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Ecological Conservatism in the "Living Fossil" Ginkgo

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Ecological Conservatism in the Paleobiology, 29(1), 2003, pp. 84-104 Ecological conservatism in the "living fossil" Ginkgo Dana L. Royer, Leo J. Hickey, and Scott L. Wing Abstract.—The living species Ginkgo biloba is phylogenetically isolated, has a relictual distribution, and is morphologically very similar to Mesozoic and Cenozoic congenerics. To investigate what adaptations may have allowed this lineage to persist with little or no morphological change for over 100 Myr, we analyzed both sedimentological and floral data from 51 latest Cretaceous to mid- dle Miocene Ginkgo-bearing fossil plant sites in North America and northern Europe. The resulting data indicate that throughout the late Cretaceous and Cenozoic Ginkgo was largely confined to dis- turbed streamside and levee environments, where it occurred with a consistent set of other plants. These inferred habitats are surprising because the life-history traits of Ginkgo (e.g., slow growth rate, late reproductive maturity, extended reproductive cycle, large and complex seeds, large and slowly developing embryos) are counter to those considered advantageous in modern disturbed habitats. Many flowering plant lineages first appeared or became common in disturbed riparian habitats, and are inferred to have had reproductive and growth traits (e.g., rapid reproduction, small easily dispersed seeds, rapid growth) suited to such habitats. Paleoecological inferences based on both morphology and sedimentary environments thus support the idea that Ginkgo was displaced in riparian habitats by angiosperms with better adaptations to frequent disturbance. Dana L. Royer* and Leo }. Hickey. Department of Geology and Geophysics, Yale University, New Haven, Connecticut 06520-8109 Scott L. Wing. National Museum of Natural History, Department of Paleobiology, Smithsonian Institution, Washington, D.C. 20560 ^Present address: Department of Geosciences, Pennsylvania State University, University Park, Pennsyl- vania 16802. E-mail: [email protected] Accepted: 20 August 2002 Introduction Ginkgoales first appeared in the Permian and achieved maximum diversity during the Ju- Members of the Ginkgoalean clade re- rassic and Early Cretaceous. Its most plausible mained a moderately important to minor as- ancestral group is the pteridosperms ("seed sociate of mid- to high-latitude paleofloras ferns") (Thomas and Spicer 1987), and espe- from the mid-Mesozoic to the mid-Cenozoic cially the Peltaspermales (Meyen 1987: p. 146). (Tralau 1967, 1968; Vakhrameev 1991). How- However, the clade is so isolated evolutionari- ever, reconstructing the ecology of the group ly that efforts to establish its closest extant sis- is problematic, given the extreme taxonomic ter group have remained controversial. Nev- isolation (Chamberlain 1935; Gifford and Fos- ertheless, there is a growing consensus, fa- ter 1989) and highly relictual distribution of vored by molecular data, that cycads are the what might well be only semi-wild stands of most plausible closest living relative (Meyen Ginkgo biloba L., the sole survivor of this once 1984; Thomas and Spicer 1987; Raubeson and moderately diverse clade (Vasilevskaya 1963; Jansen 1992; Chaw et al. 1993, 1997; Rothwell Tralau 1968). The objective of this study was and Serbet 1994; Boivin et al. 1996; Hickey to determine whether some aspects of the pa- 1996; Hasebe 1997) rather than conifers leoecology of Ginkgo could be recovered from (Chamberlain 1935; Pant 1977; Stewart 1983; (1) an interpretation of the sedimentary con- Crane 1985; Doyle and Donoghue 1986,1987). text in which its fossils occur; (2) the autecol- Undoubted remains of the genus Ginkgo (G. ogy of the modern descendants of its impor- digitata [Brongniart] Heer) first appeared in tant fossil associates; and (3) a contextual the Early Jurassic (Tralau 1968; but see Vasi- study of the fragmentary ecology of its sur- levskaya and Kara-Murza 1963 for a question- viving species. able attribution to the Late Triassic), making it According to Tralau (1968), the order Gink- the oldest extant genus among seed plants goales consists of six families and 19 genera. (Arnold 1947). At least a dozen species have 2003 The Paleontological Society. All rights reserved. 