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DOI: 10.1126/science.1246172 , 84 (2014); 344 Science et al. Yi Ge Zhang A 12-Million-Year Temperature History of the Tropical Pacific Ocean This copy is for your personal, non-commercial use only. clicking here. colleagues, clients, or customers by , you can order high-quality copies for your If you wish to distribute this article to others here. following the guidelines can be obtained by Permission to republish or repurpose articles or portions of articles ): April 3, 2014 www.sciencemag.org (this information is current as of The following resources related to this article are available online at http://www.sciencemag.org/content/344/6179/84.full.html version of this article at: including high-resolution figures, can be found in the online Updated information and services, http://www.sciencemag.org/content/suppl/2014/04/02/344.6179.84.DC1.html can be found at: Supporting Online Material http://www.sciencemag.org/content/344/6179/84.full.html#related found at: can be related to this article A list of selected additional articles on the Science Web sites http://www.sciencemag.org/content/344/6179/84.full.html#ref-list-1 , 9 of which can be accessed free: cites 32 articles This article http://www.sciencemag.org/content/344/6179/84.full.html#related-urls 1 articles hosted by HighWire Press; see: cited by This article has been http://www.sciencemag.org/cgi/collection/oceans Oceanography subject collections: This article appears in the following registered trademark of AAAS. is a Science 2014 by the American Association for the Advancement of Science; all rights reserved. The title Copyright American Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by the Science on April 3, 2014 www.sciencemag.org Downloaded from on April 3, 2014 www.sciencemag.org Downloaded from on April 3, 2014 www.sciencemag.org Downloaded from on April 3, 2014 www.sciencemag.org Downloaded from on April 3, 2014 www.sciencemag.org Downloaded from

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DOI: 10.1126/science.1246172, 84 (2014);344 Science et al.Yi Ge Zhang

A 12-Million-Year Temperature History of the Tropical Pacific Ocean

This copy is for your personal, non-commercial use only.

clicking here.colleagues, clients, or customers by , you can order high-quality copies for yourIf you wish to distribute this article to others

  here.following the guidelines

can be obtained byPermission to republish or repurpose articles or portions of articles

  ): April 3, 2014 www.sciencemag.org (this information is current as of

The following resources related to this article are available online at

http://www.sciencemag.org/content/344/6179/84.full.htmlversion of this article at:

including high-resolution figures, can be found in the onlineUpdated information and services,

http://www.sciencemag.org/content/suppl/2014/04/02/344.6179.84.DC1.html can be found at: Supporting Online Material

http://www.sciencemag.org/content/344/6179/84.full.html#relatedfound at:

can berelated to this article A list of selected additional articles on the Science Web sites

http://www.sciencemag.org/content/344/6179/84.full.html#ref-list-1, 9 of which can be accessed free:cites 32 articlesThis article

http://www.sciencemag.org/content/344/6179/84.full.html#related-urls1 articles hosted by HighWire Press; see:cited by This article has been

http://www.sciencemag.org/cgi/collection/oceansOceanography

subject collections:This article appears in the following

registered trademark of AAAS. is aScience2014 by the American Association for the Advancement of Science; all rights reserved. The title

CopyrightAmerican Association for the Advancement of Science, 1200 New York Avenue NW, Washington, DC 20005. (print ISSN 0036-8075; online ISSN 1095-9203) is published weekly, except the last week in December, by theScience

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A 12-Million-Year Temperature Historyof the Tropical Pacific OceanYi Ge Zhang,1* Mark Pagani,1 Zhonghui Liu2

The appearance of permanent El Niño–like conditions prior to 3 million years ago is foundedon sea-surface temperature (SST) reconstructions that show invariant Pacific warm pooltemperatures and negligible equatorial zonal temperature gradients. However, only a few SSTrecords are available, and these are potentially compromised by changes in seawater chemistry,diagenesis, and calibration limitations. For this study, we establish new biomarker-SST recordsand show that the Pacific warm pool was ~4°C warmer 12 million years ago. Both the warmpool and cold tongue slowly cooled toward modern conditions while maintaining a zonaltemperature gradient of ~3°C in the late Miocene, which increased during the Plio-Pleistocene.Our results contrast with previous temperature reconstructions that support the supposition of apermanent El Niño–like state.

Temperatures of the low-latitude PacificOcean substantially influence regional andglobal climates. In particular, the El Niño–

Southern Oscillation (ENSO) dominates Earth’sinterannual climate variability. El Niño is initiatedby the eastward propagation of warm westernPacific equatorial waters that deepen thermoclinedepths and attenuate upwelling rates across theeastern equatorial Pacific (EEP) (1, 2). Region-al sea-surface temperature (SST) change associ-ated with El Niño affects the position and vigorof theWalker circulation andHadley cell, leadingto substantially reduced equatorial SST gradients,higher global mean temperatures, extratropicalheat export, and regional hydrological impacts(1, 2).

The western equatorial Pacific warm pool isamong the warmest surface water on Earth,whereas the EEP, known as the cold tongue, ischaracterized by cold, nutrient-rich waters thatresult from a shallow thermocline and intenseupwelling rates. The modern SST gradient be-tween the warm pool and cold tongue averages4° to 5°C (3) and varies in response to ENSO.Accordingly, paleo-SSTreconstructions from theseregions and the resulting character of the east-west temperature gradient have been used to de-scribe broad climate states over the past 5 millionyears, particularly during the Pliocene epoch [5.3to 2.6million years ago (Ma)], when atmosphericCO2 concentrations appear similar to today (4, 5)and global temperatures are simulated to be 3° to4°C warmer than preindustrial conditions (6, 7).

Published temperature records based onmagnesium-to-calcium ratios (Mg/Ca) of theplanktonic foraminifera Globoritalia sacculifer,from Ocean Drilling Program (ODP) site 806(0°N, 159°E) (Fig. 1) (8), suggest that warm pooltemperatures remained relatively constant as Earthcooled over the past 5 million years. Curiously,existing Mg/Ca-based SST records also indicatethat the Pacific warm pool of the Pliocene warm

period (4.5 to 3 Ma) was ~0.5°C colder thanthe mean temperature of the late Quaternary (1.5to 0 Ma), implying that warm pool temperatureswere cooler or invariant during periods of globalwarmth. The appearance of invariant tropical tem-peratures during periods of global warmth impliesa “tropical thermostat” (9) in which tropical warm-ing is limited through evaporation or cloud feed-backs irrespective of the greenhouse gas forcing.However, this phenomenon is not supported byclimate simulations (10), and much warmer trop-ical SSTs are evident during “super greenhouse”climate states in Earth history (e.g., the Creta-ceous) (11).

In contrast to the western Pacific warm pool,temperature records from the eastern Pacific sites

847 (0°N, 95°W; based onMg/Ca and the alkenoneunsaturation index UK ′

37 ) (8, 12) and 846 (3°S,91°W; based on UK ′

37 ) (13) exhibit cooling for thepast 5 million years. Consequently, warm pooland cold tongue SSTs result in a negligible equa-torial temperature gradient during the early Plio-cene (8, 14) similar to those expressed duringbrief modern El Niño events (8, 14). A nearlyabsent equatorial temperature gradient is arguedto reflect a permanent El Niño–like state prior to3million years ago and has been further interpretedto reflect the establishment of a deep thermoclinein the EEP, substantially reduced cold-water up-welling (14), an attenuatedWalker circulation (7),and negligible ENSO variability (14). In contrast,high-resolution, coral d18O records (15) and iso-tope records of individual planktonic foraminiferafrom site 846 (16) indicate that the frequencyand intensity of Pliocene ENSO-like oscillationswere similar to those of today.

