Southern Ocean phytoplankton turnover in response to stepwise Antarctic 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 a

GNS Science, Lower Hutt 5040, New Zealand; bSchool of Geography, Environment and Earth Sciences, Victoria 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, which form the base of the marine food web and are a crucial element of the carbon cycle, respond to major environmental disturbance. Here, we use a new model ensemble reconstruction of diatom speciation and extinction rates to examine phytoplankton response to climate change in the southern high latitudes over the past 15 My. We identify five major episodes of species turnover (origination rate plus extinction rate) that were coincident with times of cooling in southern high-latitude climate, Antarctic ice sheet growth across the continental shelves, and associated seasonal sea-ice expansion across the Southern Ocean. We infer that past plankton turnover occurred when a warmer-than-present climate was terminated by a major period of glaciation that resulted in loss of open-ocean habitat south of the polar front, driving non-ice adapted diatoms to regional or global extinction. These findings suggest, therefore, that Southern Ocean phytoplankton communities tolerate “baseline” variability on glacial–interglacial timescales but are sensitive to large-scale changes in mean climate state driven by a combination of long-period variations in orbital forcing and atmospheric carbon dioxide perturbations. Antarctica

| diatoms | Miocene | Pliocene | phytoplankton

I

n the face of warming oceans and changing seawater chemistry and circulation, there is growing evidence of biogeographic, community, and adaptive changes in the living marine microflora (1–3). Predicting how environmental change will influence phytoplankton communities, which account for ∼50% of global primary productivity, is hampered by the large spatial scale of the forcings on the biotic system and the long response time (2). Here, we use the history of postmid-Miocene (post-15 Ma) diatoms preserved in geological archives from the Southern Ocean and Antarctic margin to reveal long-term patterns and rates of phytoplankton turnover (origination rate plus extinction rate) and to constrain interpretations of macroevolutionary processes. These floras are of critical interest today given the expected sensitivity of high-latitude ecosystems to polar amplification of climate change. Globally, diatoms are the dominant living phytoplankton group, accounting for ∼20% of primary productivity, and their macroevolutionary history is linked to changes in climate (4). Diatom species are highly endemic south of the Antarctic Polar Front, which today forms an oceanographic and biogeographic boundary (5). Within this region, there are currently two distinct biomes: a specialized flora occupying the seaice zone (6) and a high-nutrient low-chlorophyll flora occupying the open ocean (7). The climate history of the Antarctic and Southern Ocean over the past 15 My is one of stepwise cooling punctuated by transient warm periods. Highly variable ice sheets that characterized the mid-Miocene Climate Optimum (8, 9) subsequently expanded during the cooling associated with the Miocene Climate Transition ∼14 Ma (10, 11), at which time a large terrestrial ice sheet became a relatively permanent feature on the East Antarctic

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continent. Marine-based ice, grounded on bedrock below sea level in West and East Antarctica, continued to expand and contract through variable climates of the late Miocene and into the Pliocene (14–3 Ma) (12, 13), driving global sea-level fluctuations of between 20- to 30-m amplitude and up to 20 m above the present-day level (14). These marine ice sheets then stabilized as global climate cooled again in the late Pliocene and early Pleistocene (3–2.5 Ma) and perennial sea ice became a “permanent” feature in the Southern Ocean (15). The response of Southern Ocean diatoms to these major changes has been, until now, poorly resolved. To realize the potential of their rich microfossil record, it is first necessary to mitigate pervasive biases that are inherent to paleontological records (Supporting Information). To achieve this, we used a quantitative biostratigraphic method, constrained optimization [CONOP (16)] (Materials and Methods and Supporting Information), applied to a regional database of fossil species occurrences in the Southern Ocean and Antarctic margin that was drawn from 34 drill cores (17) (Fig. 1 and Table S1). Data were restricted to regions south of the present-day Antarctic Polar Front, which represents an effective biogeographic barrier to the dispersal of modern assemblages. Because of uncertainties regarding the position of this front in the past (18–20), we used alternative CONOP models based on a conservative, more southerly dataset of 27 drill cores that are situated well south of the modern front, and a less conservative dataset that included an additional seven drill cores from regions immediately south of the front. From vetted observations of local highest and lowest fossil occurrences in each drill core, CONOP produced model composite histories that were used to identify the order and timing of origination/immigration and regional extinction events for the common, Significance Based on data of unprecedented resolution, we show that phytoplankton (diatoms) in the Southern Ocean have experienced five major pulses of species extinction and origination over the past 15 My that were linked to large cooling transitions in southern high latitudes. Our findings suggest that phytoplankton communities around Antarctica have been robust to “baseline” glacial–interglacial climate variability but were sensitive to large-scale changes in mean climate state driven by a combination of long-period variations in orbital forcing and atmospheric carbon dioxide perturbations. Author contributions: J.S.C., R.D.C., and R.L. designed research; J.S.C. and R.D.C. designed and performed analyses; and J.S.C., R.D.C., R.L., D.H., R.M., and T.N. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. 1

To whom correspondence should be addressed. Email: [email protected].

