Fossil Record 27 (1) 2024, 1–11 | DOI 10.3897/fr.27.

109621

First flower inclusion and fossil evidence of Cryptocarya

(Laurales, Lauraceae) from Miocene amber of Zhangpu (China)
Simon Beurel1, Julien B. Bachelier2, Jérôme Munzinger3, Fuchen Shao2, Jörg U. Hammel4,
Gongle Shi5, Eva-Maria Sadowski1
1 Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Invalidenstraße 43, 10115 Berlin, Germany
2 Freie Universität Berlin, Institute of Biology/Dahlem Centre of Plant Sciences, Altensteinstraße 6, 14195 Berlin, Germany
3 AMAP, Université Montpellier, IRD, CIRAD, CNRS, INRAE, 34000 Montpellier, France
4 Institute of Materials Physics, Helmholtz-Zentrum Hereon, Max-Planck-Straße 1, 21502 Geesthacht, Germany
5 State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology and Center for Excellence in Life
and Palaeoenvironment, Chinese Academy of Sciences, Nanjing 210008, China

https://zoobank.org/145575FB-0BE7-4916-88D0-2CA73D69B62C

Corresponding author: Simon Beurel ([email protected])

Academic editor: Florian Witzmann  ♦  Received 17 July 2023  ♦  Accepted 16 November 2023  ♦  Published 4 January 2024

Abstract
Lauraceae have one of the oldest fossil records of angiosperms with the earliest known evidence from the mid-Cretaceous. However,
most of these records are based on leaves, especially from the Cenozoic of Asia, which are often challenging to assign to extinct or
extant genera or species. In contrast, fossils of reproductive organs are more informative, but remain scarce. We here described the
first Cenozoic Lauraceae flower of Asia and confirmed the presence of Cryptocarya in the Miocene Zhangpu flora (Fujian Province,
south-eastern China) based on an amber inclusion. We scanned the specimen using synchrotron radiation-based micro-computed
tomography (SRμCT) and then compared the fossil with extant flowers of the genus. The present fossil flower is small, bisexual,
and polysymmetric, with a whorled and trimerous perianth and androecium along with a hypanthium around the gynoecium. The
perianth comprises six undifferentiated tepals, the androecium consists of nine stamens and three innermost staminodes, and the
gynoecium of a single carpel with a superior, unilocular (and uniovulate) ovary. Our study also shows that the fossil shares an
unusual position of the typical staminal glands and a short androecial tube on the rim of the hypanthium with at least one extant
Australian species of Cryptocarya, which have not been reported before. Nowadays, Lauraceae are still present in tropical to sub-
tropical regions, mostly in American and Asian rainforests. The discovery of many Lauraceae leaf fossils in Zhangpu, as well as the
amber flower of this study, is consistent with the current reconstruction of the amber source environment as a megathermal seasonal
rainforest during the Mid-Miocene.

Key Words
Angiosperm, Cenozoic, palaeobotany, synchrotron X-ray tomography, 3D reconstruction

Introduction comprise crops and spices, such as avocado, cloves

and cinnamon (Rohwer 1993). This family has a vast
The Lauraceae are one of the most species rich fami- meso- to megafossil record, mostly consisting of leaves
lies of Magnoliidae, with worldwide ecological and from all over the world (Friis et al. 2011). Lauraceous
economic importance. Some taxa are key ecosystem leaves are notoriously difficult to assign to species but
components, especially in Asian and American trop- also to generic level, as key features are widespread
ical lowland and montane forests. Lauraceae also across extinct and extant taxa and geographical areas

Copyright Simon Beurel et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use,
distribution, and reproduction in any medium, provided the original author and source are credited.
2 Simon Beurel et al.: Cryptocarya flower from Miocene Zhangpu amber

