PALAEO-06740; No of Pages 10
Palaeogeography, Palaeoclimatology, Palaeoecology xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Palaeogeography, Palaeoclimatology, Palaeoecology
journal homepage: www.elsevier.com/locate/palaeo
Paleobiogeography of the lotus plant (Nelumbonaceae: Nelumbo) and its
bearing on the paleoclimatic changes
Ya Li a,e, Thierry Smith b, Popova Svetlana c, Jian Yang a, Jian-Hua Jin d, Cheng-Sen Li a,⁎
a
State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Xiangshan, Beijing 100093, China
Directorate Earth and History of Life, Royal Belgian Institute of Natural Sciences, 29 Rue Vautier, B-1000 Brussels, Belgium
Laboratory of Palaeobotany, Komarov Botanical Institute, Russian Academy of Sciences, Saint Petersburg 197376, Russia
d
School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China
e
University of Chinese Academy of Sciences, Beijing 100049, China
b
c
a r t i c l e
i n f o
Article history:
Received 19 October 2013
Received in revised form 25 January 2014
Accepted 26 January 2014
Available online xxxx
Keywords:
Paleobiogeography
Paleoclimatic change
Lotus
Nelumbo
Nelumbonaceae
a b s t r a c t
The historical reconstruction of the origin and dispersal of plant taxa in space and time facilitates a better understanding of their modern distribution patterns. However, most studies of paleobiogeography have focused on terrestrial plants, and the distribution changes of aquatic plants are less well understood. Here we study the lotus
plant Nelumbo (Nelumbonaceae), an aquatic perennial herb, with a disjunctive distribution across East, South
and Southeast Asia-North Australia and North America. The reproductive organs of Nelumbo changchangensis
He et Jin from the Eocene of Hainan, China are supplementarily described. Analysis of the spatial and temporal
distributions of Nelumbo in the geologic past indicates that the genus first occurs in mid-latitude area of Laurasia
in the Early Cretaceous, then becomes widespread in North America and Eurasia and expands into South America
during the Late Cretaceous, and reaches its maximum northern limit during the Eocene. The genus persists and
thrives in North America and Eurasia until the Pliocene. The Pleistocene ice age causes the extinction of Nelumbo
in Europe and central Asia, and its populations in North American and Asia are also restricted to refuges of lower
latitude. Like the terrestrial plants Metasequoia (Cupressaceae) and Nordenskioeldia (Trochodendraceae), the
fluctuations of Nelumbo distribution ranges are also linked to climatic changes in the Cenozoic. The cooling
climate and increasing seasonality in the Eocene of East Asia may favor the origin of tubers and the differentiating
of the ecotypes in lotus, which allow the deciduous type to survive in cold winters.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction
Aquatic plants constitute a common component of wetlands. Therefore their fossils carry some paleoenvironmental signals. The lotus plant
(Nelumbonaceae: Nelumbo) is one of the aquatic perennial herbs, which
is often cultivated for horticulture, food or religion purpose (WBGCAS,
Wuhan Botanical Garden, Chinese Academy of Sciences, 1987;
Wiersema, 1997; Fu and Wiersema, 2001; Stanley, 2007). This plant
also attracts the attention of paleontologists, because of its fossil record
of characteristic peltate leaves, which allows us to review its distribution in space and time. Paleobiogeographic studies have mainly focused
on terrestrial plants, such as conifers, namely, Glyptostrobus Endl., Larix
Mill., Metasequoia Hu et W.C. Cheng, Pseudolarix Gordon and Tsuga
Carrière (LePage and Basinger, 1991, 1995; LePage, 2003; LePage et al.,
2005; LePage, 2007) and angiosperms like Berberis L., Comptonia
L'Hér., Nordenskioeldia Heer, Prunus L. and Weigela Thunb. (Wang
et al., 2009; Li et al., 2010, 2011; Liang et al., 2010, 2013), but have
paid little attention to aquatic plants. Besides, Nelumbo fossils are clearly
indicators of non-marine aquatic environments, such as rivers, lakes
⁎ Corresponding author. Tel.: +86 10 62836436.
