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The phenology of sexual reproduction in Ginkgo biloba: ecological and evolutionary implications.

Abstract
Introduction
Literature Review
Pollination and Fertilization
Germination
Materials and Methods
Results
Discussion
 Evolutionary Implications
 Ginkgo Seed Dispersal
Acknowledgments
Literature Cited


Introduction

Ginkgo biloba L. is a large tree native to China that is widely cultivated throughout the temperate world. It is a dioecious, wind-pollinated, animal-dispersed gymnosperm with evolutionary affinities to both cycads and the conifers (Norstog et al., 2004). The reproductive biology of Ginkgo has fascinated botanists since the discovery of its multi-flagellated spermatozoids by Hirase in 1896. While the anatomical and developmental aspects of Ginkgo's gametophytic life cycle have been carefully documented (Lee, 1955; Favre-Duchartre, 1958; Wang & Chen, 1983; Friedman, 1987; Friedman & Gifford, 1997; Norstog et al., 2004), much less is known about the phenological and ecological aspects of its sexual reproduction cycle, mainly because of its limited distribution in the wild (Li et al., 1999; Xiang et al., 2006). In view of the absence of information on seedling reproduction in nature, the purposes of this paper are to (1) review the literature relating to pollination, fertilization, embryo development, seed abscission, and seed germination of Ginkgo in cultivation; (2) report the results of a germination experiment utilizing Ginkgo seeds produced at two different latitudes; and (3) discuss the implications of these results on the question of Ginkgo seed dispersal and seedling establishment in the modern era as well as in the geological past.

Literature Review

Questions about the extent of G. biloba's native range in China have been the subject of debate among botanists for well over a hundred years (Del Tredici et al., 1992; Li et al., 1999). Recent DNA analyses (Fan et al., 2004; Shen et al., 2005; Wei et al., 2007) have demonstrated that isolated Ginkgo populations in southwestern China, especially around the southern slopes of Jinfo Mountain in Chongqing Province (28[degrees]53'N; 107[degrees]27'E) possess a significantly higher degree of genetic diversity than populations in other parts of the country. The area has a mesic, warm-temperate climate with a mean annual temperature of 16.6[degrees]C and a mean annual precipitation of 1185 ram, with Ginkgo trees growing mainly between elevations of 800 and 1300m (Li et al., 1999). Ecological work in this area, as well as in adjacent parts of Guizhou Province (Xiang et al., 2006), has identified numerous small populations that can be considered to be either wild or remnants of wild plants, despite their proximity to small villages practicing subsistence agriculture. Within many of these populations, Ginkgo seedlings and saplings are not uncommon in the understory.

In contrast to its limited distribution as a wild plant, Ginkgo is widely cultivated as an urban street tree and for the production of its edible "nuts" and medicinally active leaves (Del Tredici, 2000). The species is highly adaptable and grows well in most regions with a distinct seasonality and moderate rainfall, including areas with warm-temperate, cold-temperate, or Mediterranean climates. In China, Ginkgo is cultivated across a broad range of moisture, temperature, and topographic gradients between 25[degrees] and 42[degrees]N latitude, where minimum winter temperatures can reach -32[degrees]C and maximum summer temperatures 42[degrees]C (He et al., 1997). Phenological studies across a north-south gradient in Japan (Matsumoto et al., 2003) have determined that spring bud break in Ginkgo occurs 40 days earlier in the extreme south of the country (30[degrees]N latitude) than in the far north (43[degrees]N latitude) and that autumnal leaf drop happens about 40 days later, making for an effective vegetative growing season range of 170 to 260 days across 13[degrees] of latitude.

Ginkgo is dioecious with male and female individuals occurring at roughly a 1:1 ratio (Santamour et al., 1983). Ginkgo shows a long juvenile period, typically not reaching sexual maturity until approximately 20 years of age. Male (microsporangiate) and female (ovulate) sex organs are produced on short shoots in the axils of bud scales and leaves. The catkins emerge before the leaves and fall off immediately after shedding their pollen. Wind pollination occurs anywhere from mid-March in areas with mild winters to late May in areas with severe winters (Del Tredici, 1989).

Ginkgo ovules are 2 to 3 mm long and produced mostly in pairs at the ends of stalks 1 to 1.5 cm long. When the ovule is receptive, it secretes a small droplet of mucilaginous fluid from its micropyle, which functions to capture airborne pollen. Retraction of this droplet at the end of the day brings the pollen into the pollen chamber. Once inside the ovule, the male gametophyte commences a 4- to 5-month-long period of development that culminates with the production of a pair of multiflagellated spermatozoids, one of which fertilizes a waiting egg cell while the ovules are still on the tree (Friedman, 1986; Friedman & Gifford, 1997). Seed drop typically occurs after fertilization, at which point the embryo can be anywhere from <1 to 5 mm in length, depending on local conditions (Li, 1934; Holt & Rothwell, 1997). Once on the ground, the embryo continues to develop until the arrival of cold weather, at which point elongation stops (Li & Chen, 1934). Under artificial storage conditions, temperatures between 5 and 10[degrees]C completely inhibit embryo growth (Li & Chen, 1934; Hatano & Kano, 1952).