2

Deceased October 4, 2015.

This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. 1073/pnas.1600318113/-/DCSupplemental.

www.pnas.org/cgi/doi/10.1073/pnas.1600318113

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). Conservatively, using three CONOP composites, we used model ensemble and bootstrapping procedures to capture uncertainties related to biogeographic constraints and varying assumptions about the nature of the fossil record, assumptions that are reflected in different CONOP compositing approaches (Supporting Information). Each model composite sequence of events produced by CONOP was dated independently to yield an average temporal resolution of ∼63,000 y (63 ky) over the study interval. This approach provides a “continuous” record of individual diatom appearance and disappearance events that is free from the biases and artificial discontinuities imposed by binning at the time resolution of zones and stages. The CONOP composites used here are given in Datasets S1–S3. We do not discriminate true global speciation and extinction of endemic species from ecologically controlled immigration and local extinction of species that are also found north of the Antarctic Polar Front, a task that would require high-resolution, global biogeographic and biostratigraphic data (Materials and Methods, and see refs. 4 and 5). For the purposes of the present study, however, we are interested in the timing and patterns of species turnover in the Southern Ocean region and, although of considerable interest, it is not essential to discriminate turnover driven by evolution/extinction from turnover driven by biogeographic changes. Results Using the ensemble of age-calibrated composite histories of diatom first and last appearances, we calculated lineage-million-year origination, extinction, and turnover (origination + extinction) rates (21) for a smoothed 200-ky moving window at 50-ky time increments since 15 Ma (Fig. 2 and Fig. S1 A–C). For comparison, Crampton et al.

the average duration of a species in our dataset is ∼7 My. This new macroevolutionary history of diatoms is an order of magnitude more finely resolved than previously available records (cf. refs. 4 and 5) and reveals hitherto unknown patterns and pulses of phytoplankton species turnover, separated by intervals of moderate to low turnover. Results are apparently unbiased by effects of drill core coverage, sampling density, or the presence of widespread hiatuses in sedimentation (Supporting Information and Figs. S2 and S3). Here, we focus on five conspicuous peaks of turnover with rates greater than 0.5 (labeled turnover pulses A–E in Fig. 2A) and explore their relationship to known paleoclimatic events. The ages of these pulses are approximately: 14.65–14.45 Ma (A), 13.75–13.55 Ma (B), 4.90–4.40 Ma (C), 3.55–3.40 Ma (D), and 3.00–1.95 Ma (E). Fig. 2 reveals that all of the turnover pulses coincide with positive excursions or maxima in benthic marine δ18O values that mark periods of global cooling and/or ice volume increase. Likewise, all except D occurred during episodes of atmospheric CO2 decline inferred from geological proxy records, although we caution that the CO2 geological proxy data are presently limited in temporal resolution and are subject to large assumptions and uncertainties (22). Turnover pulses A and B also coincide with two major middle Miocene positive excursions in δ13C, and pulses C to E align with periods of declining to low biosiliceous productivity on the Antarctic margin, represented by opal accumulation rate (MARopal). Taken together, these results suggest that the diatom turnover pulses identified here were related in some way to major global climatic and oceanographic changes, coupled to perturbations in the carbon cycle, which occurred during the middle Miocene to earliest Pleistocene. PNAS | June 21, 2016 | vol. 113 | no. 25 | 6869

EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES

Fig. 1.

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 atmospheric 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 steps within the Miocene Climate Transition, which marks progressive change from eccentricity-paced glacial–interglacial cycles to obliquity-paced cycles (11). During these cooling steps, bottom water temperatures decreased by around 3 °C and seasurface temperatures decreased by up to about 7 °C (10). At the same time, sea level dropped by between 30 and 60 m (23), consistent with expansion of a terrestrial Antarctic Ice Sheet 6870 | www.pnas.org/cgi/doi/10.1073/pnas.1600318113

across the continental shelf and into marine basins in East and West Antarctica. The presence of grounded ice on the continental shelf is indicated in the ANDRILL-1B core and by regional seismic records (9) and supported by ice-sheet-climate models (8). Model simulations also indicate that sea-ice expansion is likely to have occurred in concert with advance of grounded ice sheets onto the shelf (24). Although definitive evidence of sea ice during turnover pulses A and B is lacking, changes in diatom and Crampton et al.

