Ecological conservatism in the “living fossil” Ginkgo

q 2003 The Paleontological Society. All rights reserved. 0094-8373/03/2901-0015/$1.00

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 whatadaptations may have allowed this lineage to persist with little or no morphological change forover 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 resultingdata 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 growthrate, late reproductive maturity, extended reproductive cycle, large and complex seeds, large andslowly developing embryos) are counter to those considered advantageous in modern disturbedhabitats. Many flowering plant lineages first appeared or became common in disturbed riparianhabitats, 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 inferencesbased on both morphology and sedimentary environments thus support the idea that Ginkgo wasdisplaced in riparian habitats by angiosperms with better adaptations to frequent disturbance.

Dana L. Royer* and Leo J. 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

Members of the Ginkgoalean clade re-mained a moderately important to minor as-sociate of mid- to high-latitude paleoflorasfrom the mid-Mesozoic to the mid-Cenozoic(Tralau 1967, 1968; Vakhrameev 1991). How-ever, reconstructing the ecology of the groupis problematic, given the extreme taxonomicisolation (Chamberlain 1935; Gifford and Fos-ter 1989) and highly relictual distribution ofwhat might well be only semi-wild stands ofGinkgo biloba L., the sole survivor of this oncemoderately diverse clade (Vasilevskaya 1963;Tralau 1968). The objective of this study wasto determine whether some aspects of the pa-leoecology of Ginkgo could be recovered from(1) an interpretation of the sedimentary con-text in which its fossils occur; (2) the autecol-ogy of the modern descendants of its impor-tant fossil associates; and (3) a contextualstudy of the fragmentary ecology of its sur-viving species.

According to Tralau (1968), the order Gink-goales consists of six families and 19 genera.

Ginkgoales first appeared in the Permian andachieved maximum diversity during the Ju-rassic and Early Cretaceous. Its most plausibleancestral group is the pteridosperms (‘‘seedferns’’) (Thomas and Spicer 1987), and espe-cially the Peltaspermales (Meyen 1987: p. 146).However, the clade is so isolated evolutionari-ly that efforts to establish its closest extant sis-ter group have remained controversial. Nev-ertheless, there is a growing consensus, fa-vored by molecular data, that cycads are themost plausible closest living relative (Meyen1984; Thomas and Spicer 1987; Raubeson andJansen 1992; Chaw et al. 1993, 1997; Rothwelland Serbet 1994; Boivin et al. 1996; Hickey1996; Hasebe 1997) rather than conifers(Chamberlain 1935; Pant 1977; Stewart 1983;Crane 1985; Doyle and Donoghue 1986, 1987).

Undoubted remains of the genus Ginkgo (G.digitata [Brongniart] Heer) first appeared inthe Early Jurassic (Tralau 1968; but see Vasi-levskaya and Kara-Murza 1963 for a question-able attribution to the Late Triassic), making itthe oldest extant genus among seed plants(Arnold 1947). At least a dozen species have

85PALEOECOLOGY OF GINKGO

FIGURE 1. A, Leaf of Ginkgo biloba (left) and fossil G. adiantoides (right) (scale bar, 1 cm). Fossil leaf from ColgateMember of Fox Hills Formation (Maastrichtian; YPM 7004). Photo by W. K. Sacco. B, Seeds of extant G. biloba andPaleocene Ginkgo seeds from Almont, North Dakota. G. biloba seeds above on left have been removed from theirsarcotestas; those on the right have not. Paleocene Ginkgo seed on left (UWSP 14906) shows both sclerotesta (arrow1) and sarcotesta (arrow 2), as does fossil seed on right (UWSP 2493). Photo courtesy of Mike Nowak.

been assigned to Ginkgo, which achieved itsgreatest diversity during the Early Cretaceous(Tralau 1968). Of particular interest for thisstudy is G. adiantoides (Unger) Heer, which ismorphologically identical to G. biloba (Seward1919: p. 29; Shaparenko 1935; Manum 1966;Tralau 1968; Mosle et al. 1998). These similar-ities have led some authors to consider G.adiantoides conspecific with G. biloba (Seward1919; Tralau 1967, 1968: p. 87). Ginkgo adian-toides first appeared in the Early Cretaceousand was relatively common during the LateCretaceous and Paleogene (Tralau 1968; Vakh-rameev 1991).

Although several additional Northern Hemi-sphere species of Cenozoic Ginkgo have beenformally established, all but one of these aremorphologically identical, or nearly so, to G.adiantoides (and G. biloba). One example is G. be-ckii Scott, Barghoorn, & Prakash, a species ofMiocene wood associated with G. adiantoidesfoliage, which shows a striking similarity to G.biloba wood, with the possible exception offewer pits per unit length on the radial wallsof its tracheids (Scott et al. 1962; Mastrogiu-seppe et al. 1970). The only Cenozoic form thatpossibly merits recognition as a separate spe-cies is G. gardneri Florin (Tralau 1968), whichhas more-prominent papillae and less-sinuousadaxial epidermal cells than does G. adianto-ides (Manum 1966). G. gardneri is found only inthe late Paleocene deposits on the Isle of Mull,Scotland (e.g., Boulter and Kvacek 1989). Giv-

en this lack of morphological diversity, it ispossible that Ginkgoales has been monospe-cific (or nearly so) in the Northern Hemi-sphere for the entire Cenozoic. In the SouthernHemisphere a different, more strongly digi-tate type of Ginkgo leaf persists into the Eo-cene, but we lack data on its occurrence anddo not discuss it further here.

A number of Mesozoic species of Ginkgoclosely match the extant species as well. Forexample, Mosle et al. (1998) found strong sim-ilarities between the cuticles of the Early Cre-taceous G. coriacea Florin and G. biloba. Villarde Seoane (1997) reported similar results forthe cuticle of Early Cretaceous G. tigrensis Ar-changelsky from Argentina. Zhou (1993) com-pared the megaspore membranes of middleJurassic G. yimaensis Zhou & Zhang with G. bi-loba, and noted few morphological differences.Van Konijnenburg-van Cittert (1971) conclud-ed that the pollen of middle Jurassic G. huttoni(Sternberg) Heer was morphologically identi-cal to G. biloba. Thus, Ginkgo is a highly con-servative genus morphologically, with thelong-ranging fossil species G. adiantoides in-distinguishable from modern G. biloba.

