted to south of atmospheric carbon dioxide perturbations. the present-day Antarctic Polar Front, which represents an ef- fective biogeographic barrier to the dispersal of modern assem- Antarctica | diatoms | Miocene | Pliocene | phytoplankton blages. Because of uncertainties regarding the position of this front in the past (18–20), we used alternative CONOP models n the face of warming and changing seawater chemistry based on a conservative, more southerly dataset of 27 drill cores Iand circulation, there is growing evidence of biogeographic, that are situated well south of the modern front, and a less con- community, and adaptive changes in the living marine microflora servative dataset that included an additional seven drill cores from (1–3). Predicting how environmental change will influence phy- regions immediately south of the front. toplankton communities, which account for ∼50% of global From vetted observations of local highest and lowest fossil primary productivity, is hampered by the large spatial scale of the occurrences in each drill core, CONOP produced model composite forcings on the biotic system and the long response time (2). histories that were used to identify the order and timing of origi- Here, we use the history of postmid-Miocene (post-15 Ma) di- nation/immigration and regional extinction events for the common, atoms preserved in geological archives from the Southern Ocean and Antarctic margin to reveal long-term patterns and rates of Significance phytoplankton turnover (origination rate plus extinction rate) and to constrain interpretations of macroevolutionary processes. Based on data of unprecedented resolution, we show that These floras are of critical interest today given the expected phytoplankton (diatoms) in the Southern Ocean have experi- sensitivity of high-latitude to polar amplification of enced five major pulses of species extinction and origination . Globally, diatoms are the dominant living phy- over the past 15 My that were linked to large cooling transitions toplankton group, accounting for ∼20% of primary productivity, in southern high latitudes. Our findings suggest that phyto- and their macroevolutionary history is linked to changes in cli- plankton communities around Antarctica have been robust to mate (4). Diatom species are highly endemic south of the Ant- “baseline” glacial–interglacial climate variability but were sensi- Polar Front, which today forms an oceanographic and tive to large-scale changes in mean climate state driven by a biogeographic boundary (5). Within this , there are cur- combination of long-period variations in orbital forcing and at- rently two distinct : a specialized flora occupying the sea- mospheric carbon dioxide perturbations. ice zone (6) and a high-nutrient low-chlorophyll flora occupying the open ocean (7). Author contributions: J.S.C., R.D.C., and R.L. designed research; J.S.C. and R.D.C. designed The climate history of the Antarctic and Southern Ocean over and performed analyses; and J.S.C., R.D.C., R.L., D.H., R.M., and T.N. wrote the paper. the past 15 My is one of stepwise cooling punctuated by transient The authors declare no conflict of interest. warm periods. Highly variable ice sheets that characterized the This article is a PNAS Direct Submission. mid-Miocene Climate Optimum (8, 9) subsequently expanded 1To whom correspondence should be addressed. Email: [email protected]. during the cooling associated with the Miocene Climate Tran- 2Deceased October 4, 2015. ∼ sition 14 Ma (10, 11), at which time a large terrestrial ice sheet This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. became a relatively permanent feature on the East Antarctic 1073/pnas.1600318113/-/DCSupplemental.

6868–6873 | PNAS | June 21, 2016 | vol. 113 | no. 25 www.pnas.org/cgi/doi/10.1073/pnas.1600318113 Downloaded by guest on October 4, 2021 Fig. 1. Map of Antarctica and the Southern Ocean, showing location of sites studied here. See Table S1 for details.