foraminifera assemblages in the ANDRILL-2A core have been used to suggest that sea ice appeared after 16 Ma and became more persistent after about 15 Ma (9, 25). (We note that certain key diatom taxa used to infer the presence of sea ice in ref. 9, notably Fragilariopsis truncata and Synedropsis cheethamii, have not been consistently identified in older floral lists from the Southern Ocean and failed to meet the threshold for inclusion in the present CONOP analyses.) In addition, probable sea-ice associated Miocene diatoms have been recorded from the Ross Sea region (26, 27). Turnover pulses C and D likewise are associated with cooling episodes that culminated in deep-sea temperatures significantly colder than today (14). Evidence for the advance of grounded ice in the ANDRILL-1B core indicates that marine-based ice sheets in West Antarctica were more expansive than today, at least during the onset of pulse C (12). Whereas the onset of pulse D seems to predate significant cooling in Fig. 2C, in fact peak turnover at ∼3.4 Ma lies within the sustained, stepwise cooling trend that began at Marine Isotope Stage (MIS) MG8 at ∼3.55 Ma and persisted until MIS M2 at ∼3.3 Ma (28). The initiation of this cooling trend is coincident within uncertainty (gray region in Fig. 2A) with the onset of pulse D. Furthermore, pulse D is preceded by MIS Gi4 and Gi2, between 3.7 and 3.6 Ma, which are characterized by δ18O excursions with values that are similar to the Holocene, reflect major cooling and ice sheet advance, and may also have forced the onset of turnover. Importantly, the end of pulse D coincides with the final transition from subpolar to polar conditions on the Antarctic margin and termination of earlyto mid-Pliocene warm conditions (15, 29). Finally, the onset of turnover pulse E is associated with largescale δ18O excursions (e.g., 3.1–3.0 Ma and 2.7–2.4 Ma) and minima in deep-sea temperatures (14), a trend toward increased Antarctic summer sea-ice extent and duration (15), and stabilization of marine margins of the East Antarctic Ice Sheet by ∼2.5 Ma (30). Each of the cooling episodes described above was preceded by a warmer climate and, except in the case of turnover pulse E, followed by times of relative global warmth and high oceanic productivity, bottom-water temperature, and sea level (12, 14, 15, 23). Each successively younger “warm” interval, however, occurred on a cooler background climate state, perhaps controlled by variations in atmospheric CO2. Crampton et al.

Discussion Results from this study suggest past, region-wide sensitivity of the diatom flora to large changes in ice extent in the prePleistocene world. We propose the following model to explain this sensitivity (Fig. 3). High-latitude cooling and associated changes in atmospheric circulation, driven by global-scale processes, resulted in increased production of cold Antarctic surface waters, enhanced stratification in the Southern Ocean (31), and deepening of the pycnocline (32). These changes in ocean structure and dynamics at the Antarctic margin inhibited upwelling of warm deep water onto the continental shelf and promoted growth of perennial sea ice and expansion of winter sea ice across the Southern Ocean. We suggest that these episodes of major sea-ice expansion increased surface albedo, reduced Southern Ocean ventilation, and enhanced CO2 sequestration to the deep ocean (33), which established a positive feedback on global climate that drove major expansion of Antarctica’s ice sheets across the continental shelves. We infer that, before each of the turnover pulses discussed here, there were year-round sea-ice-free conditions in the open Southern Ocean, with well-mixed, nutrient-rich surface waters, the “Permanent Open Ocean Zone” of ref. 34 (Fig. 3A). At such times, new species were evolving in stratified coastal waters that were sea-ice-covered in winter. During significant cooling events, when winter sea ice expanded beyond the continental margin and toward the polar front, and surface waters became stratified, the open ocean environment was greatly reduced (Fig. 3B). Given that ocean frontal boundaries can represent significant biogeographic barriers (5) and that phytoplankton diversity is governed by species-area effects (35), it seems likely that loss of open-ocean habitat during these cooling events drove extinction pulses in non-ice-adapted, Southern Ocean diatoms. Throughout the mid- to late Miocene and early Pliocene, large-magnitude cooling events seem to have been paced by long-period orbital cycles and as a result were transient in nature, and thus the forcing of species evolution and community adjustment by each new climatic regime was short-lived. However, long-term cooling, especially after 5 Ma, resulted in the incremental and stepwise evolution of endemic, ice-adapted diatoms that are a dominant component of the flora today (Supporting Information and Fig. S1D). Based on evidence available to date, the model proposed above is supported PNAS | June 21, 2016 | vol. 113 | no. 25 | 6871

