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Research Article
Parartemiopsis shangrilaensis, a new species of fairy shrimp (Branchiopoda, Anostraca) from Yunnan, with a key to the Chirocephalidae of China
expand article infoShu-Sen Shu‡§|, Xiao-Yong Chen‡§, D. Christopher Rogers, Laorsri Sanoamuang|
‡ Southeast Asia Biodiversity Research Institute, Chinese Academy of Sciences, Yezin, Myanmar
§ State Key Laboratory of Genetic Resources and Evolution and Yunnan Key Laboratory of Biodiversity Conservation of Gaoligong Mountain, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China
| Khon Kaen University, Khon Kaen, Thailand
¶ The University of Kansas, Lawrence, United States of America

Corresponding author: D. Christopher Rogers ( branchiopod@gmail.com )

Corresponding author: Laorsri Sanoamuang ( la_orsri@kku.ac.th )

Academic editor: Kay Van Damme
© 2023 Shu-Sen Shu, Xiao-Yong Chen, D. Christopher Rogers, Laorsri Sanoamuang.
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: Shu S-S, Chen X-Y, Rogers DC, Sanoamuang L (2023) Parartemiopsis shangrilaensis, a new species of fairy shrimp (Branchiopoda, Anostraca) from Yunnan, with a key to the Chirocephalidae of China. ZooKeys 1168: 355-366. https://doi.org/10.3897/zookeys.1168.104005
ZooBank: urn:lsid:zoobank.org:pub:D8C5907B-F728-4BC6-83E8-A7B3B6C27345
Open Access

Abstract

The fairy shrimp genus Parartemiopsis Rogers, 2005 currently contains a single species reported from Russia and Mongolia. In 2013, an unidentified Parartemiopsis population was reported from the eastern margin of the Tibetan Plateau in China’s Yunnan Province, from Patatson National Park in Shangri-La County. Here, we describe the Chinese populations as a new species, Parartemiopsis shangrilaensis sp. nov. This new species is distinguished from its congener, P. longicornis (Smirnov, 1930), by the form of the male second antennae and the gonopod. The discovery of P. shangrilaensis sp. nov. extends the known distribution of the genus, and more Parartemiopsis species may be found in the future. We present a key to the genera and species of Chirocephalidae in China as an aid to future research.

Key words

Asia, crustacean, diversity, freshwater, taxonomy, Tibetan Plateau

Introduction

Chirocephalidae is the second largest anostracan family in terms of numbers of species, but it contains the most genera (Belk and Brtek 1995; Rogers et al. 2013). The family contains nine genera, with all but one species (Chirocephalus hardingi Brtek, 1965 from Bali) distributed entirely in the Holarctic. Parartemiopsis Rogers, 2005 was erected (Rogers 2005, 2006) to contain Chirocephalus longicornis (Smirnov, 1930). Rogers (2005, 2006) demonstrated that this species warranted a separate genus and was morphologically closer to Artemiopsis Sars, 1897 than to Chirocephalus Prévost, 1803.

An unidentified Parartemiopsis population was reported from Yunnan Province (Shu et al. 2013) in a list of crustaceans from Patatson National Park. More material was collected and is described here as a new species. A key to the species in the genus is presented, along with a key to the Chirocephalidae of China. It is our hope that this key will further future studies on the Chirocephalidae of this region.

Materials and methods

Specimens were collected from Patatson National Park in 2012 and 2019 using a dip net. Specimens were preserved on site in 95% alcohol. Specimens were examined in the laboratory under a stereomicroscope (Zeiss Stemi 508 and Wild M8) and a compound microscope (Olympus CX31). For scanning electron microscopy (SEM), specific structures were dissected from individual specimens and put into a 2.5% glutaraldehyde solution for 24 h, washed for 30 min three times with 0.01 M phosphate buffered saline, transferred to a 1% osmic acid solution for 2 h, then washed three times for 30 min each with 0.01 M phosphate buffered saline. Next, the material was treated in an ethanol gradient dehydration series at 30%, 50%, 70%, 80%, 90%, 95%, and 100% for 20 min. The specimens were then put into tertiary butyl alcohol at 40 °C for 2 h and frozen at −20 °C. The material was then freeze-dried in a JFD-310 freeze dryer. Later, the specimens were mounted on stubs and coated with gold in a JFC-1600 sputter coater. SEM images were taken using a TM 1000 Hitachi scanning electron microscope at 10 kV. The pictures were collaged in Photoshop CS.