0094-8373/03/2901-0015/$1.00 PALEOECOLOGY OF GINKGO 85 FIGURE 1. A, Leaf of Ginkgo biloba (left) and fossil G. adiantoides (right) (scale bar, 1 cm). Fossil leaf from Colgate Member of Fox Hills Formation (Maastrichtian; YPM 7004). Photo by W. K. Sacco. B, Seeds of extant G biloba and Paleocene Ginkgo seeds from Almont, North Dakota. G biloba seeds above on left have been removed from their sarcotestas; those on the right have not. Paleocene Ginkgo seed on left (UWSP 14906) shows both sclerotesta (arrow 1) and sarcotesta (arrow 2), as does fossil seed on right (UWSP 2493). Photo courtesy of Mike Nowak. been assigned to Ginkgo, which achieved its en this lack of morphological diversity, it is greatest diversity during the Early Cretaceous possible that Ginkgoales has been monospe- (Tralau 1968). Of particular interest for this cific (or nearly so) in the Northern Hemi- study is G. adiantoides (Unger) Heer, which is sphere for the entire Cenozoic. In the Southern morphologically identical to G biloba (Seward Hemisphere a different, more strongly digi- 1919: p. 29; Shaparenko 1935; Manum 1966; tate type of Ginkgo leaf persists into the Eo- Tralau 1968; Mosle et al. 1998). These similar- cene, but we lack data on its occurrence and ities have led some authors to consider G do not discuss it further here. adiantoides conspecific with G biloba (Seward A number of Mesozoic species of Ginkgo 1919; Tralau 1967, 1968: p. 87). Ginkgo adian- closely match the extant species as well. For toides first appeared in the Early Cretaceous example, Mosle et al. (1998) found strong sim- and was relatively common during the Late ilarities between the cuticles of the Early Cre- Cretaceous and Paleogene (Tralau 1968; Vakh- taceous G coriacea Florin and G biloba. Villar rameev 1991). de Seoane (1997) reported similar results for Although several additional Northern Hemi- the cuticle of Early Cretaceous G tigrensis Ar- sphere species of Cenozoic Ginkgo have been changelsky from Argentina. Zhou (1993) com- formally established, all but one of these are pared the megaspore membranes of middle morphologically identical, or nearly so, to G Jurassic G yimaensis Zhou & Zhang with G bi- adiantoides (and G biloba). One example is G be- loba, and noted few morphological differences. ckii Scott, Barghoorn, & Prakash, a species of Van Konijnenburg-van Cittert (1971) conclud- Miocene wood associated with G adiantoides ed that the pollen of middle Jurassic G huttoni foliage, which shows a striking similarity to G (Sternberg) Heer was morphologically identi- biloba wood, with the possible exception of cal to G biloba. Thus, Ginkgo is a highly con- fewer pits per unit length on the radial walls servative genus morphologically, with the of its tracheids (Scott et al. 1962; Mastrogiu- long-ranging fossil species G adiantoides in- seppe et al. 1970). The only Cenozoic form that distinguishable from modern G biloba. possibly merits recognition as a separate spe- Ecology of Ginkgo biloba.—Ginkgo biloba (Fig. cies is G gardneri Florin (Tralau 1968), which 1) has been cultivated for more than 2000 has more-prominent papillae and less-sinuous years in China and for some 1000 years in Ja- adaxial epidermal cells than does G adianto- pan as a source of food, shade, and beauty (Li ides (Manum 1966). G gardneri is found only in 1956; He et al. 1997); small stands are some- the late Paleocene deposits on the Isle of Mull, times present within the forests customarily Scotland (e.g., Boulter and Kvacek 1989). Giv- preserved adjacent to Buddhist and Taoist 86 DANA L. ROYER ET AL. 90N 60N SON 120W FIGURE 2. Geographic distribution of Ginkgo-beaiing localities used in this study. Numbers refer to the following field areas: 1 = Williston Basin; 2 = Bighorn Basin; 3 = Denver Basin; 4 = Spitsbergen; 5 = south-central Alberta; 6 = Isle of Mull; 7 = Axel Heiberg Island; 8 = north-central Idaho. Solid line represents the southern extent in the Northern Hemisphere of the genus Ginkgo for the Jurassic-Miocene. Dashed and dotted lines represent the northern extent of the genus Ginkgo during the Cretaceous-Eocene and the Miocene, respectively. Data from Tralau (1967). temples (Li 1956). However, the natural ecol- Ginkgo is a tree of medium height, reaching ogy of G. biloba is largely unknown because no approximately 30 m (Del Tredici et al. 1992; unequivocally natural stands remain today He et al. 1997), and can live as long as 3500 (see discussions in Li 1956; Franklin 1959; Del years (see He et al. 1997). Although Ginkgo is Tredici et al. 1992; He et al. 1997). The last re- frequently described as slow growing, under maining natural populations are (or were) favorable conditions with warm summers it largely in the low coastal and interior moun- exhibits growth rates of up to 30 cm/yr for the tains straddling the Yangtze River. This is the first 30 years or so of its life (Del Tredici 1989). region where G. biloba was first cultivated and During this "bolting" phase of their growth, also harbors relictual stands of other taxa with seedlings and saplings have a straight main long fossil records such as Cryptomeria, Liriod- axis, with sparse, excurrent branches. After endron, Metasequoia, Nothotaxus, and Pseudola- that, growth slows markedly—100-year-old rix. The area lies at about 30°N latitude and trees may have attained only two-thirds of has a warm temperate mesic climate (mean their mature height (Santamour et al. 1983; He annual temperature = 9-18°C; mean annual et al. 1997)—and the young tree begins to fill precipitation = 600-1500 mm) (Li 1956; Del out its crown (Del Tredici 1989). Plants do not Tredici et al. 1992; He et al. 1997). In cultiva- produce viable seeds for 20 to 30 years (Wy- tion Ginkgo tolerates a wide variety of seasonal man 1965; Santamour et al.
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