American Journal of Botany 101(9): 1486–1497, 2014.

EARLY EVIDENCE OF XEROMORPHY IN ANGIOSPERMS: STOMATAL ENCRYPTION IN A NEW EOCENE SPECIES OF BANKSIA (PROTEACEAE) FROM WESTERN AUSTRALIA1 RAYMOND J. CARPENTER2,3,7, STEPHEN MCLOUGHLIN4, ROBERT S. HILL3,5, KENNETH J. MCNAMARA6, AND GREGORY JOHN JORDAN2 2School

of Biological Sciences, University of Tasmania, Private Bag 55, Hobart, Tasmania 7001, Australia; 3School of Earth and Environmental Sciences, Benham Bldg DX 650 312, University of Adelaide, South Australia 5005, Australia; 4Department of Palaeobiology, Swedish Museum of Natural History, Box 50007 104 05 Stockholm, Sweden; 5South Australian Museum, North Terrace, Adelaide, South Australia 5000, Australia; and 6Department of Earth Sciences, University of Cambridge, Downing Street, Cambridge, CB2 3EQ, UK

• Premise of the study: Globally, the origins of xeromorphic traits in modern angiosperm lineages are obscure but are thought to be linked to the early Neogene onset of seasonally arid climates. Stomatal encryption is a xeromorphic trait that is prominent in Banksia, an archetypal genus centered in one of the world’s most diverse ecosystems, the ancient infertile landscape of Mediterranean-climate southwestern Australia. • Methods: We describe Banksia paleocrypta, a sclerophyllous species with encrypted stomata from silcretes of the Walebing and Kojonup regions of southwestern Australia dated as Late Eocene. • Key results: Banksia paleocrypta shows evidence of foliar xeromorphy ~20 Ma before the widely accepted timing for the onset of aridity in Australia. Species of Banksia subgenus Banksia with very similar leaves are extant in southwestern Australia. The conditions required for silcrete formation infer fluctuating water tables and climatic seasonality in southwestern Australia in the Eocene, and seasonality is supported by the paucity of angiosperm closed-forest elements among the fossil taxa preserved with B. paleocrypta. However, climates in the region during the Eocene are unlikely to have experienced seasons as hot and dry as present-day summers. • Conclusions: The presence of B. paleocrypta within the center of diversity of subgenus Banksia in edaphically ancient southwestern Australia is consistent with the continuous presence of this lineage in the region for ≥40 Ma, a testament to the success of increasingly xeromorphic traits in Banksia over an interval in which numerous other lineages became extinct.

Key words: Banksia; Eocene; Proteaceae; sclerophylly; silcrete; southwestern Australia; stomatal crypt; xeromorphy.

Arid and seasonally arid climates are typical of low and middle latitudes and include famous regions of Mediterranean climate in California, the Mediterranean basin, the Cape Region of South Africa, and southwestern Australia, in which there is a prolonged summer dry period. These Mediterranean-climate ecosystems are some of the most biologically diverse on Earth (Cowling et al., 1996) and are recognized biodiversity hotspots (Myers et al., 2000). The origin and evolution of arid and Mediterranean lineages and ecosystems have long attracted great interest worldwide (e.g., Andrews, 1916; Axelrod, 1958, 1975; Linder, 2003). These themes have also been the focus of several recent reviews based on molecular phylogenetic evidence (e.g., Byrne et al., 2008; Ackerly, 2009; Verboom et al., 2009; 1 Manuscript received 28 April 2014; revision accepted 27 August 2014. The authors thank the Australian Research Council (Discovery Projects 110104926 and 140100307) and Swedish Research Council (Vetenskapsrådet) for funding; the Western Australian Museum at Welshpool and the Edward de Courcy Clarke Earth Science Museum, University of Western Australia, for access and loans; and two anonymous reviewers for suggestions that improved the manuscript. 7 Author for correspondence (e-mail: raymond.carpenter@adelaide. edu.au)

doi:10.3732/ajb.1400191

Lancaster and Kay, 2013), although pertinent fossil evidence is extremely limited. Nevertheless, there is broad agreement that in each of the extant Mediterranean-climate regions, some form of pronounced climatic seasonality involving extended dry periods dates to the Early Neogene, ~15–20 mya. Progressive global aridification has been attributed to the combined effects of declining atmospheric CO2 levels, the establishment of the Antarctic circumpolar current at the end of the Paleogene, and enhanced latitudinal temperature gradients (e.g., McGowran et al., 2000; Zachos et al., 2001; Miller et al., 2009). Banksia L.f. (Proteaceae) has special significance for understanding the origins of scleromorphy and xeromorphy (Hill, 1994, 1998) and thus may help illuminate the origins of seasonally arid climates (Jordan et al., 2008). The genus is a conspicuous component of the extant Australian flora that is especially diverse in the Mediterranean-climate Southwest Australian Floristic Region (SWAFR: Hopper and Gioia, 2004), and it and its close relatives (Tribe Banksieae) have an extensive leaf fossil record from across Australia and also in New Zealand (Carpenter, 2012, and references therein). The oldest Banksia leaf fossils so far known from the Late Paleocene of eastern Australia are scleromorphic (Carpenter et al., 1994) but not xeromorphic in relation to extant species (i.e., they do not show “characters that are clearly involved in increasing the boundary layer and thus

American Journal of Botany 101(9): 1486–1497, 2014; http://www.amjbot.org/ © 2014 Botanical Society of America

