Research Article
Print
Research Article
Angiopteris nodosipetiolata (Marattiaceae), a new fern species from Yunnan, China
expand article infoTing Wang‡, Tuo Yang§, Jin-Guo Zhang|, Gui-Liang Zhang, Shi-Wei Yao#, Jian-Ying Xiang¤, Yue-Hong Yan«, Hong-Feng Chen‡
‡ South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China
§ Fairy Lake Botanical Garden, Shenzhen & Chinese Academy of Sciences, Shenzhen, China
| Protection Bureau of Gulinqing Nature Reserve, Maguan, China
¶ Hekou Branch of Management and Protection Bureau of Daweishan National Nature Reserve, Hekou, China
# Institute of Botany, Chinese Academy of Sciences in Jiangsu (Nanjing Mem. Sun Yat-Sen Botanical Garden), Nanjing, China
¤ Southwest Forestry University, Kunming, China
« Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, The Orchid Conservation and Research Centre of Shenzhen, Shenzhen, China

Corresponding author: Yue-Hong Yan ( yan.yh@126.com )

Corresponding author: Hong-Feng Chen ( h.f.chen@scbg.ac.cn )

Academic editor: Joel Nitta
© 2024 Ting Wang, Tuo Yang, Jin-Guo Zhang, Gui-Liang Zhang, Shi-Wei Yao, Jian-Ying Xiang, Yue-Hong Yan, Hong-Feng Chen.
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.
Citation: Wang T, Yang T, Zhang J-G, Zhang G-L, Yao S-W, Xiang J-Y, Yan Y-H, Chen H-F (2024) Angiopteris nodosipetiolata (Marattiaceae), a new fern species from Yunnan, China. PhytoKeys 241: 177-189. https://doi.org/10.3897/phytokeys.241.115175
Open Access

Abstract

Angiopteris nodosipetiolata Ting Wang tris, H.F.Chen & Y.H.Yan, a new fern of Marattiaceae, is described and illustrated. Morphologically, A. nodosipetiolata is similar to A. chingii with more than one naked pulvinus on the stipe and numerous jointed hairs on the undersides of the mature pinnae. However, the pinnae of A. nodosipetiolata are lanceolate and can reach up to 4–6 pairs, whereas they are elliptic and occur in 2–3 pairs in A. chingii. Phylogenetic and genetic distance analysis, based on the plastid genomes, also indicates that A. nodosipetiolata is not closely related to A. chingii. Currently, there are ca. 500 mature individuals in Gulinqing Nature Reserve and we suggest A. nodosipetiolata should be categorised as an Endangered (EN) species according to the criteria of IUCN.

Key words

Marattioid ferns, plastid genome, taxonomy, Wenshan

Introduction

Angiopteris Hoffmann (1796: 29), an early lineage of ferns, was initially established, based on A. evecta (Forster 1786: 81) Hoffmann (1796: 12). Currently, it includes other genera such as Archangiopteris Christ & Giesenhagen (1899: 72), Macroglossum Copeland (1909: 343), Protomarattia Hayata (1919: 88) and Protangiopteris Hayata (1928: 305). Angiopteris is recognised to contain about 53 species (Kew’s Plants of the World Online; https://powo.science.kew.org/taxon/urn:lsid:ipni.org:names:331099-2), but there were over 200 names in this genus in the past (Murdock 2008a). Most species of Angiopteris are widely distributed in southern China (He and Christenhusz 2013) and all are listed as Wild Plants Under State Protection in China (State Forestry and Grassland Administration and the Ministry of Agriculture and Rural Affairs, P. R. China 2021).