(Hill 1986; Christophel et al. 1996). In contrast, fossil 2021). Based on the 40Ar/39Ar dating of the basaltic units
fruits and flowers show more diagnostic features than associated the fossil layers, the age of the amber has been
leaves and are particularly valuable for generic or even well constrained at 14.8 ± 0.6 Ma to 14.7 ± 0.4 Ma, corre-
species level identification (Rohwer 1993). Such repro- sponding to the Langhian stage of the Middle Miocene
ductive structures are nevertheless rare, as they are not (Ho et al. 2003; Zheng et al. 2019; Wang et al. 2021). This
often preserved in the sedimentary fossil record (Friis is consistent with the previous palynological studies of
et al. 2011). the Fotan Group (Zheng and Wang 1994). The terpenoid
The oldest currently known lauraceous fossil flower composition of Zhangpu amber indicates that it derived
stems are from the Early Cretaceous Puddledock from the tropical Dipterocarpaceae. Additionally, fossil-
locality (von Balthazar et al. 2007). Additionally, fossils ized winged fruits with affinities to this angiosperm
of lauraceous origin from North America (Drinnan family were found in the same deposit (Shi and Li 2010;
et al. 1990; Friis et al. 2011), Europe (Kvaček 1992; Shi et al. 2014a, b). The amber piece was deposited in
Eklund and Kvaček 1998; Kvaček and Eklund 2003; the palaeobotanical collections of the Nanjing Institute
Viehofen et al. 2008; Coiffard et al. 2009; Moreau et of Geology and Palaeontology, Chinese Academy of
al. 2016) and South Asia (Poinar 2017) show that early Sciences in China (NIGPAS) under the collection number
members of the family were already widely distributed PB21525.
and diverse by the mid-Cretaceous. In Asia, the earliest Separation of the fossil flower from other syninclu-
Lauraceae fossil records date back to the Cenomanian sions in the same amber piece was achieved by using
with a flower inclusion of Cascolaurus burmitis Poinar the sawing machine ALGE. Then, the piece containing
in Burmese amber (Poinar 2017) and inflorescences the fossil was ground and polished with a LaboPol-25
and flowers of Mauldinia hirsuta Frumin, Eklund and machine (Struers, Sarasota, Florida, USA) using wet
Friis from Kazakhstan (Frumin et al. 2004). Additional silicon polishing papers with successively finer grit
Cretaceous fossils include flowers from the Coniacian sizes (250 to 4000 nm, Struers) to create even surfaces
of Japan (Takahashi et al. 1999, 2001, 2014). However, parallel to the inclusion (see Sadowski et al. 2021
molecular clock study infers that diversification of for details).
modern Lauraceae in Asia is more recent, and probably The amber specimen was studied under a Carl Zeiss
took place during the early Cenozoic (Chanderbali et AxioScope A1 compound microscope (Carl Zeiss,
al. 2001). This is supported by the large fossil leaves Oberkochen, Germany), using incident and transmitted
record, mostly from China (e.g. Hu et al. 2007; Jacques light simultaneously. Images were taken with a Canon
et al. 2011; Sun et al. 2011; Shi et al. 2014c; Huang EOS 80D digital camera (Canon, Tokyo, Japan) that was
et al. 2016; Wang et al. 2019; Wang et al. 2021), but mounted on the microscope. To accommodate the three-di-
fossil flowers from this time period remain scarce. mensionality of the inclusion, 65 single photographs were
Therefore, the discovery of additional Cenozoic laura- taken and then digitally stacked to a composite image, by
ceous reproductive organs is particularly interesting to applying the HeliconFocus 7.7 software.
gain more insight into the evolution and diversification Imaging of the flower inclusion was performed
of Lauraceae. using synchrotron-radiation based X-ray microto-
In this paper, we aim to describe a new fossil flower mography (SRμCT) at beamline P05 of the storage
of Lauraceae from Chinese Miocene Zhangpu amber ring PETRA III (Deutsches Elektronen-Synchrotron,
by using non-destructive X-ray imaging techniques. DESY, Hamburg, Germany) that is operated by
We noticed similarities, such as an the unusual position Helmholtz-Zentrum Hereon (Haibel et al. 2010;
of the staminal glands and an androecial tube, with an Greving et al. 2014; Wilde et al. 2016). The amber
extant member of Cryptocarya R. Br. from Australia, and piece was mounted on a sample-stub with beeswax and
discuss the significance of the oldest unambiguous fossil imaged using an attenuation contrast setup (Greving et
of the genus in the Miocene Zhangpu flora. al. 2014). The specimen was scanned using a commer-
cial CMOS camera system with an effective pixel size
of 0.45 µm, a sample to detector distance of 75 mm
Material and methods and a photon energy of 18 keV. A total of 3501 projec-
tions were recorded for the tomographic scan, at equal
The amber specimen derives from the Zhangpu amber intervals between 0 and π. A transport of intensity
deposit of the Fotan Group, in Zhangpu County (Fujian phase retrieval approach and a filtered back projection
province, SE China; see detailed map in Wang et al. 2021: was used to perform the tomographic reconstruction
fig. 1). The group is formed by sedimentary layers of implemented with the Astra Toolbox (Palenstijn et al.
conglomerates, sandstone and mudstone alternating with 2011; van Aarle et al. 2015, 2016) and Matlab (Math-
layers of basaltic rocks (Zheng and Wang 1994; Wang Works), integrated in a bespoke reconstruction pipeline
et al. 2021). Plant macro-remains are commonly found (Moosmann et al. 2014). Raw projections were binned
co-occurring with the amber in the same layers of blue- twice during processing, resulting in an effective voxel
grey mudstone with lignite and diatomite (Wang et al. size of 0.91 µm for the reconstructed volume.

