Abstract

The porcellanid crab Polyonyx gibbesi Haig, 1956, an obligate symbiont of Chaetopterus cf. variopedatus (Renier, 1804) in the western Atlantic, is parasitized by a rare entoniscid isopod. Crabs from coastal North Carolina and Florida, U.S.A., were dissected and examined for this internal parasite in 1966 and 1967. Two of 83 crabs (2.4 %) and 3 of 100 (3.0 %) crabs from North Carolina and Florida, respectively, were parasitized. Only female parasites were found, including five immature and three mature specimens; one host was parasitized by three immature entonicisds simultaneously. One of the mature parasites was liberating epicaridium larvae and the others had developing eggs or larvae. Parasitized female crabs were all ovigerous; the parasites did not castrate the hosts. The parasite is identified as Entoniscus creplinii Giard and Bonnier, 1887, previously known only from Brazil, and the female is redescribed.

Keywords:
Atlantic; Chaetopteridae; isopod; parasitism; symbiosis

INTRODUCTION

The symbiotic porcellanid crab Polyonyx gibbesi Haig, 1956Haig, J. 1956. The Galatheidea (Crustacea Anomura) of the Allan Hancock Atlantic Expedition with a review of the Porcellanidae of the western North Atlantic. Allan Hancock Atlantic Expedition Report, 8: 1-45. inhabits the tubes of the marine benthic polychaete worm Chaetopterus cf. variopedatus ([Renier], [1804Renier, S. A. 1804. Prospetto della Classe dei Vermi Nominati e Ordinati secondo il Sistema di Bosc. Padua. p. xv-xxvi. [Work No. 25 on the Official Index of Rejected and Invalid Works in Zoological Nomenclature; see ICZN Opinion 316.]]) from Woods Hole, Massachusetts to Uruguay (Williams, 1984Williams, A.B. 1984. Shrimps, lobsters, and crabs of the Atlantic Coast of the eastern United States, Maine to Florida. Washington, D.C., Smithsonian Institution Press, 550p.; McDermott, 2005McDermott, J.J. 2005. Biology of the brachyuran crab Pinnixa chaetopterana Stimpson (Decapoda: Pinnotheridae) symbiotic with tubicolous polychaetes along the Atlantic coast of the United States, with additional notes on other polychaete associations. Proceedings of the Biological Society of Washington, 118: 742-764.; Mantelatto et al., 2021Mantelatto, F.L.; Miranda, I.; Vera-Silva, A.L.; Negri, M.; Buranelli, R.C.; Terossi, M.; Magalhães, T.; Costa, R.C.; Zara, F.J. and Castilho, A.L. 2021. Checklist of decapod crustaceans from the coast of the São Paulo State (Brazil) supported by integrative molecular and morphological data: IV. Infraorder Anomura: superfamilies Chirostyloidea, Galatheoidea, Hippoidea and Paguroidea. Zootaxa, 4965: 558-600.). The crab’s biology and relationship with the other major symbiont of Chaetopterus cf. variopedatus, the pinnotherid brachyuran Pinnixa chaetopterana Stimpson, 1860Stimpson, W. 1860. Notes on North American Crustacea, in the museum of the Smithsonian Institution. No. II. Annals of the Lyceum of Natural History of New York 7(22): 176-246, pls. 2, 5., is relatively well known (Enders, 1905Enders, H.E. 1905. Notes on the commensals found in the tubes of Chaetopterus pergamentaceus. American Naturalist, 39: 37-40.; Pearse, 1913Pearse, A.S. 1913. On the habits of the crustaceans found in Chaetopterus tubes at Woods Hole, Massachusetts. Biological Bulletin, 24: 102-114. ; Gray, 1961Gray, I.E. 1961. Changes in abundance of the commensal crabs of Chaetopterus. Biological Bulletin, 120: 353-359.; Gore, 1968Gore, R.H. 1968. The larval development of the commensal crab Polyonyx gibbesi Haig, 1956 (Crustacea: Decapoda). Biological Bulletin, 135: 111-129. ; Grove and Woodin, 1996Grove, M.W. and Woodin, S.A. 1996. Conspecific recognition and host choice in a pea crab, Pinnixa chaetopterana (Brachyura: Pinnotheridae). Biological Bulletin, 190: 359-366.; McDermott, 2005; Sandford, 2006Sandford, F. 2006. Polyonyx gibbesi (Decapoda:Anomura: Porcellanidae) and Pinnixa chaetopterana (Decapoda: Brachyura: Pinnotheridae), two crab commensals in tubes of the polychaete Chaetopterus sp., in the northern Gulf of Mexico. In: A. Asakura (ed), Biology of Anomura II. Crustacean Research, Special Number, 6: 23-31.). However, Polyonyx gibbesi has been reported to host an entoniscid isopod in Brazil (Müller, 1871Müller, F. 1871. Bruchstücke zur Naturgeschichte der Bopyriden. Jenaische Zeitschrift für Medicin und Naturwissenschaft, 6: 53-73, pls. 3, 4.), a seemingly rare parasite considering it has not been reported on again in 150 years.