Ecology of Ginkgo biloba. Ginkgo biloba (Fig.1) has been cultivated for more than 2000years in China and for some 1000 years in Ja-pan as a source of food, shade, and beauty (Li1956; He et al. 1997); small stands are some-times present within the forests customarilypreserved adjacent to Buddhist and Taoist

86 DANA L. ROYER ET AL.

FIGURE 2. Geographic distribution of Ginkgo-bearing localities used in this study. Numbers refer to the followingfield areas: 1 5 Williston Basin; 2 5 Bighorn Basin; 3 5 Denver Basin; 4 5 Spitsbergen; 5 5 south-central Alberta;6 5 Isle of Mull; 7 5 Axel Heiberg Island; 8 5 north-central Idaho. Solid line represents the southern extent in theNorthern Hemisphere of the genus Ginkgo for the Jurassic–Miocene. Dashed and dotted lines represent the northernextent of the genus Ginkgo during the Cretaceous–Eocene and the Miocene, respectively. Data from Tralau (1967).

temples (Li 1956). However, the natural ecol-ogy of G. biloba is largely unknown because nounequivocally natural stands remain today(see discussions in Li 1956; Franklin 1959; DelTredici et al. 1992; He et al. 1997). The last re-maining natural populations are (or were)largely in the low coastal and interior moun-tains straddling the Yangtze River. This is theregion where G. biloba was first cultivated andalso harbors relictual stands of other taxa withlong fossil records such as Cryptomeria, Liriod-endron, Metasequoia, Nothotaxus, and Pseudola-rix. The area lies at about 308N latitude andhas a warm temperate mesic climate (meanannual temperature 5 9–188C; mean annualprecipitation 5 600–1500 mm) (Li 1956; DelTredici et al. 1992; He et al. 1997). In cultiva-tion Ginkgo tolerates a wide variety of seasonalclimates, ranging from Mediterranean to coldtemperate, where winter temperature mini-mums can reach 2208C. Interestingly, nearlyall fossil occurrences of Ginkgo lie poleward of408 and, concomitant with cooling and in-creased seasonality during the Tertiary, itsgeographical range progressively constrictedtoward 408N, and it disappeared all togetherfrom the Southern Hemisphere (Tralau 1967;Ziegler et al. 1996) (see Fig. 2). Thus, both itsbroad modern range of climatic tolerance andthe paleobotanical data suggest that the cli-matic parameters of its current (semi-)naturalrange at 308N are anomalous in terms of thelong-term history of Ginkgo (Ziegler et al.1996).

Ginkgo is a tree of medium height, reachingapproximately 30 m (Del Tredici et al. 1992;He et al. 1997), and can live as long as 3500years (see He et al. 1997). Although Ginkgo isfrequently described as slow growing, underfavorable conditions with warm summers itexhibits growth rates of up to 30 cm/yr for thefirst 30 years or so of its life (Del Tredici 1989).During this ‘‘bolting’’ phase of their growth,seedlings and saplings have a straight mainaxis, with sparse, excurrent branches. Afterthat, growth slows markedly—100-year-oldtrees may have attained only two-thirds oftheir mature height (Santamour et al. 1983; Heet al. 1997)—and the young tree begins to fillout its crown (Del Tredici 1989). Plants do notproduce viable seeds for 20 to 30 years (Wy-man 1965; Santamour et al. 1983; He et al.1997), but individual trees can remain fertilefor more than 1000 years (S.-A. He personalcommunication 2000). Ginkgo’s fusiform seedsare large, ranging from 1 to 2 cm in length.

In addition to sexual reproduction, Ginkgocan reproduce clonally from embedded buds,called lignotubers (or basal chichi), that occurnear the base of the trunk. If the soil in the im-mediate environment is disturbed, as by ex-cessive erosion, positive geotropic growth isstimulated within these lignotubers. Once theapex of a lignotuber penetrates below ground,it forms rhizomatous tissue that can generateboth aerial shoots and adventitious roots (DelTredici 1992). In a modern ‘‘semi-wild’’ standin the coastal mountains near the Yangtze Riv-


er studied by Del Tredici et al. (1992), 40% ofthe larger trees had at least two primary stemsbut few saplings were present, a clear indica-tion of the reproductive importance of ligno-tubers. In older individuals, these buds alsoform within secondary stems and are calledaerial chichi. As with lignotubers, aerial chichidevelop in response to a disturbance (e.g., se-vere crown damage) and can lead to success-ful clonal reproduction (Fujii 1895; Del Trediciet al. 1992).

Modern Ginkgo is typically shade intolerant,growing best on exposed sites (He et al. 1997).Del Tredici et al. (1992) observed that seeds ofG. biloba in a ‘‘semi-wild’’ stand require anopen canopy for growth and development;Jiang et al. (1990) reported a similar require-ment in another ‘‘semi-wild’’ stand. Many ofthe individual trees studied by Del Tredici etal. (1992: p. 202) were growing in disturbedmicrosites such as ‘‘stream banks, steep rockyslopes, and the edges of exposed cliffs.’’ How-ever, Del Tredici (1989) also suggests thatGinkgo may play a role as a gap opportunistand persist in the shady understory of the for-est until a gap occurs that allows it to shootup into the canopy.

At least in cultivation, Ginkgo grows best in‘‘sandy loam soils. . . along dams. . . or at thefoot of hill slopes’’ (He et al. 1997: p. 377), en-vironments that are well watered and welldrained. G. biloba is very successful as an ur-ban street tree (e.g., Handa et al. 1997), owingin part to its tolerance to air pollution (Kimand Lee 1990, Kim et al. 1997) and its high re-sistance to insects (Major 1967; Kwon et al.1996; Ahn et al. 1997; Honda 1997), fungi (Ma-jor et al. 1960; Major 1967; Christensen andSproston 1972), bacteria (Mazzanti et al.2000), and viruses (Major 1967), as well as itsability to competitively grow on exposedsites. Ginkgo’s resistance to disease is due, inpart, to its high production of secondary de-fense compounds (e.g., Yoshitama 1997).

Implications for Fossil Ginkgo. Although theclose morphological similarity of Ginkgo adian-toides to G. biloba makes it tempting to infer thepaleoecology of the fossil species from what isknown of the living, the extreme relictual na-ture of the modern form suggests that suchsurmises should be made cautiously and only

with corroboration from the fossil record (seeHickey 1977). Uemura (1997) thought thatGinkgo was ecologically conservative throughtime, and required moist environments. Ko-var-Eder et al. (1994) studied Neogene occur-rences in central Europe and considered G.adiantoides an accessory element in ripariancommunities. Spicer and Herman (2001) re-ported similar depositional associations formid-Cretaceous G. adiantoides in northernAlaska. In this paper, we will provide a quan-titative description of the floral associates (de-fined here as the plants that co-occur withGinkgo) and sedimentological contexts of fos-sil Ginkgo, concentrating primarily on the pu-tatative conspecific of Ginkgo biloba, G. adian-toides, which ranged in age from latest Creta-ceous to middle Miocene. Through the inter-pretation of Ginkgo’s sedimentological contextsand the modern ecology of the nearest livingrelatives of its floral associates, two indepen-dent lines of evidence will be used to interpretthe paleoecology of the genus.