The mature seed of Ginkgo is relatively large (20-30mm x 16-24mm) and consists of an embryo embedded in the tissue of the female gametophyte surrounded by a thick seed coat. The intact seed coat consists of a soft, fleshy outer layer (the sarcotesta), a hard, stony middle layer (the sclerotesta), and a thin, membranous inner layer (the endotesta). The seed, devoid of the fleshy sarcotesta, is generally referred to as the "nut," and its dimensions are within the range 19-30 mm x 11-14 mm (Del Tredici, 1989). The shell surrounding the Ginkgo nut is relatively thin--0.3 to 0.4mm--and it has been shown that enough light can penetrate this shell to allow the unfertilized, chlorophyll-producing female gametophyte to carry out photosynthesis (Friedman, 1986).

The developing ovules are green until they mature in the fall, when in response to cold temperatures, they turn the same yellow color that the leaves do. The rancid odor often associated with Ginkgo seeds develops only after they have lain on the ground for several days, and is primarily due to the presence of two volatile compounds, butanoic and hexanoic acids, localized in the sarcotesta (Parliment, 1995). The sarcotesta also contains numerous fatty acids and phenolic compounds (Boralle et al., 1988), one of which, ginkgoic acid, is known to cause allergic contact dermatitis in humans (Kochibe, 1997).

Pollination and Fertilization

Variations in the phenology of pollination, fertilization, and seed abscission in Ginkgo are mainly due to the latitude and the local climate of the region in which the tree is growing. In Tokyo, Japan, where spermatozoids were first discovered, Miyake (1902) noted that wind pollination occurred from the end of April to early May, while fertilization occurred over a period of several days between 7-22 September, 130-145 days later. He also noted that fertilization of Ginkgo ovules occurred about 10 days earlier in the season in Tokyo than it did in Sendai, located about 320km to the northeast. In Paris, France, Favre-Duchartre (1958) found that pollination occurred during the second half of April and fertilization during the first week in September, 139-146 days later. In Urbana, Illinois, United States, Lee (1955) observed pollination in early May and fertilization on 5-15 September, 138-148 days later. In Beijing, China, Wang and Chert (1983) reported pollen dispersal from the end of April through early May, and fertilization between 16 and 20 August, 110-114 days later. Working in Berkeley, California, Friedman (1987) recorded pollen dispersal in mid-April and fertilization in early September, 138 to 145 days later. These four detailed records suggest that the average time between pollination and fertilization is roughly 133 days.

The timing of fertilization and subsequent embryo development in relation to seed abscission is highly variable, but most authors agree that fertilization typically takes place while the seeds are still on the tree. Li (1934) and Li and Chert (1934) reported that the embryo in Ginkgo seed was between 0.1 and 4.0mm in length at the time of seed drop in Beijing. Johnson and Wickliff (1974) found "recognizable" embryos in 70% of seeds collected from trees growing in Memphis, Tennessee, in late September. In Beijing, Wang and Chen (1983) reported that fertilization occurred about 6 weeks prior to seed abscission, which usually happened in late September, at which point embryos were <0.5 mm long. Most recently, Holt and Rothwell (1997) found that -90% of seeds collected from trees growing in southeastern Ohio on 20 October, during their period of abscission, contained "well-developed" embryos--up to 5.5 mm in length--clearly indicating that fertilization had occurred well before seed drop. Eames (1955), in Ithaca, New York, and Favre-Duchartre (1958), in Paris, are the only authors to report that fertilization of Ginkgo ovules can occur on the ground, following abscission. Climatic factors may play a role in determining the timing of seed abscission in cold-temperate climates such as Boston, where 11 ovulate Ginkgo trees dropped 50% of their seeds within 3 days of experiencing a seasonal low temperature of -5[degrees]C on 31 October (Del Tredici, 1991).