There are several taxonomic and nomenclatural issuesInternational Commission on Zoological Nomenclature [ICZN]. 1954. Opinion 316. Rejection for nomenclatural purposes of the “Tavola Alfabetica delle Conchiglei Adriatische” and “Prospetto della Classe dei Vermi” of S. A. Renier commonly attributed to the year 1804. Opinions and Declarations Rendered by the International Commission on Zoological Nomenclature, 9: 91-106. involving all three species in the hypersymbiosis between C. cf. variopedatus, P. gibbesi, and the entoniscid isopod. The host in this symbiotic web (see Boyko and van der Meij, 2018Boyko, C.B. and van der Meij, S.E.T. 2018. A trifecta of Swiftian symbioses: stony corals, gall crabs and their parasites (Scleractinia; Brachyura: Cryptochiridae; Isopoda: Epicaridea and Cirripedia: Rhizocephala). Zoological Journal of the Linnean Society, 184: 304-329.), Chaetopterus cf. variopedatus, is likely part of a species complex with the type locality for the species located in the Mediterranean; specimens in the western Atlantic probably belong to an undescribed species, possibly identical with “Chaetopterus ‘variopedatus’ 2” of Tilic and Rouse (2020Tilic, E. and Rouse, G.W. 2020. Hidden in plain sight, Chaetopterus dewysee sp. nov. (Chaetopteridae, Annelida) - a new species from southern California. European Journal of Taxonomy, 643: 1-16. ). Primary symbionts within the tubes of this polychaete include pinnotherid and porcellanid crabs and investigations have revealed poorly known secondary symbionts living on or in these decapods, including hyperparasites such as endoparasitic isopods (McDermott, 2009McDermott, J.J. 2009. Hypersymbioses in the pinnotherid crabs (Decapoda: Brachyura: Pinnotheridae): a review. Journal of Natural History 43: 785-805.).

The taxonomic history of P. gibbesi is a bit complicated but necessary to understand the distribution of the species. Haig (1956Haig, J. 1956. The Galatheidea (Crustacea Anomura) of the Allan Hancock Atlantic Expedition with a review of the Porcellanidae of the western North Atlantic. Allan Hancock Atlantic Expedition Report, 8: 1-45.) discussed the nomenclatural issues surrounding the western Atlantic Polyonyx Stimpson, 1858 species formerly known as Porcellana macrocheles Gibbes, 1850Gibbes, L.R. 1850. On the carcinological collections of the United States, and an enumeration of species contained in them, with notes on the most remarkable, and descriptions of new species. Proceedings of the American Association for the Advancement of Science, 3: 167-201. (= Polyonyx macrocheles) but showed it was a junior homonym of Porcellana macrocheles Poeppig, 1836Poeppig, E. 1836. Crustacea Chilensia nova aut minus nota. Archiv für Naturgeschichte, 2: 133-145, pl. 4., and introduced Polyonyx gibbesi as a new name for the taxon. Haig (1956Haig, J. 1956. The Galatheidea (Crustacea Anomura) of the Allan Hancock Atlantic Expedition with a review of the Porcellanidae of the western North Atlantic. Allan Hancock Atlantic Expedition Report, 8: 1-45.) considered the range of this species to be from Massachusetts, U.S.A. to Panama but she considered the record of Müller (1871Müller, F. 1871. Bruchstücke zur Naturgeschichte der Bopyriden. Jenaische Zeitschrift für Medicin und Naturwissenschaft, 6: 53-73, pls. 3, 4.) to possibly refer to the same species. Ejchel (1965Ejchel, F. 1965. Notes on crustacean decapods. Anais da Academia Brasileira de Ciências, 37(suppl.): 325-326.) subsequently described Polyonix (sic) creplinii (also as “creplini” in the same paper) from Brazil but this name has also been regarded as a synonym of P. gibbesi (Gore, 1974Gore, R.H. 1974. On a small collection of porcellanid crabs from the Caribbean Sea (Crustacea, Decapoda, Anomura). Bulletin of Marine Science, 24: 700-721.). The range of the species has further been extended southward to Argentina (Belleggia et al., 2010Belleggia, M.; Boschi, E.E.; Schejter, L.; Bremec, C.; Sánchez, F. and Figueroa, D. E. 2010. First record of Polyonyx gibbesi (Anomura: Porcellanidae) in the Argentine Sea. Marine Biodiversity Records, 3: e44. doi:10.1017/S175526720999100X
https://doi.org/10.1017/S175526720999100... ; Mantelatto et al., 2021Mantelatto, F.L.; Miranda, I.; Vera-Silva, A.L.; Negri, M.; Buranelli, R.C.; Terossi, M.; Magalhães, T.; Costa, R.C.; Zara, F.J. and Castilho, A.L. 2021. Checklist of decapod crustaceans from the coast of the São Paulo State (Brazil) supported by integrative molecular and morphological data: IV. Infraorder Anomura: superfamilies Chirostyloidea, Galatheoidea, Hippoidea and Paguroidea. Zootaxa, 4965: 558-600.).