The veracity of the permanent El Niño sup-position rests on the accuracy of paleotempera-ture reconstructions. In particular, G. sacculiferMg/Ca-based SST records used to infer invariantwarm pool SSTs assume that foraminiferaMg/Cacompositions are uninfluenced by diageneticalteration or temporal changes in seawater chem-istry [e.g., seawater Mg/Ca ratio (Mg/Casw)]and/or carbonate ion effect; see supplementarymaterials). However, d18O records on the identicalsamples (8) fail to capture the modern SST gra-dient (supplementary materials) and suggest thecontribution of diagenetic carbonates. In addition,changes inMg/Casw could have lowered Pliocene

1Department of Geology and Geophysics, Yale University, NewHaven, CT 06511, USA. 2Department of Earth Sciences, TheUniversity of Hong Kong, Hong Kong SAR, China.

*Corresponding author. E-mail: [email protected]

Sea

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(°C

)

60°N

30°N

EQ

30°S

60°S

Fig. 1. Pacific sites discussed in this study. Colors represent modern mean annual SSTs. Circlesrepresent sites analyzed in this study: ODP sites 769, 806, 850, and 1143. Triangles represent sites withpreviously published SSTs: ODP sites 846, 847, and 1208 (36°N, 128°E) and Integrated Ocean DrillingProgram (IODP) site U1338 (3°N, 118°W). Map generated by Ocean Data View.

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SST estimates because fluid inclusion (17) andcarbonate veins (18) data indicate lower Mg/Caswduring the Pliocene. Notably, other warm pooltemperature records derived fromUK ′

37 values (19)are limited by the nature of the temperature proxyitself, which reaches a maximum calculable SSTvalue of ~28.5°C (20) and thus compromises itscapacity to record even higher SSTs (supplemen-tary materials).

In summary, given possible diagenetic over-printing, seawater chemistry changes, and cali-bration limitations, available SST records likelyunderestimate maximum warm pool temperaturesand potentially distort zonal SSTgradient estimates.

For this study, we established new equatorialPacific SST records using the TEX86 temperatureproxy. TEX86 thermometry is founded on the dis-tribution of the archaeal lipid membranes, glycer-ol dialkyl glycerol tetraethers, primarily producedby archaea from the phylum Thaumarchaeota.Thaumarchaeota are aerobic ammonia oxidizers(21), raising concerns that the TEX86 index canalso reflect subsurface temperatures rather than amixed-layer SST. However, available compound-specific carbon-isotope evidence indicates that theTEX86 temperature signal largely derives fromthe ocean mixed-layer (22). Using the current cal-ibration [e.g., (23)], TEX86 tends to overestimateSSTs in the high latitudes and underestimatetemperatures in the low latitudes (24). Indeed,TEX86 SSTs derived from surface sediments ofthe tropical Pacific show slightly lower tem-perature estimates than observed SSTs (see sup-

plementary materials). Nevertheless, the latePleistocene TEX86-derived zonal SST gradientagrees with the modern gradient between sites806 and 850 (supplementary materials) andbroadly captures the temperature characteristicsof these distinct regions. Finally, TEX86 temper-ature reconstructions can record much higherSSTs compared to the alkenone proxy (25),making it a more suitable proxy to evaluate theevolution of warm pool temperatures.

We reconstruct the history of equatorial Pa-cific temperature gradients for the past 12 millionyears using both TEX86 and UK ′

37 temperatureproxies at ODP sites 769 (9°N, 121°E), 806, and1143 (9°N, 113°E) in the western warm pool re-gion and site 850 (1°N, 111°W) in the easternPacific cold tongue (Fig. 1). Our results illustratea distinctly different thermal history of the Pacificwarm pool compared to previously published re-cords. For example, in contrast to relatively in-variantMg/Ca temperatures from site 806 (Fig. 2),TEX86 records from three localities near the cen-ter and edge of the modern warm pool unam-biguously show ~4°C of cooling since the lateMiocene (Fig. 3), with an ~2°C decline since theearly Pliocene (Fig. 2). TEX86 values from thelate Miocene to Pliocene also indicate that warmpool temperatures were almost always higherthan the calculable limit of UK ′

37 temperaturesuntil ~3-5 million years ago. Consequently, UK ′

37temperatures cannot be applied to interpret thetemperature history of the warm pool older than~3 Ma (Figs. 2 and 3).

Cold tongue UK ′

37 temperatures from site 850in the western portion of the eastern equatorialupwelling region (Fig. 1) compare well with pub-lished alkenone records from sites 846 (13) and847 (12) over the past 5 million years (Fig. 3). SiteU1338 shows comparativelywarmer temperatures(26), consistent with its location at the edge of theupwelling region (Fig. 1). Both TEX86 and UK ′

37temperature reconstructions in the EEP regionindicate that the cold tongue slowly cooled by~6°C since 12 Ma, with higher cooling ratesduring the Pliocene and Pleistocene. TEX86 andUK ′

37 temperature estimates begin to deviate at about6 Ma, with TEX86 SSTs showing consistentlycooler temperatures, readily explained by differ-ential changes in the depth and/or seasonality ofproduction between haptophyte algae (alkenoneproducers) and archaea (supplementarymaterials).If changes in production depth are responsible forthe temperature offset between these two proxies,production of archaea and haptophytes is stillwithin the top 50 m of the mixed layer given thesharp vertical temperature gradient in the EEP(supplementary materials). Although sites 850and U1338 represent the warmer edge of theEEP, alkenone values are still below themaximumtemperature limit for 12 million years (Fig. 3)—incontrast to UK ′

37 temperatures in the western warmpool—and thus can record the cooling history ofthe EEP (Fig. 2 and supplementary materials).

We assess the evolution of the east-westequatorial Pacific temperature gradient (DTzonal)by interpolating and averaging temperature re-sults using TEX86 and UK ′

37 temperature records,and solely using TEX86 data (Fig. 4). Integratingall of the available SST data expands the spatialassessment for each region. However, becauseUK ′

37 is mostly maximized in warm pool samplesolder than 3 Ma, warm pool temperature recon-structions largely rest on TEX86 SST recordsprior to 3 Ma (Figs. 2 and 3). In contrast, the com-posite temperature of the cold tongue is dominatedby UK ′

37 records (Figs. 2 and 3). At our localities,TEX86 values tend to yield lower temperatureestimates than UK ′

37 when both are available (Figs.2 and 3 and supplementary materials). As a re-sult, our SST trends from the integrated data setoften yield lower average temperatures in thewarmpool, higher temperatures in the cold tongue, anda smaller DTzonal relative to estimates that onlyuse our TEX86 records (Fig. 4 and supplementarymaterials). For example, the Pliocene DTzonalshows a range of 3.2°C (total data set) to 4.1°C(based solely on TEX86 data; see supplementarymaterials).

Averaging DTzonal data over the Quaternary(2.6 to 0 Ma), Pliocene (5.3 to 2.6 Ma), and lateMiocene (12 to 5.3Ma) indicates that about 60 to70% of the Quaternary DTzonal is expressed in thelate Miocene, whereas ~80% of the QuaternaryDTzonal characterizes the Pliocene and thus close-ly reflectsmodern oceanographic conditions (sup-plementarymaterials). Notably, our records indicatethat both the warm pool and the cold tongue werewarmer in the past, but that a cold EEP (relative

Fig. 2. SST reconstructions of the Pacific warm pool for the past 5Ma.Mg/Ca temperatures do notaccount for changes in seawater Mg/Ca (8). Dashed line denotes the maximum calculable temperature(~28.5°C) of the U37

K′ calibration. Calibration errors for U37K ′ (20) and TEX86 (23) are 1.1° and 2.5°C,

respectively, but vary spatially (24). Warm pool temperature trend is calculated with all TEX86-derived SSTsand U37

K ′ temperatures after 3 Ma. U37K′- SST records from site 806 (5 to 0 Ma) (4) and 1143 (4 to 0 Ma) (34)

are previously published.