Terminology follows Rogers (2005, 2006) and Rogers and Soufi (2015). Examined specimens are deposited in the Kunming Natural History Museum, the Kunming Institute of Zoology (KIZ), Chinese Academy of Sciences.

Results

Parartemiopsis Rogers, 2005

Parartemiopsis Rogers 2006, 2013.

= Pristicephalus pro partim in Smirnov 1930; Brtek 1958.

= Chirocephalus pro partim in Brtek 1966, 1967, 1997, 2002; Belk and Brtek 1995.

Diagnosis

(modified from Rogers 2006). Male genital segments expanded. Entire gonopod basal portion chitinized. Gonopod basal portion bearing a broad lamellar ventral process, originating anterior to gonopod base. Gonopod laterally with tubercle. Gonopod distal eversible portion not cirriform, bearing a few scattered denticles.

Parartemiopsis shangrilaensis sp. nov.

https://zoobank.org/5062BFD3-2DC9-4C8F-B3E7-787B458BFCFF
Figs 1A –D, 2A –F, 3A –L, 4, 5A –O

= Parartemiopsis sp. Shu et al. 2013.

Type materials

Holotype : one male in alcohol, KIZ–CR-2011010. Allotype: one female in alcohol, KIZ–CR-2011011.

Type locality

China: Yunnan Province: Shangri-La County: Patatson National Park: 27°52′2″N, 99°58′58″E, 3670 m a.s.l., a small, shallow temporal pond in Militang meadow; 20 August 2011; Shu S-S, Jiang W-S, and Zhao Y-P leg. Militang meadow is in an alpine valley surrounded by mountains covered in coniferous forest. A small river winds through the valley, which receives runoff from the surrounding slopes. The meadow has a mosaic of wetlands and uplands. This species is so far only known from the type locality.

Additional materials examined

Same data as types: one male, six females; 20 August 2011. Same location data as types: 10 males, 48 females; 16 August 2019; Jiang W-S, leg.

Similar species

Parartemiopsis longicornis (Smirnov, 1930).

Diagnosis

Typical for genus. Male antennal appendage lamellar, subtriangular, apically subacute (Fig. 3E). Second antenna proximal antennomere lacking lateral hemispherical bulge. Second antenna distal antennomere medial surface with subproximal rounded protrusion covered in spinulae (Fig. 3H). Genital segment medial lamellar projection with medial longitudinal lines of spinulae elevated on crests (Fig. 3K).

Description

Average length (head anterior margin to telson posterior margin): 7.4 mm (range 6.2–8.7 mm) in males; 7.9 mm (range 6.2–10.2 mm) in females.

Holotype male. Body red or jacinth in life (Fig. 1C). Head typical for genus. Eye plus peduncle length subequal to first antenna length. Eye large, width >0.2× second antennal proximal antennomere medial width. First antenna long, filiform, extending to second antennae distal antennomere midlength, apex with five or six aesthetascs.

Figure 1. 

Parartemiopsis shangrilaensis sp. nov. A type locality in Shangri-La, China (black spot) B environment of the type locality and collection of the specimens C male, lateral view D female, lateral view (photo by W-S Jiang). Scale bars: 2 mm (C, D).

Antennal appendage lamellar, directed anteromedially, apex broadly triangular (Figs 2A, 3E). Appendage basal portion inerm, distal portion bearing conical spinulae arranged in two or three marginal rows. Anterior surface with scattered, large, anteriodistally directed spines. Each anterior surface spine conical, 2–3× lateral spinulae.

Figure 2. 

Parartemiopsis shangrilaensis sp. nov. A–D male E, F female A second antenna, anterior view B thoracopod V, only spines are shown C genital segments, ventral view D genital segments, lateral view E head and detail of second antenna, anterior view F thoracic segments X and XI, and genital thoracic segments, lateral view.

Figure 3. 