Entoniscid isopods are endoparasitic in a wide range of decapod hosts, including pinnotherid crabs along the east coast of the United States (McDermott et al., 2019McDermott, J.J.; Williams, J.D. and Boyko C.B. 2019. A new genus and species of parasitic isopod (Bopyroidea: Entoniscidae) infesting pinnotherid crabs (Brachyura: Pinnotheridae) on the Atlantic coast of the USA, with notes on the life cycle of entoniscids. Journal of Crustacean Biology, 40: 97-114.), but only the four species in the genus Entoniscus Müller, 1862Müller, F. 1862. Entoniscus porcellanae, ein neue Schmarotzerassel. Archiv für Naturgeschichte, 28: 10-18, pl. 2. are known from porcellanid crabs (Shiino, 1942Shiino, S.M. 1942. On the parasitic isopods of the family Entoniscidae, especially those found in the vicinity of Seto. Memoirs of the College of Science, Kyoto Imperial University, series B, 17(1-2): 37-76.; Boyko et al., 2008Boyko, C.B.; Bruce, N.L.; Hadfield, K.A.; Merrin, K.L.; Ota, Y.; Poore, G.C.B.; Taiti, S.; Schotte, M. and Wilson, G.D.F. (eds). 2008 onwards. World Marine, Freshwater and Terrestrial Isopod Crustaceans database. Accessed at http://www.marinespecies.org/isopoda. Access on 07 January 2021. doi:10.14284/365.
http://www.marinespecies.org/isopoda. Ac... onwards). Müller (1871Müller, F. 1871. Bruchstücke zur Naturgeschichte der Bopyriden. Jenaische Zeitschrift für Medicin und Naturwissenschaft, 6: 53-73, pls. 3, 4.) reported an entoniscid from Porcellana (Polyonyx) creplinii, but the parasite was incompletely described and was not named. Giard and Bonnier (1887Giard, A. and Bonnier, J. 1887. Contributions á ľétude des bopyriens. Travaux de ľInstitut Zoologique de Lille et du Laboratuire de Zoologie Maritime de Wimereux, 5: 1-272, pls. 1-10. ) introduced the available name Entoniscus creplinii, based on the cursory description from Müller (1871Müller, F. 1871. Bruchstücke zur Naturgeschichte der Bopyriden. Jenaische Zeitschrift für Medicin und Naturwissenschaft, 6: 53-73, pls. 3, 4.) but examined no specimens and added no additional information on the species.

It is the purpose of this paper to provide the first report of E. creplinii since its original discovery, the first full description of females of E. creplinii from P. gibbesi, and to document its prevalence in host crab populations in North Carolina and Florida.

MATERIAL AND METHODS

Crabs were collected by the first author from the tubes of C. cf. variopedatus in June and October, 1966 in the vicinity of Beaufort, NC (34(43’N 76(40’W), and in November and December 1966 and February 1967 on Virginia Key, Miami, FL (25(40’N 80(10’W). For a review of the environmental conditions at these two locations see McDermott (2005McDermott, J.J. 2005. Biology of the brachyuran crab Pinnixa chaetopterana Stimpson (Decapoda: Pinnotheridae) symbiotic with tubicolous polychaetes along the Atlantic coast of the United States, with additional notes on other polychaete associations. Proceedings of the Biological Society of Washington, 118: 742-764.). Crabs were isolated in seawater in the laboratory in order to detect the possible emergence of epicaridium larvae, indicating the presence of one or more mature female parasites. All crabs were then dissected and observed for isopods. Vernier calipers were used to measure crab carapace width (CW) in millimeters. Female isopods and epicaridium larvae were observed with dissecting and compound microscopes; isopod size is given as maximal length of female body. Figures were produced using Adobe Illustrator to trace original drawing tube sketches or drawings made with a dissecting microscope. All specimens are deposited in the United States National Museum of Natural History, Smithsonian Institution (USNM).

SYSTEMATICS

Order Isopoda Latreille, 1817Latreille, P.A. 1817. Les Crustacés, les Arachnides et les Insectes. In: M. le C. Cuvier (ed), Le Règne Animal Distribuè d'Après son Organisation, pour Servir de Base a l'Histoire Naturelle des Animaux et d'Introduction a l'Anatomie Comparée. Paris, Deterville. Vol. 3. i-xxix+1-653p.

Suborder Epicaridea Latreille, 1825Latreille, P.A. 1825. Entomologie ou Histoire Naturelle des Crustacés, des Arachnides et des Insectes. Encyclopédie Methodique. Vol. 10. Paris, Mme.Veuve Agasse, 833p.

Superfamily Bopyroidea Rafinesque, 1815Rafinesque, C.S. 1815. Analyse de la Nature ou Tableau de l'Univers et des Corps Organisés. Palerme, L’Impremerie de Jean Barravecchia, 224 pp.

Family Entoniscidae Kossmann, 1881Kossmann, R. 1881. Die entonisciden. Mittheilungen aus der Zoologischen Station zu Neapel, 3(1-2): 149-169, pls. 8, 9.

Subfamily Entioninae Codreanu, Codreanu and Pike, 1960Codreanu, R; Codreanu, M. and Pike, R.B. 1960. Sur un nouveau type d’entoniscien, Diogenion vermifactus n. g., n. sp., parasite du pagure Diogenes senex Heller de la Mer Rouge. Comptes Rendus Hebdominaires des Séances de l'Académie des Sciences de Paris, 251: 439-441.

Genus Entoniscus Müller, 1862Müller, F. 1862. Entoniscus porcellanae, ein neue Schmarotzerassel. Archiv für Naturgeschichte, 28: 10-18, pl. 2.

Entoniscus creplinii Giard and Bonnier, 1887Giard, A. and Bonnier, J. 1887. Contributions á ľétude des bopyriens. Travaux de ľInstitut Zoologique de Lille et du Laboratuire de Zoologie Maritime de Wimereux, 5: 1-272, pls. 1-10.

(Figs. 1-2)

Figure 1.
Entoniscus crepliniiGiard and Bonnier, 1887Giard, A. and Bonnier, J. 1887. Contributions á ľétude des bopyriens. Travaux de ľInstitut Zoologique de Lille et du Laboratuire de Zoologie Maritime de Wimereux, 5: 1-272, pls. 1-10. (USNM 1660598). A) Mature female, dorsal view. B) Mature female, dorsal view. C) Mature female, lateral view. D) Pleon of female extending to opening at the merus-carpus articulation of the third right walking leg of host Polyonyx gibbesi Haig, 1956Haig, J. 1956. The Galatheidea (Crustacea Anomura) of the Allan Hancock Atlantic Expedition with a review of the Porcellanidae of the western North Atlantic. Allan Hancock Atlantic Expedition Report, 8: 1-45.. Abbreviations: ce = cephalon; he = heart; 1o-5o = oostegites 1 to 5; 1p-5p = pleomeres 1 to 5; pl = pleural lamellae. Scales = 0.5 mm (A); 1 mm (B-D).