E-mail address: [email protected] (C.-S. Li).
and ponds. Understanding the paleobiogeographic history of Nelumbo
is important in this context.
Nelumbo Adans., of which Nelumbium Juss. is a junior synonym,
is the sole extant genus of the family Nelumbonaceae, placed in the
Proteales, an order of the basal eudicots (APG III, 2009). Nelumbo consists of two extremely similar species: Nelumbo nucifera Gaertn. (sacred
lotus) and Nelumbo lutea Willd. (American lotus). The former with pink
or white tepals is distributed in East, South and Southeast Asia and
North Australia, whereas the latter with pale yellow tepals is distributed
in Central and North America (WBGCAS, Wuhan Botanical Garden,
Chinese Academy of Sciences, 1987; Wiersema, 1997; Fu and
Wiersema, 2001; Stanley, 2007). Based on literature reports and
herbarium specimens from all over the present day range of Nelumbo,
Borsch and Barthlott (1994) speculated that through human activity,
N. nucifera was introduced to tropical areas of South American, South
and Southeast Asia and Australia (Fig. 1).
Some fossil leaves similar to Nelumbo are placed into Nelumbites
Berry and Nelumbago McIver et Basinger. The genus Nelumbites was initially proposed by Berry (1911) for the leaves from the Early Cretaceous
of the Atlantic Coastal Plain. Later, Knowlton (1930) considered that
Nelumbites is more similar to Nymphaea L. rather than Nelumbo.
Nelumbago was erected by McIver and Basinger (1993) for the Paleocene
0031-0182/$ – see front matter © 2014 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.palaeo.2014.01.022
Please cite this article as: Li, Y., et al., Paleobiogeography of the lotus plant (Nelumbonaceae: Nelumbo) and its bearing on the paleoclimatic
changes, Palaeogeogr. Palaeoclimatol. Palaeoecol. (2014), http://dx.doi.org/10.1016/j.palaeo.2014.01.022
2
Y. Li et al. / Palaeogeography, Palaeoclimatology, Palaeoecology xxx (2014) xxx–xxx
Fig. 1. The present disjunctive distribution of Nelumbo.
Modified from Borsch and Barthlott, 1994.
leaves from the Ravenscrag Formation of Saskatchewan, Canada. The
leaves of Nelumbago have orthogonal reticulate or more random tertiary
veins and commonly 4-sided areoles (McIver and Basinger, 1993), while
those of Nelumbo have regular and opposite percurrent tertiary veins
and commonly 6-sided areoles.
The earliest geological record of Nelumbo is the fossil leaves of
N. lusitanica Saporta and N. choffati Saporta from the Albian of Portugal
(Saporta, 1894; Teixeira, 1945). Although their taxonomic position is
still unconfirmed (Berry, 1917; Snigirevskaya, 1964), or often doubted
(Knowlton, 1930; Gandolfo and Cúneo, 2005), these peltate leaves
indeed show similar venation patterns to those of Nelumbo. Another
fossil leaf of N. weymouthi Brown is reported from the Aspen Shale of
southwestern Wyoming, USA (Brown, 1933), dated as Albian (Crabtree,
1987). Abundant fossil leaves of Late Cretaceous age and younger have
been reported from Europe, Asia, Africa, North America and South
America (Heer, 1862; Lesquereux, 1878; Heer, 1882; Dawson, 1885;
Saporta, 1890, 1891; Hollick, 1894; Knowlton, 1900; Berry, 1903;
Hollick, 1904, 1906; Couyat and Fritel, 1910; Tuzson, 1914; Knowlton,
1916; Berry, 1917; Knowlton, 1930; Miki, 1933; Endo, 1934; Hollick,
1936; Pimenova, 1937; Dotzler, 1938; Yabe, 1944; Bell, 1949; Puri,
1950; Matsuo, 1954; Lakhanpal, 1955; Tanai, 1961; Vasilev, 1961;
Brown, 1962; Snigirevskaya, 1964; Becker, 1969; Huzioka and
Takahashi, 1970; Tanai, 1970; Snigirevskaya, 1974; Zhilin and
Snigirevskaya, 1974; Hickey, 1977; WGCPC, Writing Group of
Cenozoic Plants of China, 1978; Guo, 1979; Bhattacharyya, 1983;
Erickson, 1991; Wing et al., 1995; Budantsev, 1997; He and Tao,
1997; Tao, 2000; Johnson, 2002; Li and Chen, 2002; Gandolfo and
Cúneo, 2005; He et al., 2010; Gabrielyan et al., 2012). About 28 fossil
species have been established to accommodate these fossil leaves.
