Palaeogeography, Palaeoclimatology, Palaeoecology 515 (2019) 152–161

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Palaeogeography, Palaeoclimatology, Palaeoecology

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Significant transient pCO2 perturbation at the New Zealand Oligocene- Miocene transition recorded by fossil plant stomata T ⁎ Margret Steinthorsdottira,b, , Vivi Vajdaa, Mike Polec a Department of Palaeobiology, Swedish Museum of Natural History, SE 104 05 Stockholm, Sweden b Bolin Centre for Climate Research, Stockholm University, SE 109 61 Stockholm, Sweden c Queensland Herbarium, Brisbane Botanic Gardens, Mt. Coot-tha, Mt. Coot-tha Rd., Toowong, QLD 4066, Australia

ARTICLE INFO ABSTRACT

Keywords: The reorganisation of Earth's climate system from the Oligocene to the Miocene was influenced by complex Stomatal proxy interactions between Tethyan tectonics, orbital parameters, oceanographic changes, and carbon cycle feedbacks, Climate change with climate modelling indicating that pCO2 was an important factor. Oscillating episodes of climate change Oligocene–Miocene boundary during the Oligocene–Miocene transition (OMT) have however been difficult to reconcile with existing pCO2 Mi-1 termination records. Here we present a new pCO record from the OMT into the early Miocene, reconstructed using the Lauraceae 2 stomatal proxy method with a database of fossil Lauraceae leaves from New Zealand. The leaf database derives from three relatively well-dated sites located in the South Island of New Zealand; Foulden Maar, Mataura River

and Grey Lake. Atmospheric pCO2 values were obtained based on four separate calibrations with three nearest living equivalents, using the stomatal ratio method as well as transfer functions. Our results, based on the mean

values of each of the four calibrations, indicate pCO2 ranging ~582–732 ppm (average 650 ppm) at the OMT, falling precipitously to mean values of ~430–538 ppm (average 492 ppm) for the earliest Miocene and

~454–542 ppm (average 502 ppm) in the early Miocene. The much higher values of pCO2 at the OMT indicate that pCO played an important role in climate dynamics during this time, potentially including the abrupt ter- mination of glaciations.

1. Introduction The Oligocene–Miocene climate transition (OMT) was a transient global cooling event, culminating in significant Antarctic ice sheet ex- 1.1. The Oligocene-Miocene boundary and climate transition pansion, global sea-level fall and a cooling of 2 °C or more (Miller et al., 1991; Liebrand et al., 2011; Mawbey and Lear, 2013; Sliwinska et al., The Oligocene–Miocene boundary (OMB) is dated at 23.03 mil- 2014; Liebrand et al., 2017). Peak glaciation as interpreted from marine lion years ago (Ma) in the ICS International Chronostratigraphic Chart isotope records – the Miocene isotope zone 1 glaciation (Mi-1: (Cohen et al., 2016), based on interpretations of distinct obliquity as defined by Pälike et al. (2006)) – took place just prior to and at the patterns in marine pelagic sediments, although without preserved OMB, within the OMT, followed by ice sheet retreat/warming of similar magnetostratigraphy (Pälike et al., 2006; Shackleton et al., 2000). The magnitude (Zachos et al., 2001b; Lear et al., 2004; Larsson et al., 2006; OMB marks the important climate transition from the still relatively Pälike et al., 2006; Wilson et al., 2008; Larsson et al., 2011; Mawbey warm Paleogene to the cooler Neogene, but in contrast to e.g. the Eo- and Lear, 2013). The Mi-1 took place in two “steps” marked by max- cene–Oligocene boundary (see Coxall et al., 2005), the OMB is not imum benthic foraminifera δ18O excursions, each episode lasting easily recognizable globally and must be defined at regional bound- 200–300 kyr (Lear et al., 2004; Liebrand et al., 2011), and was a part of aries. The New Zealand stage system, and its correlation with the in- a cyclic oscillation pattern of glaciation/deglaciation during the Oli- ternational system, is documented in Cooper (2004) and updated by gocene to early Miocene (Liebrand et al., 2017). The deglaciation phase Raine et al. (2015). New Zealand's late Oligocene–Miocene palynolo- at the end of Mi-1 is marked by accelerated sedimentation rates, in- gical zones typically have wide age estimates, due to lack of sufficient terpreted to represent increased biogenic productivity (Florindo et al., marine control. As one consequence, the international stratigraphic 2015). Recent results indicate that although multiple marine isotope OMB is not identified in the New Zealand stratigraphy, but rather proxy records independently support the overall OMT trends, sig- contained within the Waitakian stage, which spans 25.2–21.7 Ma. nificant inter- and intrabasinal variability in deep water masses exists,

⁎ Corresponding author at: Department of Palaeobiology, Swedish Museum of Natural History, SE 104 05 Stockholm, Sweden. E-mail address: [email protected] (M. Steinthorsdottir). https://doi.org/10.1016/j.palaeo.2018.01.039 Received 6 July 2017; Received in revised form 21 January 2018; Accepted 27 January 2018 Available online 31 January 2018 0031-0182/ © 2018 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/). M. Steinthorsdottir et al. Palaeogeography, Palaeoclimatology, Palaeoecology 515 (2019) 152–161 together with chronological discrepancies, complicating interpretations 1 is linked to these dynamics, with a considerable increase in pro- of this global event (Florindo et al., 2015; Beddow et al., 2016) and ductivity observed shortly after the δ18O maximum (ca. 100 kyr), sig- adding further to the inherent limitations of the marine isotope proxy nalling reduced carbon burial in the oceans and rapidly increasing pCO2 records, which record both and ice sheet volumes, in (Diester-Haass et al., 2011; Florindo et al., 2015), independently sup- unknown proportions (Wilson et al., 2008). ported by dissolution events at deep water sites (Mawbey and Lear,

