JOURNAL OF CRUSTACEAN BIOLOGY, 18(3): 590-596, 1998

TIARINION TEXOPALLIUM, NEW SPECIES, AN ENTONISCID ISOPODINFESTING MAJID CRABS (TIARINIA SPP.) FROM THE

GREAT BARRIER REEF, AUSTRALIA

Jeffrey D. Shields and Landon A. Ward

;

ABSTRACT

An entoniscid isopod, Tiarinion texopallium, new species, is described from majid crabs in thegenus Tiarinia. Until now, the genus Tiarinion consisted of a single species, found from Japan andAustralia. The new species is the second member of the family Entoniscidae to be described fromAustralia, and the first to be described from the Great Barrier Reef. The female of the new speciescan be distinguished from Tiarinion fulvus by the number and arrangement of the ovarian processes;the male, by the body segmentation, spination of the pereiopods, and the distinct lack of abdomi-nal spines. The epicaridium of the new species can be distinguished from that of T.fulvus by thewell-developed antennule, the spination of the antennae and pereiopods, and the facies of the un-usual sixth pereiopod. The cryptoniscium larva has an unusual antennule that is highly modified asan apparent clasping or cutting appendage. The cryptoniscium also possesses unusual epipodal (?)spines on the antennae and pereiopods. The new species of Tiarinion was found in 3.2% (71216)of the population of Tiarinia spp. on the Lizard Island reef complex, but none (0/15) of the crabson the Heron Island reef complex. Double infestations were not observed, nor were double infes-tations with other crustacean parasites.

I ~

Entoniscid isopods are unusual internalparasites of crabs and shrimps. Female en-toniscids are usually modified beyond recog-nition of most isopod characters, with themarsupium grossly inflated as a hood that insome cases extends dorsally over the cepha-Ion. The male and larval entoniscids, how-ever, appear more isopodlike with a dorsoven-trally compressed body, complete segmenta-tion, and pereiopods. Mature females aresurrounded by a host response sheath, withan external communication to the environ-ment via a small hole or furrow in the cara-pace of their hosts (Giard and Bonnier, 1887).Most entoniscids are parasitic castrators, al-though complete castration may depend uponthe status of the host and the duration of theinfestation. In some cases, entoniscids canfeminize male hosts (e.g., Giard, 1887; Veil-let, 1945; Reinhard, 1956).

The genus Tiarinion contains a singleknown species, T. fulvus Shiino, 1942, thatparasitizes Tiarinia cornigera Latreille fromJapan (Shiino, 1942). We describe a new spe-cies of Entoniscidae from majid crabs in thegenus Tiarinia found on the Great BarrierReef, Australia. The isopod belongs in thegenus Tiarinion because (1) the first and sec-ond oostegites are well developed, while theother oostegites are not well differentiated;(2) the female possesses two ventrolateralprocesses (Shiino, 1942); (3) the epicaridium

"

possesses an elongate sixth pereiopod with ahighly modified, oblate dactylar process (Shi-ino, 1942); and (4) the parasite infests a sim-ilar host species. The new species is the firstentoniscid to be described from the GreatBarrier Reef, and the second to be describedfrom Australia (see Shields and Earley, 1993).

MATERIALS AND METHODS

The crab hosts were collected at Heron Island and Wis-tari Reef complex, Capricorn group, and Lizard Islandreef complex, Central Barrier Reef Zone, under valid sci-entific permits (GBRMPA G89/428, G90/383, G91/500,G92/499). Collections were made by hand using a snorkelon reef flats, rubble fields, and by SCUBA on subtidalreef crests and reef slopes. Coral rubble and small patchesof live coral (Acropora spp., Pocillopora spp., Seriato-pora spp.) were collected, and carefully chipped apartwith a hammer. Small crabs residing in the rubble andcoral were removed to containers of sea water for laterdissection. Only one host was identified to species,Tiarinia takedai Griffith and Tranter, 1986. Others wereidentified as Tiarinia spp.