However, N. schweinfurthi Fritel from the Late Cretaceous of Egypt
(Couyat and Fritel, 1910) is still unconfirmed, due to lack of systematic description and specimen photographs (Snigirevskaya,
1964). Kuprianova and Tarasevich (1983) summarized the fossil
pollen record of Nelumbo. Receptacles and fruits have been reported
from the Late Cretaceous to the Pleistocene of Eurasia, North America
and South America (Saporta, 1891; Fritel, 1908; McGinitie, 1941;
Weyland and Pelug, 1961; van der Burgh, 1978, 1983; Zhang and Liu,
1999; Gandolfo and Cúneo, 2005; He et al., 2010).
He et al. (2010) made a comprehensive report of Nelumbo from the
Eocene Changchang Formation including rhizomes, tubers, leaves, fruit
receptacles and fruits and erected a new species: N. changchangensis
He et Jin. Based on new well-preserved collected specimens, we can
here complete the description of the reproductive organs (tubers,
receptacles and fruits) of this species. Our research also discusses the differentiation of the ecotypes of the genus in the context of paleoclimate
changes.
2. Materials and methods
2.1. Fossil materials of Nelumbo changchangensis He et Jin and their
geological context
Specimens of Nelumbo changchangensis described here were collected from the upper Member of Changchang Formation, Changchang
Basin (19°37′56″N, 110°26′43″E), Hainan Province, China during
March 2009. Based on lithologic properties, the Changchang Formation
is subdivided into two members: a lower member of varicolored lacustrine sediments and an upper member of dark lake-swamp coal-bearing
series (Zhou and Chen, 1988; Lei et al., 1992). According to the characteristics of the sporopollen assemblages, the lower member is dated as
early Early Eocene and the upper one as late Early Eocene to early
Late Eocene (Lei et al., 1992). Palynological studies indicate that the
Changchang flora represents a subtropical evergreen or deciduous forest, close to mountains of mid-high altitude (Lei et al., 1992; Yao et al.,
2009). All specimens including 16 tubers, 20 receptacles and 30 fruits
Please cite this article as: Li, Y., et al., Paleobiogeography of the lotus plant (Nelumbonaceae: Nelumbo) and its bearing on the paleoclimatic
changes, Palaeogeogr. Palaeoclimatol. Palaeoecol. (2014), http://dx.doi.org/10.1016/j.palaeo.2014.01.022
Y. Li et al. / Palaeogeography, Palaeoclimatology, Palaeoecology xxx (2014) xxx–xxx
are kept in the Museum of Palaeobotany, Institute of Botany, Chinese
Academy of Sciences, Beijing, China.
3
(ca. 30 Ma), and Miocene (ca. 20 Ma) from Scotese (1997), Smith
et al. (2004) and LePage et al. (2005), and Pliocene (ca. 5 Ma) and
Pleistocene (ca. 1 Ma) from ArcView GIS 3.2 software.
2.2. Methods for reconstructing paleophytogeography of Nelumbo
3. Results
In total, data from 104 localities where Nelumbo was present were
collected. In 88 localities, sediments containing the fossils were dated
to epoch (see Appendix A, Table S1), and in the other 16 localities, they
could not be assigned to accurate epochs (see Appendix A, Table S2).
We plotted all localities with ArcView GIS 3.2 software, but used the 88
localities to study the phytogeographical changes of Nelumbo through
time at epoch resolution.
