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(American Journal of Botany. 2003;90:1-7.)
© 2003 Botanical Society of America, Inc.

Paleobotany

Eucommia (Eucommiaceae), a potential biothermometer for the reconstruction of paleoenvironments1

Yu-Fei Wang2,3, Cheng-Sen Li2,3,5, Margaret E. Collinson4, Jian Lin2 and Qi-Gao Sun2

2Department of Paleobotany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China; 3State Key Laboratory of Loess and Quaternary Geology, Institute of Earth Environment, Chinese Academy of Sciences, Xi'an 710075, China; 4Department of Geology, Royal Holloway University of London, Egham, Surrey TW20 0EX, UK

Received for publication May 7, 2002. Accepted for publication August 13, 2002.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The living trees of Eucommia ulmoides, an endemic species in China, grow from 200 to 1700 m above sea level, within the geographic range from 102° E to 118° E and from 25° N to 35° N. Spring temperatures in these regions vary from 12.3°C to 20.1°C. A physiological study (using germination tests) of E. ulmoides has been undertaken to test the role of spring temperature as a factor controlling the distribution of Eucommia. Results show that the spring temperature is a limiting factor for Eucommia seed germination and hence for the distribution pattern of the genus. The suitable range of temperature for seed germination, established experimentally, is from 13°C to 22°C, with an optimum of 18°C. Specimens of fossil Eucommia cf. ulmoides, preserved as a branch segment and leaves, showing the distinctive latex, were found in Middle Miocene sediments of Shanwang Formation, Shandong Province, East China. If the climatic tolerances documented here for E. ulmoides are extrapolated to Shanwang, they are in fact consistent with other predictions of the paleoclimate at this site, indicative of the potential value of Eucommia as a biothermometer. These Miocene fossils, and one previously described Eocene fruit specimen, prove the former existence of Eucommia in China in addition to North America and Europe. This confirms that the genus is not a recent arrival in China and extends our understanding of the past biogeography of the genus.

Key Words: biogeography • China • East Asia • Eucommia • Eucommiaceae • Miocene • paleoenvironments


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
In order to understand global climate change today, we need to understand the pattern and process of climate change in the past. The evolution of plants was strongly influenced by, and therefore reflects, environmental changes in the geological past. Plants have to tolerate the full climate range in their habitat and are rightly regarded as good biothermometers for the environment. Studies of fossil plants, and their closest relatives involving their systematic status, biogeography, ecology, and physiology may provide a valuable key to reconstruct past terrestrial environments.

Eucommia ulmoides Oliv. is the single extant species of the genus Eucommia (Eucommiaceae) (Cronquist, 1981 ). The living trees of E. ulmoides occur only in the hilly area of South China (Fig. 1; Ying, Zhang, and Boufford, 1993 ). The unicellular latex ducts and the structure of the samaras are unique features of Eucommia (Tippo, 1940 ; Tian and Hu, 1983 ) and have been used, as a distinctive combination of features, in tracing the history of Eucommia in the Northern Hemisphere (Call and Dilcher, 1997 ).



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  		Fig. 1. The fossil locality of Eucommia cf. ulmoides (triangle) and the distribution of E. ulmoides (circles)

 
The earliest macrofossils that can unequivocally be placed in genus Eucommia are fruits found in Eocene sediments of Hokkaido, Japan (Huzioka, 1961 ); Fushun, Northeast China (Geng, Manchester, and Lu, 1999 ); and the western and southeastern United States (Call and Dilcher, 1997 ; Manchester, 1999 ). Eucommia macrofossils also occur in western European floras from Oligocene to Upper Pliocene (Mai, 1995 ; Zhilin, 1989 ), in North America from Eocene to Oligocene (Call and Dilcher, 1997 ), and extending into the Miocene of southern Mexico (Magallon-Puebla and Cevallos-Ferriz, 1994 ). Fossil fruits of Eucommiodes orientalis Tao and Zhang (1992) reported from the early Cretaceous of Jilin Province and Eucommia brevirostria Guo (1979) found from the early Eocene of Guangdong Province have been rejected due to their lacking key features of the Eucommia samara, especially the reticulate pattern of veins and latex filaments over the seed and the medial vascular strand separating the fertile and vestigial infertile carpels (Call and Dilcher, 1997 ). Mesozoic pollen of Eucommiidites Erdtman were considered at one time as early representatives of Eucommia but have been more recently proved to be clearly gymnospermous and have been assigned to the new order Erdtmanithecales (Friis and Pederson, 1996 ).