Basic parameters of the crab population were exam-ined, including size (carapace length), sex, and repro-ductive condition of the females (i.e., ovigerous, or re-cently mated). Each crab was examined externally be-fore the carapace was gently removed, and the internalorgans were examined with a stereomicroscope.

Female entoniscids were fixed immediately in either10% Formalin-sea water solution, or Davidson's fixative(alcohol-formalin-acetic acid). Later, male entoniscidswere dissected free of the marsupium of the female. Maleand larval isopods were cleared in glycerin to aid in theobservation of various morphological features. Measure-ments were made with an ocular micrometer using stereo-and compound microscopes.

590

SHIELDS AND WARD: NEW ENTONISCID ISOPOD FROM AUSTRALIA 591

A B

Fig. 1. Female of Tiarinion texopallium. A, female within host sheath; B, female with marsupium (no host sheath);C, juvenile female. Bars = 1 mm. a = antenna, m = maxilliped, op = posterior ovarian projections, 02 = oostegite 2;pi, p2, p3, p4 = pleopods.

Representative specimens of the parasites and crabshave been lodged at the Invertebrate Zoology Collection,Queensland Museum, P.O. Box 300, South Brisbane,4101, Australia, and the Department of Invertebrate Zo-ology, Smithsonian Institution, Washington, D.C., 20560.The crab hosts, Tiarinia spp., were identified with the helpof Peter Davie (Queensland Museum).

RESULTS

Description

Tiarinion texopallium, new speciesFigs. 1-4

Type Material.-Holotype C((QM W22015) with at-tached 0 (not examined), and cryptoniscium (slide, para-type W220 16) deposited in the Invertebrate ZoologyCollection, Queensland Museum, P.O. Box 300, SouthBrisbane, 4101, Australia. The female and male were notdissected.

Paratypes.-Mature C((Mermaid Cove, Lizard Island, 22April 1991; QM W220 16) deposited in the QueenslandMuseum. Other paratypes: Juvenile C( (Lizard Island, BlueLagoon, 6 March 1992, 3-5 m depth, USNM 284169),mature C((MacGillivray Reef, Lizard Island, 14 April1990, USNM 284170), 0, and cryptoniscium (North Point,Lizard Island, 20 February 1993, USNM 284171) de-posited in the National Museum of Natural History, Crus-tacean Collection, Smithsonian Institution, U.S.A. Other

specimens (including dissected female) retained in thecollection of the first author.

Type Locality.-Australia, Queensland, Lizard Island,Mermaid Cove, at a depth of 3-5 m. Date of collection:I March 1992.

Type Host and Site of Infestation.-Tiarinia sp., in thehemocoel of the host, surrounded by a host responsesheath.

Female (from type specimen, Fig. lA-C):Approximately 9 mm on longest axis. Ce-phalogaster white. Oral cone present, with ex-ternal antennae lying on anteroventral surfaceof cephalogaster. Thorax unsegmented, withextensively modified marsupium. Marsupiumwith eggs or developing epicaridean larvae.Hood (ascendant lamella) of first oostegitemoderately developed. Transverse and recur-rent lamellae fused, extending to midportionsof ovarian processes. Oostegite 2 fingerlike,small, delicate, fused anteriorly with firstoostegite. Oostegite 2 lying ventrally on crab,and twisted to project dorsally on parasite; ap-pearing as dorsal ovarian process. Oostegites3-5 indistinct. Pereiopods not observed. Twopairs of large, laterally projecting ovarianprocesses (medioventral, posteroventral). Ab-domen white. Pleural lamellae developed asgills; with simple folds, variable in size withlamella 1 larger than lamella 2. Lamellae 3and 4 simple, weakly developed, posterior toheart. Pygidium well developed. Ova rangingin size from 100 f.lmin early development to250 f.lm as epicaridea.