Parartemiopsis shangrilaensis sp. nov., male A second antenna posteriolateral view B second antenna proximal antennomere posterior surface detail C second antenna proximal antennomere lateral surface detail and setae D second antenna anterior view E antennal appendage F medial surface detail G second antenna distal antennomere detail H second antenna distal antennomere medial protuberance I second antenna distal antennomere apex J genital segments K uneverted gonopods, ventral view L uneverted gonopods, ventrolateral oblique view.

Second antenna extending to thoracopod IV or V (Fig. 1C). Second antenna proximal antennomere (Fig. 3A) subcylindrical, length nearly 1.5× breadth. Posteriolateral surface with medial patch bearing ~10 setae (Fig. 3B). Lateral surface with rings composed of four or five micropapillae surrounding a single filiform seta (Fig. 3C). Anteromedial surface with denticulae and sparse setae (Fig. 3E). Anterior surface with five or six rows of setae, with groups of scattered micropapillae arranged as on lateral surface (Fig. 3F).

Distal antennomere laterally compressed, length ~1.5× proximal antennomere. Distal antennomere narrowing to medial bend ~70° at proximal third of antennomere length (Figs 2A, 3A, G). Just proximad to bend, medial surface with hemispherical protuberance covered in fine denticulae (Fig. 3A, H). Distal two-thirds parallel-sided with remainder straight to apex which is medially bent ~35° (Fig. 3A). Anterior margin with triangular projection midway between bend and apex. Apex subacute (Fig. 3A, I).

Thoracic segments dorsally smooth (Fig. 1C). Thoracopod I with praeepipodite divided, proximal portion oval, distal portion elongate-oval, both with margins inerm and smooth. Epipodite lamellar, length ~2× width, apex angular. Exopod elongate oval, length < epipodite, proximolateral margin with five spines, remaining margins with plumose setae. Endopod broadly oval, margined with plumose setae. Endite VI broadly rounded, with long plumose marginal setae in two groups, bearing one and two middle submarginal spines, respectively. Endite V semicircular, proximal margin with two spiniform setae, remaining margins with plumose setae. Endites VI and III each with long plumose submarginal setae and three spiniform marginal setae. Endite I + II breadth greater than endites II–VI combined, bearing long plumose submarginal setae and one stout, spiniform marginal seta. Thoracopods II–XI serially homologous (Figs 2B, 4) with respect to thoracopod I, endites III–V margined with two or three spines.

Figure 4. 

Parartemiopsis shangrilaensis sp. nov., thoracopods I–XI. Th = thoracopod. Scale bars: 1 mm.

Genital thoracic segments fused, ventrally expanded. Genital segment I (Fig. 3J) smooth, elongate, with paired longitudinal ventromedial ridges, their combined width approximately half segment width. Genital segment I distal margin with bead.

Gonopod rigid basal portion (Figs 2C, D, 3K) with ventromedial longitudinal lamellar process, projecting posteriorly, with medial and lateral margins inerm, submedially with longitudinal arcuate carina margined with dense, fine denticulae, extending onto oblique distal margin (Fig. 3K, L). Gonopod small, lateral to lamellar process, subcylindrical, posteriorly directed; eversible portion unobserved.

Telson and cercopods as typical for genus. Cercopods margined with plumose setae.

Allotype female. Body reddish brown in life (Fig. 1D). Head smooth (Figs 2E, 5A), first antenna length subequal to second antenna, apex with five or six aesthetascs (Fig. 5B). Second antenna (Figs 2E, 5C) subcylindrical, with scattered, filiform setae, apex tapering to point (Fig. 5D, E). Thoracopods as in male. Thoracic segments X and XI with dorsolateral conical projections, apex spiniform (Figs 2F, 5G–I, L). Genital thoracic segments fused (Fig. 5L). Genital thoracic segments with single dorsolateral sensory seta surrounded by four or five ridges (Fig. 5I–K). Brood pouch extending to abdominal segment II (Fig. 5G), width subequal to thorax (Fig. 5L). Telson and cercopods as in male.

Figure 5. 