Germination

As regards the germination of Ginkgo seeds, Li (1934) and Li and Chen (1934) were the first to demonstrate that the underdeveloped state of the embryo at the time of abscission is responsible for delays in germination. Subsequent studies by numerous authors have confirmed that when Ginkgo seeds are collected shortly after they fall, cleaned of their fleshy sarcotesta, and placed in a continuously warm greenhouse environment, the embryo will grow to its full size--10 to 13mm in length--and begin germination within 6 to 10 weeks of abscission (West et al., 1970; Johnson & Wickliff, 1974; Del Tredici, 1991; Holt & Rothwell, 1997). Temperatures during the period of embryo development can play a critical role in determining the speed of germination, as evidenced by the fact that Ginkgo seeds planted in a warm greenhouse (heated to a minimum temperature 20[degrees]C) on 4 November took only 66 days to begin germination, while a replicate sample planted in a cool greenhouse (heated to a minimum temperature 10[degrees]C) took 179 days, and seeds planted outdoors took 245 days (Del Tredici, 1991).

The date of germination of Ginkgo seeds cleaned of their sarcotesta and sown outdoors in the fall is strongly influenced by ambient temperatures. In Beijing, seeds collected in late September began to germinate on 22 April, roughly a year after pollination (Li &Chen, 1934). In Paris, Favre-Duchartre (1958) reported pollination in mid-April and outdoor germination in mid-May, 13 months later. And, finally, in the Boston area, seeds collected shortly after abscission at the end of October did not begin germinating until 7 July, some 13.5 months after pollination (Del Tredici, 1991). Interestingly, seeds cleaned of their sarcotesta showed a significant increase in seed germination percentage relative to seeds in which the sarcotesta was left intact under both greenhouse (Holt & Rothwell, 1997) and outdoor conditions (Del Tredici, 1991).

Cold stratification of Ginkgo seeds is not an absolute requirement for germination, but it increases overall germination percentage and accelerates and synchronizes germination in comparison with unstratified seed (West et al., 1970; Johnson & Wickliff, 1974; Del Tredici, 1991; Holt & Rothwell, 1997). West et al. (1970) attributed these germination effects to increased levels of gibberellic acid ([GA.sub.3]) equivalents in the embryo, which they found to be approximately 100 times greater in stratified versus unstratified embryos. Johnson and Wickliff (1974) reported that exposure to red light also accelerated the germination rate of intact, unstratified seed. Together, these observations indicate that Ginkgo seeds possess a form of morphophysiological dormancy (Baskin & Baskin, 1998).

Taken as a whole, these phenological reports make it clear that (1) fertilization in Ginkgo typically occurs between 130 and 140 days alter pollination: (2) both pollination and fertilization occur earlier in warmer climates than in colder ones; (3) fertilization typically occurs while the seeds are still on the tree, resulting in embryos between 0.1 and 5.5 mm long at the time of seed abscission; (4) the length of time between fertilization and seed abscission is highly variable and influenced by local weather conditions; (5) under constant warm indoor conditions, the growth of the embryo is a continuous, temperature-dependent process that begins with fertilization and ends with germination; (6) because the length of time between fertilization and seed abscission is variable, the length of time between seed abscission and germination under warm greenhouse conditions is also variable, anywhere from 6 to 10 weeks; (7) low temperatures (between 2 and 10[degrees]C) following fertilization inhibit embryo development and delay the germination of outdoor-sown seed until the following spring or summer; (8) cold stratification increases seed germination percentage and accelerates and synchronizes the rate of germination; and (9) the length of time between pollination and germination under field conditions can vary between 12 and 14 months, depending on local weather conditions.

Materials and Methods

Experiments to explore the relationship between the timing of pollination and the timing of germination in Ginkgo were undertaken in the greenhouses and nurseries of the Arnold Arboretum in Boston, Massachusetts, using seeds from trees growing in two different latitudes. One lot of approximately 500 seeds cleaned of their fleshy sarcotesta were purchased on 22 September 2002 at Tuo Le Village, Panxian, Guizhou Province, China, from trees cultivated for nut production (25[degrees]36'58.02"N; 104[degrees]32'57.94"E; mean annual temperature, 15.5[degrees]C; mean January temperature, 6.3[degrees]C; mean July temperature, 21.8[degrees]C; mean annual precipitation, 1400 ram) (Shi Jikong, personal comm.). According to local informants, the trees had shed the seeds a week prior to our visit (-15 September). In this part of southwestern China, Ginkgo pollination typically occurs between mid-March and early April, and germination occurs the following March, making for a 12-month sexual reproduction cycle.

Upon return to the Arnold Arboretum, 18 of the seeds from Tuo Le were dissected under a 10x magnifying lens on 8 October and scored for the presence or absence of an embryo. In addition, 400 Tuo Le seeds were sown in deep, plastic flats at a rate of 50 seeds per flat on 4 October 2002 (AA accession # 472-2002). Four of the flats (200 seeds total) were placed in a warm greenhouse (20[degrees]C minimum night time temperature), and four were placed in an outdoor nursery area.