Figure 2.
Entoniscus crepliniiGiard and Bonnier, 1887Giard, A. and Bonnier, J. 1887. Contributions á ľétude des bopyriens. Travaux de ľInstitut Zoologique de Lille et du Laboratuire de Zoologie Maritime de Wimereux, 5: 1-272, pls. 1-10. (USNM 1660598). A) Mature female, lateral view. B) Close-up of side of pleomere 3 showing scales. C) Terminal segment of pleon. D) Female cephalon with host sheath surrounding, en face view. E) Female cephalon with host sheath surrounding, lateral view. F) Female cephalon with host sheath removed, en face view. G) Female cephalon with host sheath removed, lateral view. H) Pleon of female with host sheath partially removed, asterisk showing position of first pleopods still covered by host sheath; stippled region shows channel within which second pleopods lay. Abbreviations: ce = cephalon; he = heart; 2-4 = pleopods 2 to 4. Scales = 0.5 mm (A, D-H); 10 µm (B, C).

Entoniscus 3 Müller, 1871Müller, F. 1871. Bruchstücke zur Naturgeschichte der Bopyriden. Jenaische Zeitschrift für Medicin und Naturwissenschaft, 6: 53-73, pls. 3, 4.: 54 (brief description; see below).

“Entoniscus…im Porcellana Creplinii” Fraisse, 1878Fraisse, P. 1878. Entoniscus cavolinii n. sp., nebst Bermerkungen über die Umwandlung und Systematik der Bopyriden. Arbeiten aus dem Zoologisch-Zootomischen Institut in Würzburg, 4: 382-440, pls. 20, 21.: 25, 387 (mention).

“L’Entoniscus de Porcellana Creplinii” Giard, 1878Giard, A. 1878. Notes pour servir a l’histoire du genre Entoniscus. Journal de l’Anatomie et de la Physiologie Normales et Pathologiques de l’Homme et des Animaux, 14: 675-700, pl. 46.: 683 (mention).- Giard and Bonnier, 1887Giard, A. and Bonnier, J. 1887. Contributions á ľétude des bopyriens. Travaux de ľInstitut Zoologique de Lille et du Laboratuire de Zoologie Maritime de Wimereux, 5: 1-272, pls. 1-10. : 89 (mention).

Entoniscus CrepliniiGiard and Bonnier, 1887Giard, A. and Bonnier, J. 1887. Contributions á ľétude des bopyriens. Travaux de ľInstitut Zoologique de Lille et du Laboratuire de Zoologie Maritime de Wimereux, 5: 1-272, pls. 1-10. : 231 (table), 236 (after Müller, 1871Müller, F. 1871. Bruchstücke zur Naturgeschichte der Bopyriden. Jenaische Zeitschrift für Medicin und Naturwissenschaft, 6: 53-73, pls. 3, 4.).- Stebbing, 1893Stebbing, T.R.R. 1893. A history of Crustacea Recent Malacostraca. The International Scientific Series. London, Kegan Paul, Trench, Trübner & Co. xvii + 466p., 19 pls.: 406 (mention).- Bonnier, 1900Bonnier, J. 1900. Contribution a l'étude des épicarides. Les Bopyridae. Travaux de la Station Zoologique de Wimereux, 8: 1-476, pls. 1-41.: 227, 380 (lists).

“Entoniscus… creplinii” Lucas, 1905Lucas, R. 1905. Crustacea für 1904. I. Malacostraca. Archiv für Naturgeschichte, 71(2, pt. 2): 995-1055.: 1048 (list).

Entoniscus creplinii- Shiino, 1942Shiino, S.M. 1942. On the parasitic isopods of the family Entoniscidae, especially those found in the vicinity of Seto. Memoirs of the College of Science, Kyoto Imperial University, series B, 17(1-2): 37-76.: 51 (mention).- Adkison, 1990Adkison, D.L. 1990. A review of the Entoniscinae (Isopoda: Epicaridea: Entoniscidae). New Orleans, Tulane University, Ph.D. Dissertation, 199p. [Unpublished].: 23, 51, 54 (mention; list).- Brasil Lima, 1998Brasil Lima, I.M. 1998. Malacostraca - Peracarida. Isopoda - Epicaridea. p. 635-644. In: P.S. Young (ed), Catalogue of Crustacea of Brazil. Rio de Janeiro, Museu Nacional.: 640 (list).- Boos et al. 2012Boos, H.; Bond Buckup, G.; Buckup, L.; Araujo, P.B.; Magalhães, C.; Almerão, M.P.; dos Santos, R.A. and Mantelatto, F.L. 2012. Checklist of the Crustacea from the state of Santa Catarina, Brazil. Check List, 8: 1020-1046.: 1036 (list).