Parartemiopsis shangrilaensis sp. nov. female A head, ventral view B first antenna apex C second antenna D second antenna proximal surface setae E second antenna lateral surface setae F labrum apex G distal thoracic segments and brood pouch in left lateral view H thoracic segments X and XI dorsal spines I thoracic segment XI and genital thoracic segment setae J thoracic segment XI seta K genital thoracic segment seta L thoracic segments X, XI and genital thoracic segment in dorsal view M brood pouch proximal part N egg O egg detail.

Egg. Subspherical (Fig. 5N), diameter ~250 μm, with dense ridges ~50 μm wide, rounded in cross section. Ridges lacking spines, rarely closing to form polygons. Ridges separated by deep grooves ≤10 μm wide. Ridges rough, with dense, regularly distributed pores (Fig. 5O).

Etymology

The specific epithet “shangrilaensis” refers to the species being from Shangri-La County. The gender is feminine.

Discussion

Parartemiopsis was erected by Rogers (2005) to accommodate the Mongolian P. mongolica; only two male specimens were known at the time. Shortly after publication, Rogers realised that P. mongolica was a junior synonym of the Russian Chirocephalus longicornis (Smirnov, 1930) (Rogers 2006), which was first described in the now unrecognised Pristicephalus Daday, 1910 and then moved to Chirocephalus (Brtek, 1967). However, the female was never properly described, although mentioned briefly by Smirnov (1930).

The males of both Parartemiopsis species share the basic form of the gonopods and the second antennae. Both share the anterior triangular projection on the distal antennomere. Parartemiopsis shangrilaensis sp. nov. is separated from P. longicornis by the form of the male second antenna. The antennal appendage is lobiform in P. longicornis and lamelliform in P. shangrilaensis sp. nov. The proximal antennomere lateral surface bears a large, medial, hemispherical bulge and a subdistal lobe in P. longicornis, which are absent in P. shangrilaensis sp. nov. The distal antennomere is straight in P. longicornis but curves medially in both the basal third and subapically in P. shangrilaensis sp. nov. In P. shangrilaensis sp. nov. the distal antennomere bears a basomedial, spiny, hemispherical protrusion in which is absent in P. longicornis. The form of the gonopod lamella also differs: it is subrectangular, with the length ~2× the length of the gonopod rigid base in P. shangrilaensis sp. nov., but triangular and subequal in length in P. longicornis. Furthermore, the medial spinulae row is elevated on an arcuate carina in P. shangrilaensis sp. nov., whereas this row is flat in P. longicornis. The female P. longicornis is incompletely known and in need of redescription according to modern standards. However, it appears from Smirnov’s (1930) description that P. longicornis has paired dorsolateral projections on thoracic segments V–X and small lateral spiniform projections on abdominal segments I–V. In contrast, P. shangrilaensis sp. nov. bears paired dorsal spiniform projections only on thoracic segments X and XI, with the abdomen inerm.

There is no information on the egg morphology of P. longicornis.

During fieldwork in 2012, the type locality was dominated by macrophytes, the water temperature was 22.1 °C, with a surface area of approximately 40 m2, and the depth was 0.3 m.

Previously, Parartemiopsis was only known from two locations, one in eastern Mongolia (Rogers 2005) and the other near Xingkai Lake or Khanka Lake (Smirnov 1930), near the border between China and Russia; both locations are in northeast Asia. The type locality of P. shangrilaensis sp. nov. is more than 2000 km from those sites. This new locality greatly enlarges the known distribution of the genus. More Parartemiopsis species may be found in future surveys in Asia.

Key to Parartemiopsis Rogers, 2005

1 Male antennal appendage lobiform, second antenna distal antennomere straight, lacking a medial, hemispherical, spiny bulge; female with dorsolateral conical projections on thoracic segments V–X and abdominal segments I–V Parartemiopsis longicornis (Smirnov, 1930)
– Male antennal appendage lamellar, second antenna distal antennomere bent medially in proximal third and subapically, bearing a medial, hemispherical, spiny bulge; female with dorsolateral conical projections on thoracic segments X and XI only Parartemiopsis shangrilaensis sp. nov.