Terrestrial vegetation records confirm a global cooling episode as- 2013). Few modelling studies exploring the relationship between pCO2 sociated with Mi-1 and a subsequent significant transient warming and ice sheet growth at the OMT and Mi-1 have so far been published (Kürschner and Kvacek, 2009; Larsson et al., 2010; Kotthoff et al., (Liebrand et al., 2011), but studies focusing on the previous rapid 2014). In New Zealand, Nothofagus pollen was usually dominant cooling and Antarctic glaciation at the Eocene–Oligocene boundary through the Oligocene and into the early Miocene, following which indicate that pCO2 played an important role in the initiation of gla- there was a marked increase in palynological diversity, with a variety of ciation, and that orbital forcing also has a strong influence on ice sheet dominant taxa. This is interpreted to reflect cooler followed by warmer growth – especially near the glaciation threshold (DeConto and Pollard, climatic conditions (Mildenhall, 1980; Pocknall, 1982a; Pocknall and 2003; Steinthorsdottir et al., 2016a). The glaciation threshold of pCO2 Mildenhall, 1984; Mildenhall and Pocknall, 1989; Morgans et al., for Antarctic glaciation however, historically assumed to be ca. 2004). 700–800 ppm, has recently been shown to be highly dependent on the type of climate model used and assumptions made (Gasson et al., 2014,

1.2. The role of pCO2 as forcing mechanism at the Mi-1 termination 2016), fully re-opening the important question of the Earth system's climate sensitivity to changing pCO2. The forcing and feedback mechanisms involved in the initiation and In order to illuminate the complex respective roles of carbon cycle termination of OMT glaciations, including the Mi-1, are still not fully dynamics vs. orbital and/or tectonic and oceanographic factors in the understood, with orbital parameters, ocean circulation changes due to abrupt climate transitions during OMT, multiple independent records of closing of the Tethys seaway and other gateway dynamics, decreasing pCO2 are needed. This will allow both inter-comparison between pCO2 atmospheric CO2 (pCO2) and the interplay with climatic records for maximum fidelity, and comparison and reconciliation with thresholds all having been implicated in various combinations and isotope-based and other geological records. Existing proportions (e.g. Kennett and Shackleton, 1976; Miller et al., 1991; Paul marine proxy-derived pCO2 estimates across the OMT indicate an et al., 2000; Zachos et al., 2001a, 2001b; DeConto and Pollard, 2003; overall trend of decreasing pCO2, from ~500 ppm during the late Lear et al., 2004; DeConto et al., 2008; von der Heydt and Dijkstra, Oligocene to “near modern values” (now below modern values) of 2008; Wilson et al., 2008; Mawbey and Lear, 2013; Zhang et al., 2013; ~370–380 ppm at the OMT (Pearson and Palmer, 2000; Pagani et al., Liebrand et al., 2017). During most of the Cenozoic, complex tectonic 2005; Zhang et al., 2013)(Fig. 1). The warming episode terminating the activity was ubiquitous, including e.g. building of the Rocky Mountains Mi-1 was not detected as a parallel feature in the marine pCO2 records, in USA as well as the Pyrenees and the main Alpine orogeny in Europe, leading to the assumption that pCO2 was not a primary driver of climate north of Tethys. The Atlas Mountains in North Africa formed south of and ice-sheet development during OMT (Pagani et al., 2005; Zhang Tethys, and major orogenic activity along the Indonesia-Malaysia- et al., 2013). Very few previously published terrestrial stomatal proxy-