Our aim in this paper is to explore the potential role of Eucommia as a biothermometer in paleoenvironmental reconstruction. The concept of the nearest living relative (NLR) based on recognition of modern genus or even species (Collinson, 1986 ; Mosbrugger, 1999 ) and the climate analysis of endemic species (Li, Wang, and Sun, 2001 ) are adopted and applied in this paper by using the assumption that the fossil species and its NLR species have similar ecological requirements.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Germination experiments
An experiment was conducted to determine seed vigor in E. ulmoides as measured by the number of germinating seeds produced under different temperature conditions. Seed vigor is defined as "that condition of active good health and natural robustness in seeds which, upon planting, permits germination to proceed rapidly and to completion under a wide range of environmental conditions" (Woodstock, 1973 , p. 134 and p. 136). The more vigorous the seed is, the bigger the chance of the seedling surviving; the less vigorous it is, the weaker its seedling (Woodstock, 1973 ; Gu, Xu, and Zheng, 1982 ; Tao and Zheng, 1991 ). Seed vigor is affected by factors from both genetic properties and environments. Germination response along a temperature gradient provided a useful measure of seed vigor (Cole, 1972 ; Woodstock, 1973 ).

Fresh ripe fruits were collected in autumn from Eucommia trees cultivated in Beijing Botanical Garden. Seeds were removed from the fruits in order to avoid imposed dormancy that is otherwise introduced in Eucommia by the fruit wall (Lin, Zheng, and Zhang, 1989 ). Seeds uniform in size and mass, and without mechanical damage, were chosen for the test to ensure that experimental results were not influenced by variations in these factors. The germination experiments were undertaken in the dark. The germination of seeds was established at temperatures of 5°C, 10°C, 13°C, 16°C, 18°C, 20°C, 22°C, and 25°C, respectively, and was controlled by a double direction temperature gradient template. One hundred seeds of each temperature set were divided into four replicates of 25 seeds per dish. Seeds were placed on moist filter paper in petri dishes (9 x 9 cm), which were placed in a seed germinator. A small quantity of distilled water was added regularly to keep the filter paper moist. The number of seeds with radicles was counted every other day for 14 d. After 14 d, the germination percentage, radicle length, and vigor index were recorded. Statistical analysis of all data was conducted using the least significant difference (LSD) test at P = 0.05. The vigor index (V) is expressed by the following equation (Tao and Zheng, 1991 ): V = S x G representing a synthetic value for seed germination and seedling growth, where S = mean of radicle length, showing seedling growth potential and G (germination index) = {Sigma}Gt/Dt, indicating the speed for seed germination where Gt = the number of seeds with radicles at day t and Dt (day t) = the number of days since the beginning of the experiment.

Germination percentage, germination index, and vigor index are used here for evaluating seed vigor. Among them, vigor index is the most important value for evaluating seed vigor because it includes both seed germination and seedling growth data.

Source of meteorological data
Spring temperatures, represented by the mean temperature in April from the region where E. ulmoides grows today, are cited from a climate database of China (National Meterorological Bureau of China, 1983 ).

Fossil material
The twig (Fig. 2) and associated leaves (Fig. 3), one whole leaf and seven other fragments, were all collected from the 22.95 m of diatomaceous shale and mudstone Unit Numbers 6, 7, and 15 as shown in Fig. 2 and Table 1 of Sun et al. (2002) of Shanwang Formation, in Xiejiahe Village (36°54' N, 118°20' E), Linqu County, Shandong Province, China. The Shanwang Formation is dated as mid-Miocene, 15 to 17.5 million years ago (mya), based on the data of its fauna and flora as well as of isotope measurements (Li, 1981 ; Yan, Qiu, and Meng, 1983 ; Liu and Leopold, 1992 ; Yang and Yang, 1994 ; Sun et al., 2002 ). Specimens studied in this paper are housed at the Department of Paleobotany, Institute of Botany, Chinese Academy of Sciences, Beijing, China. Latex ducts exposed in transverse and longitudinal sections of the branch and leaves were examined under scanning electron microscopy (SEM) in Beijing (Figs. 5–7) and a Hitachi S3000N variable pressure scanning electron microscope (Hitachi, Tokyo, Japan) in low vacuum mode, using back scattered detector with specimens in situ on rock, uncoated, at the University of London, London, UK (Figs. 8–10).