For comparative purposes, over 600 Ginkgo seeds were collected on 31 October 2002 from beneath a number of different trees growing at the Forest Hills Cemetery in Boston, Massachusetts, located 1 km from the Arnold Arboretum (42[degrees]17'50.12"N; 71[degrees]6'18.46"W; mean annual temperature, 10.9[degrees]C; mean January temperature, -1.5[degrees]C; mean July temperature, 23.3[degrees]C; mean precipitation, 1061 mm). Typically, Ginkgo trees in the Boston area shed their pollen between 10 and 25 May, with seed drop occurring between mid-October and early November (Del Tredici, 1991). The seeds were given the accession #490-2002, and 10 were dissected under a 10x magnifying lens on 7 November and scored for the presence or absence of an embryo. In addition, 400 seeds were cleaned of their fleshy sarcotesta, air dried for 2 days, divided into lots of 50, and sown in deep, plastic flats on 5 November 2002. Four of these flats (200 seeds) were placed in the warm greenhouse (20[degrees]C minimum) and four were placed in an outdoor nursery. In addition, four flats of 50 seeds each with their sarcotesta intact were placed in the outdoor nursery to determine how its presence influenced the percentage and speed of germination. The flats of all outdoor-sown seeds were set into the ground adjacent to one another, covered with 2 cm of loose soil, and then covered with heavy-duty wire mesh to protect them against rodent predation.

Results

Of the 18 Guizhou seeds dissected on 8 October 2002, 3 to 4 weeks after falling from the trees, 72% possessed a visible embryo, with a mean length of 1.14 mm (range, 1.27-0.81 mm). None of the 10 Forest Hills seeds dissected a week after they were collected from the ground possessed a visible embryo. Germination percentages for the Guizhou and Boston seeds sown both indoors and outdoors in Boston are presented in Table I. It is not clear why the percentage germination of the indoor Guizhou seed was significantly lower that that of the other seed lots, but the germination of a replicate seed lot sown outdoors was statistically equivalent to the germination of the Boston seed. The results of the sarcotesta removal experiment were particularly striking, with only 15% of the uncleaned, outdoor-sown Boston seeds germinating versus 71.5% germination for the replicated cleaned lot. Furthermore, germination of the uncleaned seed did not begin until 25 June, 9 days later than the cleaned seed. These results confirmed the work of Holt and Rothwell (1997), who found that 66% of outdoor-sown seed with the sarcotesta removed germinated, while 30% of seeds with the sarcotesta intact germinated.

Guizhou seed sown in the greenhouse began germinating on 12 November--approximately 58 days after abscission--while the Boston seed did not begin germinating until 6 January--67 days after abscission. Assuming pollination dates of 24 March for the Guizhou seed and 17 May for the Boston seed, the total time elapsed from pollination to germination under continuously warm greenhouse conditions (20[degrees]C) was 233 and 234 days, respectively, a remarkably confluent result given their different origins.

When sown outdoors in Boston, cleaned Guizhou seed began germinating on 29 May, while the cleaned Boston seed began germination on 16 June, a difference of only 18 days. It is important to note, however, that 35% of the Guizhou seed that germinated did so on the first day, and 77.5% within 6 days. In contrast, it took the Boston seed 18 days to reach 56% of its final germination total.

Discussion

Both the literature and the results of this experiment indicate that all aspects of Ginkgo's sexual reproductive cycle are strongly influenced by temperature. For seeds left outdoors immediately following seed abscission, the timing of their pollination influences the timing of their germination the following spring, which, in turn, influences their chances of surviving the following winter. In warm-temperate climates--such as Guizhou Province--Ginkgo seeds are shed in late summer or early fall, and the embryo is able to make considerable growth during the mild weather that follows immediately after. In cold-temperate climates--such as Massachusetts--seeds are shed much later in the season, and the cooler temperatures of mid- to late fall delay embryo development until warm weather arrives in the following spring. This differential timing of embryo maturation means that seeds produced by trees growing in warm-temperate climates will be ready to germinate during the favorable conditions of mid- to late spring (March through early June), while those in cold climates will not germinate until later in the summer (late June through early August), when conditions for establishment are less favorable and the seedlings have less time to accumulate carbohydrates before going into winter dormancy. In this regard, it is worth noting that in Tuo Le Village in Guizhou Province, Ginkgo seeds sown outdoors typically germinate in March, while the same seed sown outdoors in Boston did not germinate until 29 May, approximately 2 months later. From an ecological perspective, the complex phenology of Ginkgo's sexual reproduction cycle may well constrain the species' ability to migrate, independently of humans, into cold-temperate regions with short growing seasons, and probably accounts for its limited, warm-temperate distribution as a wild or semi-wild tree in the mountains of central China (Li et al., 1999; Xiang et al., 2006; Wei et al., 2007). Table II presents a comparison of the phenology of Ginkgo's sexual reproduction cycle in Guizhou Province, China, versus Massachusetts, United States.