Methods

Sources of Data. Sedimentological and flo-ral data were obtained through field observa-tions and the literature. Most data are from theFort Union and Willwood Formations (Big-horn Basin) and the Hell Creek Formation(Williston Basin). The geographic extent ofour sampling is shown in Figure 2. Datasources are given in Appendix 1.

Recognition of Sedimentological Contexts. Weassigned sites to environments of depositionaccording to the lithology, grain size, primarystratification, and overall cross-sectional andplan-view shape of their deposits, along withtheir organic content and nature of their con-tacts with surrounding sediments, using cri-teria developed by J. R. L. Allen (1964, 1965),Hickey (1980), Wing (1984), and Miall (1992).We will use the following terms for the envi-ronments of deposition that we recognizehere: relief channel, abandoned channel, cre-vasse splay, active trunk channel, backswamp,and distal floodplain.

Relief channels are represented by thin,shallow-lenticular, laterally restricted bodiesof silt to sand-sized sediment that fill minorstream axes used in time of flood. Abandoned


channels represent a segment of a stream orriver that was intermittently or permanentlycut off from its main channel, whose originaldepth can be reconstructed from the thicknessof the total sedimentary package. They oftenhave claystone or mudstone in their axes. Thebasal contacts of both types of channels arefrequently down-cut, concave upward, andveneered with a coarse (often pebble-sized)basal lag deposit. Plant remains within thesedeposits are typically parautochthonous(Wing 1984; Gastaldo et al. 1989). These chan-nel deposits are characterized by relativelythin (,5 cm for relief channels and ,1 m forabandoned channels) couplets of coarsersandstone and siltstone with finer siltstoneand mudstone that represent the alternatingperiods of flooding or channel reactivationand slack-water or subareal phases (Wing1984). Intervals within abandoned channelsoften show evidence of standing water, suchas aquatic plants and invertebrates, and suc-cessions of small-scale, fining-upwards se-quences (Wing 1984).

Crevasse splay deposits are floodplain de-posits formed by the breaching of a levee, typ-ically during flood events. They are character-ized by sand- or silt-sized sediments withgenerally tabular beds that are sometimescross-bedded or cross-laminated. These oftenoverlie finer-grained, massive floodplain sed-iments. Proximal to the break-through point,downcut contacts with concave-upward bed-ding and scour and fill structures are morecommon, but distal to the break-throughpoint basal contacts tend to be more parallelwith one another. Beds of sandstone in splaysrepresent multiple reactivation events andrange in thickness from centimeters to morethan a meter. Often these grade upward intoprogressively finer sediments that representlow-energy floodplain conditions. The modalgrain size of the sediments in these reactiva-tion events usually coarsens upwards becauseof the progressive lateral shift of the streamaxis toward a given point in the crevasse splay(Miall 1992). Crevasse splay deposits are gen-erally more laterally extensive than reliefchannels but are not traceable for long (.102

m) distances.Other sedimentological contexts distin-

guished here include backswamps, which aredominated by carbonaceous shale; activetrunk channels, which are characterized bymassive cross-bedded sandstone; and ponds/lakes, which are distinguished by laminatedmudstone and the presence of aquatic plantsand animals. Because of the convergence oftheir properties, we assigned large abandonedchannels to the pond/lake category.

Floral Associates. We generated floral listsfor most sites. When possible, we limitedthese lists to the individual beds within a de-posit where Ginkgo was found. In general, wefollow the taxonomic terminology of Wing etal. (1995). In two cases, we combined closelyrelated species of the family Platanaceae intosingle counting units. The first of these unitsconsists of the broadly trilobed Platanus ray-noldsii Newberry and P. guillelmae Goeppert,and the second of the narrowly five-lobedMacginitiea gracilis (Lesquereux) Wolfe & Wehrand M. brownii (Berry) Wolfe & Wehr.

All but two of our sites contain Ginkgoadiantoides. G. spitsbergensis, found at one site,is considered conspecific with G. adiantoides byTralau (1968), whereas G. gardneri, found atone site on the Isle of Mull, may be a distinctspecies, as discussed above.

Results

Sedimentological Contexts. Our sampling of48 sites spanning the latest Cretaceous to mid-dle Miocene indicates that Ginkgo is most of-ten found in relief/abandoned channels (44%of all sites) and crevasse splays (38%) (Table 1;raw data presented in Appendix 2). In mostrelief/abandoned channel deposits, Ginkgooccurs within the coarser-grained intervals.Ginkgo is rarely preserved in backswamps(4%). Certain depositional environments arepreserved more commonly than others or aremore likely to preserve fossil plants. The highproportion of relief/abandoned channels andcrevasse splays might therefore simply reflectthe numerical abundance of these depositscontaining plant fossils. To normalize for thispotential bias, we determined the distributionof sedimentological contexts for all fossil plantsites (including Ginkgo-bearing sites) docu-mented by Johnson (2002) (n 5 157 sites) andWing et al. (1995) (n 5 131). Together, these


TABLE 1. Summary of the distribution of sedimentological contexts and floral associates. Description of columnsare as follows: (1) % occurrence at all Ginkgo-bearing sites; (2) % occurrence at Ginkgo-bearing sites that overlapwith the data sets of Johnson (in press) and Wing et al. (1995); (3) % occurrence at all sites (including Ginkgo-bearingsites) from the data sets of Johnson (in press) and Wing et al. (1995); (4) % difference between the two restrictedsets (i.e., column [2]–[3]); (5) level of significance between the two restricted sets (G-test of independence; Sokol andRohlf 1995: p. 729). Because the sedimentological contexts are not independent of one another (i.e., columns addup to 100%), these p-values were adjusted using the Dunn-Sidak method in the following manner: a9 5 1 2 (1 2a)1/k, where k 5 6 5 the number of significance tests (Sokol and Rohlf 1995: p. 239).