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Fossil Record 27 (1) 2024, 1–11 3

The size of the resulting tomographic images was trimerous and alternate whorls around the gynoecium
decreased from 32-bit floating point data to 16-bit, (Fig. 1C–G). It is also perigynous with a hypanthium
by applying ImageJ 1.52 (Wayne Rasband, National (1.71 mm long and 0.60 mm wide) that encloses the
Institutes of Health, Bethesda, Maryland, USA). The superior ovary and lowest third of the style entirely
software Volume Graphics Studio Max, version 3.4 (Fig. 1D). The position of perianth organs forming a
(Volume Graphics, Heidelberg, Germany) was used to narrow opening and of the apical flaps still covering
complete the segmentation, 3D reconstructions, and the pollen sacs suggest a late pre-anthetic stage or early
length measurements. (female) anthetic phase.
We additionally examined flowers of some extant The tepal lobes (1.72–2.04 mm long and 0.66–1.05 mm
species of Cryptocarya from the Oceanic region, including wide) are free and arranged in an outer and inner whorl,
one from Australia (originally C. hypotephra F. Muell., and share a similar narrowly ovate to elliptic shape and an
now C. vulgaris B. Hyland; MB.Pb.HB.00569 [Schrader acute tip (Fig. 1A, B).
Herbarium (BHUPM), Museum für Naturkunde Berlin All stamens are shorter than the tepals in length and
(MfN)]), and four from New Caledonia (C. adpressa have basifixed anthers with unilocular thecae opening
Munzinger & McPherson [Munzinger et al. 5832, P, Type by two slightly lobed to flattened apically attached or
specimen], C. aristata Kosterm. [Munzinger et al. 5866, hinged flaps (Figs 1C–E, 2A, C). Stamens of the first and
P], C. cf. odorata Guillaumin [Munzinger (leg. Waikedre) second whorls have introrse, ovate and incurved anthers
6716, MPU], and Vanuatu (C. wilsonii Guillaumin (ca. 0.57–0.68 mm long and 0.40–0.50 mm wide).
[Munzinger & Bruy 8232], NOU). Each flower sample Their filaments are adnate to a tepal lobe (Fig. 1F) and
was mounted on a specimen holder to facilitate microCT distinctly shorter than their anthers (ca. 0.25–0.48 mm
scanning with a Phoenix X-ray Nanotom at the MfN. long and 0.08–0.11 mm wide). Three pairs of large
The scans comprised 1440 to 2000 projections and were glands are inserted on the hypanthium rim, between
conducted using the following settings: voltage = 80 to the united bases of the tepals and filaments (Fig. 1D).
100 kV, current = 75 to 100 µA, exposure time = 0.75 to These glands are formed by a subglobose distal part
1 s, average = 3 to 6, skip = 1 and isotropic resolution = (ca. 0.34–0.56 mm long and 0.29–0.38 mm wide) and
1.64 to 3.6 µm. a long stalk (ca. 0.31–0.40 mm long and 0.09–0.12 mm
wide; Figs 1D, F, 2B). Stamens of the third whorl have
latero-extrorse, erect and narrow anthers (ca. 0.68–0.75
Data resources mm long and 0.37–0.39 mm wide). The filaments are
just about as long as their anthers (ca. 0.64–0.74 mm
Supplementary data including SRμCT videos, 3D models long and 0.09–0.14 mm wide) and their bases form,
of the Cryptocarya flower inclusion and of extant flowers together with those of the staminodes, a short staminal
of the genus are available here: https://doi.org/10.7479/ tube projecting beyond the rim of the hypanthium (ca.
pzxg-2x16. 0.13 mm long and 0.45 mm wide; Figs 1D, G, 2C). The
staminodes have a sagittate (triangular-ovate and acum-
inate) sterile anther and a short and stout filament (ca.
Results 0.60–0.65 mm long and 0.38–0.40 mm wide and 0.31–
0.41 mm long and 0.15 mm wide respectively; Figs 1D,
Systematic palaeontology F–G, 2C).
The gynoecium consists of a single carpel (ca. 2.03 mm
Order Laurales Juss. ex Bercht. & J. Presl, 1820 long). The slender superior ovary (1.22 mm long and
Family Lauraceae Juss. 1789 0.18 mm wide) is entirely enclosed in the hypanthium.
Genus Cryptocarya R. Br., 1810 The style (ca. 0.81 mm long and 0.14 mm wide) ends
in an inconspicuous stigma (Fig. 1D). The ovary has a
Cryptocarya sp. single locule and an apical pendulous ovule (ca. 0.71 mm
Figs 1, 2 long and 0.16 mm wide).
The flower is densely pubescent with appressed simple
Specimen studied. PB21525. Nanjing Institute of acute trichomes covering all organs, except for the inner
Geology and Palaeontology, Chinese Academy of surface of the distal part of the hypanthium, the fertile and
Sciences in China (NIGPAS). sterile anthers and the gynoecium (Fig. 1).
Locality. Zhangpu County, Fujian Province, China.
Horizon and age. Middle part of the Fotan Group,
Langhian (ca. 14.7–14.8 Ma), Middle Miocene. Syninclusions
Description. The flower is 3.11 mm long and 1.66 mm
wide (without the pedicel, not preserved) (Fig. 1A, B). It The specimen contains inclusions of two Tetramorium
is perfect, polysymmetric, and comprises six tepals, nine and five Carebara ants (Formicidae), one Collembola,
stamens, and three staminodes, which are arranged in six two Chironomidae, and wood fragments.