The fact that outdoor-sown seed from Guizhou germinated only 18 days before the Boston seed, despite having a phenological advantage of 6 weeks, suggests that low temperatures in fall and spring can delay the germination of Ginkgo embryos regardless of their developmental state. During the month of April 2003, when germination in both seed lots was inhibited, the average high temperature at the Arnold Arboretum was 12.7[degrees]C, the average low was 1.5[degrees]C, and there were 12 days when the temperature was below zero. In May, the average high temperature at the Arnold Arboretum was 19.6[degrees]C, the average low was 7.6[degrees]C, and there were no days below zero. Based on this limited data, it seems as though both embryo development and germination are delayed until nighttime temperatures are consistently between 5 and 10[degrees]C and daytime temperatures between 15 and 20[degrees]C. Support for this estimate is provided by the work of Del Tredici (1991), who found that clean Ginkgo seeds sown in a warm (20[degrees]C minimum) greenhouse began germination within 66 days, while a replicate sample in a cool (10[degrees]C minimum) greenhouse required 179 days, and by the work of both Li and Chen (1934) and Hatano and Kano (1952), who found that seeds stored at temperatures between 5 and 10[degrees]C showed no measurable embryo growth during their periods of storage.

In a related phenological study, Matsumoto and colleagues (2003) have documented temperature sensitivity in Ginkgo's vegetative growth cycle that is similar to that of its sexual reproduction cycle. Using long-term data from trees cultivated along a north-south gradient in Japan, the authors found that between the years 1953 and 2000 bud burst advanced by 4 days and leaf drop by 8 days over this time period, and that both of these shifts were highly correlated with changes in air temperature over that time period.

The fact that Ginkgo seeds cleaned of their fleshy sarcotesta germinated at significantly higher percentages than those with their sarcotesta intact suggests that the animals that consume the seeds--provided they do not crush the thin-shelled nut--may play a role in promoting successful seedling germination (Rothwell & Holt, 1997; Del Tredici, 2000). The specific mechanism whereby the sarcotesta reduces the germination capacity of Ginkgo seed is currently unknown, but the exclusion of light is probably not an explanation given that female gametophytes with all their seed coats intact are capable of photosynthesis (Friedman, 1986).

EVOLUTIONARY IMPLICATIONS

The fossil species Ginkgo adiantoides existed in the northern hemisphere from the Upper Cretaceous through the Middle Miocene and is considered by most paleobotanists to be morphologically indistinguishable from the modern Ginkgo biloba (Tralau, 1968; Royer et al., 2003). Most of the Ginkgo fossils from this time period in Europe and North America come from sites that were originally disturbed stream margins or levee environments above 40[degrees]N latitude, and typically occurred as part of a consistent set of associated riparian plants, including Cercidiphyllum, Metasequoia, Platanus, and Glyptostrobus (Royer et al., 2003). Recent fossils of a new Ginkgo species from Liaoning Province, China (Zhou & Zheng, 2003; Zheng & Zhou, 2004), have pushed the lineage of G. biloba-type ovules back to the Lower Cretaceous, about 120 million years ago, which suggests the possibility that its seeds might have possessed a temperature-sensitive developmental-delay mechanism similar to that of G. biloba. Such a trait would have allowed this species to reproduce successfully in regions of the Northern Hemisphere that were undergoing dramatic cooling after a long period of stable, warm conditions (Ziegler et al., 1993). Indeed, Zheng and Zhou (2004) have proposed "that the drastic climatic changes during the Upper Jurassic and Lower Cretaceous were responsible for the transformation of the ovulate organs of the G. yimaensis type into the modern G. biloba type." According to Zhou and Wu (2006), this morphological transformation included the development of short shoots, the reduction and protection of ovulate organs, and the production of larger seeds. Ginkgo biloba's temperature-sensitive embryo developmental-delay mechanism could well have been another climate-induced Cretaceous innovation--an evolutionarily primitive, but ecologically functional, form of seed dormancy (Mapes et al., 1989).

GINKGO SEED DISPERSAL

Researchers studying various Ginkgo populations in Asia have reported a number of animals feeding on, and presumably dispersing, the odoriferous, nutrient-rich seeds of Ginkgo. In China, dispersal agents include two members of the order Carnivora: the leopard cat (Felis bengalensis, family Felidae) in Hubei Province (Jiang et al., 1990) and the masked palm civet (Paguma larvata, family Viveridae) in Zhejiang Province (Del Tredici et al., 1992). In Japan, where Ginkgo was introduced from China some 1200 years ago, another member of the order Carnivora, the raccoon dog (Nyctereutes procyonoides, family Canidae) has been documented feeding on Ginkgo seeds, and its droppings have been found to contain intact seeds that germinated the following spring (Rothwell & Holt, 1997).