Japan island arc system took place. India collided with the Asian con- based pCO2 records exist for the late Oligocene and early Miocene, tinent, resulting in uplift of the Tibetan Plateau and the establishment including across the transitional interval, but those that do generally of the Himalayan Mountains (Rosenbaum and Lister, 2002; Qin et al., converge with the marine-derived estimates at ~500–600 ppm for the 2017). A transgression that was initiated during the Late Cretaceous latest Oligocene and ~400–500 ppm for the early Miocene (Kürschner peaked around the latest Oligocene/earliest Miocene and much of the et al., 2008; Beerling and Royer, 2011; Foster et al., 2012; Grein et al., New Zealand subcontinent was submerged (Landis et al., 2008). A re- 2013; Zhang et al., 2013; Roth-Nebelsick et al., 2014; Steinthorsdottir gression commenced soon after, but major tectonic activity and et al., 2016a)(Fig. 1). However, the stomatal proxy records listed above mountain building (the Kaikoura Orogeny, resulting eventually in the have all been of fairly low resolution, with either no or few data points Southern Alps) did not occur until late Miocene–Pliocene (Youngson at the OMT, and thus liable to miss any rapid transient fluctuations in et al., 1998; King, 2000; Mortimer et al., 2001). The closing of Tethys pCO2. Recently, Reichgelt et al. (2016) published an extraordinarily thus led to the formation of numerous mountain ranges, resulting in high-resolution record of leaf physiological change focused on the OMT increased weathering and draw-down of CO2, causing an overall global (~23.02–22.94 Ma) derived from the Foulden Maar locality, New cooling. This tectonic phase also included subduction of carbonate-rich Zealand, indicating that pCO2 may have doubled during the termination oceanic crust and periodic volcanic activity, adding CO2 to the atmo- of Mi-1, from ~500 ppm briefly to ~1100 ppm (Fig. 1), before de- sphere and during some intervals causing transient episodes of global creasing again to ~425 ppm. These results thus invite renewed dis- warming (DeConto and Pollard, 2003; Edmond and Huh, 2003; Lyle cussions regarding the role of pCO2 in the OMT climate dynamics. et al., 2008). Here we present a new stomatal proxy-based pCO2 record using a Ice sheet modelling indicates that large parts of the Antarctic ice database of fossil Lauraceae specimens from three localities across the sheet, once formed, should have remained relatively stable (hysteresis OMT of New Zealand. We compare the results with previously pub- effect) and thus have not been able to account for the episodes of ice lished pCO2 records and discuss the implications for climate dynamics sheet advance and retreat – strongly indicated by geological evidence – across the OMT, particularly the role of pCO2 in terminating the Mi-1 under stable, moderate pCO2 forcing (Naish et al., 2001; Mawbey and glaciation. Lear, 2013; Zhang et al., 2013; Gasson et al., 2016). Carbon cycle feedbacks have been implicated as an important factor for the OMT 2. Material and methods transient cooling and subsequent warming, through first enhanced or- ganic carbon burial as a positive feedback to cooling climate (Mawbey 2.1. Geological setting and Lear, 2013; Florindo et al., 2015), followed by increased green- house forcing due to decrease in chemical weathering rates during The fossil Lauraceae leaves studied here were collected for previous glaciation (Lear et al., 2004), or organic matter oxidation (Mawbey and taxonomic studies (Pole, 1993a, 2007; Pole et al., 2003) and derive Lear, 2013), a negative feedback. A seafloor carbonate dissolution event from three outcrop successions in New Zealand's South Island: 1) Dia- has been interpreted to reflect an input of carbon into the ocean-at- tomite sediments from outcrops at Foulden Maar, dated to mosphere system during the deglaciation phase of the OMT (Mawbey 23.2 ± 0.2 Ma (Lindqvist and Lee, 2009), i.e. within the Waitakian and Lear, 2013). The abrupt warming and deglaciation at the end of Mi- stage and close to the International OMB; 2) Mataura River sediments

153 M. Steinthorsdottir et al. Palaeogeography, Palaeoclimatology, Palaeoecology 515 (2019) 152–161

Fig. 1. Overview of climate and pCO2 reconstructions for the Oligocene and early–middle Miocene. The Mi-1 major cooling event is indicated. Redrawn after Zhang et al. (2013), who compiled pub-

lished pCO2 data, with stomatal proxy records principally from Beerling and Royer (2011). Benthic foraminifera δ18O isotope data

from Zachos et al. (2008). Dashed lines indicate modelled pCO2 gla- ciation thresholds for Antarctica (~750 ppm) and the Arctic/ Northern Hemisphere (~280 ppm). New results showing transient

elevated pCO2 at the termination of Mi-1 from Reichgelt et al. (2016) indicated with a green dot at ~1100 ppm. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

dated to earliest Miocene (late Waitakian); and 3) the Grey Lake locality occurrences of the Gore Lignite Measures. This was probably the same (informal local name) dated to early Miocene (Otaian) (Fig. 2). as Couper's (1960) S178/513 locality, regarded as Waitakian based on The Foulden Maar fossil lake contains a high-resolution sedimentary the predominance of Nothofagidites matauraensis and N. cranwellae succession of laminated diatomite, with abundant well-preserved fossil pollen, but rarity of Nothofagus “fusca” type and Podocarpaceae pollen. plants, first documented by Cecilia Travis in an unpublished thesis and The sediments are rich in leaf material, although not always well pre- subsequently described in detail and published by Pole (1993a, 1993b, served. The R. waimumuensis Zone was regarded as mostly late Oligo- 1996: New Zealand Geological Society Fossil Record Number I43/ cene but extending into the early Miocene by Pocknall and Mildenhall f8503), Bannister et al. (2012), Conran et al. (2013) and Reichgelt et al. (1984). They showed the marine sediments at the base of drillhole (2013). Radiometric dating of associated basalts constrains the Foulden d1134 as being within the zone, and this was subsequently dated as Maar as 23.2 ± 0.2 Ma (Lindqvist and Lee, 2009), here referred to as basal Altonian by Pocknall (1982b). However, Crundwell et al. (2004) the OMT. place the R. waimumuensis Zone in the Waitakian Stage, with its lower At Mataura River, the so-called Gore Lignite Measures are exposed zone limit at the International OMB, thus the Mataura River locality in several locations along the banks of the Mataura River, between the may be regarded as ~23 ± 1 Ma (Waitakian, earliest Miocene age), towns of Mataura and Gore in Southland (Fig. 2). An exposure in the and therefore largely synchronous with Foulden Maar. Here, we plot bank of the Mataura River, within a few meters of the M1 coal seam, the results from Matauara River sediments at 22.5 Ma, which is the mid- was placed in the lower half of the Rhoipites waimumuensis pollen Zone point between the lower and upper limits of the age estimates. by Pocknall (in Isaac et al., 1990), classifying it as one of the most basal Grey Lake is a local name for an abandoned sluice‑gold-mining area