In August 2022, during a survey of the Angiopteris in south-eastern Yunnan, a particular fern caught our attention. Morphologically, it was similar to A. chingii J. M. Camus (1989: 35) with more than one naked pulvinus on the stipe and numerous joint-like hairs on the undersides of the mature pinnae. However, its laminar characteristics appeared to be closely related to A. latipinna (Ching) Z. R. He, W. M. Chu & Christen. (2013: 85) and A. subrotundata (Ching) Z. R. He & Christenhusz (2013: 85). After consulting Flora of China (He and Christenhusz 2013), related literature (Ching 1958) and online information from CVH (www.cvh.ac.cn), The Plant List (www.theplantlist.org) and Tropicos (www.tropicos.org) for all the known species of Angiopteris, we confirmed that the collection represents an undescribed species. Therefore, we described it here as Angiopteris nodosipetiolata sp. nov.

Materials and methods

Morphological analysis

Field observations were conducted in China starting in 2022. Observation of herbarium specimens were carried out at KUN, PE and PYU and the voucher specimens of Angiopteris nodosipetiolata were deposited at IBSC, CSH and SWFU. Petiole scales and the hairs on the pinnae surface were observed using an OLYMPUS-SZ61 stereoscopic microscope and an OLYMPUS-BX43 biological microscope. The ornamentation of spores was examined with a JSM-6360LV Scanning Electron Microscope.

Taxon sampling, DNA extraction and sequencing

In this study, five new Angiopteris plastomes were sequenced and completely assembled. Detailed information on the samples is provided in Table 1. All leaf samples were frozen in liquid nitrogen and stored at −80 °C. Total DNA was extracted from the leaves using a modified CTAB method and sequenced using short reads produced by the NovaSeq 6000 platform (2 × 150 bp) by Novogene (Beijing, China).

Table 1.
Download as
CSV
XLSX

List of vouchers used in this study.

GenBank No. Collection No. Species Locality Genome size (bp) LSC (bp) SSC (bp) IR (bp) GC(%)
PP056124 GLQ-1 A. nodosipetiolata China, Yunnan, Maguan 152,964 89,931 20,563 21,235 35.50%
PP056123 GLQ-2 A. nodosipetiolata China, Yunnan, Maguan 152,963 89,932 20,561 21,235 35.50%
PP056126 YYH16228-1 A. chingii China, Yunnan, Hekou 152,551 89,917 20,564 21,035 35.50%
PP056122 YYH22077 A. chingii China, Yunnan, Hekou 152,551 89,929 20,564 21,029 35.50%
PP056125 YYH16502 A. latipinna China,Yunnan, Pingbian 153,597 89,925 20,562 21,555 35.50%

Plastome assembly and annotation

The raw data of each sample were quality-filtered using FastQC 0.11.9 (Andrews 2010) with default parameters. The resulting high-quality, paired-end reads were assembled into contigs using GetOrganelle pipeline (https://github.com/Kinggerm/GetOrganelle) with the parameters set as R (Maximum extension rounds) = 15 and k (kmers) = 75, 85, 95, 105. The assembled plastomes were visually inspected and edited using Bandage (Wick et al. 2015), then a complete circular plastome was generated for each sample. The annotation of plastomes was performed using PGA (Plastid Genome Annotator; Qu et al. (2019)) with Angiopteris angustifolia (NC_026300 and KP099647), Marattia laxa (NC_051979), Danaea sellowian (NC_051976) and Eupodium kaulfussii (NC_051977) as reference plastomes and then visually inspected and edited by hand where necessary in Geneious v.11.1.5 (Kearse et al. 2012).

Phylogenetic analyses

In this study, we analysed the phylogenetic relationship of 15 Angiopteris species by combining newly-obtained data with publicly available complete plastome data from the National Center for Biotechnology Information (NCBI; https://www.ncbi.nlm.nih.gov/). To reduce the effect of different plastid regions on phylogenetic inference, we constructed the phylogeny of Angiopteris, based on the complete plastid genome sequences and coding sequences (CDS). Firstly, we used Homblocks (Bi et al. 2018) to automatically recognise locally collinear blocks and excavate core conserved fragments (protein coding genes, conserved non-coding regions and rRNA genes) amongst complete plastid genomes; these were used as “complete plastomes” for phylogenetic analysis (note that these therefore were shorter than the complete sequenced plastomes in Table 1). Next, we used the “get_annotated_regions_from_gb.py” script (https://github.com/Kinggerm/PersonalUtilities/) to extract 84 CDSs from all plastid genomes and used MAFFT v.7.475 (Katoh and Standley 2013) and trimAl (Capella-Gutiérrez et al. 2009) for alignment and trimming.