The existence of three reports of omnivorous members of the Carnivora consuming whole Ginkgo seeds suggests that the rancid-smelling sarcotesta may be attracting primarily nocturnal scavengers by mimicking the smell of rotting flesh, in essence, a carrion-mimic (Del Tredici et al., 1992). The fact that Ginkgo seed germination percentage is significantly enhanced by removal of the sarcotesta lends further credence to this theory. Projecting this concept into the Paleogene, two families of primitive Carnivora, the Viverravidae and the Miacidae are potential Ginkgo dispersers. Both groups had holarctic distributions and generalized dentitions and were relatively small, "from the size of a weasel to that of a small cat" (Kemp, 2005).

Modern tree squirrels in the genus Sciurus (family Sciuridae, order Rodentia) have been reported to teed on Ginkgo seeds in both North America (Del Tredici, 1989) and China (Del Tredici et al., 1992). Such observations led to speculation that extinct mammalian multituberculates, such as those in the Paleocene genus Ptilodus, might have consumed and dispersed Ginkgo seeds in the past (Del Tredici, 1989). This idea was later discounted on the basis of a biomechanical analysis that showed that Ptilodus' jaw structure could not handle objects the size of G. biloba nuts (Wall & Krause, 1992) and clearly illustrates the pitfalls of speculating about potential ecological relationships between extinct animals and extant plants (Tiffney, 2004).

More recently, Zhou and Zhang (2002) reported the discovery a long-tailed bird (Jeholornis sp.) from the Early Cretaceous in China with a large number of Ginkgo-like seeds in its crop, direct evidence that early birds potentially could have been involved in seed dispersal activities, although their intact nature suggests they were destined for digestion in the gizzard. In general, G. biloba seeds of do not fit the typical profile of a fruit dispersed by modern birds (van der Pijl, 1982). Prior to the discovery of Jeholornis, most of the speculation about Cretaceous Ginkgo dispersal agents centered on dinosaurs, based primarily on their temporal overlap (Janzen & Martin, 1982; van der Pijl, 1982; Tiffney, 1984; Del Tredici, 1989, 2000; Rothwell & Holt, 1997; Zhou & Wu, 2006). If dinosaurs were involved in the dispersal of Ginkgo seeds, they probably would have been carrion-feeding scavengers, with teeth adapted to tearing and swallowing flesh, rather than herbivores with grinding dentition, which would have crushed the thin-shelled seeds. At any rate, any connection between dinosaurs and Ginkgo seed dispersal is, at best, conjecture based on circumstantial evidence.

Acknowledgments

The author would like to thank Elisabeth and Jim Dudley of the Highstead Arboretum in Redding, Connecticut, for generous support by the arboretum of a trip to Guizhou Province in 2002, Professors Shi Jikong of Guizhou University and Fu Cheng-Xin of Zhejiang University for organizing the trip, Li Jianhua of the Arnold Arboretum for help with all aspects of the project, and Michael Dosmann for his editorial and statistical suggestions.

Literature Cited

Baskin, C. C. & J. M. Baskin. 1998. Seeds: ecology, biogeography, and evolution of dormancy and germination. Academic Press, New York.

Boralle, N., P. Braquet & O. R. Gottlieb. 1988. Ginkgo biloba: a review of its chemical composition. Pp. 9-25 in P. Braquet (ed.), Ginkgolides--chemistry, biology, pharmacology and clinical perspectives, vol. 1. J. R. Prous, Barcelona.

Del Tredici, P. 1989. Ginkgos and multituberculates: interactions in the Tertiary. BioSystems 22: 327-339.

--. 1991. The evolution and natural history of Ginkgo biloba. Ph.D. diss., Boston University, Boston.

--. 2000. The evolution, ecology, and cultivation of Ginkgo biloba. Pp. 7-24 in T. Vanbeek (ed.), Ginkgo biloba. Harwood Academic, Amsterdam.

--, H. Ling & Y. Guang. 1992. The Ginkgos of Tian Mu Shan. Conservation Biol. 6: 202-210. Eames, A. J. 1955. The seed and Ginkgo. J. Arnold Arbor. 36: 165-170.

Fan, X. X., L. Shen, X. Zhang, X. Y. Chen& C. X. Fu. 2004. Assessing genetic diversity of Ginkgo biloba L. (Ginkgoaceae) populations from China by RAPD markers. Biochem. Genet. 42: 269-278.