154 M. Steinthorsdottir et al. Palaeogeography, Palaeoclimatology, Palaeoecology 515 (2019) 152–161

Fig. 2. Location of the three fossil plant localities on the South Island of New Zealand. 35°S

AUCKLAND

North Island

40°S NEW ZEALAND

WELLINGTON

South Island

CHRISTCHURCH

45°S Grey Lake

Foulden Maar DUNEDIN km

Mataura River 0 200 400 170°E 175°E

near St Bathans (Fig. 2). It contains extensive outcrops of the St Bathans cells, with cuticular scales present in between (Hill, 1986). This cuticle Member (Dunstan Formation), the lowest unit of the Manuherikia morphology exists in the Australasian fossil record throughout the Group (Douglas, 1986). Douglas (1986) concluded that the St Bathans Cenozoic, as well as in the living Australasian Lauraceae (see e.g. Member was deposited by braided rivers flowing in valleys incised into Vadala and Greenwood, 2001; Pole, 2007). the basement rock (schist and greywacke). The St Bathans Member was The epidermal cuticle of the specimens in this study displays a fairly not included in Mildenhall and Pocknall's (1989) palynological study of generalized surface morphology (Fig. 3B–D). Epidermal cells are typi- the Manuherikia Group, although one sample was documented in an cally small, quadratic to rectangular-polygonal, normally unpublished report (Pocknall, 1982b). Pole and Douglas (1998) placed ~10–20 μm×8–12 μm, some slightly larger, generally with thick and palynological samples from Grey Lake into their Nothofagidites ‘brassii straight cell walls (no undulation). Trichome attachment scars are type’ Zone and ‘Myrtaceae-Arecaceae’ Zone. The age, based on paly- common, sometimes abundant (Fig. 3D), mostly located on veins and nology and regional geology, is regarded as the earliest Miocene, occurring less abundantly on areoles. The paracytic stomata are easily ~19 ± 1 Ma and the successions contain diverse and well-preserved identified and densely present in inter-vein areas. The stomatal pore plant cuticles (e.g. Pole, 2007, 2008). length is ~7–8 μm and the guard cell length ~8–10 μm(Fig. 3C). The general shape of the stomatal complexes is rectangular-circular, often 2.2. The Lauraceae leaf database appearing considerably lighter in colour than surrounding epidermal cells, indicating thinner stomatal cuticle. Veins consist of rows of epi- Our database includes 21 leaf specimens: three from Foulden Maar, dermal cells which are narrower and more elongated than areolar nine from Mataura River and nine from Grey Lake (Fig. 2). The fossil epidermal cells, typically ~7–8×20 –25 μm. Trichome attachment specimens were placed in Lauraceae based on their leaf and cuticle scars are small, round, with thickened cuticle around the perimeter, morphology (Fig. 3A–D). The cuticle morphology is characterized by surrounded by ~20 μm long epidermal cells in the anamocytic ar- paracytic stomata with overarching subsidiary cells over the guard rangement (Fig. 3B–D).

155 M. Steinthorsdottir et al. Palaeogeography, Palaeoclimatology, Palaeoecology 515 (2019) 152–161

Fig. 3. Fossil Lauraceae leaf database. A: well-preserved leaf from the Grey Lake locality, belonging to genus Cryptocarya. Scale bar is 1 cm. A B B: epidermal surface of Lauraceae leaf specimen nr. SL 6272. The image shows the typical morphology of epidermal cells and stomata in the database. The turquoise rectangle illustrates how stomata (marked by dots) and epidermal cells were counted within engraved grids, to determine stomatal indices. Scale bar is 100 μm. C: close-up of an areola and a cluster of typical Lauraceae paracytic stomata. To the left of the areola, elongated vein epidermal cells are shown. Specimen nr. D 2322. Scale bar is 20 μm. D: epidermal surface showing abundant trichome scars. Specimen nr. SL 6276. Scale bar is 100 μm. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

