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Research Article
Paguristione uniuropodus, a new genus and a new species of Pseudioninae infesting hermit crabs from China (Crustacea, Isopoda, Bopyridae)
expand article infoJianmei An, Qiuping Zhao, John C. Markham§
‡ Shanxi Normal University, Linfen, China
§ Arch Cape Marine Laboratory, Arch Cape, United States of America
Open Access

Abstract

Paguristione uniuropodus gen. n., sp. n. infests Paguristes sp. in the East China Sea. Paguristione gen. n. differs from the closely related genera Pseudione and Pagurion by its females having indistinct lateral plates on the last two pleomeres and its male with a long tapering pleon of six pleomeres, lacking both pleopoda and uropoda.

Keywords

Paguristes , East China Sea

Introduction

Bopyrid isopods infesting hermit crabs belong to the subfamilies Pseudioninae (branchial parasites) and Athelginae (dorsoabdominal parasites). An, Markham and Yu (2010), An, Williams and Yu (2011) and An, Li and Markham (2013) have reported a total of eight bopyrid species infesting hermit crabs in the South China Sea. Markham (1992) recorded six species of bopyrids infesting hermit crabs in Hong Kong. Boyko (2004)reported one such species from Taiwan. In Chinese waters as a whole, An (2006) reported ten species of bopyrids infesting hermit crabs. Currently, throughout Asia, 36 species are recorded infesting 48 hermit crabs from Asia (Table 1). Worldwide, McDermott, Williams and Boyko (2010) catalog 83 species of bopyrids infesting hermit crabs, of which 41 species in ten genera are branchial parasites. As hosts worldwide, 11 species of Paguristes are known to bear bopyrids (Table 2); their parasites, all branchially infesting members of the subfamily Pseudioninae, are in the genera Asymmetrione, Pseudione, Parapagurion and now the new genus Paguristione.

Table 1.

Bopyrid isopods infesting hermit crabs in Asian waters.