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4 Simon Beurel et al.: Cryptocarya flower from Miocene Zhangpu amber

Figure 1. Cryptocarya fossil flower from Miocene Zhangpu amber, PB21525. A. Overview of the flower inclusion, taken under
the light microscope; B–D. Virtual 3D reconstruction from segmented SRµCT data; B. Overall flower; C. Cross section; D. Longi-
tudinal section; E–G SRµCT cross-sections, indicated in D and arranged from top to bottom; E. Bilocular anthers with two valves
and laterally fused pollen sacs (septa indicated by white arrowheads); F. Style, staminodes, glands, and the filaments of the fertile
stamens adnate to a tepal lobe; G. Short staminal tube resulting from the fusion of the third whorl of stamens with the whorl of
staminodes. Perianth – grey; Stamens of the first whorl – red; Stamens of the second whorl – orange; Stamens of the third whorl –
beige; Anther valves – white; Staminal glands – pink; Staminodes – yellow; Gynoecium – purple; Ovule – blue. Scale bars: 0.5 mm
(A–D); 0.4 mm (E–F); 0.3 mm (G).

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Fossil Record 27 (1) 2024, 1–11 5

Figure 2. Androecium of the Cryptocarya flower from Miocene Zhangpu amber, PB21525. A. Stamens of the first and second
whorl; B. Staminal glands; C. Stamens of the third whorl fused with the staminodes at the base of the filaments, forming a short
staminal tube. Stamen of the first whorl – red; Stamen of the second whorl – orange; Stamens of the third whorl – beige; Anther
valves – white; Staminal glands – pink; Staminodes – yellow. Scale bars: 0.2 mm (A); 0.3 mm (B–C).