D

C

2.3. Laboratory methods climatological settings from the Palaeozoic until today and can be considered as a strong proxy for palaeo-pCO (e.g. McElwain and Sediment bulk samples were first disaggregated in hot water with Chaloner, 1996; Wagner et al., 1996; Beerling et al., 1998; McElwain, added hydrogen peroxide (H2O2). The residues were subsequently 1998; Royer et al., 2001; Wagner et al., 2002; Haworth et al., 2005; sieved and fragmentary leaf material retained. The leaf fragments were Roth-Nebelsick, 2005; Kürschner et al., 2008; Barclay et al., 2010; then heated in concentrated hydrogen peroxide for several hours until Steinthorsdottir et al., 2011b; 2013; Grein et al., 2013; Bai et al., 2015; cleared. Any adhering silica was removed with further hydrogen per- Mays et al., 2015; Steinthorsdottir and Vajda, 2015; Montañez et al., oxide treatment of the leaf fragments and the cuticle stained with sa- 2016; Steinthorsdottir et al., 2013; Steinthorsdottir et al., 2016a, franin. Finally, the fragments were mounted on microscope slides with 2016b; Wolfe et al., 2017; McElwain and Steinthorsdottir, 2017). A thymol glycerine jelly. The mounted abaxial epidermal cuticle surfaces strong argument for the reliability of SI tracking palaeo-pCO2 is that were photographed at ×200 magnification with a Leica camera (Leica cumulative mean statistical analyses show that typically less than seven DF310 FX), and associated software. Between five and seven images counts of SI per fossil leaf are sufficient to establish a robust % value for were taken of each specimen, evenly distributed across the mid-leaf that leaf, and – perhaps more importantly – a similarly small amount of areas, away from margins, midrib and veins, according to the re- leaves per time interval (i.e. sedimentary bed) yield a robust SI value commended methodology of Poole and Kürschner (1999). These images for that time slice (Poole and Kürschner, 1999; Steinthorsdottir et al., form the database used for the results presented here. Lastly, each 2011b). This robust relationship between SI and pCO2 at a given time image was annotated using the software ImageJ (1.46 h; http://imagej. installs confidence in utilizing even small fossil leaf databases such as nih.gov/ij) by engraving 300 × 300 μm or 200 × 200 μm squares on the one studied here. each image. Three methods of stomatal proxy-based palaeo-pCO2 calibration are in use: 1) the empirical stomatal ratio method, which utilizes the ratio

2.4. Stomatal analysis and calibration of palaeo-pCO2 between the SI of fossil plants and the SI of extant nearest living re- latives or equivalents (NLR or NLE), grown in known pCO2 (natural or

The stomatal proxy for palaeo-pCO2 reconstruction is based on the experimental), to estimate palaeo-pCO2 (McElwain and Chaloner, 1995; observations of the inverse relationship that exists between frequency McElwain, 1998); 2) the likewise empirical transfer function method, of stomata (pores on the leaf epidermis used for gas-exchange) and which relies on herbarium and/or experimental datasets of NLR/NLE pCO2, in order to minimize loss of water through transpiration responses to variations in pCO2 to construct regression curves on which (Woodward, 1987). This relationship is not universal, but is expressed fossil SI can be plotted to infer palaeo-pCO2 (Wagner et al., 1999; in the large majority of woody plants (> 90% in fossil studies; Royer, Royer, 2001; Beerling and Royer, 2002; Barclay and Wing, 2016); and 2001). Stomatal frequencies can be quantified as stomatal density (SD: 3) the mechanistic modelling approach, which is taxon- number of stomata per mm2) or stomatal index (SI: the proportion of independent and uses e.g. morphological cuticle measurements, but 13 stomata to all epidermal cells). It has been shown that in most cases SI requires more input of data, including leaf δ C (e.g. Konrad et al., more reliably reflects pCO2, whereas SD may be influenced by addi- 2008; Franks et al., 2014; Konrad et al., 2017). tional factor, e.g. light levels and water availability (Salisbury, 1927). In this study, we calibrated palaeo-pCO2 using the stomatal ratio The stomatal proxy has by now been applied to a wide variety of plant method and three separate transfer functions. Stomata and epidermal taxa from numerous different geological, palaeo-ecological and palaeo- cells within annotated squares on the database images were counted

156 M. Steinthorsdottir et al. Palaeogeography, Palaeoclimatology, Palaeoecology 515 (2019) 152–161

(Fig. 3B) and SI calculated as SI (%) = [SD / (SD + ED)] × 100, where calibrations are broadly inter-comparable within each of the time slices.

ED is the epidermal cell density. At least seven images, sensu Poole and Across the OMT, transfer function-derived pCO2 estimates range from Kürschner (1999) were used for mean SI determination for each spe- ~580 ppm using Ocotea foetens to ~640–650 ppm using Laurus nobilis cimen from each of the three stratigraphical levels, confirming the and Laurophyllum pseudoprinceps as NLE (Table 1; Fig. 4). Stomatal mean values by cumulative mean statistical analysis. Three previously ratio-derived estimates using L. nobilis show the highest calibrated OMT published transfer functions (Kürschner et al., 2008) in addition to the pCO2 at ~730 ppm. Earliest and early Miocene pCO2 records are by stomatal ratio method (McElwain and Chaloner, 1995) were used. The contrast considerably lower. Earliest Miocene transfer function-derived transfer functions were constructed for Miocene extinct Lauraceae, pCO2 is lowest at ~430 ppm when calibrated using L. pseudoprinceps as based on extant nearest NLR or NLE species and in the case of the fossil NLE, ~516–538 ppm when using L. nobilis and O. foetens, whereas species Laurophyllum pseudoprinceps, based on cross-calibration with the stomatal ratio-derived pCO2 estimates using L. nobilis are intermediate well-established NLE species Laurus nobilis and Ginkgo biloba, adding a at ~485 ppm (Table 1; Fig. 4). Early Miocene estimates indicate highly correction factor where appropriate (see Kürschner et al., 2008 for similar pCO2 to that of the earliest Miocene, albeit slightly higher. details). The first transfer function is based on the extant species Laurus Transfer function-derived pCO2 is again lowest when calibrated using L. nobilis (laurel, leaves commonly referred to as ‘bay leaves’), in- pseudoprinceps at ~454 ppm, ranging ~520–542 ppm when using L. dependently calibrated from historical sets of herbarium material: nobilis and O. foetens, and stomatal ratio-derived pCO2 estimates using 3.173 L. nobilis are also again intermediate at ~490 ppm (Table 1; Fig. 4). pCO2 palaeo =× 10 –[0.5499 log (SIfossil )] (1) The overall average pCO2 is thus ~650 ppm for the The second transfer function is also based on an extant species: Oligocene–Miocene Transition and ~490–500 ppm for the earliest and Ocotea foetens (Tilo or ‘the stinkwood’), independently calibrated from early Miocene (~25% lower). herbarium material: Statistical analyses (two sample t-tests for equal means) of pCO2