1486

September 2014]

CARPENTER ET AL.—XEROMORPHIC BANKSIA FOSSILS

in slowing down water loss”; Hill, 1998, p. 393). Hill (1998) reasoned that the most convincing characters of this syndrome are individual stomatal protection, stomatal pits, and revolute leaf margins. Most Banksia species show varying degrees of either or both of the latter two traits, and in most species in Banksia subgenus Banksia (which includes Dryandra) the pits (hereafter “crypts”) are very deep and have constricted entrances, which are themselves enmeshed with trichomes (Mast and Givnish, 2002; Mast and Thiele, 2007). Here, we report fossil foliage from silicified sediments of the Upper Eocene Kojonup Sandstone of Western Australia. In particular, we make the novel observation that crypt, stomatal, and trichome-base details are preserved on some of the impression fossils. These features allow the specimens to be assigned to a new species that constitutes the oldest record of stomatal encryption in the genus Banksia, and, as far as we are aware, the oldest convincing record of xeromorphy in modern angiosperms. We discuss the significance of the fossils in the context of seasonal climates in the Australian Eocene. MATERIALS AND METHODS Fossil sites and ages—Fossil plant material occurs as impressions in silicified sandstone (silcrete) referred to the Kojonup Sandstone, which is found as scattered outcrops close to the Meckering Line (Fig. 1)—a subtle topographic

1487

division between the headwaters of rejuvenated drainage systems feeding into the Indian Ocean to the west and relict paleodrainage systems, mostly defined by chains of swamps and playa lakes on the Yilgarn Craton, to the east—in southwestern Australia (Wilde and Backhouse, 1977; Scriven et al., 1995; McLoughlin and Hill, 1996; McLoughlin and McNamara, 2001). The sediments of the Kojonup Sandstone are strongly silicified and are considered to have been formed from the deep weathering of Precambrian granitic rocks. Near Walebing, fine-grained sandstones occur that are interpreted to be autochthonous (Stevens, 2002), whereas in a few other locations (e.g., at Muradup near Kojonup) the sandstones show weak stratification and inclusion of rounded pebbles that indicate limited fluvial sediment transport. The Late Eocene age of the Kojonup Sandstone is based on the close resemblances of the fossil plants to those present in the Upper Eocene Pallinup Formation (formerly Pallinup Siltstone: Cockbain, 1968), which was described in detail by Clarke et al. (2003). The Pallinup Formation is a siliceous spongolite, and like the silicified Kojonup Sandstone, records a period of intense mobilization and precipitation of silica. The specimens studied here were collected in the Walebing and Kojonup regions of southwestern Australia, which are ~370 km apart (Fig. 1). Preparation of specimens and identifications—All specimens discussed here are housed at the Western Australian Museum (WAM). Some were briefly discussed and illustrated by McLoughlin and Hill (1996: fig. 4.6) and McLoughlin and McNamara (2001: publication cover and fig. 14E). Specimens were photographed using a Nikon (Tokyo, Japan) D5000 digital SLR camera. For some specimens, silicone casts were taken using Oranwash L c-silicone impression material (Zhermack Clinical, Badia Polesine [Rovigo], Italy). Parts of some casts were mounted on scanning electron microscope (SEM) aluminum stubs, sputter coated with carbon and gold, then examined and photographed using a Philips (Eindhoven, the Netherlands) XL 30 Field Emission Gun SEM operated at 10 kV at the University of Adelaide. The SEM stubs with the silicone

Fig. 1. Map of southwestern Western Australia, showing fossiliferous silcrete locations, including those yielding the Banksia paleocrypta specimens; and sedimentary basins, paleodrainage channels, and paleodrainage divisions (after Hocking and Cockbain, 1990). The boundary of the Southwest Australian Floristic Region (SWAFR) and the distributions of the two extant Banksia species that are morphologically most similar to B. paleocrypta (B. burdettii and B. menziesii) follow FloraBase (2014).

1488

AMERICAN JOURNAL OF BOTANY

[Vol. 101

Figs. 2–7. Banksia paleocrypta sp. nov. specimens (all impressions). (2) Holotype (WAM P.89.32). Note details of venation; scale bar = 5 mm. (3) WAM P.88.43. This is a very small leaf (at left). Note also a different Banksia leaf morphospecies at right; scale bar = 5 mm. (4) WAM uncatalogued specimen

September 2014]

CARPENTER ET AL.—XEROMORPHIC BANKSIA FOSSILS

peels are currently housed at the University of Adelaide. Leaves of comparable extant Banksia species were examined at the Queensland Herbarium (BRI), and a leaf of B. burdettii Baker f. was selected from a herbarium sample (PERTH 1090798) held at the University of Adelaide for detailed study using SEM. An application of wood glue was applied to the abaxial surface of this leaf, allowed to dry, and peeled off to largely remove the cover of trichomes. Placement of the fossils within Banksia follows Carpenter et al. (2010), who recognized that because of the paraphyly of Banksia with respect to Dryandra (Mast, 1998; Mast and Givnish, 2002; Mast et al., 2005) and the consequent synonymizing of the latter genus (Mast and Thiele, 2007), well-preserved fossils with evidence of apomorphies of Banksia should now be assigned to that genus and not to Banksieaephyllum, which was originally erected by Cookson and Duigan (1950) because of the impracticability of identifying leaf fossils with either Banksia or Dryandra. The preservation of surface details on the fossils allowed some quantitative assessment of leaf scleromorphy and xeromorphy following the methods of Hassiotou et al. (2009). Thus, stomatal crypt aperture areas, stomatal lengths, and interstomatal distances were estimated from scanning electron micrographs of silicone casts from two specimens using ImageJ software (Abramoff et al., 2004). Stomatal crypt depths were estimated from two other fossil specimens loaned from WAM at the University of Adelaide using a Leica (Leica Microsystems, Wetzlar, Germany) MZ16FA stereo microscope fitted with a Leica IC 3D camera system and Leica Microscope Imaging software.