The paleocoordinates were converted from the present day coordinates of the fossil sites using PointTracker v4c software (Scotese,
2001). Sites were plotted on eight Lambert Equal-Area Azimuthal
(North Pole) projections using ArcView GIS 3.2 software, covering the
following time intervals: Early Cretaceous (ca. 100 Ma), Late Cretaceous
(ca. 80 Ma), Paleocene (ca. 60 Ma), Eocene (ca. 50 Ma), Oligocene
3.1. Systematics
Order: Proteales
Family: Nelumbonaceae
Genus: Nelumbo Adanson
Species: Nelumbo changchangensis He et Jin
3.2. Supplementary description
The tubers are elliptical, rectangular or ovate, 4.5–13.0 cm long,
2.2–5.1 cm wide (Plate I, 1–3). The surface is smooth, rough or with
longitudinal winkles. The nodes of tubers bear five to six clusters of
Plate I. The asexual propagation organ (tubers) of Nelumbo.
1–3
4
5
6
Tubers from the Eocene of Hainan Island, China. Specimen Nos. PEPB70532, 70477, and 70531. Scale bars = 5 cm in Plate I, 1, 3; 2 cm in Plate I, 2.
Transverse section of the cuticle of tuber. PEPB70531. Scale bar = 10 μm.
Tuber from the Eocene of Kamchatka, Russia. Specimen No. 2241A/960-23. Scale bar = 2 cm.
Extant tuber of Nelumbo nucifera from Jiangsu Province, China. Scale bar = 4 cm.
Please cite this article as: Li, Y., et al., Paleobiogeography of the lotus plant (Nelumbonaceae: Nelumbo) and its bearing on the paleoclimatic
changes, Palaeogeogr. Palaeoclimatol. Palaeoecol. (2014), http://dx.doi.org/10.1016/j.palaeo.2014.01.022
4
Y. Li et al. / Palaeogeography, Palaeoclimatology, Palaeoecology xxx (2014) xxx–xxx
Plate II. The reproductive organs (receptacles and fruits) of Nelumbo changchangensis He et Jin from the Eocene of Hainan Island, China.
1
2
3
4
5
6
7
8
9
A basally compressed receptacle. PEPB70538. Scale bar = 2 cm.
Enlarged basal part of 1, showing stamen and sepal scars (arrows). Scale bar = 5 mm. sta: stamen; tep: tepal.
A laterally compressed receptacle (left) and a small immature receptacle (right). PEPB70536a, b. Scale bar = 2 cm.
Top view of a fruit with stigma impression (arrow) in the center. PEPB70553. Scale bar = 5 mm. sti: stigma.
Lateral view of a fruit with the apical stigma (arrow) and the subapical respiratory pore (arrow). sti: stigma; rp: respiratory pore. PEPB70554. Scale bar = 5 mm.
SEM of fossil receptacle showing undulated cell walls. Scale bar = 40 μm.
Enlargement of 6 showing pitted cell surfaces. Scale bar = 20 μm.
SEM of fossil receptacle showing straight to rounded cell walls. Scale bar = 40 μm.
Enlargement of 8 showing the cell surfaces ornamented with hairs. Scale bar = 20 μm.
Please cite this article as: Li, Y., et al., Paleobiogeography of the lotus plant (Nelumbonaceae: Nelumbo) and its bearing on the paleoclimatic
changes, Palaeogeogr. Palaeoclimatol. Palaeoecol. (2014), http://dx.doi.org/10.1016/j.palaeo.2014.01.022
Y. Li et al. / Palaeogeography, Palaeoclimatology, Palaeoecology xxx (2014) xxx–xxx
5
Table 1
Morphological comparison of receptacles and fruits with fossil and extant species of Nelumbo.