Discussion Within this group, the fossil flower exhibits a combi-

nation of distinctive features with members of the extant
Systematic affinity genus Cryptocarya, including six tepals, nine stamens
that are all fertile and a deep hypanthium entirely encom-
Our non-invasive and non-destructive approach shows passing the ovary (Fig. 3; van der Werff 1991, 2001;
that our fossil flower exhibits essentially the same Rohwer 1993; Moraes 2007; Li et al. 2008b).
Bauplan as most extant Lauraceae, with two trimerous Extant Cryptocarya flowers are small (about 3–5 mm,
whorls of tepals, followed by three trimerous whorls Fig. 3), actinomorphic, bisexual and perigynous. The
of fertile stamens and an innermost trimerous whorl of perianth also consists of six tepals arranged in an outer
staminodes, and a unicarpellate gynoecium. In addition, and inner whorl usually of similar size and shape. The
like in all Lauraceae, the anthers are unmistakingly androecium comprises three whorls with three fertile
valvate with apical flaps, and the single ovary is supe- stamens and an innermost whorl of staminodes. The
rior and unilocular with one apical ovule (Rohwer 1993; first and second whorl of stamens have introrse anthers,
van der Werff 2001; Li et al. 2008a; Simpson 2010). while the ones of the third whorl can be extrorse, lateral
The bithecal anthers also exhibit a bilocular structure or rarely introrse (Kostermans 1937; Moraes 2007). The
with septal remains in some thecae. However, whether stamen filaments are inserted on the rim of the hypan-
lateral fusion of the two pollen sacs happened before thium, each close or connected to the base of a tepal. In
anthesis or earlier is unclear, but such anthers may addition, stamens of the first/second or third whorl bear
have evolved multiple times in Lauraceae, with inter- a pair of glands, distant or adnate to the base of their fila-
mediate forms observed in several genera (Rohwer ment (Fig. 3G; Hyland 1989; Moraes 2007). A fourth
1994). According to Rohwer (1993), bilocular anthers whorl of conspicuous, sagittate staminodes also occurs in
most likely originated in Lauraceae from the reduc- the flowers. The style is long and the stigma is small or
tion of the upper or lower pollen sac(s) but may also inconspicuous (Kostermans 1937; Moraes 2007).
have been formed by the lateral fusion of the pair of
pollen sacs, which is a synapomorphy of the “larger
part of the Cryptocarya group” that contains at least the Position of glands and staminal tube in
genera Cryptocarya, Beilschmiedia Nees, Endiandra Cryptocarya
R. Br., Aspidostemon Rohwer & H.G. Richt., Potameia
Thouars, Eusideroxylon Teijsm, & Binn., Potoxylon Androecial characters are highly variable among extant
Kosterm., Dahlgrenodendron J.J.M. van der Merwe & Lauraceae and may also vary within genera. In most cases,
A. E. van Wyk, Sinopora J. Li, N.H. Xia & H.W. Li, the pairs of staminal glands are connected to or born on
Triadodaphne Kosterm. and Yasunia van der Werff the filament bases of the third whorl of stamens (Rohwer
(Rohwer et al. 2014). 1993). However, they can also occur on the outermost

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6 Simon Beurel et al.: Cryptocarya flower from Miocene Zhangpu amber

Figure 3. Extant Cryptocarya vulgaris flower from Australia, MB.Pb.HB.00569. A. Overview of a flower, taken under the light
microscope; B–D. Virtual 3D reconstruction from segmented microCT data; B. Overall flower; C. Cross section; D. Longitudinal
section; E–G. microCT cross-sections, indicated in D and arranged from top to bottom; E. Immature bilocular anthers of the androe-
cium and the bilobed stigma; F. Style, staminodes, glands, and filaments of the fertile stamens; G. Staminal tube resulting from the
fusion of the third whorl of stamens with the whorl of staminodes; note the glands inserted at the division point of the tepal lobes.
Perianth – grey; Stamens of the first whorl – red; Stamens of the second whorl – orange; Stamens of the third whorl – beige; Stami-
nal glands – pink; Staminodes – yellow; Gynoecium – purple; Ovule – blue. Scale bars: 0.4 mm (A–D); 0.3 mm (E–G).

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Fossil Record 27 (1) 2024, 1–11 7

androecial whorl such as in Rhodostemonodaphne Due to the morphological variations in Cryptocarya