SYSTEMATICS AND RESULTS Family— Proteaceae Juss. Subfamily— Grevilleoideae Engl. Tribe— Banksieae Reichb. Subtribe— Banksiinae L. A. S. Johnson & B. G. Briggs. Genus— Banksia L.f. Species— Banksia paleocrypta R. J. Carp., McLoughlin, R. S. Hill, McNamara & G. J. Jord. sp. nov. (Figs. 2–11). Etymology— In recognition of the fossil leaves having obvious stomatal crypts. Holotype— WAM P.89.32 Western Australian Museum, Perth (Fig. 2), a specimen from the Walebing locality, Western Australia. Precise details of this locality are kept on file in the Department of Earth and Planetary Sciences at the WAM. Additional specimens— Additional specimens include (all prefixed WAM P.) 11.1 (Fig. 10), 81.16.(4), 81.19.(9), 81.21. (1), 81.24.(1) (Fig. 7), 81.26g, 81.27.(1) (Fig. 6), 81.29.(1), 81.35.(1), 81.48.(1), 86.124.(1), 86.125.(1), 86.131.(1), 86.133. (1), 87.4, 89.151, 89.59, plus several uncatalogued specimens (Figs. 4, 5) from the Walebing region; and 87.48, 87.92 and 88.43 (Fig. 3) from the Kojonup region. Silicone peels on SEM stubs taken from specimens 81.27.(1) (Figs. 8, 11) and 88.43 (Fig. 9) are stored at the University of Adelaide. Specific diagnosis— Fossil Banksia leaves thick, dentate to serrately toothed. Most major veins in mature leaves arise at

1489

~90° from midvein. Stomata in abaxial crypts. Cylindrical trichome bases abundant all over abaxial side. Description— Leaves (Figs. 2–7) thick with recurved margins and prominent midveins, regularly toothed. Leaves variable in size, typically ~10 mm wide (largest ≤20 mm wide) in specimens from the Walebing region (Figs. 2, 4, 5, 7), and 40 mya, in the Middle Eocene, and it is highly probable that the two subgenera have been in southwestern Australia for most, if not all, of this time (Mast and Givnish, 2002; Cardillo and Pratt, 2013). However, although Banksia infructescences (or “cones”) of Middle or Late Eocene age have been found in the region (McNamara and Scott, 1983), as well as the Late Eocene leaves described here and by McLoughlin and Hill (1996) and McLoughlin and McNamara (2001), on present evidence neither the cones nor the leaves show apomorphies that would allow them to be placed in either of the subgenera with confidence. Deeply encrypted stomata were reconstructed as having evolved

1494

[Vol. 101

AMERICAN JOURNAL OF BOTANY

in the most recent common ancestor of subgenus Banksia by Mast and Givnish (2002). However, Mast and Thiele (2007) did not recognize any foliar synapomorphies in their new treatment of the genus, and as discussed above, encrypted stomata do occur in subgenus Spathulatae. Therefore, although we have demonstrated that B. paleocrypta is closely similar to leaves of several extant species of subgenus Banksia, we do not formally assign our species to the crown group. Interestingly, the two closely related extant species (B. burdettii and B. menziesii) to which B. paleocrypta is most similar occur near where the fossils were found (Fig. 1), but this clade has an estimated age of only ~2 Ma (Cardillo and Pratt, 2013). Accepting this estimate suggests repeated evolution of similar foliar forms of Banksia in the same region, perhaps in response to similar selective pressures. Banksia paleocrypta probably occupied an extremely infertile, perhaps sunny niche within local, mostly sclerophyll vegetation formed on quartzose sand. Intermittent water deficits that represented the beginnings of a seasonally dry climate in the region were experienced. There appears little doubt that the early evolution in Banksia of scleromorphic leaves with small areolar regions (see Carpenter, 1994; Mast and Givnish, 2002) was instrumental in allowing increasing xeromorphy that included progressively smaller crypt apertures as the Australian climate became increasingly arid during the Neogene. An alternative strategy in thick-leaved Proteaceae of open habitats that also more readily allows diffusion to mesophyll layers is amphistomaty (Brodribb et al., 2013), a trait that occurs in nearly all of the ~250 species of subfamilies Proteoideae and Persoonioideae in the SWAFR and Proteoiodeae in the Cape Region (South Africa), and that probably also has ancient origins (Carpenter, 2012; Jordan et al., 2014). Earliest convincing evidence of xeromorphy among modern angiosperm lineages— It has been argued that modern Mediterranean-climate lineages of the Mediterranean basin and the Californian chaparral had origins in more mesic Paleogene vegetation, which contained species with leaf traits that preadapted them to seasonally dry climates (Axelrod, 1958, 1975). However, this hypothesis is not supported by recent phylogenetic evidence (e.g., Vargas et al., 2014), and fossil leaf impressions, such as those used by Axelrod, typically cannot show evidence of xeromorphy in the absence of micromorphology, even if these leaf fossils closely resemble leaves of extant species of drier vegetation types. Indeed, as far as we are aware, there are no convincing previous records of Paleogene or older xeromorphic fossil leaves among Mediterranean-climate lineages. It is also possible that the Western Australian Banksia fossils described here are the best and oldest evidence of xeromorphy in angiosperms. Although there is an emerging understanding that Cretaceous angiosperms were generally xerophobic (Feild et al., 2009) and had leaves of low mass per area (Royer et al., 2010), it should be recognized that the fossil record is strongly biased to plants of wet habitats and probably wet climates. Also, there are several records of early angiosperm taxa that show features that are at least suggestive of xeromorphy. These taxa include Sapindopsis lebanensis Krassilov & Maslova from the mid-Cenomanian of Lebanon (Krassilov and Bacchia, 2000) and Tenuiloba canalis Serlin from the Early Cretaceous of central Texas (Serlin, 1982). However, as far as we are aware, none of these taxa has stomatal crypts, and although Tenuiloba leaves are

