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Internal Details Corroborate the Occurrence of Flower Bud in the Lower Cretaceous of China

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Abstract
The Yixian Formation (Lower Cretaceous) of China is famous worldwide for its fossils of early angio-sperms, but there is only one record of flower bud hitherto. A previous fossil record of flower bud just showed the appearance and lacked any internal details. Such a lacuna in knowledge of flower buds hin-ders our understanding of the evolution of flowers. Our new specimen was collected from an outcrop of the Yixian Formation (the Barremian-Aptian, Lower Cretaceous) near Dawangzhangzi, Lingyuan, Liao-ning, China. The specimen was observed and photographed using a Sony ILCE-7 digital camera and a Nikon SMZ1500 stereomicroscope, and details were observed using a TESCAN MAIA3 SEM. Our ob-servations document a fossil flower bud, Archaebuda cretaca sp. nov, from the Lower Cretaceous of China. The occurrence of two species of Archaebuda in the Yixian Formation not only confirms the ex-istence of the expected gynoecium (and possible androecium) in a flower bud, but also underscores the occurrence of typical flowers in the Early Cretaceous.
Keywords: 
Subject: Biology and Life Sciences  -   Plant Sciences

1. Introduction

Angiosperms are indispensable components of the current ecological background for human beings’ origination and evolution. Their origin and early evolution have been foci of botanical controversies for a long time. Fossil evidence from the Yixian Formation plays an important role in improving our understanding on the origin and evolution of angiosperms. In strong contrast to the abundance and diversity of angiosperms in the Yixian Formation (including Archaefructus and other pioneer angiosperms [1,2,3,4,5,6,7,8,9,10,11,12,13]), there is only one report of flower bud in the formation [14]. This single case makes the concerned conclusion more or less tentative, as the public have long been impressed by the lack of flower bud in the geological history. Here we report a flower bud fossil from the Yixian Formation (Lower Cretaceous). In line with the preceding record, new specimen of Archaebuda with internal details re-underscores the occurrence of flower bud in the Yixian Formation. The discovery not only adds to the existing great diversity of angiosperms in the Lower Cretaceous, and sheds new light on the evolution of early flowers.

2. Materials and Methods

Various fossil animals and plants have been documented in the Yixian Formation of Northeastern China [1-3,5–36], and the age of the formation has been a focus of studies for many stratigraphers [37,38,39,40,41,42,43,44,45,46]. There is a general consensus over the age of the formation, namely, approximately 125 Ma (Barremian-Aptian, Lower Cretaceous) [47]. The present fossil specimen was collected from the Dawangzhangzi outcrop of the Yixian Formation near Lingyuan, Liaoning, China (Figure 1). The specimen was preserved as a flattened compression embedded in thin-layered siltstone (Figure 2a). The whole specimen was imaged using a Sony ILCE-7 digital camera. Morphological details were imaged using a Nikon SMZ1500 stereomicroscope equipped with a Nikon DS-Fi1 digital camera and a TESCAN MAIA3 scanning electron microscope (SEM) at Nanjing Institute of Geology and Palaeontology, CAS (NIGPAS). All figures are organized using a Photoshop 7.0.