Rohwer and Kubitzki, Urbanodendron Mez, flowers and the lack of distinctive characters in the fossil,
Chlorocardium Rohwer, Richter and van der Werff, it does not seem reasonable to assign the flower inclu-
and Brassiodendron C.K. Allen (Rohwer 1993). Also, sion to any extant species of Cryptocarya. Furthermore,
in some extant representatives of Cryptocarya from additional plants organs, such as leaves or fruits would
Australia and South America, the paired staminal glands be necessary to clarify the affiliation of the fossil to
are associated with the two outer whorls of stamens or the species level. For all these reasons, we refrain from
rather distant from the filaments (in C. brassii C.K. Allen, describing the amber inclusion as a new fossil species.
C. grandis B. Hyland, C. pleurosperma C.T. White and
W.D. Francis, C. putida B. Hyland, C. vulgaris in Hyland
1989; C. moschata Nees and Martius, C. guianensis Fossil records and challenges in assigning
Meisner, C. riedeliana P.L.R. Moraes in Moraes 2007). Cryptocarya and Lauraceae fossils
As in some of these extant species, the staminal glands
of our Cryptocarya fossil flower are free from the fila- According to molecular data, Cryptocarya diverged
ment and inserted towards the distal end of the floral cup around about 90 ± 20 million years ago and is probably
(Fig. 1D). However, it is often unclear in the literature of Gondwanan origin (Chanderbali 2001). Nevertheless,
and in our material which whorl the glands are associ- fossils with affinities to the Cryptocarya group, and more
ated with. For instance, we observed in the herbarium specifically to Cryptocarya, are only known since the
specimen C. vulgaris (MB.Pb.HB.00569) that they are Cenozoic. The oldest representatives are possibly fossil
inserted at the division point of the tepal lobes (Fig. 3G) leaves from the Eocene of Australia (Hill 1986, 1988;
whereas Hyland (1989) associates the glands with the Conran and Christophel 1998; Carpenter et al. 2004) and
first whorl of stamens (fig. 37G). North America (MacGinitie 1941). In addition, numerous
In the fossil flower from Zhangpu, as well as in putative leaves and fruit fossils were discovered in the
the herbarium flowers of Cryptocarya vulgaris (MB. Miocene and Pleistocene of New Zealand (Holden 1982;
Pb.HB.00569), the filaments of the third stamen whorl Pole 1993, 2007, 2019; Bannister et al. 2012), the Miocene
are similarly fused with those of the staminodes whorl of New Caledonia (Garrouste et al. 2021), as well as in
(Figs 1G, 2C, 3G), forming a short staminal tube the Oligocene, Miocene and Pleistocene of China (Liu
extending beyond the rim of the hypanthium. Judging 1993; Shi et al. 2014c; Wang et al. 2019), while fewer
from flowering stage, the staminal tube in the fossil is were discovered in the New World (i.e. in the Paleogene
less prominent than in the extant specimen. In addition, of Patagonia; Carpenter et al. 2018). It is only recently
the tube observed in extant Cryptocarya flowers is more that a fossil has been reliably assigned to the genus in
defined when the flower is less mature, suggesting that, Asia, based on Pleistocene wood (Huang et al. 2023).
depending on the developmental stage of the specimen, However, most of those fossils are leaf impressions
a staminal tube is only temporarily present in the early and compressions or cuticle fragments. Moreover,
development of some Cryptocarya flowers. They can the fossil pollen record of Lauraceae is scarce, as their
thus be superficially different in older stages and prevent pollen has a low fossilisation potential (Herendeen et
a detailed comparison with classic descriptions of fully al. 1994; Friis et al. 2011) and thus the pollen record for
developed flowers in the literature. These morphological Cryptocarya is inexistent. Although placement of fossil
variations should be considered in future morphological leaves in Lauraceae is unequivocal, the assignment to
studies of the genus. genera or even species is more complex with vegetative
The glands and the staminal tube are distinctive in the organs alone, as leaf morphology varies greatly. This
herbarium flower (MB.Pb.HB.00569) and in the fossil. is also the case in extant and fossil Cryptocarya (Hill
However, such a staminal tube elaborated only by the third 1986; Christophel et al. 1996; van der Werff 1991, 2001;
and fourth androecium whorls has, to our knowledge, Bannister et al. 2012). For instance, Christophel et al.
never been pictured or mentioned before in Lauraceae. (1996) observed that the presumed diagnostic cuticular
Similarly, pairs of staminal glands on different whorls “butterfly-shaped” ledges of Australian Cryptocarya also
were also only occasionally depicted (Hyland 1989, occur in other extant Lauraceae genera of South America.
figs 13G, 21G, 31I, 32G, 37G; Moraes 2007, figs 33D, Additionally, van der Werff (1991, 2001) noted that
52D). Therefore, future morphological and anatomical the majority of extant genera are defined by floral charac-
studies are needed to gain more insight into the variation ters; however, extant flower and fruit samples are difficult
of the gland position and staminal tube development in to obtain or even unavailable for study (Rohwer 1993;
Cryptocarya. Additionally, our results show that X-ray Li et al. 2008a). This makes the identification of fossil
based methods, like micro-CT scanning, is a valuable Lauraceae even more challenging. Moreover, small deli-
tool for analysing extant plant specimens, as they allow cate reproductive organs are often not preserved as fossils.
detailed observations of reproductive plant organs non-in- It should be noted that the presence of Cryptocarya in
vasively, compared to standard methods like microtome the Miocene of China was previously suggested by fossil
sections, which are usually applied in botany. fruits found in Zhangpu county which showed similarities