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to the warm pool) was present. Thus, the ocean-ographic processes that produce the modern coldtongue, including a shallow EEP thermocline andactive upwelling, were likely in play—consistentwith high rates of biogenic opal accumulation inthe EEPduring the lateMiocene and Pliocene (27).

A late Miocene–Pliocene climate state char-acterized by strong temperature asymmetry acrossthe equatorial Pacific provides the necessary con-

ditions for robust ENSO-type interannual climatevariability but does not directly prove its exis-tence. Regardless, our temperature reconstructionssupport other proxy records (15, 16) and climatesimulations (28, 29) that indicate ENSO-like be-havior during the Pliocene and beyond (30).

Today, waters of the Equatorial Undercurrentthat source upwelled waters in the eastern equa-torial Pacific derive from the extratropics and

higher latitudes, including the Subantarctic modewater (31). Geochemical tracers, drifter experi-ments, and climate simulations (32) indicate thatwaters from the eastern, subtropical Pacific sub-duct and resurface in the EEP thermocline withintwo decades. Indeed, the linkage between theeastern equatorial Pacific and anomalously warmwaters from higher latitudes was used to explaina period of prolonged warming of the EEP in theearly 1990s (32). Similarly, during the lateMioceneto Pliocene, warmer extratropical waters (7, 33)(Fig. 4) that sourced the EEP likely contributed areduction in DTzonal. As meridional temperaturegradients increased during global cooling, colderextratropical water contributed to EEP coolingand an increase in DTzonal (Fig. 4).

Given the areal extent of tropical warm poolsand their importance in regulating global temper-atures, our new warm pool temperature recordssubstantially revise the character and nature ofglobal warming in the recent past.

References and Notes1. M. J. McPhaden, S. E. Zebiak, M. H. Glantz, Science 314,

1740–1745 (2006).2. P. Molnar, M. A. Cane, Paleoceanography 17,

11-1–11-11 (2002).3. K. B. Karnauskas, R. Seager, A. Kaplan, Y. Kushnir,

M. A. Cane, J. Clim. 22, 4316–4321 (2009).4. M. Pagani, Z. H. Liu, J. LaRiviere, A. C. Ravelo, Nat. Geosci.

3, 27–30 (2010).5. O. Seki et al., Earth Planet. Sci. Lett. 292, 201–211

(2010).6. D. J. Lunt et al., Nat. Geosci. 3, 60–64 (2010).7. C. M. Brierley et al., Science 323, 1714–1718 (2009).8. M. W. Wara, A. C. Ravelo, M. L. Delaney, Science 309,

758–761 (2005).9. V. Ramanathan, W. Collins, Nature 351, 27–32 (1991).

10. I. N. Williams, R. T. Pierrehumbert, M. Huber,Geophys. Res. Lett. 36, L21805 (2009).

11. M. Pagani, M. Huber, B. Sageman, in Treatise onGeochemistry, H. D. Holland, K. K. Turekian, Eds.(Elsevier, Oxford, 2014), pp. 281–304.

12. P. S. Dekens, A. C. Ravelo, M. D. McCarthy,Paleoceanography 22, PA3211 (2007).

13. K. T. Lawrence, Z. Liu, T. D. Herbert, Science 312, 79–83(2006).

14. A. V. Fedorov et al., Science 312, 1485–1489 (2006).15. T. Watanabe et al., Nature 471, 209–211 (2011).16. N. Scroxton et al., Paleoceanography 26, PA2215

(2011).17. T. K. Lowenstein, M. N. Timofeeff, S. T. Brennan,

L. A. Hardie, R. V. Demicco, Science 294, 1086–1088(2001).

18. R. M. Coggon, D. A. H. Teagle, C. E. Smith-Duque,J. C. Alt, M. J. Cooper, Science 327, 1114–1117 (2010).

19. A. V. Fedorov et al., Nature 496, 43–49 (2013).20. M. Conte et al., Geochem. Geophys. Geosyst. 7, Q02005

(2006).21. M. Könneke et al., Nature 437, 543–546 (2005).22. S. G. Wakeham, C. M. Lewis, E. C. Hopmans, S. Schouten,

J. S. Sinnighe Damsté, Geochim. Cosmochim. Acta 67,1359–1374 (2003).

23. J. H. Kim et al., Geochim. Cosmochim. Acta 74,4639–4654 (2010).

24. J. E. Tierney, M. P. Tingley, Geochim. Cosmochim. Acta127, 83–106 (2014).

25. S. Schouten, A. Forster, F. E. Panoto, J. S. Sinnighe Damste,Org. Geochem. 38, 1537–1546 (2007).

26. G. Rousselle, C. Beltran, M.-A. Sicre, I. Raffi,M. De Rafelis, Earth Planet. Sci. Lett. 361, 412–421 (2013).

27. J. W. Farrell et al., in Proceedings of the Ocean DrillingProgram, Scientific Results, N. Pisias, L. Mayer,T. Janecek, A. Palmer-Julson, T. H. van Andel, Eds. (OceanDrilling Program, College Station, TX, 1995), vol. 138.

Fig. 4. Zonal (DTzonal) and meridional (DTmeridional) temperature gradients of the Pacific Oceanfor the past 12million years. Zonal gradient is computed with both U37

K ′ and TEX86 data, and with TEX86data only. Meridional gradient is calculated between sites 806 and 1208 (33). Fifty-point Savitzky-Golaysmoothing has been applied to the raw data. Note the different scales for DTzonal and DTmeridional.

Age (Ma)

SS

T(°

C)

U

Lim

itK

'

37

18

20

22

24

26

28

30

32

806 TEX86

806 UK’37

1143 UK’37

1143 TEX86

769 TEX86

850 UK’37

850 TEX86

846 UK’37

847 UK’37

U1338 UK’37

37769 UK’

1143 UK’37

WEP Trend EEP Trend

0 1 2 3 4 5 6 7 8 9 10 11 12

Fig. 3. Temperature evolution of the western and eastern equatorial Pacific since 12 Ma. Allpublished data [U37

K ′ from sites 806 (5 to 0Ma) (4); 846 (5 to 0Ma) (13); 847 (5 to 0Ma) (12); 1143 (4 to 0Ma)(34); and U1338 (12 to 0 Ma) (26)] are converted to temperature with the calibration of Conte et al. (20)for U37

K′ and Kim et al. (23) for TEX86. Western equatorial Pacific (WEP) temperature trend is calculated withall TEX86 from sites 769, 806, and 1143. U37

K ′ records fromODP sites 806 and 1143 are also applied for thepast 3 Ma. U37

K′ data before 3 Ma, shown in gray, are mostly maximized and are not included in trendcalculations. Temperature trend in the eastern equatorial Pacific (EEP) is calculated with U37

K′ values fromsites 846, 847, 850, and U1338 and with TEX86 results from site 850.

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28. A. M. Haywood, P. J. Valdes, V. L. Peck,Paleoceanography 22, PA1213 (2007).

29. A. S. von der Heydt, A. Nnafie, H. A. Dijkstra, Clim. Past7, 903–915 (2011).

30. S. Galeotti et al., Geology 38, 419–422 (2010).31. J. R. Toggweiler, K. Dixon, W. S. Broecker, J. Geophys.

Res. 96 (C11), 20467 (1991).32. D. Gu, S. G. H. Philander, Science 275, 805–807 (1997).33. J. P. LaRiviere et al., Nature 486, 97–100 (2012).34. L. Li et al., Earth Planet. Sci. Lett. 309, 10–20 (2011).