Bopyrids Hosts Localities References
Subfamily Pseudioninae
Asymmetrione asymmetrica (Shiino, 1933) Clibanarius bimaculatus (De Haan, 1849) Japan Shiino 1933
Clibanarius merguiensis de Man, 1888 Thailand Markham 1985a; Brunenmeister 1980
Asymmetrione sallyae Williams & Schuerlein, 2005 Diogenes avarus Heller, 1865 Singapore Williams and Schuerlein 2005
Bopyrissa dawydoffi (Codreanu & Codreanu, 1963) Clibanarius merguiensis de Man, 1888 Vietnam Codreanu and Codreanu 1963
Bopyrissa liberorum Markham, 1985 Clibanarius merguiensis de Man, 1888 Thailand Markham 1985a
Bopyrissa pyriforma (Shiino, 1958) Clibanarius bimaculatus (De Haan, 1849) Hong Kong Markham 1982
Diogenes edwardsii (De Haan, 1849) Japan Shiino 1958
Bopyrophryxus branchiabdominalis Codreanu, 1965 Oncopagurus monstrosus (Alcock, 1894) Indonesia Bourdon and Boyko 2005
Paragiopagurus acutus (de Saint Laurent, 1972) Philippines Bourdon and Boyko 2005
unidentified pagurid Indonesia Bourdon and Boyko 2005
Pagurion arrosor An, Li & Markham, 2013 Dardanus arrosor (Herbst, 1796) China An, Li and Markham 2013
Pagurion tuberculata Shiino, 1933 Dardanus scutellatus (H. Milne Edwards, 1848) Japan Shiino 1933
Dardanus aspersus (Berthold, 1846) China An, Li and Markham 2013
Pagurocryptella holthuisi Boyko & Williams, 2010 Solitariopagurus tuerkayi McLaughlin, 1997 Japan Boyko and Williams 2010
Parapagurion calcinicola Shiino, 1933 Calcinus elegans (H.Milne Edwards, 1836) Japan Shiino 1933
Calcinus linapropodus Morgan & Forest, 1991 Japan Shiino 1933
Paguristes monoporus Morgan, 1987 Indonesia Haig and Ball 1988
Paguristes sp. Thailand Markham 1985a
Pagurus aff. hedleyi or kulkarnii Hong Kong Markham 1992
Parapseudione lata Shiino, 1958 Pagurus middendorffii Brandt, 1851 Japan Shiino 1958
Propseudione rhombicosoma Shiino, 1933 Calcinus laevimanus (Randall, 1840) Japan Shiino 1933
Calcinus morgani Rahayu & Forest, 1999 Japan Shiino 1933
Pseudione calcinii Shiino, 1958 Calcinus latens (Randall, 1840) Japan Shiino 1958
Pseudione clibanaricola Shiino, 1933 Clibanarius bimaculatus (De Haan, 1849) Japan Shiino 1933
Pseudione hyndmanni (Bate & Westwood, 1868) Pagurus sp. Japan Shiino 1936
Pseudione intermedia Nierstrasz & Brender à Brandis, 1932 Lophopagurus (Australeremus) triserratus (Ortmann, 1892) Japan Shiino 1936
Pagurus sp. ? Japan Nierstrasz and Brender à Brandis 1932
Pseudione kensleyi Williams & Schuerlein, 2005 Clibanarius infraspinatus Hilgendorf, 1869 Singapore Williams and Schuerlein 2005
Pseudione nobili Nierstrasz & Brender à Brandis, 1923 Trizocheles spinosus spinosus (Henderson, 1888) Indonesia Nierstrasz and Brender à Brandis 1923
Pseudionella attenuata Shiino, 1949 Pagurus sp. Japan Shiino 1949
Pseudionella spiropaguri An, Li & Markham, 2013 Spiropagurus profundorum Alcock, 1905 China An, Li and Markham 2013
Spiropagurus spiriger (De Haan, 1849) China An, Li and Markham 2013
Parasymmetrione tuberculineata An, Markham & Yu, 2010 Clibanarius corallinus (H. Milne-Edwards, 1848) South China Sea An, Markham and Yu 2010
Asymmetrione globifera An, Markham & Yu, 2010 Dardanus hessii (Miers, 1884) Beibu Gulf An, Markham and Yu 2010
Spiropagurus sp. South China Sea An, Markham and Yu 2010
Subfamily Athelginae
Allathelges pakistanensis Kazmi & Markham, 1999 Paguristes perspicax Nobili, 1906 Pakistan Kazmi and Markham 1999
Athelges akanoshimensis var. tenuibranchiatus Shiino, 1936 Lophopagurus (Australeremus) triserratus (Ortmann, 1892) Japan Shiino 1936
Athelges japonicus Shiino, 1958 Pagurus constans (Stimpson, 1858) Japan Shiino 1958
Pagurus lanuginosus De Haan, 1849 Japan Shiino 1958
Pagurus middendorffii Brandt, 1851 Japan Shiino 1958
Athelges sp. Trizopagurus strigatus (Herbst, 1804) Indonesia Haig and Ball 1988
Table 2.

Known bopyrids infesting Paguristes species with localities and references.