Nelumbo-like receptacles
N. changchangensis
N. lacunosa
N. protospeciosa
N. megalopolitana
N. minima
N. nucifera
Shape
Height (cm)
Diameter (cm)
Fruit number
Fruit size (mm)
Locality
Obconical
2.5
1.1–1.5
5–14
No data
Patagonia, Argentina
Obconical
3.8–4.0
4.4–10.0
20–26
10.0–17.5 × 6.5–10.0
Hainan, China
No data
No data
3
ca. 35
No data
California, USA
Late Cretaceous
Gandolfo and
Cúneo (2005)
Eocene
This article
Eocene
McGinitie (1941)
No data
No data
1.7–2.0
No data
No data × 1.0
Peloponnese,
Greece
Pliocene
Weyland and
Pelug (1961)
No data
No data
0.45
22
1.5 × 1.0
Limburg,
Netherland
Pliocene
Reid and
Reid (1915)
Obconical
3.8–4.5
7.5–9.6
13–25
18 × 10
Jiangsu, China
Age
Reference
Obconical
2.3
1.8
No data
No data
Provence-AlpesCôte d'Azur, France
Miocene
Saporta (1891)
roots around each node (Plate I, 1–3). The cuticles of the tubers are
589–933 nm thick (Plate I, 4). Under the cuticle layer is a coalified
layer, which has no cellular structure, 19–40 μm thick (Plate I, 4). Receptacles are mostly basally compressed and occasionally laterally compressed (Plate II, 1, 3). They are obconical in shape, 4.4–10.0 cm in
diameter. The surface of the receptacle is usually winkled and striate
and bears elliptical protuberances (Plate II, 1, 3). The receptacle is estimated to have 200 stamens marked by stamen scars at the basal part
(Plate II, 2). Fruits are apically or laterally preserved (Plate II, 4, 5).
They are elliptical or elongate ovoid in lateral view (Plate II, 5),
10.0–17.5 mm long and 6.5–10.0 mm wide. At the apex of the fruits,
there are two characteristic structures: a small capitate persistent stigma on the top of the fruit and a small, ovate protuberance called a respiratory pore (Cronquist, 1981; Takhtajan, 1997), presenting subapically
on the fruit (Plate II, 4, 5). The respiratory pore executes air exchange
between the seed and outer environment during seed development
(Tang, 1988). SEM study on the epidermis of the receptacles also reveals
cellular structures. These cells are 4- to 6-sided, 21–47 μm (average
32 μm) long and 8–37 μm (average 19 μm) wide, and anticlinal cell
walls are undulate, straight or rounded (Plate II, 6–9). Cell surfaces are
pitted (Plate II, 7) or ornamented with hairs (Plate II, 9).
3.3. Comparisons with fossil and extant species of Nelumbo
The earliest Nelumbo-like receptacles with casts of nuts have been
reported from the Late Cretaceous (Campanian–Maastrichtian) of Patagonia, Argentina (Gandolfo and Cúneo, 2005). Three species of Nelumbo
from the Cenozoic, namely, N. lacunosa Macginitie, N. megalopolitana
Weyland et Pflug and N. minima Reid et Reid were erected on the
basis of receptacles and fruits (Reid and Reid, 1915; McGinitie, 1941;
Weyland and Pelug, 1961). The receptacle impression of N. lacunosa
from the Eocene of California, USA is ovoid in outline, 3 cm in maximum
diameter, and has about 30 depressions arranged in irregular concentric
rows (McGinitie, 1941). The receptacle impression of N. megalopolitana
from the Pliocene of Greece is 1.7–1.2 cm in diameter, with rounded
fruits of 1–2 mm in diameter (Weyland and Pelug, 1961). Nelumbo
minima is described from the Pliocene of Netherland, and has small
receptacles, about 0.45 cm in diameter (Reid and Reid, 1915). The identity of such small receptacles in N. minima was doubted and thought to
be mycothallus (fruit bodies of mushrooms) (Kirchheimer, 1941).
The receptacles of N. changchangensis from Hainan, China are not
comparable to those of the above fossil species. The Chinese fossil
receptacles are 4.4–10.0 cm in diameter with fruits 10.0–17.5 mm
long and 6.5–10.0 mm wide, and thus consistent with those of extant
N. nucifera (Table 1).
3.4. The paleophytogeography and the migration of Nelumbo in geological
times
Nelumbo first appears in the Early Cretaceous (Albian Stage, 112.0 to
99.6 Ma ago) of Portugal and Wyoming, USA (Saporta, 1894; Brown,
1933; Teixeira, 1945; Crabtree, 1987) (Figs. 2, 3A). During the Late
Extant
Personal
investigation
Cretaceous, Nelumbo spreads widely in Eurasia, North America and
South America, reaching southward to Patagonia, Argentina and northward to the lower Atane beds of Greenland (Heer, 1882; Gandolfo and
Cúneo, 2005) (Figs. 2, 3B). However, there are no records of Nelumbo
in South America after the Late Cretaceous. The spatio-temporal distribution of Nelumbo indicates that the genus apparently arises in the
Albian of Laurasia, and then becomes widespread in North America
and Eurasia and expands into South America in the Late Cretaceous.