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  		 Figs. 2–4. 2. Eucommia cf. ulmoides. A branch segment. Specimen no. PB-SW-95-0001. Scale bar = 1 cm. 3. Eucommia cf. ulmoides. A leaf lamina, showing the leaf architecture with compound teeth (indicated by arrow). Specimen no. PB-SW-98-0015. Scale bar = 1 cm. 4. Eucommia ulmoides. A leaf lamina, for comparison with Fig. 3. Scale bar = 1 cm

 

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  		Table 1. Temperature effect of seed germination in Eucommia ulmoides; within a column the values scored by the same letter are not significantly different (LSD test, P = 0.05). The vigor index (V) = S x G, representing a synthetic value for seed germination and seedling growth, where S = mean of radicle length, showing seedling growth potential, and G (germination index) = {Sigma}Gt/Dt, indicating the speed for seed germination, where Gt = the number of seeds with radicles at day t and Dt (day t) = the number of days since the beginning of the experiment

 


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  		Figs. 5–7. 5. Eucommia cf. ulmoides. Latex cells from Fig. 2 . Specimen no. PB-SW-95-0001. Scale bar = 250 µm. 6. Eucommia cf. ulmoides. Latex cells from specimen no. PB-SW-98-0016. Scale bar = 60 µm. 7. Eucommia ulmoides. Latex cells exposed along a split leaf. Scale bar = 60 µm

 


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  		Figs. 8–10. Eucommia cf. ulmoides. 8. Surface view of specimen no. PB-SW-98-0017, showing fossil leaf remains attached to diatomite and underlying diatomite. Scale bar = 1 mm. 9. Enlargement of Fig. 8 (area indicated by arrow), showing fossil latex strands. Specimen no. PB-SW-98-0017. Scale bar = 50 µm. 10. Enlargement of Fig. 8, showing underlying diatomite (arrows) is visible at top left and a fossil leaf fragment with latex strands exposed in situ between leaf cuticles. Specimen no. PB-SW-98-0017. Scale bar = 50 µm

 

   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Germination test of Eucommia ulmoides seeds
Preliminary studies have considered aspects of seed physiology of Eucommia (Lin and Zheng, 1995 ; Lin, Zheng, and Zhang, 1989 ), and we have extended these studies to constrain the temperature controls on seed germination. Our physiologic experiments show that favorite temperatures for the germination of E. ulmoides seeds, including optimum and suboptimum temperatures, range from 13°C to 22°C (Table 1, Fig. 11). The optimum temperature is 18°C, as the seeds exhibited the highest vigor index (10.37) and germination rate (98%) at that temperature. The V, G, and S (radicle length) showed no significant differences between 13°C and 16°C or between 20°C and 22°C (Table 1). The lower vigor index (lower than 1% of the highest value) at 10°C indicates much weaker seedlings. Over 25°C, germination ceases (Table 1, Fig. 11; Lin and Zheng, 1995 ).



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  		Fig. 11. Temperature effect of seed germination in Eucommia ulmoides. Germination percentage, germination index, and vigor index are used here for evaluating seed vigor. Among them, vigor index is the most important value for evaluating seed vigor because it includes both seed germination and seedling growth data

 
Data of spring temperatures cited from meteorological stations
Trees of E. ulmoides grow naturally in South China ranging from 200 m to 1700 m above sea level, and from 102° E to 118° E and from 25° N to 35° N (Fig. 1; Ying, Zhang, and Boufford, 1993 ). The spring temperatures of the distribution region of E. ulmoides in nature range from 12.3°C to 21.1°C. They vary from 13.8°C to 20.1°C at altitudes from 206 m to 1527 m at latitudes from 25° N to 27°57' N, from 15.4°C to 19.3°C at altitudes from 259 m to 972 m at latitudes from 28° N to 30°40' N, and from 12.3°C to 15°C at altitudes from 396 m to 1131 m at latitudes from 33° N to 35° N (Table 2).