2.9567 results reconstructed between each pCO2 calibration and each time pCO2 palaeo =× 10 –[0.4284 log (SIfossil )] (2) interval confirmed that earliest and early Miocene pCO2 levels are very The third transfer function is based on the extinct species similar and thus cannot be separated statistically (p vales 0.7–0.9, null Laurophyllum pseudoprinceps, established by cross-calibration with L. hypothesis confirmed), whereas the difference between the pCO2 values nobilis and Ginkgo biloba: derived for the OMT and those of the earliest and early Miocene pCO2 values respectively are statistically significant (p < 0.05, null hy- pCO2 palaeo =×+ –46.011 SIfossil 993.37 (3) pothesis rejected). In addition, we use the stomatal ratio method of McElwain and Chaloner (1995), which utilizes the ratio between stomatal indices of 4. Discussion fossil plants and their NLR or NLE in relation to the ratio between known pCO2 (modern) and palaeo-pCO2. “Modern” pCO2 was histori- 4.1. Assessment of the new OMT pCO2 record cally set at 300 ppm (defined as preindustrial pCO2 concentration), but post-industrial pCO2 can also be used when available with the appro- An emerging concern with the increasing interest in stomatal proxy- priate SI. The ratio between Cretaceous and younger SI and modern SI based pCO2 reconstructions is the question of how errors should be is estimated to be 1:1 (McElwain and Chaloner, 1995) and the stomatal quantified. Traditionally errors have been reported as standard devia- ratio calibration is thus expressed by the equation: tion or standard error, based on the spread of the data points from a mean. Although giving indication of the strength of the dataset pre- pCO2 palaeo=× SI NLE /SI fossilp CO 2 modern . (4) sented, this clearly does not take into account potential inherent

The here selected NLE is L. nobilis, with SINLE of 18.32% at 300 ppm variability caused by e.g. taxa used (fossil vs modern species, and/or pCO2 (Kürschner et al., 2008), resulting in: non species-specific records), evolutionary and environmental change, and possibly a range of other unknown factors. The community of re- pCO2 palaeo =× 18.32/SIfossil 300. (5) searchers using the stomatal proxy for palaeo-pCO2 reconstructions are Determining the genera of fossil Lauraceae is notoriously challen- working on this complex issue, but for now the best way forward may ging, but even though cuticle evidence is proving useful (e.g. Ferguson, be to reconstruct pCO2 using multiple taxa with a variety of available 1974; Christophel et al., 1996), the phylogenetic relationships of extant stomatal proxy methods, to reach the best consensus possible. It should genera remains in some flux (e.g. van der Werff and Richter, 1996; be noted here that the small sample size of just three leaves from the Rohwer, 2000; Chanderbali et al., 2001). For this reason, although L. Foulden Maar OMT locality results in smaller errors than for the larger nobilis (originally assigned as the specific NLE for extant species Laurus samples from the Mataura River and Grey Lake localities (standard abchasica in Kürschner et al., 2008) may not be the best NLE for the deviations, see Table 1) – contrary to the obvious assumption that New Zealand Lauraceae studied here, we chose to utilize it as the NLE, smaller datasets are less likely to fully capture the natural error range – for easier comparison of previously published results (Kürschner et al., illustrates this issue well.

2008; Steinthorsdottir et al., 2016a; Steinthorsdottir et al., 2016b), ef- The fact however that pCO2 values presented here, reconstructed fectively regarding it as a standardised Lauraceae. using four calibrations with three NLE species in two distinct stomatal proxy methods, show a high degree of similarity within each sample 3. Results (time slice), inspires confidence that Lauraceae SI were responding to

pCO2 and that this response can be successfully utilized to reconstruct 3.1. Stomatal indices and pCO2 across the OMT approximate levels of palaeo-pCO2. The stomatal ratio method assumes a 1:1 response of stomata of Cenozoic and younger plants and their

The fossil leaf cuticles from the oldest site, Foulden Maar from the NLEs, therefore always recording changing pCO2 levels when SI change OMT, have a mean SI of 7.5%, while the leaf cuticles from the two (McElwain and Chaloner, 1996). Transfer functions however directly younger sites, Grey Lake and Mataura River, of earliest and early record plant SI responses to known pCO2, including any non-linear re- Miocene age, show substantially higher SI at around 12% (11.7% and sponses, potentially providing more accurate calibrations (Royer, 2001; 12.2% respectively) (Table 1). SI thus increased by > 60% from the Beerling and Royer, 2002; Kürschner et al., 2008; Barclay and Wing,

OMT into the early Miocene, implying considerably higher pCO2 during 2016). It has previously been shown that the stomatal ratio method and the OMT than in the early Miocene. transfer functions produce similar results when used with the same leaf

Atmospheric pCO2 values obtained using the four separate fossils (e.g. Steinthorsdottir et al., 2016b; McElwain and

157 M. Steinthorsdottir et al. Palaeogeography, Palaeoclimatology, Palaeoecology 515 (2019) 152–161

Table 1

Stomatal indices and atmospheric pCO2 across the OMT and into the early Miocene of New Zealand.