Acknowledgments: We thank M. Huber, H. Dijkstra, G. Foster,A. von der Heydt, M. Leckie, P. Hull, H. Spero, J. Zachos,A. Ravelo, A. Fedorov, and S. Hu for helpful discussions andfour anonymous reviewers for their thoughtful reviews. Thisresearch used samples and data provided by the IntegratedOcean Drilling Program (IODP). Funding for this research wasprovided by NSF AGS 1203163 (to M.P.) and a SchlangerOcean Drilling Fellowship (to Y.G.Z.), which is part of theNSF-sponsored U.S. Science Support Program for IODP that isadministered by the Consortium for Ocean Leadership, Inc.

Supplementary Materialswww.sciencemag.org/content/344/6179/84/suppl/DC1Materials and MethodsFigs. S1 to S7Tables S1 to S4ReferencesDatabase S1

18 September 2013; accepted 14 February 201410.1126/science.1246172

Construction of a VertebrateEmbryo from Two OpposingMorphogen GradientsPeng-Fei Xu,* Nathalie Houssin,* Karine F. Ferri-Lagneau,*† Bernard Thisse, Christine Thisse‡

Development of vertebrate embryos involves tightly regulated molecular and cellular processesthat progressively instruct proliferating embryonic cells about their identity and behavior. Whereasnumerous gene activities have been found to be essential during early embryogenesis, little isknown about the minimal conditions and factors that would be sufficient to instruct pluripotentcells to organize the embryo. Here, we show that opposing gradients of bone morphogeneticprotein (BMP) and Nodal, two transforming growth factor family members that act as morphogens,are sufficient to induce molecular and cellular mechanisms required to organize, in vivo orin vitro, uncommitted cells of the zebrafish blastula animal pole into a well-developed embryo.

The formation of vertebrate embryos de-pends on the activity of an organizing cen-ter, corresponding to the dorsal blastopore

lip in amphibians and known as the Spemann-Mangold or dorsal organizer (1). When graftedventrally into a host, this organizer results in theformation, at the site of the graft, of a secondaryembryonic axis. The molecular nature of the ac-tivity carried by this dorsal tissue has been iden-tified (2), and its main components are dorsallysecreted factors that act as antagonists of ventralmorphogens and help to establish a ventral-to-dorsal gradient of their activity (fig. S1A). How-ever, when placed in a neutral environment suchas the blastula animal pole, the Spemann orga-nizer has very limited organizing activity, leadingonly to induction of axial mesendodermal tis-sues (3).

We previously established that, in zebrafish,the organizing activities controlling the develop-ment of the embryo are not restricted to the dorsalorganizer but are distributed all along the em-bryonic margin (3, 4) and result from the com-bined activity of two signaling pathways: bonemorphogenetic protein (BMP) and Nodal. Wefound that the organizing activity of each portionof the embryonic margin varies depending on theBMP/Nodal ratio of activities (fig. S1B): A highBMP/Nodal ratio organizes the tail; a low BMP/Nodal ratio organizes the posterior head, whereas

intermediate ratios of activity induce formationof the trunk (4). Based on these observations, wehypothesized that exposing uncommitted embry-onic cells to a continuous variation of BMP/Nodal ratios may be sufficient to organize a com-plete embryonic axis (fig. S1C).

To test this hypothesis, we engineered op-posing gradients of BMP and Nodal by injectingtheir corresponding mRNAs, at the 128-cell stage,into two different animal pole blastomeres thatgive rise to distinct clones of cells secreting thesefactors (Fig. 1A). The animal pole of the blastulawas chosen as the territory to instruct because itcontains all elements necessary to mediate the mo-lecular and cellular responses to BMP and Nodalstimulation (3, 4). Additionally, because the ani-mal pole is distant from the margin, the influenceof the primary axis and of maternal determinantsis expected to be minimal.

In support of our hypothesis, these two se-creting centers organize the animal pole cells (seesupplementary materials and methods) into a sec-ondary embryonic axis that forms at the animalpole (Fig. 1, B to E), solely from animal pole cells(fig. S2). These ectopic axes contain tissues andorgans present in the primary axis and extendfrom the forebrain to the tip of the tail (Fig. 1B).Inmost cases, the primary and secondary axes fusein the cephalic region, where animal pole cellsare recruited by both growing structures. How-ever, in some cases (1.3%; n = 1012 embryos),clones are in such a position that the two em-bryonic axes do not fuse (Fig. 1, C to E), witheach displaying a forebrain, eyes, and a beatingheart and exhibiting spontaneous myotomal con-tractions indicative of a functional nervous system(movie S1). Although the antero-posterior (A-P)

axis of the primary embryo always parallels theanimal-vegetal (An-Vg) axis of the egg, we foundno correlation between the An-Vg axis of the eggand the A-P axis of the secondary embryo, whichcan be parallel, perpendicular, or even antipar-allel to the A-P axis of the primary embryo and,therefore, to the An-Vg axis of the egg (Fig. 1, Cto E). This demonstrates that, in zebrafish, thereis no intrinsic information present in the egg orin the early embryo determining the orientationof the A-P axis that cannot be reversed by ap-plication of appropriate signals.

To understand the relative contribution of thetwo signaling pathways to the organization of thesecondary embryonic axis, we examined the con-sequence of adding BMP or Nodal individually.At the blastula stage, BMP signaling is alreadyactive at the animal pole (5); adding more BMPto this region has very little effect (fig. S3). Con-versely, at the blastula stage, stimulating the ani-mal pole with Nodal results in a thickening of theanimal pole blastoderm (Fig. 2A). At the onset ofgastrulation, the central part of the resulting pro-trusion internalizes (Fig. 2, B and C), forming ablastopore with a circular, radially symmetricalblastopore lip where mesodermal cells involute(movie S2).

At blastula and gastrula stages, epiboly dis-perses cells of the animal pole over the ectoderm.However, in the presence of a Nodal-expressingclone, the surrounding animal pole cells do notspread but converge toward the center of theNodal-secreting source (fig. S4). It is known thatthe guidance cues for convergence movementsin the zebrafish gastrula are controlled by januskinase/signal transducer and activator of transcrip-tion 3 (JAK/STAT3) signaling (6, 7). Activation ofSTAT3 is independent of Nodal signaling butdependent on the maternal b-catenin signalingpathway (6). Because ectopic Nodal signaling in-duces an attracting center at the animal pole, wehypothesized that STAT3may be activated in thatdomain. Consistent with this, in STAT3morphantembryos, ectopic Nodal signaling fails to induceradial convergence movements, whereas internal-ization of the mesendoderm is not affected (Fig.2D). Furthermore, Nodal induction of expressionof liv1 (Fig. 2E), a downstream target of STAT3(8), is abolished in STAT3 morphant embryos(Fig. 2F), demonstrating that although Nodal isnot required for activation of STAT3 in the dorsaldomain of the blastula (7), it is sufficient to in-duce this activation at the animal pole.

In zebrafish, Nodal is known to be essentialfor inducing the organizing activity carried by the

Department of Cell Biology, University of Virginia, Charlottesville,VA 22908, USA.

*These authors contributed equally to this work.†Present address: Biomedical/Biotechnology Research In-stitute, North Carolina Central University, Kannapolis, NC28081, USA.‡Corresponding author. E-mail: [email protected]

www.sciencemag.org SCIENCE VOL 344 4 APRIL 2014 87

REPORTS

www.sciencemag.org/344/6179/84/suppl/DC1

Supplementary Materials for A 12-Million-Year Temperature History of the Tropical Pacific Ocean

Yi Ge Zhang,* Mark Pagani, Zhonghui Liu

*Corresponding author. E-mail: [email protected]

Published 4 April 2014, Science 344, 84 (2014)

DOI: 10.1126/science.1246172

This PDF file includes:

Materials and Methods Supplementary Text Figs. S1 to S7 Tables S1 to S4 Caption for database S1 References

Other Supplementary Material for this manuscript includes the following: (available at www.sciencemag.org/344/6179/84/suppl/DC1)

Database S1: TEX86- and 37UK ′ -SSTs at ODP Site 769, 806, 850 and 1143, and the equatorial Pacific zonal temperature gradient for the past 12 million years.