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  		Table 2. Data from Chinese meteorological stations based on 30-yr averages from 1951 to 1980 for spring temperatures (represented by the mean temperature in April) in the area of the recent distribution of Eucommia ulmoides. Data taken from a climate database of China (National Meteorological Bureau of China, 1983)

 
Systematic assignment of fossil material from Shanwang
Description
Branch segment, comprising secondary xylem and bark, is 8 cm long, 1.94 cm wide, and 3 mm thick (Fig. 2). Phloem of bark contains abundant unicellular latex ducts arranged in longitudinal strands (Fig. 5; Wang, 1995 ). Leaves are elliptic, serrate, up to 9.4 cm long and 4.7 cm wide. The widest part of the leaf is in the middle of the lamina. Leaf apex is attenuate. Leaf base is acute. Petioles are 1 mm wide and up to 6 mm long. Compound teeth, composed of both main tooth and secondary tooth, are curved apically so that the tooth apex is appressed to the leaf margin (Fig. 3). Leaf venation is camptodromous (Fig. 12), at least six pairs of alternating secondary veins depart from the midrib at an acute angle and arch strongly toward the apex (Fig. 12). The unicellular latex ducts in leaves (Figs. 6 and 8–10) are the same as those in the branch (Fig. 5), at least 0.2 mm long and 4.0 to 5.6 µm in diameter, with inflated ends.



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  		Fig. 12. Partial reconstruction of leaf architecture of Eucommia cf. ulmoides, showing camptodromous venation, alternating secondary veins, and compound teeth (see Fig. 3 ; specimen nos. PB-SW-98-0015 and PB-SW-98-0016)

 
Discussion
Their occurrences in the same rock unit and identity of their latex cells form the basis for regarding both twig and leaves as a single species. The fossil leaves are very similar to those of E. ulmoides in terms of leaf venation and compound teeth (Figs. 3 and 4). The latex ducts in phloem of stem, branches, and leaves of E. ulmoides range from 0.4 to 3.5 mm long, 3 mm at average, 2.5 to 6 µm in diameter (Tian and Hu, 1983 ). The unicellular latex ducts of fossil branches (Fig. 5) and leaves (Figs. 6 and 8–10) are very similar to those of E. ulmoides (Fig. 7) in dimension and structure. Based on the similarities of fossil specimens to E. ulmoides, we assigned these specimens to E. cf. ulmoides.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Habitat of modern Eucommia
Living floras containing Eucommia in South China are mostly subtropical; for example, the flora in the Wuling Mountains (108°47' E–111°33' E; 27°05' N–30°09' N) consists of 164 families of angiosperms, nine families of gymnosperms, and 44 families of pteridophytes (Wang et al., 1995 ). Trees of E. ulmoides in that flora occur together with Rhus chinensis Mill, Liquidambar mollis Oliv., Quercus acutissima Carr., and Q. variabilis Bl. (Zhang, Gao, and Chen, 1990 ). Close fossil relatives of the latter four species were also found in the Shanwang flora (WGCPC, 1978 ).

Occurrence of fossil Eucommia and related paleoenvironments
The discovery of fossil Eucommia in the Tertiary sediments of China (Wang, 1995 ; Geng, Manchester, and Lu, 1999 ) proves the former existence of Eucommia in China in addition to North America and Europe. This confirms that the genus is not a recent arrival in China and refutes previous suggestions that the genus migrated to China from North America via Europe during the Tertiary (Szafer, 1952 ).

Wang (1995) briefly reported Eucommia cf. ulmoides as a new occurrence in the Shanwang Flora. The specimens, a piece of branch and leaves collected from Shanwang Formation of Middle Miocene in Shandong Province, China, are here shown to be much closer to the extant species E. ulmoides than to any other fossil Eucommia species and are therefore assigned to Eucommia cf. ulmoides.

The Shanwang flora is Miocene in age and composed largely of angiosperms, including 43 families, 87 genera, and 125 species (Hu and Chaney, 1940 ; WGCPC, 1978 ). These families of angiosperms are mainly typical temperate trees, such as those in Betulaceae, Aceraceae, Ulmaceae, Fagaceae, Salicaceae, Tiliaceae, Juglandaceae, Rhamnaceae, and some subtropical evergreen trees, i.e., Cinnamomum (Lauraceae), Magnolia (Magnoliaceae), Ficus (Moraceae), and Eriobotrya (Rosaceae) (Hu and Chaney, 1940 ; WGCPC, 1978 ). The paleoclimate inferred from this Shanwang flora and its associated fauna is warm temperate to subtropical (Hu and Chaney, 1940 ; WGCPC, 1978 ; Yan, Qiu, and Meng, 1983 ; Zhang, 1986 ; Liu and Leopold, 1992 ; Yang and Yang, 1994; Sun et al., 2002 ).