Material examined herein (subset of specimens originally examined). North Carolina: 3 immature females, all parasitizing a single female Polyonyx gibbesi (13.3 mm CW) associated with Chaetopterus cf. variopedatus, Beaufort, coll. J.J. McDermott, 21 June 1966 (specimens fixed 3 July 1966) (USNM 1660598; specimens in pieces and combined in one lot). Florida: 2 mature females, 1 each parasitizing separate male specimens (7.8 and 8.5 mm CW) of P. gibbesi and 1 immature female parasitizing an ovigerous female (10.1 mm CW) P. gibbesi associated with C. cf. variopedatus, Miami, coll. J. J. McDermott, 9 November 1966 (USNM 1660599; specimens in pieces and combined in one lot).

Type locality. Desterro (= Florianópolis, state of Santa Catarina), Brazil.

Type host. Porcellana (Polyonyx) creplinii Müller, 1871Müller, F. 1871. Bruchstücke zur Naturgeschichte der Bopyriden. Jenaische Zeitschrift für Medicin und Naturwissenschaft, 6: 53-73, pls. 3, 4. (nomen nudum) (= Polyonyx gibbesi Haig, 1956Haig, J. 1956. The Galatheidea (Crustacea Anomura) of the Allan Hancock Atlantic Expedition with a review of the Porcellanidae of the western North Atlantic. Allan Hancock Atlantic Expedition Report, 8: 1-45.).

Description of female (Figs. 1, 2). Mature specimens occupying most of host hemocoel, lying under host stomach, pleon extending dorsally through digestive gland of host to an opening on pereopods 2-4, such as the merus-carpus articulation of right fourth pereopod (Fig. 1D), or unidentified positions in the antero-lateral dorsal quarter of the crab; brood chambers of ovigerous specimens extending into spaces of host pleon. Sheath formed by host surrounds entire parasite. Body of mature parasites orange color due to gonad extending as 2 bands along length of body.

Pereon approximately straight from cephalon to posterior end (Figs. 1A-C, 2A). Cephalon rounded, dorsally divided into 2 bulbous lobes (Figs. 1A-C, 2A, D-G), ventrally undivided, bearing 2(?) pairs of fused flattened antennae (Fig. 2D-G), maxillipeds not observed. Pereon lacking ovarian processes, pereopods apparently absent. Five pairs of subequal oostegites, margins highly crenulate (Figs. 1A-C, 2A). Oostegite 1 not subdivided in lobes. Oostegites 2-5 not fused, not covering oostegite 1 (Figs. 1A-C, 2A).

Pleon elongate (nearly as long or even longer than rest of body in mature specimens), S-shaped, composed of 5 pleomeres, 1 and 2 indistinctly delineated, 3-5 distinct, pleomere 1 as long as remaining pleomeres combined (Figs. 1A-C, 2A, H), pleomeres 3-5 with scales (Fig. 2B). One pair of crenulate pleural lamellae on pleomere 1, similar in size and shape to oostegites, positioned immediately posterior to oostegite 5 (Figs. 1B, C, 2A). Triangular extension on pleomere 1 between pleural lamella and bulbous heart (Figs. 1A, B, 2A, H). Pleomeres 1-5 each with pair of uniramous filamentous pleopods, pleopods 1 and 2 widely separated, 3-5 overlapping (Figs. 1A-C, 2A, H), pleopods 1 and 2 laying within ventral channel on pleomeres 1 and 2. Terminal pleomere with shallow ventral notch, terminally fringed with minute setae (Fig. 2C).

Remarks. Müller’s (1871Müller, F. 1871. Bruchstücke zur Naturgeschichte der Bopyriden. Jenaische Zeitschrift für Medicin und Naturwissenschaft, 6: 53-73, pls. 3, 4.) description of this species, which he did not name, was very short and the only characters noted were that the ovaries of the female parasites were yellow and not purple as in Entoniscus porcellanae Müller, 1862 and that the oostegites were less divided with smoother margins than those of the latter species. Giard and Bonnier (1887Giard, A. and Bonnier, J. 1887. Contributions á ľétude des bopyriens. Travaux de ľInstitut Zoologique de Lille et du Laboratuire de Zoologie Maritime de Wimereux, 5: 1-272, pls. 1-10. ) saw no specimens but named the species based on Müller’s (1871Müller, F. 1871. Bruchstücke zur Naturgeschichte der Bopyriden. Jenaische Zeitschrift für Medicin und Naturwissenschaft, 6: 53-73, pls. 3, 4.) account. Brief as Müller’s (1871Müller, F. 1871. Bruchstücke zur Naturgeschichte der Bopyriden. Jenaische Zeitschrift für Medicin und Naturwissenschaft, 6: 53-73, pls. 3, 4.) description was, it was sufficient to make the name available from Giard and Bonnier’s (1887Giard, A. and Bonnier, J. 1887. Contributions á ľétude des bopyriens. Travaux de ľInstitut Zoologique de Lille et du Laboratuire de Zoologie Maritime de Wimereux, 5: 1-272, pls. 1-10. ) translation of Müller’s (1871Müller, F. 1871. Bruchstücke zur Naturgeschichte der Bopyriden. Jenaische Zeitschrift für Medicin und Naturwissenschaft, 6: 53-73, pls. 3, 4.) text into French. Müller (1871Müller, F. 1871. Bruchstücke zur Naturgeschichte der Bopyriden. Jenaische Zeitschrift für Medicin und Naturwissenschaft, 6: 53-73, pls. 3, 4.) noted that the parasitized hosts were each found alone in the “Chätopterus” burrows, not in a pair as is typical; he speculated that the parasitized nature of the crabs made them poor choices for mates. The present material also had orange gonads and the oostegites are more compact and less divided than those of E. porcellanae, and so match both the characters described by Müller (1871Müller, F. 1871. Bruchstücke zur Naturgeschichte der Bopyriden. Jenaische Zeitschrift für Medicin und Naturwissenschaft, 6: 53-73, pls. 3, 4.) for E. creplinii.