2

Materials and Methods

Summary and chronology for Sites 769, 806, 850 and 1143

Sites 769 (Sulu Sea) and 1143 (South China Sea) are located in the marginal seas of

the western Pacific, whereas Pacific Ocean Site 806 is from the Ontong Java plateau of

the open Pacific Ocean. Hole 769B is about 290 m in length and spans the Neogene (1).

The upper Pliocene to Holocene section is a mixture of pelagic biogenic carbonate

sediment and hemipelagic clay. Sediments are primarily clay from the middle Miocene to

upper Pliocene, with minor marls and silts. Hole 1143C is 500 m long and ranges from

the late Miocene to Pleistocene. This core represents continuous hemipelagic

sedimentation of fine-grained terrigenious material and calcareous nannofossils (2). Hole

806B is ~743 m, includes the lowermost Miocene, and composed of foraminifer

nannofossil ooze and chalk to nannofossil ooze and chalk with foraminifers (3). Site 850

is from the eastern equatorial Pacific (EEP), ~400 m deep, captures the middle Miocene

to Pleistocene, and is comprised of nannofossil ooze with varying proportions of other

microfossil constituents (4).

Sample ages were determined by interpolating sample depth to the established

chronology framework detailed in Table S2. Absolute age determinations were calibrated

to the Geomagnetic Polarity Time Scale (GPTS) of Berggren et al. (5, 6). Age data of the

SST time-series from Sites 846 (7),847 (8), 1208 (9) and U1338 (10) derive from their

original publications.

For the past 12 million years, the geographic location of our studied sites moved due

to plate tectonics. The impact of this effect on the paleotemperature records, however, is

difficult to specifically assess. Nevertheless, our multi-site approach demonstrates that

this effect is likely small. For example, Site 850 is currently north of the equator (~1°N)

and reconstructions indicate that it was slightly south of the equator at 5 Ma (4). However,

the record from Site 850 compares well with that from Site 846 (~3°S), which

probably remained in its current position for the entire 5 million years (7).

Lipid extraction and analyses

Sediment samples (30-80g) from Sites 769, 806, 850 and 1143 were freeze-dried

and subject to total lipid extraction using a Dionex ASE 300 extractor with 2:1 (v/v)

dichloromethane/methanol. Total lipid extracts (TLEs) were concentrated under a stream

of purified N2 and subsequently separated into compound fractions by silica-gel

chromatography. Ashed Pasteur pipettes loaded with approximately 0.5 g deactivated

silica gel (70–230 mesh) were sequentially eluted with 2 ml hexane, 4 ml

dichloromethane and 4 ml of methanol to obtain aliphatic, aromatic and polar fractions,

respectively. The methanol fraction containing tetraethers was further purified through a

column of activated alumina dissolved in dichloromethane/methanol (1:1, v/v), dried

3

under pure N2 stream, dissolved in an azeotrope of hexane/isopropanol (99:1, v/v),

filtered through 0.7μm glass microfiber filter, and analyzed on an Agilent 1200 series

high performance liquid chromatography coupled with an Agilent 6130 atmospheric

pressure chemical ionization – mass spectrometer following the methodology of

Hopmans et al., (2000) (11).

Quantification of GDGTs was based on peak intensities of the [M+H]+ ion. Relative

abundances of GDGTs were used to calculate the TEX86 index and then converted to

SSTs using the logarithmic calibration of Kim et al. 2010 (12). Other calibrations

including, the linear (13) and reciprocal relationships (14) were also applied (Fig. S2).

Repeated measurements of an in-house laboratory standard indicate that analytical

precision was ±0.01 TEX86 unit.

The ketone fraction was analyzed on a Thermo Trace 2000 gas chromatography

equipped with a Restek column (60m × 0.25mm × 0.25μm), a Programmable

Temperature Vaporization (PTV) injector and a Flame Ionization Detector (FID).

Relative abundances of C37:3 and C37:2 alkenones were used to compute and

subsequently converted to SSTs using the surface sediment linear calibration of Conte et

al. (2006) (15). Analytical precision, determined through multiple measurements of an in-

house alkenone standard, was ±0.05 unit.

Supplementary Text

1. Uncertainty with Published Mg/Ca-thermometry

Potential biases and complications associated with Mg/Ca records include secular

changes in seawater Mg/Ca, preservation and diagenesis of carbonate material, and non-

temperature controls on Mg partitioning (e.g. salinity and pH).

1.1. Changes in Seawater Mg/Ca

Mg/Ca ratios of Globoritalia sacculifer from Site 806 suggest that Pacific warm

pool temperatures were relatively stable over the past 5 million years (16) — key for

maintaining the appearance of a negligible Pacific zonal temperature gradient during the

Pliocene. Mg/Ca-derived SSTs do not agree with organic temperature proxies and

TEX86, which indicate an ~4°C temperature decrease since the late Miocene and an ~2°C

cooling of the western Pacific warm pool since the early Pliocene. Also, a constant warm

pool temperature over the past 5 Ma is difficult to explain by greenhouse gas forcing,

with atmospheric CO2 levels shown to be some 100 ppm higher in the Pliocene than the

glacial-interglacial levels (17, 18). Previous studies that use the warm pool to calibrate

Earth System climate sensitivity argue that this region is very sensitive to CO2 radiative

forcing (19, 20).

4

Although the evolution of seawater Mg/Ca is not known in detail and Pliocene

seawater ratios have not been directly determined, existing evidence using fluid

inclusions and carbonate veins found on the flanks of mid-ocean ridges support a clear

pattern of increasing Mg/Ca ratios through the Neogene toward the present (21-23).

Geochemical modeling used to simulate Mg/Casw variations (24) have been applied to

correct for foraminiferal Mg/Ca-SSTs for Site 806 (16). These corrections increase warm

pool temperatures in the Pliocene, but when the same correction is applied to the cold

tongue Site 847, the equatorial zonal temperature gradient remains small (25).

1.2. Diagenetic Alterations

The tests of shallow-dwelling foraminifera fall through the water column into

undersaturated (with respect to calcite) waters and interact with pore-water and

potentially experience partial dissolution, recrystallization and the addition of diagenetic

(secondary) calcite. These processes alter the original geochemical signal of the primary

calcite test and might be particularly pronounced for planktonic foraminifera collected

from tropical oceans because of the large surface-to-bottom temperature gradient (26).

Diagenetic abiotic calcite formed in cool bottom waters will have disparate δ18

O values

from planktonic biogenic material and inclusion of this secondary carbonate in the whole-

shell analyses increases δ18

O values and leads to cold-biased temperature estimates. More

pristine foraminiferal tests often have a “glassy” appearance, whereas diagenetically

altered tests appear “frosty” (27). Well-preserved “glassy” foraminifera are often found in

near shore environments with high clay mineral content (28), whereas open ocean

environments of the tropics are associated with carbonate-rich sediments. Indeed,

carbonate diagenesis was responsible for the appearance of cool tropical surface waters

during periods of extreme global warming of the Cretaceous, and promoted the

supposition of a “cool tropic paradox” (29). However, subsequent δ18

O analyses of

“glassy” foraminifera yield distinctly warmer temperature estimates for this period (30).

In particular, well-preserved foraminifera from tropical waters of Tanzania during the

Eocene provide tropical temperature estimates that are higher by 10˚C from previous

estimates (31) and these warmer temperatures agree well with TEX86-SST analyzed on

the same samples. Recently, advances of in situ microanalysis techniques, such as

secondary ion mass spectrometry (SIMS) on foraminifera shells, allow the detection of

diagenetic crystallites from biogenic carbonates and show that the oxygen isotopic values

could differ as much as 4.8‰ on the same test (28).