Estimate of spring temperatures for natural regeneration of Eucommia
Seeds of E. ulmoides mature in the autumn and then germinate in the following spring. Therefore, a suitable temperature for seed germination in the spring is an important factor in the life cycle of E. ulmoides. The range of spring temperatures in the area or distribution region of this species is consistent with the results of the temperature test for seed germination of E. ulmoides, although experimental data yield slightly higher temperatures than meteorological data. The overlapping temperature range (from 13°C to 20°C) between experimental data and meteorological data represents the natural germination conditions of living Eucommia. Natural regeneration, from germinating seeds, is of fundamental importance for the maintenance of natural plant populations, especially in trees like Eucommia where vegetative reproduction is lacking or very limited. Our results, combining evidence from experimental studies of seed vigor and the climatic conditions under which modern Eucommia grows today, show that spring temperature is an important factor controlling Eucommia distribution. We do not exclude the possibility that other factors may also be relevant but these would require further research.

Considering the concept of NLR (Collinson, 1986 ; Mosbrugger, 1999 ) and the climate analysis of endemic species (Li, Wang, and Sun, 2001 ), the temperature requirement for seed germination of fossil E. cf. ulmoides is inferred to have been close to that of its nearest living relative species. The spring temperatures of the Shanwang locality in the Middle Miocene are therefore estimated to be from 13°C to 20°C, ranging from 0.1°C to 7°C higher than present 12.9°C in spring, which is cited from Weifang meteorological station [36°45' N, 119°11' E] near Shanwang [36°54' N, 118°20' E]. This is consistent with other research work depicting the climate of Middle Miocene in Shanwang locality as warm temperate to subtropical (see above). The global warming in the Middle Miocene (Tanai, 1967 ; Wolfe, 1978 ; Graham, 1999 ), together with the paleolatitude of Shanwang being at 27°30' N (Ye and Yuan, 1980 ), or between 28.3° N and 32.4° N (Liu and Shi, 1989 ) as indicated by paleomagnetic data, might be responsible for the higher spring temperature of Shanwang in the Middle Miocene than the present day.

Paleoclimatic and paleobiogeographic significance
Combined evidence from the natural distribution and germination experiments has shown that spring temperatures of 13°C to 20°C are a limiting factor on the distribution of Eucommia ulmoides (Eucommiaceae). If this climatic tolerance is extrapolated to the Middle Miocene of Shanwang (with fossil E. cf. ulmoides) it proves to be consistent with other predictions of palaeoclimate at this site. This new evidence for climatic tolerances of Eucommia can in future be incorporated into palaeoclimate analysis of other fossil assemblages containing this genus. The Miocene fossils, and one previously described Eocene fruit specimen, prove the former existence of Eucommia in China in addition to North America and Europe. This confirms that the endemic genus Eucommia is not a recent arrival in China and focuses attention on the significance of Chinese fossils for understanding the evolution and biogeography of the genus.


   FOOTNOTES
 
1 The authors thank Professors W. G. Chaloner, E. M. Friis, and F. M. Hueber for their valuable comments and revisions on the manuscript. Thanks are due to Professor E. Zastawniak, Drs. J. J. Wójcicki, and A. A. Bruch for their checking the citation of Polish and German references. This work is supported by the projects of the Natural Science Foundation of China (30070046 and 30070056), the Chinese Academy of Sciences (KZ951-B1-105, STZ-00-30, and SKLLQG0221) and the Royal Society in Great Britain/Chinese Academy of Sciences (RS/CAS) joint project. Back

5 Author for reprint requests (lics{at}95777.com ) Back


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
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J. Yang, Y.-F. Wang, R. A. Spicer, V. Mosbrugger, C.-S. Li, and Q.-G. Sun
Climatic reconstruction at the Miocene Shanwang basin, China, using leaf margin analysis, CLAMP, coexistence approach, and overlapping distribution analysis
Am. J. Botany, April 1, 2007; 94(4): 599 - 608.
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