highly dissected, with stomata restricted to grooves on each side of the midvein, the margins are only slightly revolute, the cuticle is very thin, the stomata are not sunken, and the regional climate at the time of deposition was relatively damp and equable (Serlin, 1982). Moreover, subsequent authors have questioned whether Tenuiloba has angiospermous affinities (Upchurch et al., 1994), and the relationships of the other taxa to extant lineages are at best obscure. Whatever the main driver of the evolution of encryption in angiosperms, B. paleocrypta shows this feature >20 Ma before the widely accepted timing for the Miocene onset of aridity in Australia (Byrne et al., 2008), and before the records of other Banksia species with encrypted stomata from Oligo-Miocene lignites of southeastern Australia (Cookson and Duigan, 1950). Conclusion— Banksia paleocrypta is a new Late Eocene species found in southwestern Australia, the center of diversity of the genus and the extant home of species with remarkably similar foliage. The fossils are the oldest to show stomatal encryption, a trait that has widely been described as xeromorphic, well before climatic aridity is asserted to have expanded globally in the Neogene. Sclerophylly and stomatal encryption in B. paleocrypta evolved in a region of extreme edaphic infertility, in a warm climate and under conditions that promoted a fluctuating water table, probably as a result of increasingly seasonal rainfall. Increasing Neogene aridity led to the evolution of greater xeromorphy in Banksia in the form of deeper crypts with narrower apertures, but these more extreme climates eventually contributed to the extinctions of numerous, less welladapted mesic lineages in southwestern Australia. LITERATURE CITED ABRAMOFF, M. D., P. J. MAGELHAES, AND S. J. RAM. 2004. Image processing with ImageJ. Biophotonics International 11: 36–42. ACKERLY, D. D. 2009. Evolution, origin and age of lineages in the Californian and Mediterranean floras. Journal of Biogeography 36: 1221–1233. ALVIN, K. L. 1982. Cheirolepidiaceae: Biology, structure and palaeoecology. Review of Palaeobotany and Palynology 37: 71–98. ANDREWS, E. C. 1916. The geological history of the Australian flowering plants. American Journal of Science 42: 171–232. AXELROD, D. I. 1958. Evolution of the Madro-Tertiary geoflora. Botanical Review 24: 433–509. AXELROD, D. I. 1975. Evolution and biogeography of Madrean-Tethyan sclerophyll vegetation. Annals of the Missouri Botanical Garden 62: 280–334. BEADLE, N. C. W. 1966. Soil phosphate and its role in molding segments of the Australian flora and vegetation, with special reference to xeromorphy and scleromorphy. Ecology 47: 992–1007. BELL, D., AND L. STEPHENS. 1984. Seasonality and phenology of Kwongan species. In J. Pate and J. Beard [eds.], Kwongan, plant life of the sandplain, 205–226. University of Western Australia Press, Perth, Western Australia. BINT, A. N. 1981. An early Pliocene pollen assemblage from Lake Tay, south-western Australia, and its phytogeographic implications. Australian Journal of Botany 29: 277–291. BRODRIBB, T., AND R. S. HILL. 1998. The photosynthetic drought physiology of a diverse group of southern hemisphere conifer species is correlated with minimum seasonal rainfall. Functional Ecology 12: 465–471. BRODRIBB, T. J., G. J. JORDAN, AND R. J. CARPENTER. 2013. Unified changes in cell size permit coordinated leaf evolution. New Phytologist 199: 559–570. BUTT, C. R. M. 1985. Granite weathering and silcrete formation on the Yilgarn Block, Western Australia. Australian Journal of Earth Sciences 32: 415–432.