Foraminifer preservation at tropical Pacific Sites 806 and 847 have not been

thoroughly evaluated. However, late Quaternary stable oxygen isotope records from the

identical samples used for the Mg/Ca records from Site 806 and 847 show a much

smaller Pacific zonal temperature gradient compared to the modern conditions,

highlighting the possible impact of carbonate diagenesis. For example, we converted G.

5

sacculifer δ18

O values (16) to SST, considering modern salinity and seawater δ18

O

differences at the two sites (Table S3). Calculations were made for 0-130 kyr (roughly

the last glacial-interglacial cycle) and 0-500 kyr assuming a range of values for δ18

Osw

from modern to glacial values. The value of glacial δ18

Osw was approximated by adding

0.8‰ to modern δ18

Osw, as suggested by pore-fluid evidence for the last glacial

maximum (32). The resulting SST differences between Sites 806 and 847 is 3.6°C for the

past 130 kyr and 2.9°C since 500 kyr, and represent temperature gradients that are

substantially smaller than the modern gradient of 4.8°C between these two sites.

The diagenetic impact of foraminiferal trace metal content is more complicated than

for oxygen isotopes. The dissolution of foraminiferal tests, which preferentially removes

magnesium, could occur as early as the shell reaches the deeper part of the water column

above lysocline (33, 34) and surface sediments (35). A universal dissolution correction

(36) is not able to account for regional-specific Mg losses (35). The addition of

diagenetic carbonates, on the other hand, could contribute to a much higher Mg/Ca ratio

in the whole shell. This is because the partition coefficient for Mg2+

between seawater

and calcite predict much more Mg incorporation during inorganic precipitation of calcite

(37) relative to foraminiferal calcification. To date, information on the dissolution history

and carbonate regrowth for foraminifera in our studied tropical Pacific sites is not

available. Although δ18

O evidence indicate that diagenetic carbonates at Sites 806 and

847 samples are very likely, the exact influence on foraminiferal Mg/Ca thermometry

cannot be precisely assessed.

1.3. Carbonate Ion Influence

Mg/Ca temperatures are also potentially compromised by seawater carbonate ion

concentration during Mg incorporation into foraminiferal tests. Culture experiments on

Orbulina universa and Globigerina bulloides show that Mg/Ca ratios decrease by 7 ±5%

to 16 ±6% per 0.1 unit increase in pH when average pH is below 8.2 (38). Notably,

surface water pH is usually below 8 in the Pacific cold tongue due to intense upwelling of

cold, CO2-rich deep waters (39). More acidic condition in this region would facilitate

higher Mg incorporation and contribute to overestimates of SST and the appearance of a

reduced zonal temperature gradient. Since deep-water upwelling in the cold tongue

probably persisted over the Pliocene and beyond (e.g. Fig. 4), we anticipate that the

carbonate ion effect would reduce the Mg/Ca and temperature offset between the western

and eastern equatorial Pacific in the Pliocene.

2. Applications of in the tropical Pacific

Another line of evidence that has been used to show invariant temperatures of

Pacific warm pool during the Plio-Pleistocene are -based SSTs from Site 806 (40).

6

But, because the index reaches a maximum value of 1 at about 28.5°C, the proxy is

incapable of recording higher temperatures. 46% of the high-resolution alkenone

measurements from warm pool Site 806 (Fig. S1A) reach the maximum possible SST

value between 0.5-1.5 Ma (41). Alkenone data from warm pool Site 1143 (Fig. S1B)

shows slightly cooler temperatures during the Pleistocene compared with Site 806 —

consistent with the site’s position ~9° further north of the equator and on the edge of the

current warm pool (43). Nevertheless, almost all of the data from Site 1143 reach

maximum values prior to 3 Ma (Fig. S1B), and when values are below this upper limit, a

long-term cooling trend of the warm pool is expressed between 3 to 0 Ma (Fig. S1B),

consistent with patterns of global cooling during this time. However, it has been argued

that a “contraction” of the warm pool dimensions since 3 Ma contributed to the apparent

cooling at Site 1143 (40) and that the southern South China Sea, Site 1143, reflects

regional temperature change, rather than the thermal history of the warm pool, and

therefore should not be included in the compilation (40). Several lines of evidence argue

against this assertion. First, Site 1143 has a modern SST of 28.43°C and is within the

western Pacific warm pool defined by the 28°C isotherm (42). Second, the modern

temperature difference between Sites 1143 and 806 (29.33°C) in the center of the warm

pool is only 0.9°C. Temperature records show that Site 1143 cooled by over 2˚C over the

past 3 million years, implying that Site 1143 was warmer than Site 806 and established

the modern gradient as Site 806 SSTs remained invariant. If valid, this would suggest that

the warm pool shifted eastward and did not simply contract, thus requiring a revision of

oceanographic assumptions and interpretations of the position of the warm pool. Third,

our new TEX86 temperature record from Site 806 is highly consistent with patterns of

cooling at Site 1143, and the totality of these data strongly suggest the entire region

cooled over the past 3 million years. We conclude that the supposition of a “stable” warm

pool at Site 806 since the early Pliocene as viewed through ODP 806 temperatures is

largely an artifact of the proxy limitations.

The is perhaps the best sea surface proxy available for this line of work, in

terms of calibration uncertainty which is about ± 1.1˚C (15). In a geologic context,

uncertainty is related to changes in ecology (43), nutrient level and light limitation (44),

depth/season of production (45) and perhaps diagenesis (46). In modern studies,

community distributions of haptophyte algae across the tropical Pacific (47) show a

major shift in the dominant species, from Emiliania huxleyi to Gephyrocapsa oceanica,

from north to south of the equator. These two species have different responses to

temperature and -SST calibrations (43) and changes in distribution over time have the

capacity to impact temperature interpretations. Indeed, Emiliania huxleyi originated only

recently (48, 49) and the use of a single calibration over time is not necessary the most

correct approach.

7

In the South China Sea, core-top sediments show that the -SST relationship

yields reliable SSTs (50). Within our study area in the tropical Pacific, Kienast et al.,

2012 (51) examined hundreds of alkenone measurements in the surface sediments of the

EEP region and concluded that most records follow the global relationship between SST

and values, except a few sites that overestimate SSTs which might be biased towards

El Niño events. If the impact of El Niño events during our studied interval influenced our

records, then EEP temperature reconstructions are likely biased towards higher values

and again suggest that our calculated Pacific zonal temperature gradients are conservative

estimates. Our application of alkenone thermometry in the tropical Pacific show that

records compare well with other sites from the same region (e.g. Sites 850 and U1338, 0-

12 Ma; Sites 846, 847, 850 and U1338, 0-5 Ma), and suggest that reconstructed

temperatures based on this proxy are robust.

In Fig. 2 and 3 we apply the linear calibration of Conte et al., 2006 (15) to convert

alkenone measurements to SSTs. Applying other calibrations including the polynomial

relationship derived from surface seawater (15) and the core-top calibration of Müller et

al., 1998 (52) yields very similar temperature estimates (see Database S1).

3. Applications of TEX86 in the tropical Pacific

TEX86 is a relatively new proxy based on the distribution of archaeal membrane

lipids glycerol dialkyl glycerol tetraethers (GDGTs). Marine core-top sediments (53, 54),

water column (55, 56), mesocosm incubations (57, 58) and pure culture incubations (59)

reveal that Thaumarchaeota, the phylum of the cosmopolitan archaea that produce

GDGTs in seawater, respond to growth temperature by adjusting their relative GDGT

distribution. Incubation experiments indicate that marine archaeal can live up to 40°C

(58). Thus, the application of TEX86 thermometry in the reconstruction of very warm

pool SSTs has an advantage over . However, the

calibration has a significantly

larger uncertainty compared to the (e.g. ±2.5°C for the

calibration, (12), see

below).