Key to Chirocephalidae of China

Chirocephalus is in great need of revision (Rogers 2013). Recent attempts to erect or resurrect genera from Chirocephalus sensu lato based on small genetic sampling from the genus (Weekers et al. 2002; Naganawa et al. 2020) have only created confusion. The genus, as it currently stands, is probably polyphyletic, but with 60+ species (Rogers 2013), phylogenetic studies on only a handful of species cannot accurately elucidate evolutionary relationships within the group. Until a larger number of species are analysed using standard, modern molecular and morphological techniques, the resurrection or establishment of new genera only creates more confusion. First and foremost, we need a definition of what Chirocephalus is. We need this before we can decide what is not Chirocephalus. Until then, the various proposed generic names remain available.

There are several records of Chirocephalus from China that are questionable. Chirocephalus spinicaudatus var. chyzeri (Daday, 1890) was reported from Tibet by Chiang (1983), but his figures do not agree with the description of that taxon, which is only known from Slovakia and Romania (Belk and Brtek 1995). Similarly, C. graziellae Alonso & Naganawa, 2008 was reported from Tibet by Deng et al. (2021); again, the description provided of the Tibetan material disagrees with the original description and is insufficient to determine what species Deng et al. had. The material from Tibet of both populations needs to be examined and identified according to modern standards. Neither of these forms are included in the key below.

1 Male distal antennomere anterior margin without a medial triangular projection; male genital segments not expanded, lacking a ventral transverse ridge; gonopod basal portions separated by their width; gonopod rigid basal portion bearing a medial, digitiform projection, with medial surface bearing spinulae; gonopod everted portion a short cone (Chirocephalus) 2
– Male distal antennomere anterior margin with a medial triangular projection; male genital segments enlarged and chitinized with a transverse ridge along ventroposterior margin; gonopod basal portions separated by 3–4× their width; gonopod rigid basal portion bearing a large, ventromedial, subtriangular and broadly lamellar projection, with medioventral margin lined with spinulae; gonopod everted portion subcylindrical with apex digitiform Parartemiopsis shangrilaensis sp. nov.
2(1) Apophyses subconical, cylindrical, or broadly expanded 3
– Apophyses subglobular, spherical Chirocephalus mongolianus Uéno, 1940
3(2) Second antennae distal antennomere with a basal projection(s) 4
– Second antennae distal antennomere without a basal projection Chirocephalus wangi Hsü, 1933
4(3) Second antenna distal antennomere nearly straight Chirocephalus nankinensis (Shen, 1933)
– Second antenna distal antennomere bending medially nearly 90º Chirocephalus sinensis Thiele, 1907

Acknowledgements

This research was funded by a grant from Khon Kaen University International College of Thailand and the Southeast Asia Biodiversity Research Institute, the Chinese Academy of Sciences (Y4ZK111B01). We are grateful to Dr Wansheng Jiang for his assistance in collecting material.

Additional information

Conflict of interest

The authors have declared that no competing interests exist.

Ethical statement

No ethical statement was reported.

Funding

This work was funded by a grant from Khon Kaen University International College of Thailand and the Southeast Asia Biodiversity Research Institute, the Chinese Academy of Sciences (Y4ZK111B01).

Author contributions

SSS was responsible for literature review, specimen collection, methodology, identifying specimens, photographs, and preparation of figures and the first draft of the manuscript. XYC organized and provided funding for the sampling trips and added methodology. DCR and LS were responsible for conceptualization, methodology, writing and editing of the final manuscript, and general revisions.