abundant, and robust diatom species (Supporting Information). the average duration of a species in our dataset is ∼7 My. This new Conservatively, using three CONOP composites, we used model macroevolutionary history of diatoms is an order of magnitude ensemble and bootstrapping procedures to capture uncertainties more finely resolved than previously available records (cf. refs. 4 related to biogeographic constraints and varying assumptions about and 5) and reveals hitherto unknown patterns and pulses of phy- the of the fossil record, assumptions that are reflected in toplankton species turnover, separated by intervals of moderate to different CONOP compositing approaches (Supporting Information). low turnover. Results are apparently unbiased by effects of drill Each model composite sequence of events produced by CONOP core coverage, sampling density, or the presence of widespread was dated independently to yield an average temporal resolution of hiatuses in sedimentation (Supporting Information and Figs. S2 ∼ 63,000 y (63 ky) over the study interval. This approach provides a and S3). “ ” continuous record of individual diatom appearance and disap- Here, we focus on five conspicuous peaks of turnover with pearance events that is free from the biases and artificial dis- rates greater than 0.5 (labeled turnover pulses A–E in Fig. 2A) continuities imposed by binning at the time resolution of zones and explore their relationship to known paleoclimatic events. and stages. The CONOP composites used here are given in – – The ages of these pulses are approximately: 14.65 14.45 Ma (A), Datasets S1 S3. 13.75–13.55 Ma (B), 4.90–4.40 Ma (C), 3.55–3.40 Ma (D), and We do not discriminate true global speciation and extinction 3.00–1.95 Ma (E).

of endemic species from ecologically controlled immigration and EARTH, ATMOSPHERIC,

Fig. 2 reveals that all of the turnover pulses coincide with AND PLANETARY SCIENCES local extinction of species that are also found north of the positive excursions or maxima in benthic marine δ18O values that Antarctic Polar Front, a task that would require high-resolution, mark periods of global cooling and/or ice volume increase. Like- global biogeographic and biostratigraphic data (Materials and wise, all except D occurred during episodes of atmospheric CO Methods, and see refs. 4 and 5). For the purposes of the present 2 study, however, we are interested in the timing and patterns decline inferred from geological proxy records, although we cau- of species turnover in the Southern Ocean region and, although tion that the CO2 geological proxy data are presently limited in of considerable interest, it is not essential to discriminate turn- temporal resolution and are subject to large assumptions and over driven by evolution/extinction from turnover driven by uncertainties (22). Turnover pulses A and B also coincide with two δ13 biogeographic changes. major middle Miocene positive excursions in C, and pulses C to E align with periods of declining to low biosiliceous productivity Results on the Antarctic margin, represented by opal accumulation rate Using the ensemble of age-calibrated composite histories of di- (MARopal). Taken together, these results suggest that the diatom atom first and last appearances, we calculated lineage-million-year turnover pulses identified here were related in some way to major origination, extinction, and turnover (origination + extinction) global climatic and oceanographic changes, coupled to perturba- rates (21) for a smoothed 200-ky moving window at 50-ky time tions in the carbon cycle, which occurred during the middle increments since 15 Ma (Fig. 2 and Fig. S1 A–C). For comparison, Miocene to earliest Pleistocene.

Crampton et al. PNAS | June 21, 2016 | vol. 113 | no. 25 | 6869 Downloaded by guest on October 4, 2021 Fig. 2. Turnover pulses of diatoms in the Southern Ocean and Antarctic margin over the past 15 million years (Ma) compared with key paleoenvironmental proxies. (A) Species lineage-million-year (lmy) turnover rate. The bold line is the model ensemble and bootstrapped median, the dark region is the model ensemble (nonbootstrapped) ±1 SD uncertainty bound, and the pale region is the bootstrapped uncertainty bound (Supporting Information). Pink bars identify turnover pulses discussed here. (B) Benthic δ18O curve from ref. 42; raw data shown in gray, loess smooth in black. (C) Benthic δ18O curve from ref. 28;

raw data shown in gray, loess smooth in black. (D) Opal accumulation rates (MARopal) at ODP Sites 1095 (black) and 1096 (blue), from ref. 43; this measure is taken as a proxy for sea-ice extent on the Antarctic margin such that declining opal accumulation indicates an expansion in sea ice. (E) Estimates of at-

mospheric pCO2 based on various proxies, from ref. 44 (1, alkenone; 2, boron), ref. 45 (3, alkenone), and ref. 46 (4, boron); raw data in pink, loess smooth in red. (F) Benthic δ18O curve for the time interval 15–13 Ma, from ref. 11; raw data shown in gray, loess smooth in black. (G) Benthic δ13C curve from ref. 11; raw

data shown in gray, loess smooth in black. (H) Estimates of atmospheric pCO2 based on various proxies, from ref. 47 (1, boron), ref. 45 (2, alkenone), and ref. 48 (3, B/Ca and 4, alkenone).