By using penalized likelihood (PL) and nonparametric rate smoothing
(NPRS) respectively, it has been suggested that the stem lineage of
Nelumbonaceae appears 115 or 121 million years (Ma) ago, and the
crown lineage appears 3 or 108 Ma ago (Anderson et al., 2005). By
using Bayesian relaxed clocks, based on nuclear genes 18S rDNA and
26S rDNA, chloroplast genes atpB and rbcL as well as combined gene
data, it has been estimated that Nelumbonaceae diverged from its sister
lineage (Platanaceae) 113.13, 109.38 or 110.35 Ma ago, and the two extant species diverged 3.77, 4.34 or 5.85 Ma ago (Tian, 2008). Recently,
the complete chloroplast genome reveals that the estimated divergent
times are 109 Ma between Nelumbonaceae and Platanaceae and 1.5
Ma between the two extant species of Nelumbo (Xue et al., 2012).
Both fossil records and molecular phylogenic studies suggest an Early
Cretaceous origin of the genus.
Nelumbo remains have been reported from several localities of North
America in the Paleocene (Figs. 2, 3C), and occur in Europe, Asia and
North America, reaching northward to Kamchatka Peninsula (63.9°N,
about the southern part of the Bering Land Bridge), Russia (Budantsev,
1997) and southward to Garo Hills, Meghalaya, India (Bhattacharyya,
1983) in the Eocene (Figs. 2, 3D). So the migration of lotus between
East Asia and North America via the Bering Land Bridge seems possible.
In addition, the North Atlantic land bridge connected Europe and eastern North America in the latest Paleocene or earliest Eocene (Tiffney,
1985), allowing another route for exchange. Fossil records also confirm
the migration or exchange of Nelumbo throughout the Northern Hemisphere during the Eocene. Nelumbo protospeciosa Saporta from the
Eocene of Russia and China (Saporta, 1891; Zhilin and Snigirevskaya,
1974; Budantsev, 1997; Li and Chen, 2002) is similar to coeval North
American species, N. protolutea Berry, in leaf morphology (Berry, 1917).
Collision between the Indian and Asian Plates is initiated around the 52
Ma (Najman et al., 2010; van Hinsbergen et al., 2012), but terrestrial biotic
exchanges between India and Asia have already started by the end of the
Early Eocene (Clyde et al., 2003; Missiaen and Gingerich, 2012). Nelumbo
probably colonizes the Indian Subcontinent from Asia at that time
(Borsch and Barthlott, 1994). Nelumbo is living in several places within
Eurasia in the Oligocene (Figs. 2, 3E), and occurs widely in Eurasia and
North America in the Miocene (Figs. 2, 3F). Nelumbo still survives in
Europe in the Pliocene (Figs. 2, 3G). The genus disappears in Europe
and central Asia during the Pleistocene (Berry, 1917; Snigirevskaya,
1964) and its populations in North American and Asia are also restricted
to refuges of lower latitude (Snigirevskaya, 1964), with several occurrences in Japan, China and India (Figs. 2, 3H). Today, Nelumbo exhibits
a disjunctive distribution across East, South and Southeast Asia-North
Australia and North America (WBGCAS, Wuhan Botanical Garden,
Please cite this article as: Li, Y., et al., Paleobiogeography of the lotus plant (Nelumbonaceae: Nelumbo) and its bearing on the paleoclimatic
changes, Palaeogeogr. Palaeoclimatol. Palaeoecol. (2014), http://dx.doi.org/10.1016/j.palaeo.2014.01.022
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Y. Li et al. / Palaeogeography, Palaeoclimatology, Palaeoecology xxx (2014) xxx–xxx
Fig. 2. The distribution of fossil records of Nelumbo on modern world map.