September 2014]

CARPENTER ET AL.—XEROMORPHIC BANKSIA FOSSILS

BYRNE, M., D. K. YEATES, L. JOSEPH, M. KEARNEY, J. BOWLER, M. A. J. WILLIAMS, S. COOPER, ET AL. 2008. Birth of a biome: Insights into the assembly and maintenance of the Australian arid zone biota. Molecular Ecology 17: 4398–4417. CANHAM, C. A., R. H. FROEND, W. D. STOCK, AND M. DAVIES. 2012. Dynamics of phreatophyte root growth relative to a seasonally fluctuating water table in a Mediterranean-type environment. Oecologia 170: 909–916. CARDILLO, M., AND R. PRATT. 2013. Evolution of a hotspot genus: geographic variation in speciation and extinction rates in Banksia (Proteaceae). BMC Evolutionary Biology 13: 155. CARPENTER, R. J. 1994. Cuticular morphology and aspects of the ecology and fossil history of North Queensland rainforest Proteaceae. Botanical Journal of the Linnean Society 116: 249–303. CARPENTER, R. J. 2012. Proteaceae leaf fossils: Phylogeny, diversity, ecology and austral distributions. Botanical Review 78: 261–287. CARPENTER, R. J., M. P. GOODWIN, R. S. HILL, AND K. KANOLD. 2011. Silcrete plant fossils from Lightning Ridge, New South Wales: New evidence for climate change and monsoon elements in the Australian Cenozoic. Australian Journal of Botany 59: 399–425. CARPENTER, R. J., R. S. HILL, D. R. GREENWOOD, A. D. PARTRIDGE, AND M. BANKS. 2004. No snow in the mountains: Early Eocene plant fossils from Hotham Heights, Victoria, Australia. Australian Journal of Botany 52: 685–718. CARPENTER, R. J., AND G. J. JORDAN. 1997. Early Tertiary macrofossils of Proteaceae from Tasmania. Australian Systematic Botany 10: 533–563. CARPENTER, R. J., G. J. JORDAN, AND R. S. HILL. 1994. Banksieaephyllum taylorii (Proteaceae) from the Late Palaeocene of New South Wales and its relevance to the origin of Australia’s scleromorphic flora. Australian Systematic Botany 7: 385–392. CARPENTER, R. J., G. J. JORDAN, D. E. LEE, AND R. S. HILL. 2010. Leaf fossils of Banksia (Proteaceae) from New Zealand: An Australian abroad. American Journal of Botany 97: 288–297. CARPENTER, R. J., AND M. POLE. 1995. Eocene plant fossils from the Lefroy and Cowan Paleodrainages, Western Australia. Australian Systematic Botany 8: 1107–1154. CHILEFLORA. 2012. Website: http://www.chileflora.com. CLARKE, J. D. A., P. R. GAMMON, B. HOU, AND S. J. GALLAGHER. 2003. Middle to Upper Eocene stratigraphic nomenclature and deposition in the Eucla Basin. Australian Journal of Earth Sciences 50: 231–248. COCKBAIN, A. E. 1968. The stratigraphy of the Plantagenet Group, Western Australia. Geological Survey of Western Australia Annual Report 1967: 61–63. COMMONWEALTH OF AUSTRALIA, BUREAU OF METEOROLOGY. 2014. Website: http://www.bom.gov.au/climate/averages/tables/. COOKSON, I. C., AND S. L. DUIGAN. 1950. Fossil Banksieae from Yallourn, Victoria, with notes on the morphology and anatomy of living species. Australian Journal of Scientific Research, Series B 3: 133–165. COWLING, R. M., P. W. RUNDEL, B. B. LAMONT, M. K. ARROYO, AND M. ARIANOUTSOU. 1996. Plant diversity in Mediterranean-climate regions. Trends in Ecology & Evolution 11: 362–366. DODSON, J. R., AND M. K. MACPHAIL. 2004. Palynological evidence for aridity events and vegetation change during the Middle Pliocene, a warm period in southwestern Australia. Global and Planetary Change 41: 285–307. FEILD, T. S., D. S. CHATELET, AND T. J. BRODRIBB. 2009. Ancestral xerophobia: A hypothesis on the whole plant ecophysiology of early angiosperms. Geobiology 7: 237–264. FLEXAS, J., A. DIAZ-ESPEJOB, J. GAGOA, A. GALLÉA, J. GALMÉSA, J. GULÍASA, AND H. MEDRANO. 2014. Photosynthetic limitations in Mediterranean plants: A review. Environmental and Experimental Botany 103: 12–23. FLORABASE. 2014. FloraBase: The Western Australian Flora. Western Australian Herbarium, Western Australian Department of Parks and Wildlife, Perth. http://florabase.dpaw.wa.gov.au/. GAMMON, P. R., AND N. P. JAMES. 2003. Paleoenvironmental controls on Upper Eocene biosiliceous neritic sediments, southern Australia. Journal of Sedimentary Geology 73: 957–972.