Male (from para types, Fig. 2A-C): Totallength of males approximately 3.5 mm; totalwidth, 500-600 f.lm. Cephalon fused withfirst thoracic segment. Antennules absent. An-tennae developed as short plates, fused me-dially, with several blunt setae on lateral mar-

AB

Fig. 2. Male of Tiarinion texopallium. A, lateral view, bar = 250 !lm; B, pereiopod I, s = spine, bar = 50 !lm; C,telson, bar = 100 !lm.

A c 0

E

Fig. 3. Epicaridium larva of Tiarinion texopallium. A, lateral view, bar = 50 !lm; B, pereiopod I, bar = 25 !lm; C,highly developed pereiopod 6, bar = 25 !lm; D, antenna, bar = 10 !lm; E, antennule, bar = 10 !lm.

B

SHIELDS AND WARD: NEW ENTONISCID ISOPOD FROM AUSTRALIA 593

A

E

H

B

D

rfff{Ja(

Fig. 4. Cryptonsicium larva of Tiarinion texopallium. A, body, bar = 250 11m; B, antenna, bar = 25 11m; C, highlymodified antennule, bar = 50 11m; D, maxilliped, bar = 25 11m; E, pereiopod 1, bar = 25 11m; F, tuft of spines adja-cent to basis of antenna (and adjacent to coxae of pereiopods), bar = 25 11m; G, pereiopod 6, bar = 25 11m; H, mo-pod, bar = 25 11m; I, pleopod, bar = 25 11m.

594 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 18, NO.3, 1998

gin. Mandibles within oral cone. Maxillipedsand maxillae not observed. Thorax with 6 freesegments; segment 7 without limbs. Pereio-pods simple, 5-segmented; dactyl and prop-odus barely spinulose; short, single spine onpropodus. Abdomen with 6 free segments;without abdominal spines on segments 2 or3. Telson nude, bifurcated.

Epicaridium Larva (from 6 specimens, Fig.3A-E): Observations made on developing lar-vae; completely developed larvae not ob-served. Spination possibly incomplete. Totallength approximately 250 ~m (withouturopods) by 65-70 ~m in width (excludinglimbs). Antennules with 4 segments; basalsegment bearing 2 distal spines; apical seg-ment blunt, without setae. Antennae with 7segments; fourth segment with distally pro-jecting, lateral spine. Mandibles, maxillipeds,and maxillae not observed. Pereiopods 1-5subchelate. Pereiopod 6 subchelate, elongate,setose, highly modified. Chela an oblate pro-cess; without setae. Dactyl arising from me-dial margin of propodus. Pleopods simple, bi-ramous, without setae. Uropods simple, bi-ramous, without setae.

Cryptoniscium Larva (from 2 specimens, Fig.4A-I): Total length approximately 800 ~m bywidth of approximately 125 ~m. Antennulehighly modified. Segment 1 robust, highlysclerotized with knifelike digitations project-ing posteriorly. Segment 2 projecting antero-laterally to segment 1, highly sclerotized,with 4 or 5 digitate processes. Segment 3thinly flattened, with numerous hairlike aes-thetascs. Segments 4 and 5 cylindrical, bear-ing 2 or 3 elongate setae. Antenna with 8 seg-ments, each segment bearing spine as distalprocess. Prominent tuft of spines as epipod(?) on coxal segment 0) at base of antenna.Maxilliped robust; basis with strong lateralridges. Thoracic segments widely flanged,with spinules along posterior margin of eachsegment. Pereiopods with robust spines;epipodal (?) tuft of coxal spines. Dactyl of pe-reiopod 1 elongate, bearing 3 spinules; car-pus with elongate spine. Pereiopod 6 bear-ing single ventral spine on basis, ischium, andmerus; carpus with 2 spines; dactyl unarmed.Abdominal segments unadorned. Pleopodsuniform with robust spine projecting medially;smaller spine at base of endopod. Endopodand epipod with numerous robust setae. Uro-

pod bifurcated; with elongate spine arisingfrom base; robust spine arising medially.

Etymology.-The specific name is derivedtexo (L., twist) and pallium (L., coat) andrefers to the orientation of the second ooste-gite, which is twisted dorsolaterally to givethe appearance of a dorsal ovarian process.