Ginkgo sites (%)

AllRestricted

set

All sites fromrestricted set(weighted %)

Differencein restricted

set (%) p

Sedimentological contexts (n 5 48) (n 5 41) (n 5 288)Relief channel/abandoned channelCrevasse splayChannelBackswampDistal floodplainOther (mostly stable ponds/lakes)

43.837.5

8.34.24.24.2

41.541.5

9.84.94.90.0

14.317.8

5.553.2

0.88.4

27.223.7

4.3248.4

4.028.4

0.0040.0120.98

,0.0010.600.08

Floral associates (n 5 47) (n 5 41) (n 5 289)(Ginkgo adiantoides)Cercidiphyllum genetrixMetasequoia occidentalisPlatanus raynoldsii/guillelmaeGlyptostrobus europaeus

59.644.742.629.8

63.446.348.831.7

8.432.927.723.344.3

30.518.725.5

212.6

,0.0010.0220.0020.19

data sets span the interval from the latest Cre-taceous to the early Eocene and include thelate Cretaceous Hell Creek Formation and ear-liest Paleocene part of the Fort Union Forma-tion in the Williston Basin and the Paleocenethrough early Eocene Fort Union and Will-wood Formations in the Bighorn Basin. Weconsidered only our Ginkgo-bearing sites in-cluded in these data sets (n 5 41 sites) andweighted the full data sets of Johnson (2002)and Wing et al. (1995) to reflect the distribu-tion of these Ginkgo-bearing sites (22% fromthe Williston Basin, 78% from the Bighorn Ba-sin).

For these two geographic regions, Ginkgo ispreferentially found in both relief/abandonedchannel (42% for Ginkgo localities vs. 14% forall plant localities) and crevasse splay (42% vs.18%) deposits (Table 1, Fig. 3). Equally strik-ing is that the likelihood of finding Ginkgo ina backswamp is far less than the backgroundpercentage of backswamp deposits (5% vs.53%). The differences for all three of these sed-imentological contexts are significant at the a5 0.02 level (G-test of independence).

Floral Associates of Ginkgo. A sampling of47 Ginkgo-bearing sites spanning the latestCretaceous to middle Miocene reveals thatGinkgo most commonly is fossilized with Cer-

cidiphyllum genetrix (Newberry) Hickey (co-oc-curs at 60% of all Ginkgo sites), Metasequoia oc-cidentalis (Newberry) Chaney (45%), Platanusraynoldsii/guillelmae (43%), and Glyptostrobuseuropaeus (Brongniart) Heer (30%) (Table 1;raw data presented in Appendix 3). All four ofthese associates have temporal ranges thatspan the latest Cretaceous to middle Miocene.Analogous to the potential sedimentologicaltaphonomic bias, it is possible that these floralassociates simply dominate the megafloral re-cord during this interval, which, if true, woulddiminish the paleoecological significance ofour results. As with the data on sedimentaryenvironments, then, we compared a weightedaverage of the overall floral distribution pat-terns for the Hell Creek and Fort Union For-mations in the Williston Basin (n 5 158 sites)(Johnson 2002) and the Fort Union and Will-wood Formations in the Bighorn Basin (n 5131) (Wing et al. 1995) with the Ginkgo-bear-ing sites that overlap with these studies (n 541). C. genetrix and P. raynoldsii/guillelmae oc-cur more often with Ginkgo relative to theiroverall occurrence rate (63% vs. 33% and 49%vs. 23%, respectively) (Table 1, Fig. 3). Thesedifferences are significant at the a 5 0.003 lev-el (G-test of independence). Ginkgo also pref-erentially associates with M. occidentalis (46%


FIGURE 3. Deviations of the proportion of sedimentological contexts and floral associates at Ginkgo-bearing sitesfrom the background occurrence rate of these sedimentological contexts and floral associates. Data taken from sec-ond-to-last column in Table 1. Methodology of calculation discussed in text. Asterisks represent whether the dif-ferences in proportionality are significant at the a 5 0.05 level (*) or a 5 0.001 level (**) (G-test of independence).

vs. 28%; p 5 0.02; G-test of independence). Thebackground occurrence rate of G. europaeus,however, is higher than its co-occurrence ratewith Ginkgo (44% vs. 32%) (Table 1, Fig. 3),suggesting that it is not useful in determiningthe paleoecology of Ginkgo.

Discussion

Paleoecology of Ginkgo. The sedimentologi-cal features at the majority of Ginkgo localitiesindicate that it grew primarily in disturbedenvironments along stream margins and thedistal sides of levees. These environments aretypically well watered (owing to a shallowwater table) yet well-drained (owing to theirprimarily coarse-grained substrate and higherelevation relative to other flood plain settings).Because of their high disturbance rate, open-canopy forests are common in these settings(e.g., Hack and Goodlett 1960; Everitt 1968;Carr 1998).

As reported above, Cercidiphyllum genetrixand a form of Platanus delimited by the pair P.raynoldsii and P.guillelmae are two of the more

common floral associates of Ginkgo. C. japoni-cum Siebold & Zuccarini, the nearest livingrelative (NLR) of C. genetrix, grows in the wildtoday in Japan and China. It usually occurs insmall gaps or along stream margins (Seiwaand Kikuzawa 1996). It is a fast growing pio-neer species, often reproduces by sprouting,and prefers mesic, disturbed sites (Ishizukaand Sugawara 1989). Interestingly, at mid-el-evations (1450–3500 m) in the mountains ofsouth-central China, C. japonicum occurs onscree slopes (Tang and Ohsawa 1997) and inother highly disturbed habitats (Wang 1961).Although plant remains are rarely preservedin alluvial fan facies, at Ardtun Head (Isle ofMull, Scotland) Ginkgo is found in fine-grained sediments within an alluvial fan de-posit (see Appendix 2). As noted above, mod-ern Ginkgo has been observed growing onsteep rocky slopes and along edges of exposedcliffs (Del Tredici et al. 1992). It is possible,then, that disturbance is the overriding eco-logical filter for Ginkgo, and that the fluvial de-posits where Ginkgo is most commonly pre-


served represent only a small fraction of itspotential habitat range.

The NLRs of P. raynoldsii and P. guillelmae areP. occidentalis L., P. orientalis L., and their hybridP. 3 acerifolia Willdenow. These living speciesare most commonly found in riparian habitats(Tang and Kozlowski 1982; Ware et al. 1992;Thomas and Anderson 1993; Atzmon andHenkin 1998; Everson and Boucher 1998); forexample, P. occidentalis often grows on the low-est stream terrace (McClain et al. 1993), whereflood frequency is highest (Bell 1980). P. occi-dentalis can develop adventitious roots andlenticels in response to flooding (Tsukaharaand Kozlowski 1985); however it appears torequire aerated soils during the growing sea-son (Everson and Boucher 1998).