1495

GEORGE, A. S. 1999. Banksia. Flora of Australia 17B: 175–251. GORDENKO, N. V., AND A. V. BROUSHKIN. 2010. A new bennettitalean genus from the Middle Jurassic of the Mikhailovskii Rudnik locality (Kursk region, Russia). Paleontological Journal 44: 1308–1320. GREENWOOD, D. R., P. T. MOSS, A. I. ROWETT, A. J. VADALA, AND R. L. KEEFE. 2003. Plant communities and climatic change in southeastern Australia during the early Paleogene. In S. L. Wing, P. D. Gingerich, B. Schmitz, and E. Thomas [eds.], Causes and consequences of globally warm climates in the early Paleogene. Geological Society of America Special Paper 369: 365–380. HASSIOTOU, F., J. R. EVANS, M. LUDWIG, AND E. J. VENEKLAAS. 2009. Stomatal crypts may facilitate diffusion of CO2 to adaxial mesophyll cells in thick sclerophylls. Plant, Cell & Environment 32: 1596–1611. HAWORTH, M., AND J. MCELWAIN. 2008. Hot, dry, wet, cold or toxic? Revisiting the ecological significance of leaf and cuticular micromorphology. Palaeogeography, Palaeoclimatology, Palaeoecology 262: 79–90. HILL, R. S. 1994. The history of selected Australian taxa. In R. S. Hill [ed.], History of the Australian vegetation: Cretaceous to Recent, 390–419. Cambridge University Press, Cambridge, UK. HILL, R. S. 1998. Fossil evidence for the onset of xeromorphy and scleromorphy in Australian Proteaceae. Australian Systematic Botany 11: 391–400. HILL, R. S., AND H. E. MERRIFIELD. 1993. An Early Tertiary macroflora from West Dale, southwestern Australia. Alcheringa 17: 285–326. HOCKING, R. M., AND A. E. COCKBAIN. 1990. Regolith. Geology and mineral resources of Western Australia. Western Australian Geological Survey Memoir 3: 591–602. HOPPER, S. D. 2009. OCBIL theory: Towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes. Plant and Soil 322: 49–86. HOPPER, S. D., AND P. GIOIA. 2004. The Southwest Australian Floristic Region: Evolution and conservation of a global hot spot of biodiversity. Annual Review of Ecology, Evolution, and Systematics 35: 623–650. JOHNSON, L. A. S., AND B. G. BRIGGS. 1975. On the Proteaceae—The evolution and classification of a southern family. Botanical Journal of the Linnean Society 70: 83–182. JORDAN, G. J., R. J. CARPENTER, AND T. J. BRODRIBB. 2014. Using fossil leaves as evidence for open vegetation. Palaeogeography, Palaeoclimatology, Palaeoecology 395: 168–175. JORDAN, G. J., R. J. CARPENTER, AND R. S. HILL. 1998. The macrofossil record of Proteaceae: a review with new species. Australian Systematic Botany 11: 465–501. JORDAN, G. J., P. H. WESTON, R. J. CARPENTER, R. A. DILLON, AND T. J. BRODRIBB. 2008. The evolutionary relations of sunken, covered, and encrypted stomata to dry habitats in Proteaceae. American Journal of Botany 95: 521–530. KEMP, E. M. 1978. Tertiary climatic evolution and vegetation history in the south-east Indian Ocean region. Palaeogeography, Palaeoclimatology, Palaeoecology 24: 169–208. KERSHAW, A. P., H. A. MARTIN, AND J. R. C. MCEWEN MASON. 1994. The Neogene: A period of transition. In R. S. Hill [ed.], History of the Australian vegetation: Cretaceous to Recent, 299–327. Cambridge University Press, Cambridge, UK. KRASSILOV, V., AND F. BACCHIA. 2000. Cenomanian florule of Nammoura, Lebanon. Cretaceous Research 21: 785–799. LAMBERS, H., M. C. BRUNDRETT, J. A. RAVEN, AND S. D. HOPPER. 2010. Plant mineral nutrition in ancient landscapes: High plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant and Soil 334: 11–31. LAMBERS, H., G. R. CAWTHRAY, P. GIAVALISCO, J. KUO, E. LALIBERTÉ, S. J. PEARSE, W.-R. SCHEIBLE, ET AL. 2012. Proteaceae from severely phosphorus-impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus-use efficiency. New Phytologist 196: 1098–1108. LANCASTER, L. T., AND K. M. KAY. 2013. Origin and diversification of the California flora: Re-examining classic hypotheses with molecular phylogenies. Evolution 67: 1041–1054.