DISCUSSION

Female entoniscids have few distinguish-ing characters. The female of T. texopalliumis distinguished from that of T. fulvus by thepoorly developed oostegites, the consistentlytwisted orientation of oostegite 2 as a dorso-medial projection, and the lack of develop-ment of oostegites 3, 4, and 5. In contrast, T.fulvus has well-developed oostegites (Shiino,1942).

The dwarf male of T. texopallium can bedistinguished from that of T. fulvus by thespine on the dactyl of the pereiopods, the lackof the chitinous spines on the abdomen, andthe nude telson. Males of T. fulvus have nospination on the pereiopods, a distinct spineon abdominal segments 1 and 2, and a"thorny" tel son (Shiino, 1942).

The epicaridia of T. texopallium were notfully developed. Hence, comparisons withthat of T.fulvus may not be complete. In spiteof that, the epicaridium of T. texopallium isdistinguished from that of T. fulvus by thewell-developed antennule with two prominentspines, a spine on the fourth antennular seg-ment, and the general facies of the sixth pe-reiopod, which has a different spination pat-tern (the tip of the process is less developed,and the ventral spine on the dactyl is absent).The epicaridium of T. fulvus has a spine onthe merus of the pereiopods, a spine on thepenultimate antennal segment, and a morehighly developed dactylar process on thesixth periopod (Shiino, 1942).

The cryptoniscium of T. texopallium differsnoticeably from that of T. fulvus. The cryp-toniscium of T. texopallium has well-devel-oped spines on the pereiopods, a robust spineon each segment of the antenna, an unusualand highly modified antennule, and uropodswith two robust spines. The presence of thedistinct tufts of robust spines on the anten-nae and pereiopods has not been reported forthis genus nor has it been reported in othermembers of the family. While members of the

SHIELDS AND WARD: NEW ENTONISCID ISOPOD FROM AUSTRALIA 595

Table I. Location, date, and prevalence data for Tiarinion texopallium from the Great Barrier Reef. Location key:nw = Wistari north, sb = Shark Bay, bp = Blue Pools, cg = Coral Garden, cy = Canyons, se = Lagoon southeast, mr= MacGillivrays Reef, si = South Island, bl = Blue Lagoon, mc = Mermaid Cove, bis = near Bird Island, cc = Co-conut Beach, yr = Yonge Reef, np = North Point. Locations shown in boldface had crabs with the parasite.

Epicaridea may have robust antennules (e.g.,Nielsen and Stromberg, 1973), the highlymodified nature of the antennule of T. tex-opallium has not been noted in the family.The antennule is markedly different from anyyet described. The cryptoniscium of T. ful-vus has a single spine on the pereiopod, acompletely different spination pattern on theantenna, a simple antennule with elongate se-tae, and a series of spines on the uropod (Shi-ino, 1942).

Without consideration of castration, therewas little gross pathology associated with theinfestations. In patent infestations, the midgutof the host was pressed laterally against theinternal struts of the branchial carapace. Thehepatopancreas and surrounding connectivetissues were displaced laterally by the devel-oping female. The developing and matureparasites were found in the hemocoels of theirhosts with their cephalons adjacent and dor-sal to the foregut, but ventral to the he-patopancreas. A pore through the carapaceof the host for communication with the ex-ternal environment was not observed, but theorientation of the abdomen of the parasitesuggests that the exit pore was located ven-trally on the sternum.

Tiarinion texopallium was not found in thesmall collections made from the Heron Islandreef complex (Table 1). The isopod had anoverall prevalence at the Lizard Island reef

complex of 3.5%. Two juvenile females werefound, and all of the female parasites occurredsingly in each host. One to two males werefound at the junction between the abdomenand the thorax of each mature female. Twocryptoniscium larvae were found on maturefemale isopods.