We used Maximum Likelihood (ML) and Bayesian Inference (BI) methods for phylogenetic construction. The best-fit model of evolution of ML and BI methods were selected by ModelTest-NG (Darriba et al. 2020) under the Bayesian Information Criterion (BIC) with “ -T raxml” and “-T mrbayes” parameters, respectively. ML analyses were conducted with RAxML v.8.2.10 (Stamatakis 2014) and node support was assessed using rapid bootstrap (RBS) analysis with 1000 pseudo-replicates. BI analyses were constructed with MrBayes v.3.2 (Ronquist et al. 2012), using ten million generations and sampling trees every 1000 generations. Two runs each with three heated and one cold chain were performed in parallel. Each chain started with a random tree and the first 25% of sampled generations were discarded as burn-in to construct a majority-rule consensus tree and estimate the posterior probabilities (PP). The convergence of runs was assumed when the average standard deviation of split frequencies dropped below 0.01 according the MrBayes manual.

Genetic distance estimation

The intraspecific genetic distances for both complete plastomes and 84 CDSs of Angiopteris nodosipetiolata were calculated using the two-parameter (K2P) model in MEGA 11.0 (Tamura et al. 2021). We also computed interspecific genetic distances between A. nodosipetiolata and three morphologically similar species, A. latipinna, A. subrotundata and A. chingii. Subsequently, the “ggplot2” (Wickham 2011) and “ggpubr” (https://rpkgs.datanovia.com/ggpubr/) package in R was employed to analyse and visualise potential significant differences between the intraspecific and interspecific genetic distances using the Wilcoxon test.

Results

Characteristics of Angiopteris plastomes

All newly-sequenced plastomes were assembled completely and can be accessed from GenBank (Table 1). All five newly-sequenced Angiopteris plastome sizes ranged from 152,551–153,597 bp. They were composed of an LSC region (89,917–89,932 bp), SSC region (20,561–20,564 bp) and two IR copies (21,029–21,555 bp), with 84 unique genes. Overall G/C content was almost identical across the samples (35.50%).

Phylogenetic relationships within Angiopteris

Complete plastid genomes and 84 CDSs were each used to construct phylogenetic relationships. These had total lengths of 110,566/71,779 bp, amongst which, there were 358/199 bp, 1,012/512 bp and 109,196/71,068 bp of parsimony-informative sites, singleton sites and constant sites, respectively (Table 2). Phylogenetic relationships derived from different regions displayed identical topologies in both Bayesian Inference (BI) and Maximum Likelihood (ML) trees (Fig. 1). The results indicated that specimens of the newly-discovered species, Angiopteris nodosipetiolata, form a monophyletic group with high support (RBS = 100/99, PP = 1/1) and this was recovered as sister to A. danaeodes, rather than a close relative of A. latipinna, A. subrotundata or A. chingii.

Table 2.
Download as
CSV
XLSX

The detailed parameters for the phylogenetic tree construction.

Region Total sites (bp) parsimony-informative sites(bp) singleton sites(bp) constant sites(bp) Method Best-fit model Likelihood/AvgStdDev
Complete plastomes 110,566 358 1,012 109,196 RAxML GTR+I+G4 -159,782.61
Mrbayes GTR+I+G4 0.000327
CDSs 71,779 199 512 71,068 RAxML GTR+I+G4 -103,156.87
Mrbayes GTR+I+G4 0.001325
Figure 1. 