1496

AMERICAN JOURNAL OF BOTANY

LINDER, H. P. 2003. The radiation of the Cape flora, southern Africa. Biological Reviews of the Cambridge Philosophical Society 78: 597–638. LÖSCH, R., J. D. TENHUNEN, J. S. PEREIRA, AND O. L. LANGE. 1982. Diurnal courses of stomatal resistance and transpiration of wild and cultivated Mediterranean perennials at the end of the summer dry season in Portugal. Flora 172: 138–160. MARTIN, H. A. 2006. Cenozoic climatic change and the development of the arid vegetation in Australia. Journal of Arid Environments 66: 533–563. MAST, A. R. 1998. Molecular systematics of subtribe Banksiinae (Banksia and Dryandra; Proteaceae) based on cpDNA and nrDNA sequence data: Implications for taxonomy and biogeography. Australian Systematic Botany 11: 321–342. MAST, A. R., AND T. J. GIVNISH. 2002. Historical biogeography and the origin of stomatal distributions in Banksia and Dryandra (Proteaceae) based on their cpDNA phylogeny. American Journal of Botany 89: 1311–1323. MAST, A. R., E. H. JONES, AND S. P. HAVERY. 2005. An assessment of old and new DNA sequence evidence for the paraphyly of Banksia and Dryandra (Proteaceae). Australian Systematic Botany 18: 75–88. MAST, A. R., AND K. THIELE. 2007. The transfer of Dryandra R.Br. to Banksia L.f. (Proteaceae). Australian Systematic Botany 20: 63–71. MCGOWRAN, B. 1989. Silica burp in the Eocene ocean. Geology 17: 857–860. MCGOWRAN, B., M. ARCHER, P. BOCK, T. A. DARRAGH, H. GODTHELP, S. HAGEMAN, S. J. HAND, ET AL. 2000. Australasian palaeobiogeography: The Palaeogene and Neogene record. Memoir of the Association of Australasian Palaeontologists 23: 405–470. MCLOUGHLIN, S., AND A. N. DRINNAN. 1996. Anatomically preserved Noeggerathiopsis leaves from east Antarctica. Review of Palaeobotany and Palynology 92: 207–227. MCLOUGHLIN, S., AND R. S. HILL. 1996. The succession of Western Australian Phanerozoic terrestrial floras. In S. D. Hopper, J. A. Chappill, M. S. Harvey, and A. S. George [eds.], Gondwanan heritage: Past, present and future of the Western Australian biota, 61–80. Surrey Beatty & Sons, Chipping Norton, Australia. MCLOUGHLIN, S., AND K. MCNAMARA. 2001. Ancient floras of Western Australia. Western Australian Museum, Perth, Western Australia. MCNAMARA, K. J., AND J. K. SCOTT. 1983. A new species of Banksia (Proteaceae) from the Eocene Merlinleigh Sandstone of the Kennedy Range, Western Australia. Alcheringa 7: 185–193. MELETIOU-CHRISTOU, M.-S., AND S. RHIZOPOULOU. 2012. Constraints of photosynthetic performance and water status of four evergreen species co-occurring under field conditions. Botanical Studies (Taipei, Taiwan) 53: 325–334. MEYEN, S. V. 1963. Anatomy and nomenclature of Angara Cordaites leaves. Палеонmолоƨический журнал 3: 96–107 [in Russian]. MEYEN, S. V., AND H. G. SMOLLER. 1986. The genus Mostotchkia Chachlov (upper Palaeozoic of Angaraland) and its bearing on the characteristics of the Order Dicranophyllales (Pinopsida). Review of Palaeobotany and Palynology 47: 205–223. MILLER, K. G., J. D. WRIGHT, M. E. KATZ, B. S. WADE, J. V. BROWNING, B. S. CRAMER, AND Y. ROSENTHAL. 2009. Climate threshold at the Eocene–Oligocene transition: Antarctic ice sheet influence on ocean circulation. In C. Koeberl and A. Montanari [eds.], The Late Eocene earth—hothouse, icehouse and impacts. Geological Society of America Special Publications 452: 169–178. MOTT, K. A., AND D. PEAK. 2013. Testing a vapour-phase model of stomatal responses to humidity. Plant, Cell & Environment 36: 936–944. MYERS, N., R. A. MITTERMEIER, C. G. MITTERMEIER, G. A. B. DA FONSECA, AND J. KENT. 2000. Biodiversity hot spots for conservation priorities. Nature 403: 853–858. PATE, J. S., G. WEBER, AND K. W. DIXON. 1984. Growth and life form of kwongan species. In J. Pate and J. Beard [eds.], Kwongan, plant life of the sandplain, 84–100. University of Western Australia Press, Perth. POTT, C., M. KRINGS, AND H. KERP. 2008. The Carnian (Late Triassic) flora from Lunz in Lower Austria: Paleoecological considerations. Palaeoworld 17: 172–182.

[Vol. 101

POTT, C., AND S. MCLOUGHLIN. 2009. Bennettitalean foliage in the Rhaetian–Bajocian (latest Triassic–Middle Jurassic) floras of Scania, southern Sweden. Review of Palaeobotany and Palynology 158: 117–166. READ, J., AND J. FRANCIS. 1992. Responses of some Southern Hemisphere tree species to a prolonged dark period and their implications for high-latitude Cretaceous and Tertiary floras. Palaeogeography, Palaeoclimatology, Palaeoecology 99: 271–290. ROTH-NEBELSICK, A. 2007. Computer-based studies of diffusion through stomata of different architecture. Annals of Botany 100: 23–32. ROTH-NEBELSICK, A., F. HASSIOTOU, AND E. J. VENEKLAAS. 2009. Stomatal crypts have small effects on transpiration: A numerical model analysis. Plant Physiology 151: 2018–2027. ROYER, D. L., I. M. MILLER, D. J. PEPPE, AND L. J. HICKEY. 2010. Leaf economic traits from fossils support a weedy habit for early angiosperms. American Journal of Botany 97: 438–445. ROYER, D. L., C. P. OSBORNE, AND D. J. BEERLING. 2005. Contrasting seasonal patterns of carbon gain in evergreen and deciduous trees of ancient polar forests. Paleobiology 31: 141–150. SARGENT, O. H. 1930. Xerophytes and xerophily, with special reference to Protead distribution. Proceedings of the Linnean Society of New South Wales 55: 577–586. SCRIVEN, L. J., S. MCLOUGHLIN, AND R. S. HILL. 1995. Nothofagus plicata (Nothofagaceae), a new deciduous Eocene macrofossil species, from southern continental Australia. Review of Palaeobotany and Palynology 86: 199–209. SERLIN, B. S. 1982. An Early Cretaceous fossil flora from northwest Texas: Its composition and implications. Palaeontographica Abteilung B 182: 52–86. SPECHT, R. L., AND P. RAYSON. 1957. Dark Island heath (Ninety-Mile Plain, South Australia) I. Definition of the ecosystem. Australian Journal of Botany 5: 52–85. STEVENS, A. 2002. The palaeoclimatic and palaeoenvironmental significance of an early Cenozoic flora from the Darling Range. Honours thesis, Curtin University, Perth, Western Australia. SULPICE, R., H. ISHIHARA, A. SCHLERETH, G. R. CAWTHRAY, B. ENCKE, P. GIAVALISCO, A. IVAKOV, ET AL. 2014. Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species. Plant, Cell & Environment 37: 1276–1298. THIELE, K., AND P. Y. LADIGES. 1996. A cladistic analysis of Banksia (Proteaceae). Australian Systematic Botany 9: 661–733. THIRY, M. 1989. Geochemical evolution and paleoenvironments of the Eocene continental deposits in the Paris Basin. Palaeogeography, Palaeoclimatology, Palaeoecology 70: 153–163. THIRY, M. 2000. Palaeoclimatic interpretation of clay minerals in marine deposits: An outlook from the continental origin. Earth-Science Reviews 49: 201–221. THIRY, M., AND A. R. MILNES. 1991. Pedogenic and groundwater silcretes at Stuart Creek opal field, South Australia. Journal of Sedimentary Petrology 61: 111–127. THIRY, M., A. R. MILNES, V. RAYOT, AND R. SIMON-COINÇON. 2006. Interpretation of palaeoweathering features and successive silicifications in the Tertiary regolith of inland Australia. Journal of the Geological Society 163: 723–736. TOSOLINI, A.-M. P., S. MCLOUGHLIN, B. E. WAGSTAFF, D. J. CANTRILL, AND S. J. GALLAGHER. 2014. Cheirolepidiacean foliage and pollen from Cretaceous high-latitudes of southeastern Australia. Gondwana Research 26: in press. TURNER, I. M. 1994. Sclerophylly: Primarily protective? Functional Ecology 8: 669–675. ULLYOTT, J. S., D. J. NASH, AND P. A. SHAW. 1998. Recent advances in silcrete research and their implications for the origin and palaeoenvironmental significance of sarsens. Proceedings of the Geologists’ Association 109: 255–270. UPCHURCH, G. R., P. R. CRANE, AND A. N. DRINNAN. 1994. The Megaflora from the Quantico Locality (Upper Albian), Lower Cretaceous Potomac Group of Virginia. Virginia Museum of Natural History Memoir 4. Martinsville, Virginia, USA.