Some TEX86-derived paleoemperatures appear to deviate from other proxy-based

temperature records (e.g. in the Miocene – Pliocene, (60, 61); in the Eocene, (14, 62)).

Here we examine the applicability of this proxy in the tropical Pacific by evaluating the

available core-top and late Pleistocene samples from this region, perform a detailed

comparison between TEX86- and - derived SST records, and discuss the potential

causes for offsets between proxies.

Recent work examining global TEX86-based SST offsets from observed SST by

employing the most popular non-linear calibrations (e.g. reciprocal (14), hereafter refer to

8

as Liu09 and logarithmic (12), hereafter refer to as Kim10) found distinct patterns for

low-latitudes in contrast to high-latitudes (63). TEX86 tends to overestimate SSTs in the

high latitudes and underestimate SSTs in the tropics, and the most recent attempt at

improving the calibration applies a spatially-varying coefficient model (63). We

evaluated 67 available surface sediment TEX86 measurements from the tropical Pacific.

In general, TEX86-SSTs using the calibration of Kim10 (12) agree well with satellite

SSTs, with the mean residue = 0.37°C, SD = 1.87°C. However, when samples are divided

into three geographic regions: the open western Pacific warm pool (WPWP), the South

China Sea (SCS) and the eastern equatorial Pacific (EEP), regional-specific residual

patterns emerge (Fig S2). Specifically, we note:

a) TEX86 in the WPWP tends to slightly underestimate SSTs (mean residual = -

1.69°C, SD = 0.78°C, n = 17), consistent with the pattern found in open tropical

oceans (63).

b) TEX86 in the Pacific marginal sea of the SCS appears to slightly overestimate

SSTs (mean residue = 1.51°C, SD = 0.60°C, n = 40).

c) TEX86 in the EEP shows more scattered SST residuals with slightly cooler TEX86

temperatures on average and large standard deviations (mean residue = -0.73°C,

SD = 2.80°C, n = 10).

There is a limited number of core-top data in the tropical Pacific, especially in the EEP

and WPWP, and this contributes to a larger uncertainty using the current regional-

specific Bayesian regression calibration (63).

We estimated the accuracy of TEX86-SSTs for the late Quaternary at Sites 806 and

850 using various TEX86 calibrations (Table S4). Ideally, Holocene TEX86 should be

used to compare with modern temperatures. However, due to the limitation of sample

resolution, TEX86-SSTs are averaged for 0-500 kyr, 0-1000 kyr, and 3-4.5 Ma (the

Pliocene warm period). All late Quaternary estimates appear cooler than modern SSTs at

these two sites. Even if glacial-interglacial variations are considered, which lowers the

“expected” late Quaternary value by 1-2°C (e.g., 64), TEX86-derived SSTs are still on the

low end. This is consistent with core-top data which suggest that current universal

calibrations for TEX86 underestimate SSTs in the open tropical Pacific. However, the

modern temperature gradient between Sites 806 and 850 (4.4°C) are in fact well

documented by applying the Kim et al., 2008 (13) (hereafter refer to Kim08) calibration

for the past 500 kyr (4.5°C), and the Kim10 calibration for the past 1000 kyr (4.4°C). If

we assume the modern temperature gradient at Sites 806 and 850 was maintained over

the past a few glacial-interglacial cycle, agreement between TEX86-based estimation and

the modern gradient suggests that this proxy is a robust tool to survey zonal temperature

gradient of the tropical Pacific in the geological past (Fig. 4). Using Kim08 and Kim10

calibrations, the zonal gradient during the Pliocene warm period was 3.4°C on average

9

(Table S4), consistent with our estimates utilizing all available data (Fig. 4), but different

from the foraminiferal δ18

O thermometry which shows almost no difference across the

equatorial Pacific. (Table S4).

Unlike the variety of calibrations for which have small impacts on the

differences of temperature estimate (Database S1), application of existing TEX86

calibrations alter SST estimates by several degrees (Database S1, Fig. S3). This is

particularly valid for reconstructions of very warm temperatures (e.g. the Miocene part of

the records from Sites 806 and 1143, Fig. S3), which could be partially explained by the

differences between liner calibration (Kim08) and nonlinear calibrations (Liu09, Kim10).

Culture experiments up to 40°C reveal a linear response of TEX86 to temperature changes

(58). In our application, the Kim08 calibration yields the largest cooling of the warm pool

and the largest zonal temperature gradient in the tropical Pacific, whereas the Liu09

calibration yields the smallest cooling and smallest gradient. Estimates using Kim10

calibration provide results in between Kim08 and Liu09 (Fig. S3). Importantly,

applications of a range of TEX86 calibrations do not change our conclusions regarding the

long-term evolution of temperature and temperature gradients in the tropical Pacific.

4. Comparisons between TEX86 and

Available data from Sites 806 and 850 have the appropriate temporal range and

resolution for a detailed TEX86- and -SST comparison (Fig. S4, S5).

-SST data

since 5 Ma were previously published for Site 806 (17) and range between ~26-28.5°C

for 0-3 Ma. Between 3-5 Ma, many SST estimates approach the upper calibration limit of

28.5°C. After 5 Ma, all data reach the maximum limit of values within analytical

uncertainties. We also note slightly cooler temperatures from Pagani et al., 2010 (17)

compared to McClymont et al., 2005 (41) when the data overlap between 0.5-1.5 Ma at

Site 806. We suspect that this is because larger sediment volume was used in the Pagani

et al. study (~50 cc) which allowed higher compound abundances and better detection of

the C37:3 alkenone. Given these constraints, the range of variability gradually

increases from 5 Ma, suggesting that the frequency of temperature reaching the 28.5°C

threshold decreases (Fig. S4). This could imply that (1) the warm pool cooled and SST

variability increased, or (2) the warm pool cooled and variability was similar but the

upper limit is not expressed by the limitations of the proxy itself. Evidence for the warm-

pool cooling trend is supported by the TEX86-SST between 5 to 0 Ma, although TEX86

tends to yield lower temperature estimates relative to . Before 5 Ma,

values are

pinned to the upper limit of the calibration while TEX86 values record an even warmer

late Miocene compared to the Pliocene. In the cold tongue Site 850, both TEX86 and

exhibit long-term cooling since ~12 Ma (Fig. S5). TEX86-SST is generally more scattered

than , but the average value agrees well before ~6 Ma. After 6 Ma, TEX86 tends to

10

give lower temperature estimates until ~1.5 Ma when the temperature offsets reaches the

highest value of ~4°C. Since 1.5 Ma, the deviation between proxies is characterized by a

broad decreasing trend, with TEX86 1-2°C cooler than in the latest Quaternary (Fig.

S5).

Lower TEX86-SSTs relative to in the tropical Pacific could be the result of a

cold bias of current TEX86 calibrations. However, the appearance of a temperature offset

at Site 850 only emerges after ~6 Ma and suggest changes in season and/or depth of

production related to Haptophyte algae or archaea. Given the fact that Thaumarchaeota

are ammonia-oxidizers, the biosynthesis of GDGTs probably occur throughout the entire

water column, with a particular focus near the chlorophyll maximum. However, current

evidence argues that the sedimentary TEX86 signal is primarily exported form the surface.