Locality International zone New Zealand Age (Ma) SI (%) pCO2 (ppm): transfer functions* pCO2 (ppm): stomatal Average pCO2 zone Lauraceae ratio** (ppm)***

L. nobilis O. foetens L. pseudoprinceps L. nobilis

Grey Lake Early Miocene Otaian 19 ±2 11.72 ± 2.7 542.3 ±49 519.8 ±31 454.2 ± 122 490.8 ± 110 501.8 ±88 Mataura River Earliest Miocene Late Waitakian 22.5 ±1 12.24 ± 3.1 537.6 ±69 516.5 ±43 430.0 ± 142 485.1 ± 169 492.3 ± 118 Foulden Maar Oligocene-Miocene transition Waitakian 23.2 ± 0.2 7.53 ± 0.5 641.3 ±17 581.5 ±11 646.9 ±22 731.8 ±47 650.4 ±58

*, **Four pCO2 calibrations were used: three transfer functions and the stomatal ratio method. The results are recorded with standard deviations, with the exception of age estimates, which are based on previous geological studies. ***The results indicate that pCO2 levels were considerably higher at the OMT, close to the termination of the Mi-1 glaciation, compared to the earliest and early Miocene levels.

Fig. 4. Reconstructed atmospheric pCO2 across the Oligocene–Miocene transition and during the earliest, and early Miocene of New Zealand, CO (ppm) using four separate calibrations (tree transfer 2 functions and the stomatal ratio method) with three nearest living equivalent species. Earliest Age

Period Epoch 400 500 600 700 800 New Zealand Stages Age (Ma) and early Miocene pCO2 are highly comparable

19 (average pCO2 ~500 ppm), whereas pCO2 for the latest Oligocene, near OMT, is significantly Grey Lake higher (average pCO2 ~650 ppm). The data 20 points are shown without error bars for visual

Burdigalian clarity; see Table 1 for standard deviations. Otaian

21

Neogene Legend 21.7 22 Transfer functions Aquitanian Laurus nobilis Mataura River Ocetea foetens 23 23.03 Foulden Maar Laurophyllum pseudoprinceps

24 Waitakian Stomatal ratio Laurus nobilis

Chattian p 25 Oligocene Miocene Average CO2 (all) Paleogene

Steinthorsdottir, 2017). Here, we were unable to reconstruct pCO2 4.2. Comparison with previously published OMT pCO2 records using the gas exchange modelling approach (the third available sto- 13 matal proxy method), principally due to lack of δ C data for the leaf The few previously published stomatal proxy pCO2 records largely database. However, previous pCO2 reconstructions using both the sto- agree with each other and with marine records regarding the trend and matal ratio method and the gas exchange model of Franks et al. (2014) magnitude of pCO2 across the OMT (see Fig. 1), with a few exceptions with fossil leaf material from the late Pennsylvanian, recorded com- recording stable levels across the OMT. Considering that the stomatal parable pCO2 values (Montañez et al., 2016), and the overall compat- pCO2 records have been constructed using four calibrations with two ibility between pCO2 results obtained using all the various methods stomatal proxy methods and various fossil plant species, this inspires (discussed below in Section 4.2), suggests that the stomatal proxy confidence in the emerging pattern. Kürschner et al. (2008), using methods generally produce comparable results. transfer functions with the stomatal densities of multiple herbarium and Standard deviations, measuring the dispersion of the data, are lar- fossil plant species from Central Europe, including several Lauraceae, gest for the pCO2 values calibrated using Laurophyllum pseudoprinceps as recorded a significant overall decrease in pCO2 from ~600 ppm in the NLE in a transfer function, reflecting perhaps the non-linear response of Late Oligocene to ~340 ppm in the early Miocene. Grein et al. (2013), this species (Table 1). Laurus nobilis was applied as NLE both in the using a leaf gas-exchange model for several fossil plant species from stomatal ratio method and in the transfer function, recording higher Germany, later reported two possible scenarios depending on which variability when using the stomatal ratio method (highest pCO2 at the taxa were included in the calibrations: either an overall pCO2 decrease OMT, but intermediate in the earliest and early Miocene when com- from ~700 ppm in the latest Oligocene to ~500 ppm in the early pared to the transfer function results). This may either indicate that the Miocene when including Lauraceae in the fossil dataset, or considerably stomatal ratio method, which directly translates the SI signal to pCO2, lower, stable pCO2 of ~400 ppm across the OMT when excluding overestimates plant response to pCO2, or that the transfer function used Lauraceae. Roth-Nebelsick et al. (2014), using a single species dataset underestimates the response, and this needs to be further tested. The with a leaf gas-exchange model from the late to latest Oligocene of overall agreement regarding the volume and direction of change of Germany likewise recorded stable pCO2 of ~400 ppm throughout the pCO2 from the OMT and into the early Miocene does however indicate period. SI values do change during the studied intervals of Grein et al. that the average pCO2 reported here may be reflecting values ap- (2013) and Roth-Nebelsick et al. (2014), suggesting that the pCO2 proaching “true” palaeo-pCO2. signal may have been lost in the calibration. The model they use, the gas-exchange model of Konrad et al. (2008), has recently been tested