The hosts, Tiarinia spp., had an unusuallyhigh diversity of other pathogenic parasites.A rhizocephalan barnacle, a bopyrid isopod(Portunicepon tiariniae Shiino) with a cabir-opsid hyperparasite, a haplosporidian in sporo-cysts, a trematode (metacercaria), and pre-sumptive infestations with a Synophyra-likeciliate were all found in individual hosts.While double infestations of two different spe-cies of parasitic castrators may be commonin some crustaceans (Giard and Bonnier, 1887;Shiino, 1942; Veillet, 1945), no double infes-tations were observed in Tiarinia spp.

ACKNOWLEDGEMENTS

We thank Rob Gould, Ted Warren, Ingo Ernst, JulieShields, and Fiona Wood for their help with the collec-tions and dissections, and Peter Davie of the QueenslandMuseum for the identification of Tiarinia spp. Lyle Vail,Anne Hoggett, and Lance and Marianne Pearce providedlogistical and technical services at Lizard Island MarineStation. This work was supported, in part, by a Univer-sity of Queensland Postdoctoral Fellowship to JDS, anAustralian Research Council Grant (A191940) to JDS,and an NSF REU and Rouse-Bottom Undergraduate Fel-lowship to LAW. This is Contribution Number 2090 fromthe Virginia Institute of Marine Science.

Numberof NumberofDate hostsinfested hostsexamined Prevalence (%) Location

Heron Island October-November 1990 0 4 0 nw, sbMarch 1991 0 II 0 bp, cg, cy, nw,

sb, se

Lizard Island April 1990 I 3 33 mr, si, blOctober 1990 I 8 13 mc, mrApril 1991 0 13 0 bis

0 5 0 bl2 40 5 mc0 II 0 mr

March 1992 I 20 5 hi0 I 0 ccI 32 3 mc0 12 0 yr

February-March 1993 I 42 2 hi0 26 0 mcI 2 50 np

Total 8 230 3.5

596 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 18, NO.3, 1998

LITERATURE CITED

Giard, A. 1887. Parasitic castration and its influenceupon the external characters of the male sex, in the dec-apod Crustacea.-Annals and Magazine of Natural His-tory, 5th series, 19: 325-345. [French Version: Bulletinscientifique du Nord, Series 2, 10: 1-28.]

-, and J. Bonnier. 1887. Contribution a l'etude desBopyriens.-Travaux de I'Institut Zoologique de Lilleet du Laboratoire de Zoologie Maritime de Wimereux(Pas de Calais) 5: 3-272.

Nielsen, S.-O., and J.-O. Stromberg. 1973. Surface struc-ture of aesthetascs in Cryptoniscina (Isopoda Epi-caridea).-Sarsia 52: 59-74.

Reinhard, E. G. 1956. Parasitic castration of Crus-tacea.-Experimental Parasitology 5: 79-107.

Shields, J. D., and C. H. Earley. 1993. Cancrion aus-traliensis new species (Isopoda: Entoniscidae) foundin Thalamita sima (Brachyura: Portunidae) from Aus-tralia.-International Journal for Parasitology 23:601-608.

Shiino, S. M. 1942. On the parasitic isopods of the fam-ily Entoniscidae, especially those found in the vicinityof Seto.-Memoirs of the College of Science, KyotoImperial University, series B 17: 37-76.

Veillet, A. 1945. Recherches sur Ie parasitisme desCrabes et des Galathees par les Rhizocephales et lesEpicarides.-Annales de I'Institut Oceanographique deMonaco 22: 193-341.

RECEIVED: 3 April 1997.ACCEPTED: 29 October 1997.

Addresses: (JDS) Chesapeake Bay National EstuarineResearch Reserves in Virginia, and Department of Envi-ronmental Sciences, Virginia Institute of Marine Science,College of William and Mary, P.O. Box 1346, Glouces-ter Point, Virginia 23602, U.S.A. (e-mail: jeff@vims.edu);(LAW) Department of Marine Biology, Texas A&M Uni-versity, Galveston, P.O. Box 1981, Drop 561, Galveston,Texas 77553, U.S.A.