Ecology

North Carolina

Eighty-three crabs were collected, isolated, measured, dissected and examined for entoniscids from North Carolina; the prevalence was 2.4 % (2 of 83). Mean CW values are given in Tab. 1; females were significantly wider than males (t = 4.480; p = ( 0.0001). Two ovigerous female crabs (2.4 %) were parasitized with entoniscids (Tab. 2). One crab (13.3 mm) had three immature female parasites in its hemocoel (one on the left side and two on the right); their marsupia did not contain ova, nor were males present. The elongated tubular pleon of one female was traced to an opening at the merus-carpus articulation of the third right walking leg (pereopod 4) (Fig. 1D). The other crab (14.5 mm; lost) had one immature female lying directly under the stomach with the cephalon oriented anteriorly; the elongated pleon doubled back on the body and extended toward the antero-lateral dorsal quarter of the crab and did not appear to extend into any appendage. The pleon was observed to undergo vigorous worm-like contortions; the mean heartbeat of a specimen from North Carolina was 141.7 ( 6.4/min, n = 3.

Florida

One hundred specimens of P. gibbesi collected in Miami, Florida yielded three parasitized individuals (3.0 %) (Tabs. 1, 2), morphologically similar to those found in North Carolina. Female crabs were significantly larger than males (t = 2.620; p = 0.0104). A recently ovigerous female P. gibbesi (10.1 mm) with diminished gonads was parasitized with an immature female entoniscid situated in the right side of the hemocoel near the gonad. The pleon was extended anteriorly, but was damaged and could not be traced to its external opening.

Epicaridium larvae were liberated in the laboratory from a male crab host (8.7 mm). The marsupia of the mature female isopod, filled with these pigmented larvae, could be seen through the transparent ventral junction between the carapace and the abdomen. Within the host’s hemocoel, the main body of the parasite enclosed in a sheath produced by the host was under the crab’s heart. Its expanded marsupia filled nearly all space in the hemocoel. The anterior (cephalic) end of the parasite faced the left side and the body extended posteroventrally to the right side and under the sperm duct. The distal end of the tubular pleon entered the second right walking leg (third pereopod) exiting via an opening at the merus-carpus articulation. The gonad of the parasite was orange. The other parasitized male host (7.8 mm) harbored a mature female whose marsupia were filled with developing embryos. These were also observed at the ventral carapace-abdomen junction of the crab. The cephalic end of the female parasite was on the right side of the hemocoel. Its body crossed to the left side where the terminal pleomere passed into the first left walking leg (second pereopod) to a distinct external opening (0.105 mm diameter) in the exoskeleton of the carpus.

DISCUSSION

Boyko et al. (2008Boyko, C.B.; Bruce, N.L.; Hadfield, K.A.; Merrin, K.L.; Ota, Y.; Poore, G.C.B.; Taiti, S.; Schotte, M. and Wilson, G.D.F. (eds). 2008 onwards. World Marine, Freshwater and Terrestrial Isopod Crustaceans database. Accessed at http://www.marinespecies.org/isopoda. Access on 07 January 2021. doi:10.14284/365.
http://www.marinespecies.org/isopoda. Ac... onwards) list three species of described and one unidentified porcellanid crab as hosts for the four named species of entoniscids in the genus Entoniscus. The female parasite found in P. gibbesi in the present study is superficially similar to Paguritherium alatum Reinhard (1945Reinhard, E.G. 1945. Paguritherium alatum n. g., n. sp., an entoniscian parasite of Pagurus longicarpus. Journal of Parasitology, 31: 198-204.) that was described from the hermit crab host Pagurus longicarpus Say, 1817Say, T. 1817. An account of the Crustacea of the United States (continued). Journal of the Academy of Natural Sciences at Philadelphia, 1: 155-169., collected at Woods Hole, Massachusetts, USA. The developing female of P. alatum is enclosed in a sheath produced by the host, and is characterized by a long, thin, tubular pleon (“respiratory tube”), which makes contact with the external environment via a pore in the exoskeleton of the eyestalks of the host, through which the epicaridium larvae are released. Reinhard (1945Reinhard, E.G. 1945. Paguritherium alatum n. g., n. sp., an entoniscian parasite of Pagurus longicarpus. Journal of Parasitology, 31: 198-204.) recognized that this entoniscid was closely related to members of the genus Entoniscus but differed enough from other species in this genus so that the new genus, Paguritherium Reinhard, 1945, was established. Reinhard’s (1945Reinhard, E.G. 1945. Paguritherium alatum n. g., n. sp., an entoniscian parasite of Pagurus longicarpus. Journal of Parasitology, 31: 198-204.) observations were verified many years later in parasitized crabs collected in New Jersey (McDermott, 1998McDermott, J.J. 1998. Prevalence of two epicaridean isopods (Bopyridae and Entoniscidae) associated with the hermit crab Pagurus longicarpus Say, 1817 (Anomura) from the New Jersey coast (U.S.A.). Journal of Parasitology, 84: 1042-1045.). Thus, E. creplinii from North Carolina and Florida resembles other species of Entoniscus and Paguritherium in which the elongated, tubular pleon of the female appears to be a major morphological characteristic. This structure is illustrated in the species descriptions of Shiino (1942Shiino, S.M. 1942. On the parasitic isopods of the family Entoniscidae, especially those found in the vicinity of Seto. Memoirs of the College of Science, Kyoto Imperial University, series B, 17(1-2): 37-76.) in Entoniscus japonicus Shiino, 1942 from Petrolisthes japonicus (De Haan, 1849De Haan, W. 1833-1850. Crustacea. Vol. 1. Fauna Japonica sive Descriptio Animalium, quae in itinere per Japoniam, Jussu et Auspiciis Superiorum, qui Summum in India Batava Imperium Tenent, Suscepto, Annis 1823-1830 Collegit, Notis, Observationibus et Adumbrationibus Illustravit. Lugduni Batavorum, xvi + 244; xxi + circfl. Tab. 2 + Tab. a-q + Tab. 1-55.), and Müller (1862Müller, F. 1862. Entoniscus porcellanae, ein neue Schmarotzerassel. Archiv für Naturgeschichte, 28: 10-18, pl. 2.) in Entoniscus porcellanae from an unidentified Brazilian porcellanid.