September 2014]

CARPENTER ET AL.—XEROMORPHIC BANKSIA FOSSILS

VAN DE GRAAFF, W. J. E. 1983. Silcrete in Western Australia: geomorphological settings, textures, structures, and their genetic implications. In R. C. L. Wilson [ed.] Residual deposits: surface related weathering processes and materials, 159–166. Geological Society of London, Special Publication. VAN DE GRAAFF, W. J. E., R. J. CROWE, J. A. BUNTING, AND M. J. JACKSON. 1977. Relict of early Cenozoic drainage in arid Western Australia. Zeitschrift für Geomorphologie 21: 379–400. VARGAS, P., L. M. VALENTE, J. L. BLANCO-PASTOR, I. LIBERAL, B. GUZMÁN, E. CANO, A. FORREST, AND M. FERNÁNDEZ-MAZUECOS. 2014. Testing the biogeographical congruence of palaeofloras using molecular phylogenetics: snapdragons and the Madrean–Tethyan flora. Journal of Biogeography 41: 932–943. VENEKLAAS, E. J., AND P. POOT. 2003. Seasonal patterns in water use and leaf turnover of different plant functional types in a species rich woodland, south-western Australia. Plant and Soil 257: 295–304. VERBOOM, G. A., J. K. ARCHIBALD, F. T. BAKKER, D. U. BELLSTEDT, F. CONRAD, L. L. DREYER, F. FOREST, ET AL. 2009. Origin and diversification of the Greater Cape flora: Ancient species repository, hot-bed of recent radiation, or both? Molecular Phylogenetics and Evolution 51: 44–53. VERBOOM, W. H., AND J. S. PATE. 2006a. Bioengineering of soil profiles in semiarid ecosystems: The ‘phytotarium’concept. A review. Plant and Soil 289: 71–102.

1497

VERBOOM, W. H., AND J. S. PATE. 2006b. Evidence of active biotic influences in pedogenetic processes. Case studies from semiarid ecosystems of south-west Western Australia. Plant and Soil 289: 103–121. VERBOOM, W. H., AND J. S. PATE. 2013. Exploring the biological dimension to pedogenesis with emphasis on the ecosystems, soils and landscapes of southwestern Australia. Geoderma 211-212: 154–183. VILLAR DE SEOANE, L. 2001. Cuticular study of Bennettitales from the Springhill Formation, Lower Cretaceous of Patagonia, Argentina. Cretaceous Research 22: 461–479. WARNAAR, J., P. K. BIJL, M. HUBER, L. SLOAN, H. BRINKHUIS, U. RÖHL, R. SRIVER, AND H. VISSCHER. 2009. Orbitally forced climate changes in the Tasman sector during the Middle Eocene. Palaeogeography, Palaeoclimatology, Palaeoecology 280: 361–370. WILDE, S. A., AND J. BACKHOUSE. 1977. Fossiliferous Tertiary deposits on the Darling Plateau. Geological Survey of Western Australia Annual Report 1976: 49–53. WRIGHT, I. J., P. B. REICH, M. WESTOBY, D. D. ACKERLY, Z. BARUCH, F. BONGERS, J. CAVENDER-BARES, ET AL. 2004. The worldwide leaf economics spectrum. Nature 428: 821–827. ZACHOS, J., M. PAGANI, L. SLOAN, E. THOMAS, AND K. BILLUPS. 2001. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292: 686–693.