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8 Simon Beurel et al.: Cryptocarya flower from Miocene Zhangpu amber

to extant Cryptocarya bhutanica Long (Wang et al. 2019), (Wang et al. 2021, supplementary material, table S1). The
but could not be unambiguously assigned to the genus. palaeoclimate of Zhangpu, as well as the fossil plant taxa
Therefore, the fossil flower of this study confirms the are similar to tropical rainforests of Southeast Asia today,
occurrence of Cryptocarya in the Miocene of Zhangpu suggesting that the Zhangpu amber forest was a megath-
and gives new insight into its flower morphology in the ermal seasonal rainforest during the Mid-Miocene Climatic
geological past. Optimum (Jacques et al. 2015; Zheng et al. 2019; Wang
et al. 2021). Nowadays, Cryptocarya is still an important
element of evergreen broad-leaved forests in South China,
Extant biodiversity and palaeoecological where it is part of the canopy and subcanopy (Wang et al.
implications 2003; Li et al. 2008b). For instance, C. chinensis Hemsl.
can be found in lower subtropical monsoon evergreen
Lauraceae are pantropical with about 50 genera and broad-leaved forests (Wang et al. 2003). Thus, the presence
probably 2500 to 3500 species that are mostly evergreen of Cryptocarya in the Zhangpu amber forest is consistent
trees and shrubs (Rohwer 1993). While they are mainly with the current palaeoclimatic and palaeoenvironmental
distributed in tropical to subtropical regions of Central interpretations (Jacques et al. 2015; Wang et al. 2021).
and South America as well as Southeast Asia, the family
is particularly diverse and sometimes dominant in rainfor-
ests (Rohwer 1993; Li et al. 2008a; Simpson 2010). About Conclusion
25 genera and 445 species occur in China and mainly
inhabit the southern provinces (Li et al. 2008a, Tan et al. In our study, we present the first Cenozoic Lauraceae
2023). In the family, Cryptocarya is one of the most wide- flower of Asia, based on an amber inclusion from Zhangpu.
spread genera throughout the tropics, with between 200 The application of non-invasive X-ray computed tomog-
and 350 species growing in South America, South Africa, raphy techniques facilitated a detailed morphological
Madagascar, Asia, Australia and Oceania, and a centre of examination of the amber inclusion and an in-depth
diversity in Malaysia (Hyland 1989; van der Werff 1992, comparison of the fossil flower with extant Cryptocarya
2001; Rohwer 1993; Moraes 2007; Li et al. 2008b; Rohwer flowers, revealing their remarkable resemblances. The
et al. 2014). It has been noted that the disjunct distribution fossil and extant flowers both have a perianth with six
of some Cryptocarya species was probably caused by fruits tepals, an androecium comprising nine fertile stamens
dispersion of birds from Gondwana across the Pacific, but with bilocular anthers and three staminodes, and a gynoe-
that the genus was nonetheless, explicitly monophyletic cium with a unicarpellate carpel forming a superior ovary
(Rohwer et al. 2014). Although Cryptocarya as a whole with one apical ovule surrounded by a hypanthium. The
still requires a global extensive revision (Rohwer 1993; distinct presence of a similar staminal tube and position
Rohwer et al. 2014), some studies have recently improved of staminal gland pairs are reported for the first time in
our knowledge of the taxonomy of this genus in South Asia Cryptocarya, in both the examined extant C. vulgaris
(de Kok 2015, 2016; Nishida et al. 2016). from Australia and our fossil. This highlights the need to
The Zhangpu amber deposit, where the fossil flower re-evaluate the occurrence (and potential significance) of
was collected, is a highly diverse megathermal rainforest those characters in other species.
biome. Amber inclusions of arthropods include more than In addition, the amber fossil supports the morpho-
250 families, with at least 200 being insects. Bryophytes logical stasis of Zhangpu plant communities alongside
are represented by about seven liverworts genera, as well insects in tropical rainforests of Asia since at least the
as five extant moss taxa (Wang et al. 2021). In contrast, Middle Miocene (Wang et al. 2019, 2022; Wang et al.
seed plant inclusions from Zhangpu amber are rare and 2021; Beurel et al. 2023). However, it should be noted
up to date; only three species were described (Canarium that previous affinities of Lauraceae fossil leaves to
wangboi Beurel et al. and Canarium leenhoutsii Beurel et Cryptocarya are still debatable, as the family exhibits
al. (Burseraceae); Beurel et al. 2023; Parrotia zhiyanii Wu a wide range of leaf characters and morphological
et al. (Hamamelidaceae); Wu et al. 2023). Nevertheless, convergence between genera (Christophel et al. 1996).
plant megafossils from the amber-bearing sedimentary Nevertheless, the inclusion of this study represents the
rocks are extremely rich, including about 24 families. Most first fossil record of a flower of Cryptocarya and confirms
of them are megathermal pantropical plant families, such the presence of this genus in the Miocene Zhangpu flora,
as Annonaceae, Melastomataceae and Moraceae. Among which was only previously assumed from putative fossil
these taxa, Dipterocarpaceae, Leguminosae, Lauraceae fruits (Wang et al. 2019).
and Clusiaceae are the most abundant and diverse ones,
with only slight morphological variations compared to
their modern members, indicating a possible morpholog- Acknowledgements
ical stasis in the plant community (Wang et al. 2019, 2022;
Wang et al. 2021). Within Lauraceae, fossils leaves with We would like to thank Bo Wang (NIGPAS) and Vincent
probable affinities to Alseodaphne Nees, Cinnamomum Perrichot (Univ. Rennes) for the fossil specimen acqui-
Schaeff. and Lindera Thunb. were recently discovered sition. We recognise the provision of beamtime, related