Chinese Academy of Sciences, 1987; Wiersema, 1997; Fu and
Wiersema, 2001; Stanley, 2007), a distribution that is probably formed
after the Pleistocene.
4. Discussion
4.1. The origin of lotus tubers
The lotus plant has two ecological types: a hardy form that grows in
temperate and subtropical areas, and goes dormant in autumn after the
distal parts of rhizomes enlarge to become tubers, and a tropical form
that keeps growing all year round and does not develop tubers (Zhang
and Wang, 2006; Huang, 2009; Yang et al., 2013). The tubers, acting
as dormant organs and for asexual reproduction, perform a key
survival function for plants under unfavorable conditions (Masuda
et al., 2006). Short day length rather than low temperature is the main
environmental factor leading to the induction of dormancy in hardy
lotus plants (Masuda et al., 2006), and the critical photoperiod for
rhizome transition to storage organ is between 12 and 13 h (Masuda
et al., 2007). Tubers, receptacles and scattered fruits of Nelumbo preserved together in the Eocene of Hainan suggested that the hardy
lotus appeared as early as 56.0–33.9 Ma. Another fossil locality yielding
lotus tuber (Plate I, 5) and leaves is the Late Eocene of Kamchatka, East
Russia (Budantsev, 1997).
The origin of lotus tubers in the Eocene of East Asia is probably related to the cooling climate and increasing seasonality. Global climate was
warm during the Late Cretaceous and Early Paleogene (see the Earth's
climate Chart at http://www.scotese.com/climate.htm), with the
extreme case being the Early Eocene Climatic Optimum (EECO), 53–51
Ma ago (Zachos et al., 2001). There is also evidence of cooler episode
in the Early Eocene (Wing et al., 2000). Progressive global cooling during the Late Paleogene (Zachos et al., 2001) causes a climatic deterioration and an increase in seasonality occurred during the Late Eocene
(Collinson et al., 1981; Keller, 1983) and the Eocene–Oligocene boundary (Buchardt, 1978; Wolfe, 1978), and extends into the Oligocene
(Keller, 1983). More recent quantitative data shows that seasonality is
apparently present in the Eocene of East Asia (Quan et al., 2012a,b). A
comparison with the Paleogene climate of Central Europe shows that
an obvious cooler climate is present in the Early–Middle Eocene of
East Asia (Zhang, 2012). Global cooling starting in the Early Eocene
may have favored the evolution of the deciduous form of lotus. The
palynological assemblage indicates that the mean temperature of the
coldest month in the Eocene of Changchang Formation, Hainan, China
was 1.7–11.9 °C (Yao et al., 2009), which is below 13 °C, namely the
hardy lotus dormant temperature (Zhang and Wang, 2006). This
explains why fossil tubers are present in the Changchang flora. The
development of tubers, which only occurs in the deciduous form, allows
hardy lotus to survive in cold winters.
4.2. Relationships of lotus phytogeography to the past climatic changes
The intrinsic and extrinsic factors that determine the distribution
patterns of plant taxa may include the physiological requirements of
the plant, plant–animal relationships, soil characteristics, climate and
topography. Plant distribution is strongly influenced by climatic factors,
especially temperature (Woodward, 1987; Criddle et al., 1994; Wing
et al., 2005; Liu et al., 2007; Yang et al., 2007; Wang et al., 2009). The
range changes of Nelumbo are most conspicuous in its northern limits,
suggesting a link to temperature. Nelumbo's northern limits respond
to the periods of warming or cooling in the Cenozoic: 1) the northern
limit extends from 59.0°N in the Paleocene to 63.9°N in the Eocene,
and this represents the maximum northern limit in lotus phytogeographical history. The opportunity to move northward is probably due
to the warming trend that resulted in the Early Eocene climatic optimum; 2) the northern limit retreats to 53.3°N in the Oligocene as a
result of obvious cooling; 3) the northern limit extends a little northwards to 57.5°N in the Miocene, as a consequence of climatic amelioration, especially the Middle Miocene climatic optimum; 4) the northern
limit retreats a little to 51.0°N in the Pliocene and then contracts a lot
to 35.1°N in the Pleistocene, as a function of climatic cooling; and
Please cite this article as: Li, Y., et al., Paleobiogeography of the lotus plant (Nelumbonaceae: Nelumbo) and its bearing on the paleoclimatic
changes, Palaeogeogr. Palaeoclimatol. Palaeoecol. (2014), http://dx.doi.org/10.1016/j.palaeo.2014.01.022
Y. Li et al. / Palaeogeography, Palaeoclimatology, Palaeoecology xxx (2014) xxx–xxx
7
Fig. 3. Palaeogeographic maps show the distribution of Nelumbo from the Early Cretaceous to the Pleistocene. TU = Turgai Strait; NA = North America.