Entoniscus creplinii makes contact with the external environment using its terminal pleomere through openings produced in the walking legs of the host whereas Paguritherium alatum and E. japonicus produce external openings near the base of the host’s compound eyes. External pores produced by most other species of entoniscids (those found in brachyuran crabs) are found in the inner wall of the crabs’ branchial chambers. While none of the known species of Entoniscus have been recorded in multiple hosts (Boyko et al., 2008Boyko, C.B.; Bruce, N.L.; Hadfield, K.A.; Merrin, K.L.; Ota, Y.; Poore, G.C.B.; Taiti, S.; Schotte, M. and Wilson, G.D.F. (eds). 2008 onwards. World Marine, Freshwater and Terrestrial Isopod Crustaceans database. Accessed at http://www.marinespecies.org/isopoda. Access on 07 January 2021. doi:10.14284/365.
http://www.marinespecies.org/isopoda. Ac... onwards), P. paguritherium also parasitizes the closely related hermit crab Pagurus annulipes (Stimpson, 1860Stimpson, W. 1860. Notes on North American Crustacea, in the museum of the Smithsonian Institution. No. II. Annals of the Lyceum of Natural History of New York 7(22): 176-246, pls. 2, 5.) (Adkison and Heard, 1978Adkison, D.L. and Heard, R.W. 1978. Description of a new genus and species of Pseudioninae (Isopoda: Bopyridae) parasite of the hermit crab Pagurus annulipes (Stimpson) from North Carolina. Proceedings of the Biological Society of Washington, 91: 408-417. ).

Males of the present species were not found, possibly due to a lack of care in dissecting the female parasites in the 1960s; entoniscid males are very small (< 1mm) compared to females and easily overlooked. The males known from other Entoniscus spp. and P. alatum appear to be characteristic in that the pereopods are poorly developed unsegmented swellings.

Crabs parasitized by ovigerous female entoniscids are normally detected by observing liberated epicaridium larvae, but they are also recognized by observing oostegites with developing larvae through the thin exoskeleton at the ventral carapace-abdomen junction of the host. Reinhard (1945Reinhard, E.G. 1945. Paguritherium alatum n. g., n. sp., an entoniscian parasite of Pagurus longicarpus. Journal of Parasitology, 31: 198-204.) and McDermott (1998McDermott, J.J. 1998. Prevalence of two epicaridean isopods (Bopyridae and Entoniscidae) associated with the hermit crab Pagurus longicarpus Say, 1817 (Anomura) from the New Jersey coast (U.S.A.). Journal of Parasitology, 84: 1042-1045.) noted that mature female parasites could be detected in hermit crabs through the thin exoskeleton of their abdomens. Atkins (1933Atkins, D. 1933. Pinnotherion vermiforme Giard and Bonnier, an entoniscid infecting Pinnotheres pisum. Proceedings of the General Meetings for Scientific Business of the Zoological Society of London, 1933: 319-363, 4 pls.) was also able to recognize mature entoniscid females of Pinnotherion vermiforme Giard and Bonnier, 1887Giard, A. and Bonnier, J. 1887. Contributions á ľétude des bopyriens. Travaux de ľInstitut Zoologique de Lille et du Laboratuire de Zoologie Maritime de Wimereux, 5: 1-272, pls. 1-10. through the poorly calcified carapace of the pinnotherid crab host Pinnotheres pisum (Linnaeus, 1767Linnaeus, C. 1767. Systema Naturae Sive Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, Cum Characteribus, Differentiis, Synonymis, Locis. 12th Ed. v. 1 (Pt 2). Holmiae, Laurentii Salvii.), a parasitic species in bivalve mollusks. Mature females of Pinnixion sexdecennia McDermott, Williams and Boyko, 2019 McDermott, J.J.; Williams, J.D. and Boyko C.B. 2019. A new genus and species of parasitic isopod (Bopyroidea: Entoniscidae) infesting pinnotherid crabs (Brachyura: Pinnotheridae) on the Atlantic coast of the USA, with notes on the life cycle of entoniscids. Journal of Crustacean Biology, 40: 97-114.were able to be detected at the thin carapace-abdomen junction of the pinnotherid Pinnixa chaetopterana (see McDermott et al., 2019McDermott, J.J.; Williams, J.D. and Boyko C.B. 2019. A new genus and species of parasitic isopod (Bopyroidea: Entoniscidae) infesting pinnotherid crabs (Brachyura: Pinnotheridae) on the Atlantic coast of the USA, with notes on the life cycle of entoniscids. Journal of Crustacean Biology, 40: 97-114.). The carapace of the latter is heavily calcified, unlike the pinnotherids in bivalve hosts in which the carapace is thin and translucent (McDermott, 2005McDermott, J.J. 2005. Biology of the brachyuran crab Pinnixa chaetopterana Stimpson (Decapoda: Pinnotheridae) symbiotic with tubicolous polychaetes along the Atlantic coast of the United States, with additional notes on other polychaete associations. Proceedings of the Biological Society of Washington, 118: 742-764.).