Maximum Likelihood and Bayesian Inference tree of Angiopteris species, based on (A) complete plastid genome sequences and (B) 84 CDSs. Maximum Likelihood bootstrap support (RBS) and Bayesian Inference posterior probability (PP) are given above the branches. NA: written abbreviation for not available, used to show the sampling site cannot be provided.

Genetic Distance within Angiopteris

The genetic distances between A. nodosipetiolata and three Angiopteris species ranged from 0.0005881 to 0.0010409 for complete plastid genome and from 0.0005296 to 0.0009341 for 84 CDSs. In contrast, the intraspecific genetic distances amongst A. nodosipetiolata sequences were notably smaller, measuring 0.0000452 for complete plastid genome and 0.0000697 for 84 CDSs. These intraspecific distances within A. nodosipetiolata were significantly smaller (P < 0.01) than the distances observed between A. nodosipetiolata and A. latipinna, A. subrotundata or A. chingii (Fig. 2).

Figure 2. 

Intraspecific and interspecific genetic distance of Angiopteris nodosipetiolata.

Taxonomic treatment

Angiopteris nodosipetiolata Ting Wang tris, H.F.Chen & Y.H.Yan, sp. nov.

urn:lsid:ipni.org:names:77340978-1
Figs 3, 4

Holotype

China. Yunnan: Maguan County, Gulinqing Village, ca. 1400 m elev., 26 Aug 2022, Ting Wang, YYH16537 (holotype: IBSC [1010884!]).

Figure 3. 

Angiopteris nodosipetiolata Ting Wang tris, H.F.Chen & Y.H.Yan A, B habitat C, D, E lamina F portion of stipes showing pulvini G rhizome H, I sporangia J pinnae backside, showing a dense covering of hairs K exospores L petiole scales.

Diagnosis

Angiopteris nodosipetiolata is morphologically quite similar to A. chingii J.M. Camus in terms of having more than one naked pulvinus on the stipe and numerous joint-like hairs on the undersides of the mature pinnae. However, the former’s pinnae are lanceolate, occurring in 4–6 pairs, in contrast with the elliptical pinnae of the latter, which consist of only 2–3 pairs. Judging from the shape of laminae, A. nodosipetiolata also closely resembles A. latipinna (Ching) Z. R. He, W. M. Chu & Christenh. and A. subrotundata (Ching) Z. R. He & Christenh. Nonetheless, these two species exhibit only one naked pulvinus on the stipe and the surfaces of their mature pinnae, apart from the mid-rib, are smooth and hairless (Table 3). The phylogenetic and genetic distance analysis also showed that A. nodosipetiolata is not the closest relative of A. latipinna, A. subrotundata or A. chingii (Figs 1, 2).

Table 3.
Download as
CSV
XLSX

Morphological comparison of Angiopteris nodosipetiolata and its similar taxa.

Characters A. nodosipetiolata A. chingii A. latipinna A. subrotundata
Frond 70–120 cm 50–85 cm 40–85 cm 50–120 cm
Stipe 40–70 cm ca. 50 cm 30–60 cm 18–70 cm
Rhizome long creeping long creeping long creeping long creeping
Pulvinus of stipe 2–3 4–5(–7) 1 1
Scales of stipe brown, lanceolate brown, lanceolate brown, lanceolate Reddish-brown, linear ciliate
Laminae laminae once pinnate, pinnae 4–6 pairs, lanceolate, 15–20 × 3.5–4.5 cm laminae once pinnate, pinnae 2–3 pairs, elliptic, 15–20 × 5–7 cm laminae once pinnate, pinnae 2–4 pairs, lanceolate, 17–30 × 4.5–6.5 cm laminae once pinnate, pinnae 4–6 pairs, lanceolate, 10–30 × 4.5–7.5 cm
Hairs on the undersides of the mature pinnae densely covered with jointed hairs densely covered with jointed hairs absent absent
Sori sori medial, yet closer to the main vein, 0.5–1.8 cm, composed of up to 120 sporangia sori medial, 3–3.5 cm, with 160–240 sporangia sori medial, 0.5–2 cm, composed of up to 160 sporangia sori medial, 0.3–2 cm, composed of up to 160 sporangia
Exospores with forked ornamentation with forked ornamentation with forked ornamentation with forked ornamentation
References / Ching (1958) Ching (1958); He and Christenhusz (2013) Ching (1958); He and Christenhusz (2013)
Figure 4. 