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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, representative 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, Antarctic bottom water; ASW, Antarctic surface water; PF, polar front; UDW, upper deep water; WDW, warm deep water (red, relatively warmer; green, relatively cooler).

most strongly for turnover pulses C to E. We argue that the model would still have operated during times of lesser sea-ice extent— perhaps pulses A and B—when the entire biogeographic system may have been more sensitive to relatively brief but significant episodes of cryospheric expansion and/or was located closer to the Antarctic margin than today. We cannot identify here specific ecological or physiological mechanisms that drove species turnover—whether presence of seasonal ice per se, or stratification, water temperature, nutrient supply, duration of growing season in open water, and so on— but all of these are strongly regulated by sea-ice extent in the Southern Ocean, and threshold effects in response to cryospheric expansion seem to have been the predominant factors in driving phytoplankton turnover in the Southern Ocean over the past 15 Ma. Also, as noted elsewhere, we cannot yet discriminate whether turnover was driven by regional or global extinction, and in situ evolution or immigration, or the precise relative timings of these components. We note, however, that our findings may be consistent with recent models of evolution in response to fluctuating but trending global temperature change, which reproduce patterns of bounded trait evolution (stasis) on short time frames with pulses of accelerated evolutionary divergence at time spans of longer than a million years (36). The turnover pulses we document apparently were consequences of cooling, but our findings suggest that Southern Ocean phytoplankton communities are sensitive to large-scale changes in mean climate state driven by a combination of long-period variations in orbital forcing and atmospheric carbon dioxide perturbations. The potential for irreversible change in these phytoplankton communities in response to future, geologically abrupt warming in southern high latitudes—a consequence of polar amplification of global warming—remains an open question. This question will be addressed by a growing and diverse body of evidence that spans geological to ecological timescales, such as data on past, regional-, and planetary-scale ecological state changes (37), ecological niche models that are informed by both theory and empirical observations (3, 38), observations of adaptive evolution in phytoplankton (39, 40), and physiological experiments (41).

Antarctic Polar Front (Fig. 1 and Table S1). All data were vetted before analysis, to eliminate records that may have been reworked, and species with fewer than three occurrences, with highly inconsistent or ambiguous stratigraphic ranges, or ranges that extend through the entire interval of interest. The final dataset contains 2,396 lowest and highest occurrences for 139 species that existed during the past 15 My. To mitigate the effects of biases in the fossil record, we used the quantitative biostratigraphic method of constrained optimization, as implemented in the computer program CONOP9 (16), to generate best-fit, composite sequences or timelines of first and last appearances of species. These composites were age-calibrated using paleomagnetic polarity reversal data and one 40Ar/39Ar age on a volcanic tephra (Table S2). We calculated species-level, lineage-million-year origination and extinction rates (21), which are insensitive to the effects of overall diversity, and from these derived turnover as origination + extinction. To incorporate uncertainties relating to 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 composites from three different CONOP models (Table S2 and Datasets S1–S3) that were integrated using a model ensemble procedure; at the same time, bootstrapping was used to capture uncertainties inherent in the selection of species (details are given in Supporting Information). About half (46%) of the species included here are apparently endemic to the Antarctic margin and Southern Ocean (Fig. S1D). For these taxa, our modeled times of first and last appearance represent the best available approximations to the true times of speciation and extinction. In contrast, the remaining species are known also from records north of the Antarctic Polar Front and are cosmopolitan, or restricted to southern polar to temperate or subtropical water masses, or bipolar in distribution. Their modeled times of first and last appearance may correspond, therefore, either to immigration and local extinction (e.g., ref. 5) or to true global evolution and extinction. Without recourse to high-resolution biogeographic and biostratigraphic data from north of the Antarctic Polar Front, we cannot discriminate between these possibilities but, as noted above, here we are focused on the timing and patterns of species turnover in the Southern Ocean region and its relationship to environmental drivers, and not on the wider biogeographic relationships of taxa.

Our dataset was constructed from diatom occurrences recorded in 34 drill cores from the Antarctic margin and Southern Ocean south of the present-day

ACKNOWLEDGMENTS. We gratefully acknowledge the constructive reviews of two anonymous referees and the journal editor, all of which improved the final paper. We thank Peter Sadler, who developed the CONOP program, made this freely available, and contributed advice during analysis. Scientific research was supported jointly by the Sarah Beanland Memorial Scholarship (R.D.C.); New Zealand Ministry of Business, Innovation and Employment Contract 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 Discovery Fellowship RDF-13-VUW-003 (to R.M.), and the US National Science Foundation Cooperative Agreement 0342484 to the University of Nebraska–Lincoln (to D.H.).

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