Metasequoia occidentalis, another commonGinkgo associate (Table 1), has remained large-ly unchanged morphologically throughout theCenozoic (Chaney 1951; Christophel 1976; Liuet al. 1999) and is represented today by M.glyptostroboides H. H. Hu & Cheng. Like Gink-go, the geographic range of Metasequoia hasbeen severely restricted; however, areas ofnear-natural stands still grow in one moun-tain valley in south-central China. It occursthere along stream banks and at seepages atthe bases of slopes (Chu and Cooper 1950).These modern observations contrast in partwith the paleobotanical observations thatshow Metasequoia most often occurring inswamp, swamp margin, and distal splay en-vironments (e.g., Hickey 1980; Momohara1994; Wing et al. 1995; Falder et al. 1999). Thisdiscrepancy may result either from the factthat most of the valley floor where Metasequoiapresently makes its last stand has been con-verted to agriculture and habitat space hasbeen lost, or from a shift in the ecologicalniche of Metasequoia during the Cenozoic.

In summary, the sedimentological recordstrongly indicates that Ginkgo most commonlygrew along streamsides and on the proximalslope of levees. The ecology of the NLRs oftwo genera of Ginkgo’s common floral associ-ates (Cercidiphyllum and Platanus) supportsthese sedimentological interpretations. Gink-go’s association with Metasequoia proves prob-lematic, however, as the latter most commonlygrew in swamps and distal levees during the

Tertiary. It is possible, then, either that Ginkgoalso grew in more stable distal floodplain set-tings or that Metasequoia was a minor associatein disturbed levee and riparian-type environ-ments. This latter option is supported, albeitweakly, by modern ecological observations ofMetasequoia.

In general, NLR-derived paleoecological in-terpretations are less reliable than sediment-derived interpretations because a given line-age of plants can shift its ecological tolerancesover geologic time (e.g., Hickey 1977; Wolfe1977), and because few late Cretaceous andearly Tertiary plants have close modern rela-tives. In contrast, the sedimentology of an au-tochthonous fossil plant site retains a primarypaleoecological signal. Only recently have pa-leobotanists begun to analyze the sedimen-tological contexts of their assemblages in aneffort to extract paleoecological information(e.g., Hickey 1980; Spicer 1980; Burnham 1988,1994; Wing et al. 1995; Spicer and Herman2001; Spicer et al. 2002). The results of thisstudy highlight the potential of applying sed-imentological data from a large number of fos-sil plant sites, and we hope that the applica-tion of such data becomes more common inthe future.

Implications for the Relationship between G. bi-loba and G. adiantoides. Analysis of our dataindicates that there were no striking changesin the sedimentological context of Ginkgo dur-ing the latest Cretaceous to early Eocene (Fig.4A). Ginkgo consistently associated with un-stable crevasse splay and relief/abandonedchannel environments. Although there is ashift to more relief/abandoned channel local-ities in the early Eocene, this is driven by adrying trend in the Bighorn Basin that restrict-ed the preservation of fossil plants to these en-vironments and to tabular carbonaceous lay-ers representing swampy floodbasins (Wing1984).

Ginkgo’s floral associates also remain stablethrough the early Paleogene (Fig. 4B). Thisstability is striking considering the large num-ber of factors that influence plant migrationsand evolution. The one minor change in thistime series is the lack of Metasequoia duringthe early Eocene, although this may be due tothe paucity of early Eocene backswamp de-


FIGURE 4. Temporal distribution of sedimentologicalcontexts (A) and principal floral associates (B) for latestCretaceous–early Eocene Ginkgo-bearing sites. Datafrom Appendices 2 and 3.

posits relative to the late Paleocene in the Big-horn Basin (Wing et al. 1995). If correct, thisobservation provides additional support forinferring Ginkgo’s preferential association forstreamside and levee habitats.

Data are generally lacking for the Neogene.However, at the middle Miocene Juliaetta sitein Idaho, Ginkgo occurs in sandy delta foresetbeds (Appendix 2). Although the overall de-positional setting is lacustrine, Ginkgo is foundonly in this high-energy delta environment,and so perhaps it grew in a nearby ripariansetting and was carried by the river to thelakeshore. Amentotaxus gladifolia (Ludwig),Ferguson, Jahnichen, & Alvin is the single flo-ral associate of Ginkgo at the Juliaetta site. A.gladifolia is also present in the late PaleoceneArdtun Head site, some 40 million years ear-lier. Its nearest living relative, A. formosana Li,grows along streams on mountain flanks(Page 1990).

On the basis of our sedimentological andfloral data, Ginkgo appears to have been eco-logically conservative throughout the Tertiary.Furthermore, the environments of growth ofthe modern G. biloba match the paleoecologicalinterpretations generated here. This markedstability in ecology supports previous work,

based upon morphology alone, that G. adian-toides and G. biloba are conspecific.

The Ecological Paradox of Ginkgo and a Possi-ble Mechanism for Its Decline. Woody plantssuccessful in highly disturbed habitats todayusually share a suite of traits described as thecompetitive-ruderal strategy, sensu Grime(2001). These may include an early-succes-sional habit, shade intolerance, high growthrates, ability for clonal reproduction (Everitt1968; Eriksson 1993), early reproductive ma-turity, small seed size (Harper et al. 1970; Wes-toby et al. 1992), the production of few sec-ondary defense compounds (Coley et al.1985), short life span, and a rapid rate of evo-lution (Eriksson and Bremer 1992). Ginkgoshares some of these characteristics, namelyshade intolerance, rapid early growth, and aclonal habit, but many of its life-history traitscounter those considered beneficial in dis-turbed environments. Ginkgo requires morethan 20 years to reach reproductive maturity,produces large seeds needing a protracted pe-riod for fertilization and embryo develop-ment, manufactures an impressive array ofsecondary defense compounds, can live morethan 3000 years, and has an extremely slowrate of evolution.

Ginkgo therefore represents an ecologicalparadox: it appears to favor disturbed habi-tats, and has likely done so for more than 65million years, yet the living species has few ofthe life-history traits typical of plants thatprosper in modern disturbed settings. One so-lution to this paradox is to accept a non-uni-formitarian view that plants in the geologicpast operated in a different ecological regime,and that it is therefore not appropriate to pi-geonhole Ginkgo into Grime’s system of strat-egies. Angiosperms dominate the canopy to-day in most riparian and crevasse-splay-typeenvironments, and are the principal taxonfrom which modern ecological concepts fordisturbed habitats are derived. The Ginkgo-alean clade first appeared in the Permian andthe Genus Ginkgo in the early Jurassic, makingit possible that, prior to the radiation of an-giosperms early in the Early Cretaceous(Doyle and Hickey 1976), certain competitive-ruderal ecological strategies were less highly


FIGURE 5. Temporal trends of the number of Ginkgo-ales genera and the percent of total plant species that areangiosperms and ‘‘other seed plants’’ (Ginkgoales, Ben-nettitales, Caytoniales, cycads, Czekanowskiales, andGnetales). Ginkgoales data from Tralau (1968); otherdata from Ligard and Crane (1990).

developed than in the present (see Knoll 1984;Bond 1989; Midgley and Bond 1989).