3. Results

Genus Archaebuda Chen and Wang, emended
Emended generic diagnosis: Flower bud long-stalked. Stalk straight, bearing scaly leaves. Scaly leaves long-triangular, spirally arranged along stalk. Bud elongated oval, including two types of foliar appendages. Foliar appendage type I smaller, keeled, round-tipped. Foliar appendage type II bigger, keel free, papery, notched at the tip, overlapping each other, of at least three layers. Gynoecium and possible androecium surrounded by foliar appendage type II.
Type species: Archaebuda lingyuanensis Chen and Wang, 2022 [14].
Species: Archaebuda cretaca sp. nov.
Species diagnosis: (in addition to that of genus), gynoecium bottom-positioned.
Description: The specimen is a compression, 20 mm long and 9 mm wide, preserved as two facing parts embedded in a siltstone (Figure 2a, Figure 3a and S1a-c). Foliar appendages type I are at the base of the bud, smaller than the foliar appendages type II, 2.9-3.5 mm long and 1.1-1.2 mm wide (Figs. 2a, 3a, S1c). Foliar appendages type II are bigger than the foliar appendage type I, 6.4-7 mm long and 3.6-4.6 mm wide, keel-free, papery, notch at the tip not obvious, multiple layers overlapping each other, with longitudinally oriented texture (Figs. 2a, c, 3a, c, S1a-c). Possible trace of androecium is seen, but no pollen grains can be recognized under SEM (Figs. 2a, 3a, S1c). The gynoecium is bottom-position in the flower bud, only 3 mm long and 1.4 mm wide, secluded by an ovary wall that is broken and exposes its internal content (Figs. 2a-b, 3a-b, d, S1c).
Etymology: cretaca-, for the Cretaceous, the age of the fossil.
Holotype: BMM79926 (Figs. 2-3, S1).
Type locality: Dawangzhangzi, Lingyuan, Liaoning, China (41˚15ꞌN, 119˚15ꞌE, Figure 1).
Type horizon and age: the Yixian Formation, equivalent to the Barremian-Aptian, Lower Cretaceous (approximately 125 Ma).
Depository: Blue Miracle Museum Science Research Studio, Guangzhou, China.
Remarks: The general appearance and dimensions of Archaebuda cretaca are comparable to those of the type species A. lingyuanensis [14] (Table 1), therefore these features allow us to place our new species in the genus Archaebuda. Different from the type species, Archaebuda lingyuanensis [14], our new species has internal details, gynoecium (and possible androecium), of the flower bud preserved. Someone may be hesitant to accept the interpretation given by Chen and Wang [14], considering they could exclude the possibility for the fossil being certain kind of cones. A cone usually has a cone axis, which is now shown missing in Archaebuda cretaca sp. nov, excluding any possibility Archaebuda being a cone. These additional details confirm the flower bud identity claimed for the type species Archaebuda lingyuanensis by Chen and Wang (2022) [14] and our new species, Archaebuda cretaca sp. nov.

4. Discussions

The great diversity of angiosperms in the Yixian Formation is well known [1,2,3,4,5,6,7,8,9,10,11,12,13,14], including various reproductive organs of angiosperms [1,2,3,14,48]. Among these fossil, flower buds are a rarity: there is only one previous record, Archaebuda lingyuanensis [14]. Such a sparse record of flower bud not only restricts us from better understanding of flower evolution, but also the credibility of interpreting such precious fossil as a flower bud.
It is well known that previously reported reproductive organs of fossil angiosperms from the Yixian Formation showed little resemblance to extant flowers, as they usually lack a perianth that is frequently seen in extant flowers. Their unusual morphologies make it hard to convince the general public of the truthful occurrence of Cretaceous fossil flowers. To make the situation worse, restricted by the techniques extracting fossil specimens out of sediments, some palaeobotanists even hypothesized that early flowers are of small size. These palaeobotanists forgot that, even there were plant megafossil of flowers, their processing would have destroyed them completely. The combining effects of these two factors heavily inflict our understanding of early flower s and their evolution.
Hitherto there were only two reports of fossil flower buds. One of them is Florigerminis [49] recovered from the middle-late Jurassic Jiulongshan Formation of Inner Mongolia, China, and it is physically connected with branches and a fruit. These connected organs demonstrated a phenomenon rarely seen in the fossil world, flowers in various developmental stages. The other is the congeneric species of Archaebuda cretaca, A. lingyuanensis, from exactly the same outcrop of the Yixian Formation. [14]. This fossil was identified as a fossil flower bud based on its general morphology, three overlapping petals (foliar appendages type II), arrangement of the petals and their textures [14]. However, it is unfortunate that the supposed androecium and gynoecium could not be demonstrated in Archaebuda lingyuanensis. This shortcoming more or less reduces the credibility of the claim made by Chen and Wang [14]. Now with the discovery of Archaebuda cretaca, with information of gynoecium and possible androecium, from the same outcrop, it is more convincing that flower buds did exist in the Early Cretaceous, as the androecium and gynoecium impossible to prove in Archaebuda lingyuanensis are now verified in Archaebuda cretaca.
It is noteworthy that the occurrence of both Archaebuda lingyuanensis and A. cretaca in the same outcrop of the Yixian Formation are much bigger than the mesofossil flowers [50]. Formerly, early angiosperms were thought small. Such a conclusion was more or less hinged with the abundant discoveries of mesofossil flowers. However, this may be another six-inch-fishes story in history of science: the technique applied in mesofossil extracting process targets only small (usually <10 mm) parts of plants, while big ones may well have been destroyed during the processing. Now with the discoveries of Archaebuda lingyuanensis and Archaebuda cretaca, this biased view on early flower evolution should be corrected.
Compared to the Jurassic flower bud Florigerminis [49], two species of Archaebuda have much bigger flower bud. The flower bud of Florigerminis is only 3.8 mm long and 3.3 mm in diameter [49], much smaller than Archaebuda, which is about 20 mm long and 9 mm in diameter. It is noteworthy that the fruit of Florigerminis is 11.5 mm long and 7.7 mm in diameter [49], also smaller than the flower bud of Archaebuda. These data indicate that the stark size contrast between Florigerminis and Archaebuda is not due to different development stages. This big size of Archaebuda makes their flowers more conspicuous. This fact is apparently conducive to the success of pollination process, especially when it is pollinated by animals.