Author ORCIDs

Shu-Sen Shu https://orcid.org/0000-0001-6476-004X

Xiao-Yong Chen https://orcid.org/0000-0002-0924-5560

D. Christopher Rogers https://orcid.org/0000-0003-3335-7287

Laorsri Sanoamuang https://orcid.org/0000-0003-0377-1225

Data availability

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

References

  • Brtek J (1958) Pristicephalus shadini (Smirnov, 1928) eine fur die Fauna der C.S.R. neue art des Kiemenflussus und einige Betrachtungen zu den europaischen Arten der Gattung Pristicephalus. Zborník Slovenského Národného Múzea. Prírodné Vedy 4: 3–15.
  • Brtek J (1965) Eine neue Art and eine neue Gattung der Ordnung Anostraca. Annotationes Zoologicae et Botanicae (Bratislava) 21: 1–4.
  • Brtek J (1966) Einige Notizen zur Taxonomie der Familie Chirocephalidae Daday 1910. Annotationes Zoologicae et Botanicae (Bratislava) 33: 1–65.
  • Brtek J (1967) Beiträge zur Kenntnis der Fauna Afghanistans Anostraca. Acta Musei Moraviae 52: 217–221.
  • Chiang X-Z (1983) Branchiopoda from Tibet plateau. In: Jiang X-Z, Shen Y-F, Gong X-J (Eds) Aquatic Invertebrates of the Tibetan Plateau. Series of the Scientific Expedition to Qinghai-Xizang Plateau. Science Press, Beijing, 443–492.
  • Daday E (1910) Monographie systématique des phyllopodes anostracés. Annales des Sciences Naturelles. Zoologie Series 9(11): 91–489.
  • Deng Z-X, Chen Y-T, Ma X-L, Hu W, Yin M-B (2021) Dancing on the top: Phylogeography and genetic diversity of high-altitude freshwater fairy shrimps (Branchiopoda, Anostraca) with a focus on the Tibetan plateau. Hydrobiologia 848(10): 2611–2626. https://doi.org/10.1007/s10750-021-04584-z
  • Hsü F-Z (1933) The Anostraca of Nanking and its vicinity. Contributions from the Biological Laboratory of the Science Society of China 9: 329–340.
  • Naganawa H, Naumova E-Y, Denikina NN, Kondratov IG, Dzyuba EV, Iwasawa A (2020) Does the dispersal of fairy shrimps (Branchiopoda, Anostraca) reflect the shifting geographical distribution of freshwaters since the late Mesozoic? Limnology 21(1): 25–34. https://doi.org/10.1007/s10201-019-00589-9
  • Prévost B (1803) Histoire d’un Insecte (ou d’un Crustace’) que I′auteur a cru devoir appeler Chirocéphale diaphane. Journal de Physique, de Chimie, dHistoire Naturelle et des Arts 57: 37–54.
  • Rogers DC (2006) Parartemiopsis longicornis (Smirnov), senior synonym of P. mongolica Rogers (Crustacea: Branchiopoda: Anostraca), with remarks on the validity of the genus. Zootaxa 1188(1): 49–54. https://doi.org/10.11646/zootaxa.1188.1.4
  • Rogers DC (2013) Anostraca catalogus (Crustacea: Branchiopoda). The Raffles Bulletin of Zoology 61: 525–546.
  • Rogers DC, Thaimuangphol W, Saengphan N, Sanoamuang L (2013) Current knowledge of the South East Asian large branchiopod Crustacea (Anostraca, Notostraca, Laevicaudata, Spinicaudata, Cyclestherida). Journal of Limnology 72(s2): 69–80. https://doi.org/10.4081/jlimnol.2013.s2.e5
  • Sars GO (1897) The Phyllopoda of the Jana-Expedition. Annals of the Museum of the Zoological Academy of Sciences, St. Petersburg 2: 461–493.
  • Shen C-J (1933) On two species of Chinese Branchiopoda of the family Chirocephalidae. Bulletin of the Fan Memorial Institute of Biology 4: 1–8.
  • Shu S-S, Chen F-Z, Yang J-X, Yang X-J, Chen X-Y (2013) Diversity and faunal analysis of crustaceans in Patatson National Park, Shangri-La, China. Zoological Research 34: 204–208.
  • Smirnov SS (1930) Sur une espèce nouvelle des Phyllopoda Anostraca, provenant de la région de l’Ous-souri. Doklady Akademii Nauk SSSR, Series A: 75–78.
  • Thiele J (1907) Einige neue Phyllopoden-Arten des Berliner Museums. Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin 9: 288–297.
  • Uéno M (1940) Phyllopod Crustacea of Manchoukuo. Bulletin of the Biogeographic Society of Japan 10: 87–102.
  • Weekers PHH, Murugan G, Vanfleteren JR, Belk D, Dumont HJ (2002) Phylogenetic analysis of anostracans (Branchiopoda: Anostraca) inferred from nuclear 18S ribosomal DNA (18S rDNA) sequences. Molecular Phylogenetics and Evolution 25(3): 535–544. https://doi.org/10.1016/S1055-7903(02)00289-0
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