It is difficult to test this hypothesis directlybecause detailed sedimentological data forpre-angiospermous Mesozoic plant fossil-bearing sites are rare, and many lineages thatmay have dominated these disturbed habitatsare extinct. However, from at least the Jurassic,members of Ginkgoales at high latitudes areoften associated with sandy channel deposits(Hughes 1976; Spicer and Parrish 1986; Fal-con-Lang et al. 2001; Spicer and Herman 2001;Spicer et al. 2002; L.J.H. unpublished fielddata from the Jurassic in Yorkshire, England).In the subtropical Lower Cretaceous Wealdenbeds of northwest Germany, Baiera is restrict-ed to barrier sands, whereas Ginkgoites isfound in environments ranging from muddyfloodplains to backswamps (Pelzer et al.1992).

Before the flowering plants, ferns dominat-ed the early seral stages in unstable, fluvialsettings (Hughes 1976; Hickey and Doyle1977; cf. Wing et al. 1993; Taylor and Hickey1996) and probably provided the chief com-petition for Ginkgo from germination to theyoung sapling stage. In competition with theferns, Ginkgo’s large seed reserves and ‘‘bolt-ing’’ habit are inferred to have been sufficientto carry it beyond the herbaceous pterido-phyte canopy. Among arborescent plants,Ginkgo’s chief competitors for crown space be-fore the rise of the angiosperms were probablyBennettitales and various pteridosperms andtree ferns, plants whose sedimentary context,growth-habit, wood, and leaf structure sug-gest that they produced a relatively low, opencanopy on disturbed sites (Hughes 1976;Crane 1985). The growth strategy of livingGinkgo, which undergoes rapid vertical elon-gation to a height of 10 m before elaboratinglateral branches, would have been adaptive insuch a situation.

Many of the early flowering plant lineagesappear to have evolved in disturbed riparianhabitats (Hickey and Doyle 1997; Taylor andHickey 1996), and so could have been directlycompeting with Ginkgo for resources. For ex-ample, studies of the mid-Cretaceous (Albian–Cenomanian) of both northern Alaska (Spicerand Herman 2001) and the Antarctic Penin-

sula (Falcon-Lang et al. 2001) indicate ginkgo-angiosperm-fern communities in riparian de-positional environments. If the combination ofrapid life cycles, high dispersal potential, andabundant foliage production in angiospermswas sufficient to out-compete Ginkgo in thesesettings, then it is possible that they played arole in the decline of Ginkgo.

Moreover, a striking temporal correlationexists between the rise of relative diversity inangiosperms (Ligard and Crane 1990; Lupiaet al. 1999) and the decline in Ginkgoalean di-versity (Tralau 1968) (Fig. 5). This comparisonis not ideal as one must assume that all Gink-goales possessed adaptive strategies similarto those of G. adiantoides. Nonetheless, evenwithin the genus Ginkgo there is a large dropin diversity between the Early and Late Cre-taceous (Tralau 1968). The relative diversity of‘‘other seed plants’’ (see Fig. 5), consisting ofGinkgoales, Bennettitales, Caytoniales, Cyca-dales, Czekanowskiales, and Gnetales, but notconifers, also declines concomitantly with therise of angiosperm diversity (Fig. 5) (Ligardand Crane 1990). The relative diversity offerns, some of which preferred disturbedstreamside environments (Taylor and Hickey1996), drops sharply as well in the mid-Cre-taceous, while the diversity of conifers, whichpreferred backswamp environments, remains


largely unchanged (Ligard and Crane 1990;Lupia et al. 1999). These observations furthersuggest that angiosperms restructured theecology of disturbed floodplain environmentsduring the Cretaceous.

Perhaps the most surprising fact is thatGinkgo survives to the present at all. The per-sistence of the Ginkgo lineage may relate to itsoccurrence in mid- and high-latitude areas(see Fig. 2). Wing and Boucher (1998) arguedthat lower temperatures and less light at high-er latitudes make it more difficult for fast-growing competitive-ruderal trees to prosper,and that this explained the delayed increase inangiosperm diversity and dominance at high-er latitudes during the Cretaceous (e.g., Lupiaet al. 1999). If so, Ginkgo may have persistedbecause it was a mid- to high-latitude lineagefor most of its existence (cf. Bond 1989); withgrowth limited by light and temperature, arelatively slow-growing competitive-ruderalsuch as Ginkgo could persist in the face of an-giosperm competitors with the potential forfaster rates of growth.

Conclusions

Ginkgo is an extreme example of a geologi-cally long-lived genus, with its one living spe-cies arguably having a temporal range of.100 Myr. A quantitative survey of sedimen-tological and floral data from 51 Ginkgo-bear-ing fossil sites, spanning the latest Cretaceousto middle Miocene, indicates that Ginkgo waslargely confined to disturbed stream marginand levee environments. Furthermore, the sta-bility of Ginkgo’s sedimentological and floralassociations through the time series parallelsthe morphological identity of the fossil speciesG. adiantoides and the living G. biloba. As manyof Ginkgo’s life-history traits (e.g., long lifespan, large seeds, and late sexual maturity)are not considered advantageous today inhighly disturbed habitats, it is possible thatGinkgo represents the survival of a pre-angio-spermous strategy for growth in well-drained,disturbed habitats.

Acknowledgments

This work was supported by Department ofEnergy grant DE-FG02–01ER15173, a Nation-al Science Foundation Graduate Research Fel-

lowship, and the Smithsonian Institution. Wethank K. Johnson for providing pre-publica-tion data; M. Bernet for help in preparing Fig-ure 2; W. Rember for his hospitality as well asfor guidance to the Juliaetta site and discus-sions of it; W. Green for field assistance andvaluable discussion; T. Tsuihiji for translatingan article; and R. Burnham, P. Del Tredici, J.Carroll, and M. Kraus for manuscript com-ments.