158 M. Steinthorsdottir et al. Palaeogeography, Palaeoclimatology, Palaeoecology 515 (2019) 152–161 with modern material and was shown to produce the most accurate 5. Conclusions pCO2 estimates when used with multiple species, to derive a consensus pCO2 (Grein et al., 2013). Therefore, single-species records are perhaps The Oligocene–Miocene transition (OMT) was a global cooling not appropriate for this model, and the results of Grein et al. (2013) event characterized by expansion of Antarctic ice volume as well as when using multiple fossil species, including Lauraceae, should be re- transient ice sheet retreat episodes and associated climate warming. In garded as the more reliable. Steinthorsdottir et al. (2016a) used a single New Zealand, the transition from the Oligocene to the Miocene is species dataset from the middle Eocene to latest Oligocene in the sto- marked by a change from a low-diversity Nothofagus-dominated pollen matal ratio method, and record pCO2 of ~475 ppm for the latest Oli- assemblage to one of higher diversity, interpreted to reflect relatively gocene. cool climate followed by warmer conditions. Oscillating episodes of

Most recently, a high-resolution pCO2 record from Foulden Maar in climate change across the OMT, including the transient Mi-1 glaciation, New Zealand indicated a brief “spike” or doubling in pCO2 to have long been difficult to reconcile with existing pCO2 records, but ~1100 ppm at the OMT for ~20 kyr, during the termination of Mi-1 recently, pCO2 data for this interval suggested that the termination of (Fig. 1)(Reichgelt et al., 2016) based on data derived using a separate Mi-1 was associated with a brief pulse of highly elevated pCO2 leaf gas-exchange model (Franks et al., 2014), and (Reichgelt et al., (Reichgelt et al., 2016). The new pCO2 record from the OMT into the 2016). This transient spike in pCO2 is interpreted to have occurred early Miocene of New Zealand presented here confirms highly elevated coincident with hydrological changes, i.e. increased moisture avail- pCO2 across the OMT at ~650 ppm compared to the pCO2 levels of ability in the area (Reichgelt et al., 2016), a concurrence that has also ~500 ppm estimated for the earliest and early Miocene. This implies been shown to have taken place during a doubling of pCO2 across the that pCO2 may have played a more important role in the termination of Tr–J boundary, due to the repression of stomatal transpiration the glaciation than previously thought. Although it is too early to assert

(Steinthorsdottir et al., 2012). Reichgelt et al., 2016 also tested the whether a significant transient excursion in pCO2 was, together with responsiveness of their chosen NLE (Litsea calicara) by plotting SD and orbital parameters, the forcer in the termination of Mi-1, it is timely to

SI derived from herbarium material to measured pCO2, but found that it state that this may have been the case, and should be investigated was not responsive and therefore did not cross-check their pCO2-record further. using additional stomatal proxy methods (stomatal ratio or transfer). We tested their published SI data with L. nobilis as NLE in the stomatal Acknowledgments ratio method, consistent with the methods used in this paper, and ob- tained very similar results to those presented by Reichgelt et al. (2016): We gratefully acknowledge funding from the Swedish Research a brief spike of ~1100 ppm, bounded by lower values of ~600 ppm Council (VR Starting Grant NT-7 2016 04905 to M.S. and VR 2015 4264 before, and ~500 ppm after the spike. We do not record as high pCO2 as to V.V.) and with additional funding from the Bolin Centre for Climate Reichgelt et al. (2016) in the present study, but speculate that this may Research, Stockholm University to M.S. V.V. further acknowledges be due to the lower stratigraphic resolution of our record, i.e. we record support from the Linnaeus Centre Lund University Carbon Cycle Centre the increased pCO2 but not the full increase – i.e. the spike. Although (LUCCI), funded by the Swedish Research Concil (VR 349 2007 8705). the high pCO2 values recorded here are also based on leaves from the M. Huber (Purdue University) is thanked for helpful discussions and Foulden Maar section, potentially raising worries regarding specific C.H. Lear (Cardiff University) provided constructive feedback on an local conditions causing the remarkably low SD/SI and thus high cali- earlier version of the manuscript. brated pCO2, the surrounding lower pCO2 values from Foulden Maar in Reichgelt et al. (2016) and from the additional regional sites reported References here mutually support the emerging pattern. However, the transient spike in pCO2 at the OMT needs to be replicated using stomatal den- Bai, Y.J., Chen, L.Q., Ranhotra, P.S., Wang, Q., Wang, Y.F., Li, C.S., 2015. Reconstructing – sities of fossil leaves from additional stratigraphic sections before full atmospheric CO2 during the Plio Pleistocene transition by fossil Typha. Glob. Chang. – fi Biol. 21, 874 881. con dence can be declared. Bannister, J.M., Conran, J.G., Lee, D.E., 2012. Lauraceae from rainforest surrounding an early Miocene maar lake, Otago, Southern New Zealand. Rev. Palaeobot. Palynol. 178, 13–34.

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