Holotype of Angiopteris nodosipetiolata (Ting Wang, IBSC [1010884!]).

Description

Plants terrestrial, 70–120 cm tall. Rhizomes long creeping. Stipes 40–70 cm long, 0.7–1.5 cm in diam., with 2–3 naked pulvini (occasionally with 1); stipe scales peltate, brown, lanceolate, margins with hair-like outgrowths, apex acuminate, cells clathrate and elongate. Laminae 35–50 × 25–30 cm; once pinnate, pinnae 4–6 pairs, lanceolate, ca. 15–20 × 3.5–4.5 cm, bases round-cuneate, margins coarsely dentate, apices caudate, densely covered with jointed hairs on the undersides of the mature pinnae. Veins free, simple or bifurcate, false veins absent. Sori medial, yet closer to the main vein, ranging in length from ca. 0.5 cm on the basal pinnae to ca. 1.8 cm in the middle pinnae. Exospores with forked rod-like ornamentation.

Additional specimens examined

(paratypes; all have the same locality as the holotype): CHINA. Yunnan: Maguan County, Gulinqing Village, ca. 1400 m elev., 27 Sept 2023, Gui-Liang Zhang, GLZ-2023001 (CSH!), GLZ-2023002 (IBSC [1010885!]); CHINA. Yunnan: Maguan County, Gulinqing Village, ca. 1400 m elev., 17 July 2023, Ting Wang, GLQ-1 (SWFU!), GLQ-2 (CSH!).

Geographical distribution

Currently, Angiopteris nodosipetiolata is only found in Gulinqing Nature Reserve of Yunnan Province based on our current knowledge and may represent a species endemic to Yunnan, China.

Ecology

Angiopteris nodosipetiolata is observed at the edge of montane forests, growing at an elevation of approximately 1400 m.

Etymology

The species exhibits 2–3 naked pulvini (nodos-) on the stipe (-petiolata).

Vernacular name

瘤柄观音座莲 (liu bing guan yin zuo lian).

Conservation status

There are ca. 500 mature individuals of Angiopteris nodosipetiolata has been found at the type locality and it thrives in forest edge areas that are susceptible to human disturbance. The status of the new species should be classified as Endangered (EN), based on current information and following the International Union for Conservation of Nature and Natural Resources guidelines. In addition, it should be listed and protected as second grade Wild Plants Under State Protection like all other taxa in Angiopteris.

Discussion

Cryptic species are phenotypically highly similar species (Struck and Cerca 2019), but which represent distinct evolutionary lineages (Mayo 2022). In recent years, an increasing number of cryptic species that were hidden in plain sight have been unveiled, driven in part by the rise of DNA barcoding (Ni et al. 2012; Tyagi et al. 2019; Labe et al. 2022; Takenaka et al. 2023). Notable groups that include cryptic species encompass organisms like Isoetes Linnaeus (1753: 1100; Gu et al. (2022)), Ceratopteris Brongn. (1822: 186; Yu et al. (2021)) and jellyfish (Moura et al. 2023). Angiopteris nodosipetiolata shares a remarkable morphological resemblance with A. chingii, like the presence of more than one naked pulvinus on the stipe and numerous jointed hairs on the undersides of the mature pinnae (Ching 1958; He and Christenhusz 2013). This likeness renders A. nodosipetiolata susceptible to potential misidentification as A. chingii. Upon re-examining the morphological characteristics of A. nodosipetiolata and A. chingii, the pinnae morphology (lanceolate vs. elliptic) and the arrangement of pinna pairs (4–6 vs. 2–3) can serve as distinguishing characteristics (Table 3). Besides, a deeper insight obtained from phylogenetic analysis in plastid genomes also provides a new perspective (Figs 1, 2). Contrary to expectations of a close relationship with A. latipinna, A. subrotundata and A. chingii, A. nodosipetiolata is considered the sister clade to A. danaeodes. The distinguishing feature is that A. danaeodes has only one naked pulvinus on the stipe, pinnae 2–3 pairs and the surfaces of their mature pinnae, apart from the mid-rib, are smooth and hairless. In contrast, A. nodosipetiolata has more than one naked pulvinus on the stipe and numerous joint-like hairs on the undersides of the mature pinnae.