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Appendix 1Sources of Data

Site Source

Williston BasinSedimentology and floral dataDating

Johnson 2002; Crane et al. 1990 (Almont site)Hicks et al. 2002

Bighorn BasinSedimentology and floral dataDating

Hickey 1980; Wing et al. 1995; field observationsGingerich 2000; Wing et al. 2000 (Age Model 2)

Denver Basin (Site DMNH 2360)SedimentologyDating

R. S. Barclay unpublished dataRaynolds et al. 2001 (p. 25)

Basilika site (Spitsbergen)Sedimentology and floral dataDating

Manum 1963Kvacek et al. 1994

South-central AlbertaSedimentology and floral dataDating

Speirs 1982; Hoffman and Stockey 1999Fox 1990

Ardtun Head site (Scotland)Sedimentology and floral dataDating

Boulter and Kvacek 1989Royer et al. 2001

Stenkul Fiord site (Ellesmere I.)Sedimentology and floral dataDating

Field observationsKalkreuth et al. 1996

Beaver Creek site (Montana)Sedimentology and floral dataDating

K. R. Johnson unpublished dataC. N. Miller unpublished data

Juliaetta site (Idaho)Sedimentology and floral dataDating

Field observationsReidel and Fecht 1986


App

endi

x2

Sum

mar

yof

sed

imen

tolo

gy

atG

inkg

o-b

eari

ng

site

s.W

5W

illi

ston

Bas

in(w

este

rnN

orth

and

Sou

thD

akot

a,U

.S.A

.);B

HB

5B

igh

orn

Bas

in(W

yom

ing

and

Mon

tan

a,U

.S.A

.);D

B5

Den

ver

Bas

in(C

olor

ado,

U.S

.A.)

;S5

sou

thw

este

rnSp

itsb

erg

en(N

orw

ay);

A5

sou

th-c

entr

alA

lber

ta(C

anad

a);I

M5

Isle

ofM

ull

(Sco

tlan

d);

E5

sou

th-

wes

tern

Ell

esm

ere

Isla

nd

(Can

ada)

;M

T5

wes

tern

Mon

tan

a(U

.S.A

.);

ID5

nor

th-c

entr

alId

aho

(U.S

.A.)

.Se

dim

ento

log

ical

con

text

sw

ith

ques

tion

mar

ks

not

incl

ud

edin

anal

ysi

s.

Site

no.

Site

nam

eL

ocat

ion

Ag

e(M

a)Se

dim

enta

ryfe

atu

res

Inte

rpre

tati

on

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16

DM

NH

571

DM

NH

1492

DM

NH

572

DM

NH

425

DM

NH

2087

DM

NH

568

DM

NH

566

DM

NH

1489

KJ

8310

1/84

15L

JH74

23L

JH74

24c

LJH

7425

/76

53L

JH76

59D

MN

H23

60B

asil

ika

LJH

7861

W W W W W W W W BH

BB

HB

BH

BB

HB

BH

BD

BS B

HB

65.9

65.9

65.8

65.6

65.5

65.5

65.5

65.4

64.5

64.5

64.5

64.5

64.5

64.1

64 64

San

dst

one-

mu

dst

one

cou

ple

tsTa

bula

rsa

nd

wit

hro

ottr

aces

onto

pSa

nd

ston

e-m

ud

ston

eco

up

lets

Cro

ss-b

edd

edsa

nd

ston

eSa

nd

ston

e-m

ud

ston

eco

up

lets

Cro

ss-b

edd

edsa

nd

ston

eG

leye

dm

ud

ston

ew

ith

abu

nd

ant

root

trac

esSa

nd

ston

e-m

ud

ston

eco

up

lets

Tabu

lar

san

dSa

nd

ston

e-sh

ale-

lig

nit

eu

pw

ard

sequ

ence

;Gin

kgo

insa

nd

Led

gey

cros

s-b

edd

edsa

nd

ston

eL

edg

eycr

oss-

bed

ded

san

dst

one

Silt

ston

e(r

elie

fch

ann

el)

atb

ase

ofcl

ayp

lug

(ab

and

oned

cuto

ff)

Gra

ycl

ayst

one

w/

occa

sion

alfi

ne/

med

san

dp

arti

ng

s;

8m

silt

son

tes/

san

dst

ones

rest

ing

on;

30cm

peb

ble/

cobb

leco

ng

lom

.Si

ltst

one/

san

dst

one

over

lyin

gli

gn

ite;

Gin

kgo

insa

nd

Rel

ief

chan

nel

Cre

vass

esp

lay

Rel

ief

chan

nel

Ch

ann

elR

elie

fch

ann

elC

han

nel

Dis

tal

floo

dp

lain

Rel

ief

chan

nel

Cre

vass

esp

lay

Cre

vass

esp

lay

Cre

vass

esp

lay

Cre

vass

esp

lay

?R

elie

fch

ann

elC

reva

sse

spla

yR

elie

fch

ann

elC

reva

sse

spla

y17 18 19 20 21 22 23 24 25 26 27 28 29 30 31

Joff

reB

rid

ge

Bu

rban

kSL

W00

29SL

W00

25L

JH72

127

SLW

0019

Ch

ance

Alm

ont

SLW

993

SLW

992

SLW

991

SLW

0051

LJH

7214

1-1

SLW

9155

SLW

9427

/94

37

A A BH

BB

HB

BH

BB

HB

BH

BW B

HB

BH

BB

HB

BH

BB

HB

BH

BB

HB

58.5

58.5

57.8

57.3

57 56.7

56.4

56 55.9

55.9

55.9

55.9

55.8

55.7

55.5

Car

bon

aceo

us

mu

dst

one;