Favre-Duehartre, M. 1958. Ginkgo: an oviparous plant. Phytomorphology 8: 377-390.

Friedman, W. E. 1986. Photosynthesis in the female gametophyte of Ginkgo biloba. Amer. J. Bot. 73: 1261-1266.

--. 1987. Morphogenesis and experimental aspects of growth and development of the male gametophyte of Ginkgo biloba within the ovule (in vivo). Amer. J. Bot. 74:1797-1815.

--& E. M. Gifford. 1997. Development of the male gametophyte of Ginkgo biloba: a window into the reproductive biology of early seed plants. Pp. 29-50 in T. Hori, R. W. Ridge, W. Tulecke, P. Del Tredici, J. Tremouillaux-Guiller & H. Tobe (eds.), Ginkgo biloba--a global treasure. Springer, Tokyo.

Hatano, K. & T. Kano. 1952. A brief report on the alter-ripening of the seeds of Ginkgo biloba. J. Jap. Forest. Soc. 34:369-370 (in Japanese).

He, S. A., Y. Gu & Z. J. Pang. 1997. Resources and prospects of Ginkgo biloba in China. Pp. 373-383 in T. Hori, R. W. Ridge, W. Tulecke, P. Del Tredici, J. Tremouillaux-Guiller & H. Tobe (eds.), Ginkgo biloba--a global treasure. Springer, Tokyo.

Hirase, S. 1896. On the spermatozoid of Ginkgo biloba. Bot. Mag. (Tokyo) 10: 325-328 (in Japanese).

Holt, B. & G. W. Rothwell. 1997. Is Ginkgo biloba (Ginkgoaceae) really an oviparous plant? Amer. J. Bot. 84: 870-872.

Janzen, D. H. & P. S. Martin. 1982. Neotropical anachronisms: the fruits the gomphotheres ate. Science 215: 19-27.

Jiang, M. Y. Jin & Q. Zhang. 1990. A preliminary study on Ginkgo biloba in Dahongshan region, Hubei. J. Wuhan Bot. Res. 8: 191-193 (in Chinese).

Johnson, M. I. & J. L. Wickliff. 1974. Seed germination of Ginkgo biloba L. I. Influences of cold treatment, gibberellic acid and red light. Proc. Arkansas Acad. Sci. 28: 34-36.

Kemp, T. S. 2005. The origin and evolution of mammals. Oxford Univ. Press, Oxford.

Kochibe, N. 1997. Allergic substances of Ginkgo biloba. Pp. 301-307 in T. Hori, R. W. Ridge, W. Tulecke, P. Del Tredici, J. Tremouillaux-Guiller & H. Tobe (eds.), Ginkgo biloba--a global treasure. Springer, Tokyo.

Lee, C. L. 1955. Fertilization in Ginkgo biloba. Bot. Gaz. 117: 79-100.

Li, J. W., Z. G. Liu, Y. G. Tan & M. B. Ren. 1999. Studies on the Ginkgo at Jinfoshan Mountain. Forest Res. 12: 197-201 (in Chinese).

Li, T. T. 1934. The development of embryo of Ginkgo biloba. Sci. Rep. Natl. Tsing Hua Univ., Ser. B, Biol. Sci. 2: 29-35.

-- & S. M. Chert. 1934. Temperature and the development of the Ginkgo embryo. Sci. Rep. Natl. Tsing Hua Univ., Ser. B, Biol. Sci. 2: 37-39.

Mapes, G., G. W. Rothwell & M. T. Haworth. 1989. Evolution of seed dormancy. Nature 337: 645-646.

Matsumoto, K., T. Ohta, M. Irasawa & T. Nakamura. 2003. Climate change and extension of the Ginkgo biloba L. growing season in Japan. Global Change Biol. 9: 1634-1642.

Miyake, K. 1902. The spermatozoid of Ginkgo. J. Appl. Microscop. Lab. Meth. 5: 1773-1780.

Norstog, K. J., E. M. Gifford & D. W. Stevenson. 2004. Comparative development of the spermatozoids of cycads and Ginkgo biloba. Bot. Rev. 70: 5-15.

Parliment, T. 1995. Characterization of the putrid aroma compounds of Ginkgo biloba fruits. Pp. 276-279 in R. Rouseff & M. Leahy (eds.), Fruit flavors: biogenesis, characterization, and authentication, Amer. Chem. Soc. Symp. Ser. 596.

Rothwell, G. W. & B. Holt. 1997. Fossils and phenology in the evolution of Ginkgo biloba. Pp. 223-230 in T. Hori, R. W. Ridge, W. Tulecke, P. Del Tredici, J. Tremouillaux-Guiller & H. Tobe (eds.), Ginkgo biloba--a global treasure. Springer, Tokyo.