Relying on macroscopic morphological classification in the past has frequently resulted in treating groups with subtle morphological differences as a single species due to subjective interpretations of morphology (Gu et al. 2022). For instance, Didymochlaena Desvaux (1811: 303) was historically considered to contain only one (PPG I 2016) or six species (Shang et al. 2020), based on morphological characters, while a recent study utilising morphological and molecular variation has identified 22 species within the genus (Shang et al. 2023), marking a threefold increase in the previously known number of species. Similarly, Ptisana soluta (Compton) Murdock & Perrie (2023:53), a member of the Marattiaceae, was long regarded as the widespread South Pacific species P. salicina (Sm.) Murdock (2008b: 746) in New Caledonia. However, a recent study, based on sequence data and morphology, suggested it to be an endemic species with a vulnerable conservation ranking (Shepherd et al. 2023). Thus, integrating research results from morphological classification, molecular systematics, ecology and other fields, holds significant guiding significance for the rapid and accurate identification of cryptic species (Kabus et al. 2023; Meghana et al. 2023).

Conclusion

Utilising interdisciplinary approaches to investigate species boundaries forms the foundation for the proper understanding, conservation and utilisation of biodiversity resources. Whether in natural reserves or in urban and rural areas with frequent human activity, it is believed that there are additional undiscovered groups, akin to the Angiopteris nodosipetiolata. We hope that these groups are not lost to extinction before humanity can gain a comprehensive understanding of them.

Key to the species with once pinnate laminae of Angiopteris

1 Naked pulvini 2–5 (7) per stipe 2
– Naked pulvinus only 1 per stipe 3
2 Pinnae 4–6 pairs, lanceolate A. nodosipetiolata
– Pinnae 2–3 pairs, elliptic A. chingii
3 Synangium, ca. 4–6 mm A. tonkinensis
– Sporangia are independent of each other, ca. 0.5–2 cm 4
4 Sorus near margin A. cadieri
– Sours medial 5
5 Exospore with spinose ornamentation A. subrotundata
– Exospore with rod-like ornamentation 6
6 Pinnae opposite or alternate, margins of pinnules dentate 7
– Pinnae clearly alternate, margins of pinnules entire or undulate, crenate towards apex 8
7 Pinnule apices long caudate A. danaeodes
– Pinnule apices acuminate A. tamdaoensis
8 Pinnae elliptic A. latipinna
– Pinnae oblanceolate A. somae

Acknowledgements

The authors express their gratitude to Ms. Xiao-Ying Hu (South China Botanical Garden) for her assistance with exospore photography.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

This study was funded by the National Natural Science Foundation of China (NSFC) to Ting Wang (32300180), Guangdong Basic and Applied Basic Research Foundation (2021A1515010920), Research and Development of Key Field in Guangdong (2020B1111530004) and the Project for Wild Plant Conservation and Management of State Forestry and Grassland Administration (20190730).

Author contributions

TW: paper writing, plant identification and examination. TY: paper review and editing. TW, JGZ, GLZ, SWY and JYX: investigation. HFC and YYH: funding acquisition and conceptualisation.