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Fossil Record 27 (1) 2024, 1–11 9

to the proposal BAG-20210019 at beamline P05 at Conran JG, Christophel DC (1998) A new species of triplinerved Lauro-
PETRA III at DESY, a member of the Helmholtz phyllum from the Eocene of Nerriga, New South Wales. Alcheringa
Association (HGF). This research was supported in 22(4): 343–348. https://doi.org/10.1080/03115519808619332
part through the Maxwell computational resources De Kok RPJ (2015) A revision of Cryptocarya (Lauraceae) from Thai-
operated at Deutsches Elektronen-Synchrotron DESY, land and Indochina. Gardens’ Bulletin Singapore 67(2): 309–350.
Hamburg, Germany. https://doi.org/10.3850/S2382581215000277
We are grateful to Kristin Mahlow (MfN) for the scan- De Kok RPJ (2016) A revision of Cryptocarya R. Br. (Lauraceae)
ning of the extant Cryptocarya flowers and to David Bruy of peninsular Malaysia. Kew Bulletin 71(1): 1–26. https://doi.
(NOU, IRD), Pete Lowry (Missouri Botanical Garden), org/10.1007/s12225-016-9613-1
Chrissen Gemmill (Univ. Waikato), Sven Buerki (Univ. Drinnan AN, Crane PR, Friis EM, Pedersen KR (1990) Lauraceous
Boise), Martin Callmander (Conservatoire et Jardin flowers from the Potomac Group (mid-Cretaceous) of eastern
Botaniques de Genève), and Jean Waikedre (IRD, North America. Botanical Gazette 151(3): 370–384. https://doi.
Nouméa) for help in the field. Cryptocarya wilsonii was org/10.1086/337838
collected thanks to the Plants mo Pipol blong Vanuatu Eklund H, Kvaček J (1998) Lauraceous inflorescences and flowers from
project (National Science Foundation grant 1555657 the Cenomanian of Bohemia (Czech Republic, central Europe). In-
to the New York Botanical Garden). Angelika Haufe ternational Journal of Plant Sciences 159(4): 668–686. https://doi.
(MfN) provided access to extant specimens of Australian org/10.1086/297585
Cryptocarya from the Schrader herbarium (MfN, Berlin). Friis EM, Crane PR, Pedersen KR (2011) Early flowers and angio-
We also thank Raymond J. Carpenter (Univ. Adelaide) sperm evolution. Cambridge University Press, 585 pp. https://doi.
for literature discussion and Corentin Jouault (MNHN) org/10.1017/CBO9780511980206
for insect identification. Conservation authorities of the Frumin S, Eklund H, Friis EM (2004) Mauldinia hirsuta sp. nov., a
North and South Provinces of New Caledonia (DDEE new member of the extinct genus Mauldinia (Lauraceae) from
and DDDT) provided JM with collecting permits. This the Late Cretaceous (Cenomanian-Turonian) of Kazakhstan. In-
study was supported by the German Research Foundation ternational Journal of Plant Sciences 165(5): 883–895. https://doi.
[DFG, grant no. 423862824]. We would like to thank org/10.1086/421479
Yong Yang and Maria von Balthazar for their comments, Garrouste R, Munzinger J, Leslie A, Fisher J, Folcher N, Locatelli E,
which have improved the manuscript. Foy W, Chaillon T, Cantrill DJ, Maurizot P, Cluzel D, Lowry II PP,
Crane P, Bahain JJ, Voinchet P, Jourdan H, Grandcolas P, Nel A
(2021) New fossil discoveries illustrate the diversity of past terres-
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