5. Conclusion

Discoveries of two species of flower bud, Archaebuda lingyuanensis and A. cretaca, indicate that at least some of angiosperms in the Early Cretaceous have big flowers, and, together with those atypical ones, typical angiosperms and flowers were already diversified 125 Ma ago.

Author Contributions

X.W. designed the research. W. J. H. collected the fossil specimen. X.W. and W. J. H. analysed the data and wrote the manuscript. All authors agreed on the manuscript.

Ethics Statement

This research involves no living animal/plant material, no conserved fossil materials.

Funding Information

This research was supported by the National Natural Science Foundation of China (42288201).

Acknowledgments

We thank Mr. Yan Fang for help photography using SEM and Dr. Mike Pole for his help on English.

Conflicts of Interest

The authors claim no conflict of interest.

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Figure 1. The fossil locality of Archaebuda cretaca sp. nov, Dawangzhangzi, Lingyuan, Liaoning, China. Reproduced from Han et al. [12], with permission and courtesy of Acta Geologica Sinica (English edition). a. Fossil locality (black dot) in northeastern China. b. Detailed position of fossil locality (red star) in suburb of the City of Lingyuan, Liaoning.
Figure 1. The fossil locality of Archaebuda cretaca sp. nov, Dawangzhangzi, Lingyuan, Liaoning, China. Reproduced from Han et al. [12], with permission and courtesy of Acta Geologica Sinica (English edition). a. Fossil locality (black dot) in northeastern China. b. Detailed position of fossil locality (red star) in suburb of the City of Lingyuan, Liaoning.
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Figure 2. The holotype of Archaebuda cretaca sp. nov. and its details. a. The general view of the specimen. Possible androecium is marked with white triangles. Scale bar = 5 mm. b. Detailed view of the rectangle in Figure 2a, showing the gynoecium. Scale bar = 0.5 mm. c. Detailed view of tip of the bud in Figure 2a, showing different textures on and border between different petals (1-4). Scale bar = 1 mm.
Figure 2. The holotype of Archaebuda cretaca sp. nov. and its details. a. The general view of the specimen. Possible androecium is marked with white triangles. Scale bar = 5 mm. b. Detailed view of the rectangle in Figure 2a, showing the gynoecium. Scale bar = 0.5 mm. c. Detailed view of tip of the bud in Figure 2a, showing different textures on and border between different petals (1-4). Scale bar = 1 mm.
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Figure 3. SEM of Archaebuda cretaca sp. nov. a. General view of the specimen. Possible androecium is marked with white triangles. Scale bar = 5 mm. b. Detailed view of the gynoecium, enlarged from the bottom of Figure 3a. Scale bar = 1 mm. c. Detailed view of the tip of the flower bud shown in Figure 3a. Note the textures on different petals (1-3). Scale bar = 0.5 mm. d. Detailed view of the gynoecium shown in Figure 3b, shown broken ovary wall and exposed internal details in the gynoecium. Scale bar = 0.1 mm.
Figure 3. SEM of Archaebuda cretaca sp. nov. a. General view of the specimen. Possible androecium is marked with white triangles. Scale bar = 5 mm. b. Detailed view of the gynoecium, enlarged from the bottom of Figure 3a. Scale bar = 1 mm. c. Detailed view of the tip of the flower bud shown in Figure 3a. Note the textures on different petals (1-3). Scale bar = 0.5 mm. d. Detailed view of the gynoecium shown in Figure 3b, shown broken ovary wall and exposed internal details in the gynoecium. Scale bar = 0.1 mm.
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Table 1. Comparison between Archaebuda lingyuanensis and A. cretaca.
Table 1. Comparison between Archaebuda lingyuanensis and A. cretaca.
Archaebuda lingyuanensis Archaebuda cretaca
Stalk 15 mm long Not preserved
Length of bud 16 mm 20 mm
Width of bud 9 mm 9 mm
Foliar appendages type I, width 3 mm 1.1-1.2 mm
Foliar appendages type I, length 2.6 mm 2.9-3.5 mm
Foliar appendages type II, width 4.1-6.7 mm 3.6-4.6 mm
Foliar appendages type II, length 4.8-16.8 mm 6.4-18 mm
Androecium Not visible Possible
Gynoecium Not visible Present
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