In more detail, pulses A and B coincide with two major cooling across the continental shelf and into marine basins in East and steps within the Miocene Climate Transition, which marks . The presence of grounded ice on the continental progressive change from eccentricity-paced glacial–interglacial shelf is indicated in the ANDRILL-1B core and by regional seis- cycles to obliquity-paced cycles (11). During these cooling steps, mic records (9) and supported by ice-sheet-climate models (8). bottom water temperatures decreased by around 3 °C and sea- Model simulations also indicate that sea-ice expansion is likely to surface temperatures decreased by up to about 7 °C (10). At the have occurred in concert with advance of grounded ice sheets onto same time, sea level dropped by between 30 and 60 m (23), the shelf (24). Although definitive evidence of sea ice during consistent with expansion of a terrestrial Antarctic Ice Sheet turnover pulses A and B is lacking, changes in diatom and

6870 | www.pnas.org/cgi/doi/10.1073/pnas.1600318113 Crampton et al. Downloaded by guest on October 4, 2021 Fig. 3. Schematic environmental reconstructions for the Antarctic continental shelf and Southern Ocean during intervals of (A) warmth and ice minimum and (B) peak cold and maximum ice extent; exact limits of Pliocene and Miocene sea ice unknown. Relatively rapid transition between these two end-member environmental states drives extinction/speciation of warm/cold-adapted phytoplankton (diatoms), causing major species turnover. Two schematic, repre- sentative diatom taxa are illustrated. Flow of Antarctic Circumpolar Current and westerly winds is out of the page. Flow of polar easterlies is into the page. Latitudinal position of peak flow is indicated by circles and relative strength of flow is indicated by bold (strongest) to dashed (weakest) lines. Ventilation of

CO2-enriched deep water is indicated by wavy arrows (thin line indicates reduced ventilation due to stratified surface water and sea-ice cover). AABW, ; ASW, Antarctic surface water; PF, polar front; UDW, upper deep water; WDW, warm deep water (red, relatively warmer; green, relatively cooler).

foraminifera assemblages in the ANDRILL-2A core have been Discussion used to suggest that sea ice appeared after 16 Ma and became Results from this study suggest past, region-wide sensitivity more persistent after about 15 Ma (9, 25). (We note that certain of the diatom flora to large changes in ice extent in the pre- key diatom taxa used to infer the presence of sea ice in ref. 9, Pleistocene . We propose the following model to explain notably Fragilariopsis truncata and Synedropsis cheethamii,havenot this sensitivity (Fig. 3). High-latitude cooling and associated been consistently identified in older floral lists from the Southern changes in atmospheric circulation, driven by global-scale pro- Ocean and failed to meet the threshold for inclusion in the present cesses, resulted in increased production of cold Antarctic surface CONOP analyses.) In addition, probable sea-ice associated Mio- waters, enhanced stratification in the Southern Ocean (31), and cene diatoms have been recorded from the region (26, 27). deepening of the pycnocline (32). These changes in ocean struc- Turnover pulses C and D likewise are associated with cooling ture and dynamics at the Antarctic margin inhibited of episodes that culminated in deep-sea temperatures significantly warm deep water onto the continental shelf and promoted growth colder than today (14). Evidence for the advance of grounded ice of perennial sea ice and expansion of winter sea ice across the in the ANDRILL-1B core indicates that marine-based ice sheets Southern Ocean. We suggest that these episodes of major sea-ice in West Antarctica were more expansive than today, at least expansion increased surface albedo, reduced Southern Ocean during the onset of pulse C (12). Whereas the onset of pulse D ventilation, and enhanced CO2 sequestration to the deep ocean seems to predate significant cooling in Fig. 2C, in fact peak (33), which established a positive feedback on global climate that turnover at ∼3.4 Ma lies within the sustained, stepwise cooling drove major expansion of Antarctica’s ice sheets across the con- trend that began at Marine Isotope Stage (MIS) MG8 at tinental shelves. We infer that, before each of the turnover pulses ∼3.55 Ma and persisted until MIS M2 at ∼3.3 Ma (28). The ini- discussed here, there were year-round sea-ice-free conditions in tiation of this cooling trend is coincident within uncertainty (gray the open Southern Ocean, with well-mixed, nutrient-rich surface region in Fig. 2A) with the onset of pulse D. Furthermore, pulse D waters, the “Permanent Open Ocean Zone” of ref. 34 (Fig. 3A). At is preceded by MIS Gi4 and Gi2, between 3.7 and 3.6 Ma, which such times, new species were evolving in stratified coastal waters are characterized by δ18O excursions with values that are similar to that were sea-ice-covered in winter. During significant cooling