Gin

kgo

inh

ard

mol

lusc

laye

rC

oars

esa

nd

ston

eb

oun

ded

bysh

ales

Gra

ysi

ltst

one

abov

eca

rbon

aceo

us

shal

eSi

ltst

one-

mu

dst

one

cou

ple

ts;G

inkg

om

ain

lyin

silt

ston

eL

ign

ite-

silt

ston

e-sa

nd

sequ

ence

Cro

ss-b

edd

edm

ediu

mto

fin

esa

nd

ston

e;la

rge-

scal

ecr

oss-

cuts

Coa

rsen

ing

-up

war

ds

sequ

ence

;Gin

kgo

insa

nd

Sili

ceou

s,ir

on-s

tain

edsh

ale

con

tain

ing

fish

scal

esov

erly

ing

fin

esa

nd

Bas

eof

chan

nel

fill

dir

ectl

yab

ove

bas

alla

gd

epos

its

(peb

bles

)In

terl

amin

ated

fin

e/co

arse

silt

ston

esL

amin

ated

gra

ysi

ltst

one

Lam

inat

edsi

ltst

one

and

fin

esa

nd

ston

e3

mab

ove

brow

nfi

ssil

eli

gn

ite

Inte

rlam

inat

edsi

ltst

one-

san

dst

one

Th

inly

bed

ded

san

dst

one

Ab

and

oned

chan

nel

Cre

vass

esp

lay

Cre

vass

esp

lay

Rel

ief

chan

nel

Cre

vass

esp

lay

Ch

ann

elC

reva

sse

spla

yA

ban

don

edch

ann

elA

ban

don

edch

ann

elA

ban

don

edch

ann

elA

ban

don

edch

ann

elC

reva

sse

spla

y? C

reva

sse

spla

yC

reva

sse

spla

y32 33 34 35 36 37 38

SLW

9411

SLW

9412

SLW

9438

SLW

9434

SLW

9050

SLW

9715

/98

1SL

W99

36

BH

BB

HB

BH

BB

HB

BH

BB

HB

BH

B

55.5

55.5

55.5

55.4

55.3

55.3

55.3

Inte

rbed

ded

silt

ston

ean

dsa

nd

ston

eab

ove

aca

rbon

aceo

us

shal

eL

amin

ated

fin

esa

nd

Th

inly

bed

ded

san

dst

one

Inte

rlam

inat

edcr

oss-

bed

ded

silt

ston

e-sa

nd

ston

e;G

inkg

oin

silt

ston

eIn

terl

amin

ated

silt

ston

e-sa

nd

ston

eL

amin

ated

fin

ing

-up

war

ds

sequ

ence

s;b

asal

lag

con

tain

sm

ollu

sks

Silt

ston

eov

erly

ing

san

dst

one

Cre

vass

esp

lay

Dis

tal

floo

dp

lain

Cre

vass

esp

lay

Cre

vass

esp

lay

Cre

vass

esp

lay

Rel

ief

chan

nel

?


App

endi

x2.

Con

tin

ued

.

Site

no.

Site

nam

eL

ocat

ion

Ag

e(M

a)Se

dim

enta

ryfe

atu

res

Inte

rpre

tati

on

39 40 41 42 43 44 45 46 47 48 49 50 51

SLW

8612

Ard

tun

Hea

dSL

W98

12St

enk

ul

Fio

rdSL

W99

11SL

W99

15SL

W84

1SL

WL

BSL

WH

SLW

nea

rY

PM

67L

JH99

15B

eave

rC

reek

Juli

aett

a

BH

BIM B

HB

E BH

BB

HB

BH

BB

HB

BH

BB

HB

BH

BM

TID

55.3

55.2

55.1

55 54.8

54.8

54.3

53.9

53.5

53.5

53.4

36 16.5

Car

bon

aceo

us

shal

eW

hit

e/g

ray

clay

ina

clay

/sa

nd

ston

ese

quen

cein

terb

edd

edw

ith

bas

alt

Gra

ysh

ale-

mu

dst

one

cou

ple

tsM

ediu

mto

fin

ecr

oss-

bed

ded

san

dst

one

wit

hcl

imbi

ng

rip

ple

sM

ud

ston

e/si

ltst

one

cou

ple

ts;g

reen

san

dat

bas

eSa

nd

ston

e-ca

rbon

aceo

us

shal

e-si

ltst

one

un

it;G

inkg

oin

top

silt

ston

eC

arb

onac

eou

ssh

ale

Coa

rse

carb

onac

eou

ssi

ltst

one

San

dy

silt

ston

e

Th

inca

rbon

aceo

us

len

ticu

lar

pap

ersh

ale

san

dw

ich

edb

etw

een

soil

s

Coa

rse

san

d;d

elta

fore

sets

Bac

ksw

amp

Rel

ief

chan

nel

Rel

ief

chan

nel

Ch

ann

elR

elie

fch

ann

elR

elie

fch

ann

elB

ack

swam

pR

elie

fch

ann

elR

elie

fch

ann

elR

elie

fch

ann

elR

elie

fch

ann

elL

ake

Lak

e


Appendix 3Summary of flora at Ginkgo-bearing sites. Only those species that occur at four or more sites are tabulated here.

n 5 number of occurrences for a given species. See Appendix 2 for full description of sites, and Appendix 4 forauthors for all species names used in the body of this paper.


Appendix 3. Extended.


Appendix 3. Extended.


Appendix 4

Complete list of species names with authors used in the textand appendices

Acer silberlingii BrownAesculus hickeyi ManchesterAmentotaxus formosana LiAmentotaxus gladifolia (Ludwig) Ferguson, Jahnichen, & AlvinArchaeampelos acerifolia (Newberry) McIver & BasingerAthyrium Felix-femina L.Averrhoites affinis (Newberry) HickeyBaiera sp. F. BraunBeringiaphyllum cupanoides (Newberry) Manchester, Crane & Go-

lovnevaBetulaceae sp. 1 (sensu Wing et al. 1995)Cercidiphyllum genetrix (Newberry) HickeyCercidiphyllum japonicum Siebold & ZuccariniCorylus insignis HeerDryophyllum subfalcata LesquereuxErlingdorfia montana Johnson‘‘Ficus’’ artocarpoides Lesquereux‘‘Ficus’’ planicostata LesquereuxGinkgo adiantoides (Unger) HeerGinkgo beckii Scott, Barghoorn & PrakashGinkgo biloba L.Ginkgo coriacea FlorinGinkgo digitata (Brongniart) HeerGinkgo gardneri Florin

Ginkgo huttoni (Sternberg) HeerGinkgo spitsbergensis ManumGinkgo tigrensis ArchangelskyGinkgo yimaensis Zhou & ZhangGinkgoites SewardGlyptostrobus europaeus (Brongniart) HeerLeepierceia preartocarpoides JohnsonMacginitiea brownii (Berry) Wolfe & WehrMacginitiea gracilis (Lesquereux) Wolfe & WehrMenispermites parvareolatus HickeyMetasequoia glyptostroboides H. H. Hu & ChengMetasequoia occidentalis (Newberry) ChaneyNyssidium arcticum (Heer) IljinskayaParanymphaea crassifolia (Newberry) BerryPlatanaceaePlatanus 3 acerifolia WilldenowPlatanus guillelmae GeoppertPlatanus occidentalis L.Platanus orientalis L.Platanus raynoldsii Newberry‘‘Rhamnus’’ cleburni LesquereuxTaxodium olrikii (Heer) BrownTrochodendroides nebrascensis (Newberry) DorfVitis stantoni (Knowlton) BrownWardiaphyllum daturaefolia (Ward) HickeyZingiberopsis isonervosa HickeyZizyphoides flabella (Newberry) Crane, Manchester & Dilcher

Documents

Ecological conservatism in the “living fossil” Ginkgo