Prevalence of the E. creplinii was based on a relatively small sample of 183 crabs. Crabs of both sexes were parasitized. Shiino (1942Shiino, S.M. 1942. On the parasitic isopods of the family Entoniscidae, especially those found in the vicinity of Seto. Memoirs of the College of Science, Kyoto Imperial University, series B, 17(1-2): 37-76.) recorded 36 parasitized individuals of E. japonicus among 664 host specimens (5.4 %). Reinhard (1943Reinhard, E.G. 1943. Epicaridean parasites of Pagurus longicarpus at Woods Hole. Anatomical Record, 87: 468 (abstract).; 1945Reinhard, E.G. 1945. Paguritherium alatum n. g., n. sp., an entoniscian parasite of Pagurus longicarpus. Journal of Parasitology, 31: 198-204.) recorded that P. alatum had a prevalence of 0.8 % (38 of 4600) in P. longicarpus collected in Massachusetts. Similarly, in New Jersey, only 4 of 3703 (0.11 %) of the same hermit crab were parasitized with P. alatum (McDermott, 1998McDermott, J.J. 1998. Prevalence of two epicaridean isopods (Bopyridae and Entoniscidae) associated with the hermit crab Pagurus longicarpus Say, 1817 (Anomura) from the New Jersey coast (U.S.A.). Journal of Parasitology, 84: 1042-1045.); both sexes of crabs harbored entoniscids. Adkison and Heard (1978Adkison, D.L. and Heard, R.W. 1978. Description of a new genus and species of Pseudioninae (Isopoda: Bopyridae) parasite of the hermit crab Pagurus annulipes (Stimpson) from North Carolina. Proceedings of the Biological Society of Washington, 91: 408-417. ) found 1.0 % (3 of ~300) of the same hermit crab parasitized in North Carolina. Reinhard (1945Reinhard, E.G. 1945. Paguritherium alatum n. g., n. sp., an entoniscian parasite of Pagurus longicarpus. Journal of Parasitology, 31: 198-204.) concluded that even if the hemocoel of crabs was more carefully examined for developing parasites and the mature females dissected in search of males, it was unlikely that the prevalence would be more than about 2 %.

Entoniscids such as P. alatum have been documented to cause castration of hosts and the reduction in size and morphology of the egg-bearing pleopods (Reinhard and Buckeridge, 1950Reinhard, E.G. and Buckeridge, F.W. 1950. The effect of parasitism by an entoniscid on the secondary sex characters of Pagurus longicarpus. Journal of Parasitology, 36: 131-138.; McDermott, 1998McDermott, J.J. 1998. Prevalence of two epicaridean isopods (Bopyridae and Entoniscidae) associated with the hermit crab Pagurus longicarpus Say, 1817 (Anomura) from the New Jersey coast (U.S.A.). Journal of Parasitology, 84: 1042-1045.). However, in the present study, E. creplinii was not found to hinder host gonad development, reproduction or impact secondary sex characteristics; this is similar to the lack of such impacts on hosts caused by some other entoniscids (McDermott et al., 2019McDermott, J.J.; Williams, J.D. and Boyko C.B. 2019. A new genus and species of parasitic isopod (Bopyroidea: Entoniscidae) infesting pinnotherid crabs (Brachyura: Pinnotheridae) on the Atlantic coast of the USA, with notes on the life cycle of entoniscids. Journal of Crustacean Biology, 40: 97-114.). As found by Müller (1871Müller, F. 1871. Bruchstücke zur Naturgeschichte der Bopyriden. Jenaische Zeitschrift für Medicin und Naturwissenschaft, 6: 53-73, pls. 3, 4.), the parasitized hosts from North Carolina and Florida were found singly in their chaetopterid tubes; however, these porcellanids are almost always (> 90 % of the time) found as male-female pairs (McDermott, 2005McDermott, J.J. 2005. Biology of the brachyuran crab Pinnixa chaetopterana Stimpson (Decapoda: Pinnotheridae) symbiotic with tubicolous polychaetes along the Atlantic coast of the United States, with additional notes on other polychaete associations. Proceedings of the Biological Society of Washington, 118: 742-764.). Thus, the parasites may induce changes (subtle morphological, chemical or behavioral) that make the hosts unsuitable mates. Additional studies on E. creplinii are needed to allow the description of male specimens of this species as well as expand our knowledge of the potential impacts of this parasite on its host and other symbiotic web members.

ACKNOWLEDGEMENTS

John McDermottWilliams, J.D. 2018. Obituary: Dr. John J. McDermott (1927-2017). Proceedings of the Biological Society of Washington, 131: 1-6. appreciated the help of many individuals during several years of field studies along the Atlantic coast (C. G. Bookhout, J. D. Costlow and F. J. Vernberg at Duke University and A. A. Myrberg at University of Miami). In addition, he was thankful for assistance in the field from W. R. Belzer, J. A. Cole, J. J. McDermott III, T.M. McDermott, M. H. Taylor and F. R. Weis. This research was partially supported by funds to J. McDermott from National Science Foundation grants (G11448, G22068, and B959), post-doctoral research grants from Duke University Marine Laboratory, and Franklin and Marshall College.

REFERENCES

Publication Dates

History