the Holocene, reflect major cooling and ice sheet advance, and events, when winter sea ice expanded beyond the continental EARTH, ATMOSPHERIC, may also have forced the onset of turnover. Importantly, the end margin and toward the polar front, and surface waters became AND PLANETARY SCIENCES of pulse D coincides with the final transition from subpolar to stratified, the open ocean environment was greatly reduced (Fig. polar conditions on the Antarctic margin and termination of early- 3B). Given that ocean frontal boundaries can represent significant to mid-Pliocene warm conditions (15, 29). biogeographic barriers (5) and that phytoplankton diversity is Finally, the onset of turnover pulse E is associated with large- governed by species-area effects (35), it seems likely that loss of scale δ18O excursions (e.g., 3.1–3.0 Ma and 2.7–2.4 Ma) and open-ocean habitat during these cooling events drove extinction minima in deep-sea temperatures (14), a trend toward increased pulses in non-ice-adapted, Southern Ocean diatoms. Throughout Antarctic summer sea-ice extent and duration (15), and stabilization the mid- to late Miocene and early Pliocene, large-magnitude of marine margins of the by ∼2.5 Ma (30). cooling events seem to have been paced by long-period orbital Each of the cooling episodes described above was preceded by cycles and as a result were transient in nature, and thus the forcing a warmer climate and, except in the case of turnover pulse E, of species evolution and community adjustment by each new cli- followed by times of relative global warmth and high oceanic matic regime was short-lived. However, long-term cooling, espe- productivity, bottom-water temperature, and sea level (12, 14, 15, cially after 5 Ma, resulted in the incremental and stepwise evolution 23). Each successively younger “warm” interval, however, occurred of endemic, ice-adapted diatoms that are a dominant component on a cooler background climate state, perhaps controlled by vari- of the flora today (Supporting Information and Fig. S1D). Based on ations in atmospheric CO2. evidence available to date, the model proposed above is supported