Bopyrids Host Type locality References
Asymmetrione aequalis Pardo, Boyko & Mantelatto, 2009 P. tomentosus H. Milne Edwards, 1848 Peru Pardo et al. 2009
Asymmetrione desultor Markham, 1975 P. tortugae Schmitt, 1933 Brazil Bourdon 1979
Asymmetrione foresti (Bourdon, 1968) P. eremita (Linnaeus, 1767) Mediterranean Bourdon 1968
Parapagurion calcinicola Shiino, 1933 P. monoporus Morgan, 1987 Indonesia Haig and Ball 1988
P. sp. Thailand Markham 1985a
Parapagurion imbricata Markham, 1978 P. tortugae Schmitt, 1933 Cuba Markham 1978
Pseudione biacuta Bourdon, 1979 P. robustus Forest & de Saint Laurent, 1967 Uruguay Bourdon 1979
Pseudione quasimodo Boyko & Williams, 2004 P. grayi Benedict, 1901 Bahamas Boyko and Williams 2004
P. invisisacculus McLaughlin & Provenzano, 1974 Bahamas Boyko and Williams 2004
P. anahuachis Glassell, 1938 Gulf of California Brusca 1980
Allathelges pakistanensis Kazmi & Markham, 1999 P. perspicax Nobili, 1906 Pakistan Kazmi and Markham 1999
Athelges pelagosae Babiç, 1912 P. eremita (Linnaeus, 1767) Adriatic Babiç 1912
Parathelges piriformis Markham, 1972 P. oxyophthalmus Holthuis, 1959 Colombia Markham 1978
Parathelges whiteleggei Nierstrasz & Brender à Brandis, 1931 P. monoporus Morgan, 1987 Indonesia Haig and Ball 1988
Pseudostegias otagoensis Page, 1985 P. barbatus (Heller, 1862) New Zealand Page 1985

Specimens used in this study were collected from the East China Sea in 1958, and one of the authors (An 2006) examined the parasites and reported Parapagurion glabra sp. n. infesting Paguristes sp. in her doctoral dissertation (not a published work in the sense of the ICZN). Further examination shows that they represent a new species in a new genus. The name Parapagurion glabra is here entered into its synonymy.

Material and methods

Materials for this study originated from Chinese Comprehensive Oceanographic Survey. All materials examined have been deposited in the Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China (IOCAS). Specimens were viewed and drawn using a Zeiss Stemi SV Apo microscope.

Taxonomy

Family BOPYRIDAE Rafinesque-Schmaltz, 1815
Subfamily Pseudioninae R. Codreanu, 1967

Paguristione gen. n.

Diagnosis

Female. All body segments distinct, almost symmetry. Rudimentary coxal plates present in first four segments. Marsupium complete. Oostegite 1 with simple tubercules on internal ridge. Palp of maxilliped with long setae. All pleomeres distinct. First three pleomeres with lateral plates and biramous pleopoda. Fourth and fifth pleomeres with biramous pleopoda, but lateral plates without lateral plates. Sixth pleomere without lateral plates, uropoda uniramous. Male. All segments distinct. First and last pereomeres respectively much broader than adjacent head and first pleomere. Pereopods of first pair smaller than those of following 3 pairs. Pleon elongate, of 6 distinct pleomeres. No pleopoda or uropoda.

Etymology

Combination of the genus name of its host, Paguristes and bopyrid genus name Ione. Gender feminine.

Type species

Paguristione uniuropodus sp. n., herein designated.

Paguristione uniuropodus sp. n.

Fig. 1

Parapagurion grabla An, 2006 (unpublished thesis): 30–31, fig. 8 (invalid name).

Material examined

Infesting Paguristes sp. Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China (IOCAS). Chinese Comprehensive Oceanographic Survey, East China Sea, Station 4081, 28°00'N, 128°30'E, 74m, 5 April 1958, Yulin Liao, coll. Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China (IOCAS). 1♀holotype, CIEA408101; 1 ♂, allotype, CIEA408102.

Description of holotype female

Length 5.20 mm, maximal width 3.41 mm across third pereomere, head length 1.0 mm, head width 1.31 mm. Body distorted about 16° (Fig. 1A).

Figure 1. 

Paguristione uniuropodus sp. n. A–I holotype female J–N allotype male. A Dorsal view B Ventral view C Left antennae D Right maxilliped, external view E Palp of right maxilliped F Left side of barbula G Right oostegite 1, external view H Right oostegite 1, internal view I Pereopod 4 J Dorsal view K Ventral view L Left antennae M Pereopod 2 N Pereopod 7. Scale: 1.00 mm (A, B); 0.36 mm (D); 0.17 mm (C, E); 0.50 mm (F–I); 0.47 mm (J, K); 0.23 mm (L–M).