Royer, D. L., L. J. Hickey & S. L. Wing. 2003. Ecological conservatism in the "living fossil" Ginkgo. Paleobiology 29: 84-104.

Santamour, F. S. Jr., S. A. He & T. E. Ewert. 1983. Growth, survival and sex expression in Ginkgo. J. Arboric. 9: 170-171.

Shen, L., X. Y. Chen, X. Zhang, Y. Y. Li, C. X. Fu & Y. X. Qiu. 2005. Genetic variation of Ginkgo biloba L. (Ginkgoaceae) based on cpDNA PCR_Rflps: inference of glacial refugia. Heredity 94: 396-401.

Tiffney, B. H. 1984. Seed size, dispersal syndromes, and the rise of angiosperms: evidence and hypothesis. Ann. Missouri Bot. Gard 71(2): 551-576.

--. 2004. Vertebrate dispersal of seed plants through time. Annual Rev. Ecol. Evol. Syst. 35: 1-29.

Tralau, H. 1968. Evolutionary changes in the genus Ginkgo. Lethaia 1: 63-101.

Van der Pijl, L. 1982. Principles of dispersal in higher plants, 3rd ed. Springer, Berlin.

Wall, C. E. & D. W. Krause. 1992. A biomechanical analysis of the masticatory apparatus of Ptilodus (Multituberculata). J. Vertebrate Paleontol. 12:172-187.

Wang, F. H. & Z. K. Chen. 1983. A contribution to the embryology of Ginkgo with a discussion of the affinity of the Ginkgoales. Acta Bot. Sin. 25: 199-211 (in Chinese).

Wei, G., Y.-X. Qui, C. Chen, Q. Ye, C.-X. Fu. 2007. Glacial refugia of Ginkgo biloba L and human impact on its genetic diversity: evidence from chloroplast DNA. J. Integr. Pl. Biol. 49(11).

West, W. C., F. J. Frattarelli & K. J. Russin. 1970. Effect of stratification and gibberellin on seed germination of Ginkgo biloba. Bull. Torrey Bot. Club 98: 380-388.

Xiang, B. X, Z. H. Xiang & Y. H. Xiang. 2006. Investigation of wild Ginkgo biloba in Whchuan County of Guizhou, China. Guizhou Sci. 24: 56-67 (in Chinese).

Zheng, S. & Z. Zhou. 2004. A new Mesozoic Ginkgo from western Liaoning, China and its evolutionary significance. Rev. Palaeobot. Palynol. 131: 91-103.

Zhou, Z. & X. W. Wu. 2006. The rise of Ginkgoalean plants in the early Mesozoic: a data analysis. Geol. J. 41: 363-375.

--& F. C. Zhang. 2002. A long-tailed, seed-eating bird from the early Cretaceous of China. Nature 418: 405-409.

--& S. Zheng. 2003. The missing link in Ginkgo evolution. Nature 423: 821-822.

Ziegler, A. M., J. M. Parrish, Y. Jiping, E. D. Gyllenhaal, D. B. Rowley, J. T. Parrish, N. Shangyou, A. Bekker & M. L. Hulver. 1993. Early Mesozoic phytogeography and climate. Philos. Trans. Roy. Soc. London, Ser. B 341: 297-305.

PETER DEL TREDICI

Arnold Arboretum of Harvard University

Boston, MA 02130, U.S.A.
Table I
Germination percentages of Ginkgo biloba seed from Guizhou Province,
China compared to those from Boston, Massachusetts, United States.
All seeds were cultivated either indoors in the greenhouse or
outdoors in the nurseries of the Arnold Arboretum in Boston. Seed
coats were removed from all seeds except for one treatment of the
Boston seed where the seed coat was left intact. Each treatment
consisted of four replicates of 50 seeds.

 Percent germination

Seed treatment Guizhou seed Boston seed

Seed coat removed
 Sown indoors 51.5 (b) 68.0 (a)
 Sown outdoors 73.5 (a) 71.5 (a),(A)
Seed coat intact
 Sown outdoors -- 15.0 (B)

Different lowercase and uppercase letters following means indicate
significant differences at P < 0.05 or P < 0.0001, respectively,
using Tukey's HSD test.

Table II
A comparison of the phenology of the sexual reproduction cycle
of Ginkgo biloba growing in Guizhou Province, China, versus
Massachusetts, United States.

 Germination
Location Pollination Seed abscission (outdoors)

Guizhou, China mid-March to mid-September mid-March
 (25[degrees] early April
 North latitude)

Massachusetts, USA mid-May late October to mid- to
 (42[degrees] early November late June
 North latitude)
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