5) the northern limit expands to 47.8°N in recent times (Fig. 4). The fluctuations in the northern limit of the distribution of Nelumbo appear congruent with the general trend of global temperature changes based on
terrestrial plant fossil proxy (Wolfe, 1994; Wolfe, 1995; Mosbrugger
et al., 2005; Zhang, 2012) and marine oxygen isotope data (Zachos
et al., 2001) in the Cenozoic (Fig. 4).
The northern limit changes of Nelumbo are generally comparable to
those of the living fossil plant Metasequoia (Cupressaceae) (Liu et al.,
2007) and the basal eudicot taxon Nordenskioeldia (Trochodendraceae)
(Wang et al., 2009), but also display some differences. Firstly, the geographical range of Nelumbo expanded in the Paleocene while those of
the other genera contracted. Secondly, since the Eocene, the geographical
Please cite this article as: Li, Y., et al., Paleobiogeography of the lotus plant (Nelumbonaceae: Nelumbo) and its bearing on the paleoclimatic
changes, Palaeogeogr. Palaeoclimatol. Palaeoecol. (2014), http://dx.doi.org/10.1016/j.palaeo.2014.01.022
8
Y. Li et al. / Palaeogeography, Palaeoclimatology, Palaeoecology xxx (2014) xxx–xxx
Fig. 4. Paleolatitude distribution of Nelumbo based on fossil records from 89 localities. Red line links northern limit of Nelumbo paleolatitudes, compared with those of Nordenskioeldia and
Metasequoia, and the curve of global mean ocean temperature based on marine oxygen isotope (δ18O) data (Zachos et al., 2001).
range of Nelumbo has changed only moderately, while the range of
Nordenskioeldia contracted dramatically in the Oligocene and the genus
finally became extinct after the Miocene. The range of Metasequoia shrank
continuously from the Eocene until today (Fig. 4). The differences above
can be explained as: 1) the different sensitivities of aquatic and terrestrial
plants to climatic change; 2) the ecological habits of lotus splitting into
evergreen and deciduous types in the Eocene, thus promoting its adaptation to the following climatic changes.
Acknowledgments
Special thanks are due to Tong-Xing Sun, Yancheng Teachers University, China Xiu-Qun Liu, Huazhong Agricultural University, China and
Kathy Stephens, Queensland Herbarium, Australia for their help regarding modern species of Nelumbo and ecotypes. We are also grateful to
Garland Upchurch, Southwest Texas State University, USA; Yu-Sheng
Liu, East Tennessee State University, USA; Wilhelm Barthlott, University
of Bonn, Germany; Bruce Erickson, Science Museum of Minnesota, USA;
Kirk Johnson, Denver Museum of Natural History, USA; and James
Basinger, University of Saskatchewan, Canada for giving access to specific literatures. This research was supported by the International S & T
Cooperation Project of China No. 2009DFA32210, and the bilateral
cooperation project BL/36/C54 supported by the Belgian Federal Science
Policy Office. This work was also a contribution to the National Natural
Science Foundation of China (Nos. 31370254, 41072022, 41210001).
Appendix A. Supplementary data
Supplementary data to this article can be found online at http://dx.
doi.org/10.1016/j.palaeo.2014.01.022.
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Please cite this article as: Li, Y., et al., Paleobiogeography of the lotus plant (Nelumbonaceae: Nelumbo) and its bearing on the paleoclimatic
changes, Palaeogeogr. Palaeoclimatol. Palaeoecol. (2014), http://dx.doi.org/10.1016/j.palaeo.2014.01.022