Crampton et al. PNAS | June 21, 2016 | vol. 113 | no. 25 | 6871 Downloaded by guest on October 4, 2021 most strongly for turnover pulses C to E. We argue that the model Antarctic Polar Front (Fig. 1 and Table S1). All data were vetted before would still have operated during times of lesser sea-ice extent— analysis, to eliminate records that may have been reworked, and species perhaps pulses A and B—when the entire biogeographic system with fewer than three occurrences, with highly inconsistent or ambiguous may have been more sensitive to relatively brief but significant stratigraphic ranges, or ranges that extend through the entire interval of interest. The final dataset contains 2,396 lowest and highest occurrences for episodes of cryospheric expansion and/or was located closer to 139 species that existed during the past 15 My. the Antarctic margin than today. To mitigate the effects of biases in the fossil record, we used the quan- We cannot identify here specific ecological or physiological titative biostratigraphic method of constrained optimization, as imple- mechanisms that drove species turnover—whether presence of mented in the computer program CONOP9 (16), to generate best-fit, seasonal ice per se, or stratification, water temperature, nutrient composite sequences or timelines of first and last appearances of species. supply, duration of growing season in open water, and so on— These composites were age-calibrated using paleomagnetic polarity reversal but all of these are strongly regulated by sea-ice extent in the data and one 40Ar/39Ar age on a volcanic tephra (Table S2). We calculated Southern Ocean, and threshold effects in response to cryospheric species-level, lineage-million-year origination and extinction rates (21), which expansion seem to have been the predominant factors in driving are insensitive to the effects of overall diversity, and from these derived + phytoplankton turnover in the Southern Ocean over the past turnover as origination extinction. To incorporate uncertainties relating to 15 Ma. Also, as noted elsewhere, we cannot yet discriminate different assumptions about the nature of biases in the fossil record and the position of the polar front through time, our final analyses were based on whether turnover was driven by regional or global extinction, and composites from three different CONOP models (Table S2 and Datasets S1–S3) in situ evolution or immigration, or the precise relative timings of that were integrated using a model ensemble procedure; at the same time, these components. We note, however, that our findings may be bootstrapping was used to capture uncertainties inherent in the selection of consistent with recent models of evolution in response to fluctu- species (details are given in Supporting Information). ating but trending global temperature change, which reproduce About half (46%) of the species included here are apparently endemic to patterns of bounded trait evolution (stasis) on short time frames the Antarctic margin and Southern Ocean (Fig. S1D). For these taxa, our with pulses of accelerated evolutionary divergence at time spans of modeled times of first and last appearance represent the best available longer than a million years (36). approximations to the true times of speciation and extinction. In contrast, The turnover pulses we document apparently were conse- the remaining species are known also from records north of the Antarctic Polar quences of cooling, but our findings suggest that Southern Ocean Front and are cosmopolitan, or restricted to southern polar to temperate or subtropical water masses, or bipolar in distribution. Their modeled times of phytoplankton communities are sensitive to large-scale changes first and last appearance may correspond, therefore, either to immigration in mean climate state driven by a combination of long-period and local extinction (e.g., ref. 5) or to true global evolution and extinction. variations in orbital forcing and atmospheric carbon dioxide Without recourse to high-resolution biogeographic and biostratigraphic data perturbations. The potential for irreversible change in these from north of the Antarctic Polar Front, we cannot discriminate between these phytoplankton communities in response to future, geologically possibilities but, as noted above, here we are focused on the timing and abrupt warming in southern high latitudes—a consequence of patterns of species turnover in the Southern Ocean region and its relationship polar amplification of global warming—remains an open question. to environmental drivers, and not on the wider biogeographic relationships This question will be addressed by a growing and diverse body of of taxa. evidence that spans geological to ecological timescales, such as ACKNOWLEDGMENTS. We gratefully acknowledge the constructive reviews data on past, regional-, and planetary-scale ecological state changes of two anonymous referees and the journal editor, all of which improved (37), ecological niche models that are informed by both theory and the final paper. We thank Peter Sadler, who developed the CONOP program, empirical observations (3, 38), observations of adaptive evolution made this freely available, and contributed advice during analysis. Scientific in phytoplankton (39, 40), and physiological experiments (41). research was supported jointly by the Sarah Beanland Memorial Scholarship (R.D.C.); New Zealand Ministry of Business, Innovation and Employment Con- Materials and Methods tract C05X1001 (to J.S.C., R.L., and R.M.); New Zealand Antarctic Research Institute Grant NZARI 2013-1 (to R.L. and R.M.); Rutherford Fellow- Our dataset was constructed from diatom occurrences recorded in 34 drill cores ship RDF-13-VUW-003 (to R.M.), and the US National Science Foundation Co- from the Antarctic margin and Southern Ocean south of the present-day operative Agreement 0342484 to the University of Nebraska–Lincoln (to D.H.).

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