Head subelliptical, fully embedded in pereomere 1, with short frontal lamina completely across anterior margin. Eyes absent (Fig. 1A). Antennae with two articles and three articles respectively (Fig. 1C). Maxilliped (Fig. 1D, E) with prominent round articulating palp, that fringed on medial margin by sparse setae. Plectron short and blunt. Barbula (Fig. 1F) with 2 large sharp falcate projections on each side, medially unornamented.

Pereon broadest across third pereomere. First 3 pereomeres with coxal plates. Brood pouch completely enclosed by oostegites. First oostegite (Fig. 1G, H) with deep groove separating 2 articles externally; internal ridge bearing 4-7 simple projections; posterolateral point extending laterally. Pereopods rudimentary, not extending beyond margins of brood pouch, visible only ventrally; all pereopods with all articles distinct, of nearly same size and structure (Fig. 1I).

Pleon of 6 distinct pleomeres, first three produced into small lateral plates and bearing biramous pleopods; fourth and fifth pleomeres lacking lateral plates. Terminal pleomere greatly reduced and deeply embedded in fifth, bearing uniramous uropoda. All pleopodal rami produced into tapering points and progressively smaller posteriorly, extending to sides of pleon and leaving ventral surface of pleon uncovered.

Description of allotype male

Body outline suboval. Length 2.52 mm, maximal width across third pereomere, 1.05 mm, head length 0.30 mm, head width 0.42 mm, first pleomere width 0.50 mm, fifth width 0.20 mm. All segments distinct (Fig. 1J, K).

Head semicircular, broader than long, much narrower than first pereomere, distinctly separated from first pereomere and not at all embedded into it (Fig. 1J). Eyes absent. Antennae visible only ventrally, not extending to margins of head, of 3 and 4 articles respectively; second antenna with sparse short setae on terminal article (Fig. 1L).

Pereon smoothly rounded, slightly broadest across third pereomere. No midventral tubercles. All pereopods with all articles distinct. Pereopod 1 somewhat smaller than pereopods 2-4, those 3 pairs largest and all of about same size; pereopods 5-7 progressively smaller (Fig. 1M, N). Pereopods 1-4 bearing sharp extended dactyli, dactyli of pereopods 5-7 much reduced.

Pleon elongate, extending far posteriorly, of 6 distinct pleomeres deeply separated laterally, each markedly narrower than that before it; pleomere 1 abruptly narrower than last pereomere, it and pleomere 2 much shorter than pleomeres 2-6; every pleomere broadest across posterior edge. Pleopods and uropods completely absent, not even indicated by scars.

Etymology

Latin noun uniuropodus, referring to the uniramous uropoda of the female, used in apposition.

Remarks

The new genus differs from other closely similar hermit-crab-infesting genera Pseudione, Pagurion and Parapagurion thus: female with only rudimentary pleonal lateral plates (only first three pleomeres with small lateral plates) and uniramous uropoda, male with head and pleon abruptly narrower than contiguous pereomeres, first pereopod smaller than pereopods 2-4 and pleopodal appendages completely lacking. Females of Pseudione have distinct pleonal lateral plates on pleomeres 1-5; its males have pleopods, and their heads and pleons are smoothly narrower than the pereon. Females of Pagurion have distinct lamellar pleopodal appendages on all pleomeres 1-6 and biramous uropoda; its males have equally width pereopods and uniramous pleopods. Females of Parapagurion are nearly symmetrical and bear well-developed lateral plates on pleomeres 1-5 and uniramous uropods; the first pereopods of the males are never smaller than the second ones.

Acknowledgments

This work was supported by the National Natural Science Foundation of China [No. 31471970]. We are indebted to Prof. Yulin Liao of IOCAS for making the collections.

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