Carbon isotopic compositions of GDGTs show agreement between surface sediments and

the surface seawater, but not deeper waters (65). This is interpreted as reflecting active

grazing and repackaging of large particles which occur in the photic zone (55). Also, the

slope of the regression between TEX86 values from suspended particles and in situ

temperature measured within the upper 100 m in the ocean is similar to the global core-

top calibration (66). If a substantial subsurface water-column component was associated

with surface sediments, one would expect that the correlation between TEX86 from

suspended particles and temperature would have a much steeper slope relative to the

core-top calibration (66). Regardless, given the shallow thermocline depth in the EEP, as

well as the sharp temperature change with depth (Fig. S6), it is remarkable that TEX86

and estimates agree so well, and offsets easily explained by only slight differences in

production depth between Haptophyte algae and archaea (both within the top 50 m in

modern condition).

To examine if long-term cooling and zonal temperature gradient trends shown in Fig.

2 and 3 are biased by certain sites or proxies, we plot individual SST records from each

site (Sites 806, 1143 and 850) using smoothed lines (Fig. S7). This exercise shows that

the broad cooling trends since 12 Ma that characterize the integrated “warm pool” and

“cold tongue” temperatures (Fig. 3) are also expressed at each individual site (Fig. S7A).

At the same time, a clear temperature offset between the warm pool and the cold tongue

sites is maintained throughout the entire time period. Temperature changes relative to the

late Pleistocene values show a faster cooling rate in the cold tongue than the warm pool

(Fig. S7B), which explains the increasing zonal temperature gradient since late Miocene

(Fig. 4).

11

Fig. S1.

temperatures in the Pacific warm pool at Sites 806 and 1143. Published high-

resolution records of (A) ODP 806, 0.5-1.5 Ma (41) and (B) ODP 1143, 0-4 Ma (67).

12

Fig. S2

Histogram of the temperature residue of SSTs calculated by using (12), minus the

satellite-based mean annual SST, using core-top sediment samples from the open western

Pacific warm pool (WPWP), South China Sea (SCS) and the eastern equatorial Pacific

(EEP). Data from (12, 68, 69). Y-axis represents the number of samples.

13

Fig. S3

Comparisons between TEX86-based SSTs at Sites 806, 850 and 1143 using three different

calibrations: Kim 08 (13), Liu 09 (14) and Kim 10 (12). Dashed line represents the Kim

10 calibration which is used in the main text and Fig. 2, 3 and 4. The upper and lower

band is confined by either Kim 08 or Liu 09.

14

Fig. S4

Comparisons between TEX86- and -derived SSTs at ODP Site 806.

data before 5

Ma are reported by Pagani et al. 2010 (17). Gray diamonds denotes that samples that

reach saturation points of within analytical error therefore should only be used as

minimum temperature estimates.

15

Fig. S5

Comparisons between TEX86- and -derived SSTs at ODP Site 850 and their offsets

since 12 Ma.

16

Fig. S6

Modern water temperature distribution versus depth near ODP Site 850 (0.5°N, 110.5°W).

Different lines represent different seasons (JFM: January – March; AMJ: April – June;

JAS: July – September; OND: October – December). Data from World Ocean Atlas 09

(70).

17

Fig. S7

Smoothing of the SST records at Site 806, 850 and 1143 by applying 10-point FFT filters

to the original data (A). Also shown are the relative changes in temperature with respect

to the late Pleistocene values at Sites 806 and 850 (B).

18

Table S1.

Equatorial Pacific zonal temperature gradients for the Quaternary, Pliocene and late

Miocene. TEX86 ΔTzonal estimates equatorial temperature gradients using only TEX86 SST

records. Total ΔTzonal estimates are based on both TEX86- and record. ΔTzonal (%)

reflects the percent of the Quaternary ΔTzonal average expressed during other time

intervals.

Interval TEX86 ΔTzonal (°C) ΔTzonal (%) Total ΔTzonal (°C) ΔTzonal (%)

Quaternary (0-2.6 Ma) 5.1 100 4.0 100

Pliocene (2.6-5.3 Ma) 4.1 82 3.2 79

Late Miocene (5.3-12 Ma) 3.0 59 2.8 70

19

Table S2.

Summary and chronology for ODP Sites 769, 806, 850 and 1143. Modern SSTs

according to World Ocean Atlas (70).

Sites Coordinates Water

Depth (m)

SST

(°C)

Bio Ref Magneto Ref Foram

δ18

O

Ref

769 8°47' N /

121°18' E

3643

28.49

Y (CN,

PF, D, R)

(71) Yes (71) No N/A

806 0°19' N /

159°22' E

2520

29.33

Y (CN,

PF, D, R)

(3,

72)

Yes (3) Yes (73)

850 1°18' N /

110°31' W

3786

24.93

Y (CN,

PF, D, R)

(4,

74)

Yes (4, 74) No N/A

1143 9°21' N /

113°17' E

2774

28.43

Y (CN,

PF)

(2,

75)

Yes (2) Yes (76)

Abbreviations: Bio – biostratigraphy, Magneto – magnetostratigraphy, CN – calcareous

nannofossils, PF – planktonic foraminifers, D – diatoms, R – radiolarians.

20

Table S3.

Converting foraminiferal oxygen isotopes to SSTs at ODP Sites 806 and 847, using the

equation of Erez and Luz (77). Modern δ18

Osw is interpolated from the global dataset of

LeGrande and Schmidt (78). Last glacial maximum (LGM) δ18

Osw is calculated by

adding 0.8‰ (32) to the modern value at each individual site.

Sites δ18

Osw δ18

OCarb SST

(°C)

Zonal Gradient

(°C)

Comments

806 0.34 29.33 4.8 Modern

0.34 -1.51 25.3 3.5 δ18

OCarb: last 130 kyr. δ18

Osw: modern

1.14 -1.51 29.2 3.7 δ18

OCarb: last 130 kyr. δ18

Osw: LGM

0.34 -1.24 24.0 2.8 δ18

OCarb: last 500 kyr. δ18

Osw: modern

1.14

-1.24

27.8

3.0 δ18

OCarb: last 500 kyr. δ18

Osw: LGM

-1.41

δ18

OCarb: the Pliocene warm period (3-4.5

Ma)

847 0.22 24.53 4.8 Modern

0.22 -0.87 21.8 3.5 δ18

OCarb: last 130 kyr. δ18

Osw: modern

1.02 -0.87 25.5 3.7 δ18

OCarb: last 130 kyr. δ18

Osw: LGM

0.22 -0.74 21.2 2.8 δ18

OCarb: last 500 kyr. δ18

Osw: modern

1.02 -0.74 24.9 3.0 δ18

OCarb: last 500 kyr. δ18

Osw: LGM

-1.43 δ18

OCarb: the Pliocene warm period (3-4.5

Ma)

21

Table S4.

Comparisons between three calibrations, Kim10 (12), Kim08 (13) and Liu09 (14) for the

TEX86 thermometry at Sites 806 and 850. Three time slices include the 0-500 kyr, 0-1000

kyr and the Pliocene warm period (3-4.5 Ma).

Sites Modern (°C) Kim10 (°C) Kim08 (°C) Liu09 (°C) Comments

806 29.33 Modern

26.5 26.7 25.9 last 500 kyr

26.5 26.6 25.9 last 1000 kyr

28.5 29.2 27.5 Pliocene warm period (3-4.5 Ma)

850 24.93 Modern

22.7 22.1 22.5 last 500 kyr

22.2 21.6 22.0 last 1000 kyr

25.5 25.4 25.1 Pliocene warm period (3-4.5 Ma)

Gradient 4.40 Modern

3.8 4.5 3.4 last 500 kyr

4.4 5.1 3.9 last 1000 kyr

3.0 3.8 2.4 Pliocene warm period (3-4.5 Ma)

22

Additional Data table S1 (separate file)

TEX86- and -SSTs at ODP Site 769, 806, 850 and 1143, and the equatorial Pacific

zonal temperature gradient for the past 12 million years.

23

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