Author ORCIDs

Ting Wang https://orcid.org/0000-0002-8622-5459

Tuo Yang https://orcid.org/0000-0002-2147-2475

Gui-Liang Zhang https://orcid.org/0000-0003-0501-7533

Jian-Ying Xiang https://orcid.org/0000-0001-8398-7119

Yue-Hong Yan https://orcid.org/0000-0003-3911-4868

Hong-Feng Chen https://orcid.org/0000-0002-8415-3260

Data availability

All of the data that support the findings of this study are available in the main text.

References

  • Bi GQ, Mao YX, Xing QK, Cao M (2018) HomBlocks: A multiple-alignment construction pipeline for organelle phylogenomics based on locally collinear block searching. Genomics 110: 18–22. https://doi.org/10.1016/j.ygeno.2017.08.001
  • Camus JM (1989) The limits and affinities of Marattialean fern genera in China and the west Pacific. Proceedings of the International Symposium on Systematic Pteridology, 34–35.
  • Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25(15): 1972–1973. https://doi.org/10.1093/bioinformatics/btp348
  • Ching RC (1958) Icones Filicarum Sinicarum Vol. 5. Science Press, Beijing, 27–63.
  • Christ H, Giesenhagen K (1899) Pteridographische Notizen. 1. Archangiopteris nov. gen. Marattiacearum. Flora 86: 72–79.
  • Copeland EB (1909) New genera and species of Bornean ferns. Philippine Journal of Science 3: 343.
  • Darriba D, Posada D, Kozlov AM, Stamatakis A, Morel B, Flouri T (2020) ModelTest-NG: A new and scalable tool for the selection of DNA and protein evolutionary models. Molecular Biology and Evolution 37(1): 291–294. https://doi.org/10.1093/molbev/msz189
  • Desvaux NA (1811) Observations sur quelques nouveaux genres de fougères et sur plusieures espéces nouvelles de la même famille. Magazin für die Neuesten Entdeckungen in der Gesammten Naturkunde, Gesellschaft Naturforschender Freunde zu Berlin 5: 297330.
  • Hayata B (1919) Protomarattia, A new genus of Marattiaceae, and Archangiopteris. Botanical Gazette (Chicago, Ill. ) 67(1): 84–92. https://doi.org/10.1086/332399
  • He ZR, Christenhusz MJM (2013) Marattiaceae. In: Wu ZY, Raven PH, Hong DY (Eds) Flora of China Vol. 2–3. Science Press, Beijing, Missouri Botanical Garden Press, St. Louis, 82–89.
  • Hoffmann GF (1796) Descriptiones et icons plantarum. Commentationes Societatis Regiae Scientiarum Gottingensis 12: 22–37.
  • Kabus J, Cunze S, Dombrowski A, Karaouzas I, Shumka S, Jourdan J (2023) Uncovering the Grinnellian niche space of the cryptic species complex Gammarus roeselii. PeerJ 11: e15800. https://doi.org/10.7717/peerj.15800
  • Katoh K, Standley DM (2013) MAFFT Multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution 30(4): 772–780. https://doi.org/10.1093/molbev/mst010
  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12): 1647–1649. https://doi.org/10.1093/bioinformatics/bts199
  • Labe O, Picart N, Francisco M, Castillo RM, Quilang J (2022) DNA barcoding of Glossogobius species (Teleostei: Gobiidae) from major lakes in the Philippines reveals the presence of cryptic species and species complexes. Conservation Genetics Resources 14(3): 1–12. https://doi.org/10.1007/s12686-022-01278-z
  • Linnaeus C (1753) Species Plantarum 2. Impensis Laurentii Salvii, Holmiae [Stockholm], 561–1200.
  • Mayo SJ (2022) Cryptic species: A product of the paradigm difference between taxonomic and evolutionary species. In: Monro AK, Mayo SJ (Eds) Cryptic Species: Morphological Stasis, Circumscription, and Hidden Diversity. Systematics Association Special Volume Series. Cambridge University Press, Cambridge, 14–35. https://doi.org/10.1017/9781009070553.002
  • Meghana R, Anand PP, Vardhanan YS (2023) Molecular and morphometric analyses reveal host-specific cryptic speciation in a mite species, Tetranychus neocaledonicus (Andre, 1933) (Acari: Tetranychidae). Zootaxa 5306(1): 61–96. https://doi.org/10.11646/zootaxa.5306.1.3
  • Moura C, Magalhães B, Gonçalves J (2023) DNA barcoding of moon jellyfish (Cnidaria, Scyphozoa, Ulmaridae, Aurelia): Two cryptic species from the Azores (NE Atlantic, Macaronesia), and evaluation of the non-indigenous species (NIS). Diversity 15(3): 323. https://doi.org/10.3390/d15030323
  • Murdock AG (2008a) Phylogeny of marattioid ferns (Marattiaceae): Inferring a root in the absence of a closely related outgroup. American Journal of Botany 95(5): 626–641. https://doi.org/10.3732/ajb.2007308
  • Murdock AG (2008b) A taxonomic revision of the eusporangiate fern family Marattiaceae, with description of a new genus Ptisana. Taxon 57(3): 737–755. https://doi.org/10.1002/tax.573007
  • Ni L, Kong L, Huang S, Li L (2012) DNA barcoding and phylogeny in the family Mactridae (Bivalvia: Heterodonta): Evidence for cryptic species. Biochemical Systematics and Ecology 44: 164–172. https://doi.org/10.1016/j.bse.2012.05.008
  • PPG I (2016) A community-derived classification for extant lycophytes and ferns. Journal of Systematics and Evolution 54(6): 563–603. https://doi.org/10.1111/jse.12229
  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61(3): 539–542. https://doi.org/10.1093/sysbio/sys029
  • Shang H, Xue ZQ, Liang ZL, Kessler M, Pollawatn R, Lu NT, Gu YF, Fan XP, Tan YH, Zhang L, Zhou XM, Wan X, Zhang LB (2023) Splitting one species into 22: an unusual tripling of molecular, morphological, and geographical differentiation in the fern family Didymochlaenaceae (Polypodiales). Cladistics 39: 273–292. https://doi.org/10.1111/cla.12539
  • Shepherd L, Murdock A, Amice R, Perrie L (2023) A synopsis of Ptisana Murdock ferns (Marattiaceae) in New Caledonia based on sequence data and morphology with the recognition of a new vulnerable species, P. soluta (Compton) Murdock & Perrie, comb. nov., stat. nov. Adansonia 45: 41. https://doi.org/10.5252/adansonia2023v45a3
  • State Forestry and Grassland Administration and the Ministry of Agriculture and Rural Affairs P. R. China (2021) List of Wild Plants Under State Protection. Decree No.15. https://www.forestry.gov.cn/search/272693 [In Chinese] [accessed 08.09.2021]
  • Takenaka M, Yano K, Suzuki T, Tojo K (2023) Development of novel PCR primer sets for DNA barcoding of aquatic insects, and the discovery of some cryptic species. Limnology 24(2): 121–136. https://doi.org/10.1007/s10201-022-00710-5
  • Tyagi K, Kumar V, Kundu S, Pakrashi A, Prasad P, Caleb J, Chandra K (2019) Identification of Indian Spiders through DNA barcoding: Cryptic species and species complex. Scientific Reports 9(1): 1–13. https://doi.org/10.1038/s41598-019-50510-8
  • Yu JH, Zhang R, Liu QL, Wang FG, Yu XL, Dai XL, Liu YB, Yan YH (2021) Ceratopteris chunii and Ceratopteris chingii (Pteridaceae), two new diploid species from China, based on morphological, cytological, and molecular data. Plant Diversity 44(3): 300–307. https://doi.org/10.1016/j.pld.2021.10.002
login to comment