Hemioniscus pagurophilus, Williams & Boyko, 2006

Williams, Jason D. & Boyko, Christopher B., 2006, A new species of Tomlinsonia Turquier, 1985 (Crustacea, Cirripedia, Trypetesidae) in hermit crab shells from the Philippines, and a new parasite species of Hemioniscus Buchholz, 1866 (Crustacea, Isopoda, Hemioniscidae), Zoosystema 28 (2), pp. 285-305 : 298-304

Hemioniscus pagurophilus n. sp.

(Figs 7-9)

TYPE MATERIAL. — Philippines. Bataan, Morong, 14°41’N, 120°16’E, in Tomlinsonia mclaughlinae n. sp. from shell of Cantharus undosus inhabited by ♀ Calcinus gaimardii , 25.IV.1999, ♂ holotype 1.0 mm ( USNM 1084119 ), 1 ♂ paratype ( ZRC 2006.0006 ); in Tomlinsonia mclaughlinae n. sp. from shell of C. undosus inhabited by ♀ C. gaimardii , 25.IV.1999, 5 ♂♂ paratypes ( USNM 1084120 ). — Oriental Mindoro, Puerto Galera, Big Lalaguna Beach , 13°30’N, 120°57’E, in Tomlinsonia mclaughlinae n. sp. from shell of Peristernia incarnata inhabited by ovigerous ♀ C. gaimardii (3.8 mm SL), 21.VII.1997, immature ♀ allotype 0.9 mm (USNM 1084121 ), 2 immature ♀♀ paratypes ( USNM 1084122 ), 2 ♂♂ paratypes 0.86 mm ( USNM 1084123 ; 1 on SEM stub, 1 in alcohol) .

ADDITIONAL MATERIAL EXAMINED. — Philippines. Bataan, Morong , 14°41’N, 120°16’E, in Tomlinsonia mclaughlinae n. sp. from shell of Cantharus undosus inhabited by ♀ Calcinus gaimardii , 25.IV.1999, 1 ♂ (JDW personal collection).

ETYMOLOGY. — From the Greek, pagouros (= kind of crab) and philos (= who loves), latinized as pagurophilus , and meaning lover of hermit crabs. The name refers to the role played by the isopod in sterilizing the cirripede and therefore helping hermit crabs by avoiding weakening of their shells by the barnacle and for the inordinate fondness for paguroids by Patsy A. McLaughlin, the best friend a hermit ever had.

DISTRIBUTION. — Found in the mantle cavity of Tomlinsonia mclaughlinae n. sp., in shells of Calcinus gaimardii hermit crabs from Bataan and Oriental Mindoro provinces, central Philippines; shallow subtidally (<5 m).

DIAGNOSIS. — Male: cuticular surface with distinct striations, prominent on coxal plates. Head widest at posterolateral junction with pereomere 1, eyes present. Antennule of three articles, basal article with seven teeth and cuticular scale-like ridges, article 1 overlapping basal article of antenna. Antennae of nine articles, articles 1-3 cylindrical with cuticular ridges; flagellar articles much narrower than peduncular articles, proximal flagellar article longest, flagellar articles 2-5 of approximately equal length. Oral cone anteriorly directed. Pereomeres 5 and 6 broadest. Body pigmentation lacking. Pereomeres with entire coxal plates. Pereopods 1 and 2 stout, gnathopodal, with dactyli entire; propodus smooth; ventral surfaces of carpus and merus with large flat cuticular ridges. Pereopods 3-7 ambulatory, smooth; dactyli long, straight, slender, smooth margins, with ventral setal comb, tip hooked with long (pereopods 3-5) or short (pereopods 6, 7) seta at base of hooked tip; propodi straight, medially inflated (pereopods 3-5 broader than 6 and 7), with ventral setal comb. Pleon with five pleopods. Ventral abdominal lobe between first pair of pleopods with two lateral projections and median smooth concave margin. Pleotelson quadrangular, endopods approximately twice as long as exopods.

Immature female with posterior four pleon segments fused with lateral undulations.

DESCRIPTION

Male (Figs 7A, B, D; 8; 9)

Length 1.00 mm, maximum width 0.33 mm at pereomere 4, head length 0.12 mm, pleon length 0.44 mm (holotype); body tear-drop-shaped (Figs 7A; 8A). Cuticular surface with distinct striations, prominent on coxal plates (Fig. 8C, D).

Head anterior margin ovate, posterior margin concave, widest at posterolateral junction with pereomere 1 (Fig. 7A). Eyes diffuse, moderately large (approximately 40 µm in maximal length) located proximolaterally, eyes with irregular pigment most prominent around laterally directed edge (Fig. 7A). Antennule of three articles (Figs 7B; 8B, C), first (basal) article with seven teeth approximately three times longer than broad, cuticular scale-like ridges present, most prominent on mesial margin, proximolateral lobe distally tapered with group of setae along sinuous cuticular ridge; article 1 slightly overlapping basal article of antenna, article 2 with cuticular scale-like ridges along distal margin, 4-6 setae on distal margin, article 3 with two flagella and bundle of aesthetascs (Figs 7B; 8C). Antennae of nine articles (four peduncular and five flagellar) (Fig. 7B); articles 1-3 cylindrical with cuticular scale-like ridges (Fig. 8C); flagellar articles much narrower than peduncular articles, each with a terminal seta, proximal flagellar article longest, flagellar articles 2-5 of approximately equal length, article 5 with four distal setae (Fig. 7B). Oral cone anteriorly directed (Figs 7B; 8B).

Pereomeres 5 and 6 broadest, tapering anteriorly and posteriorly. Body pigmentation lacking. Pereomeres with entire (not toothed) coxal plates 1-7 (Fig. 8B, D). Pereopods 1 and 2 short and stout, gnathopodal with dactyli entire (non-bifid) and having few large cuticular scale-like ridges and rows of minute setae on dorsal edge (Fig. 8E); propodus smooth with few rows of short setae distodorsally, rows of minute setae along distal edge of propodus around joint with dactylus, with setae along edge apposed to dactylus; ventral surfaces of carpus and merus with large flat cuticular scale-like ridges and few long setae (Fig. 8E). Pereopods 3-7 ambulatory, smooth; dactyli long, straight, slender, smooth margins, with ventral setal comb, tip hooked via ventral indentation of margin with long (pereopods 3-5) or short (pereopods 6, 7) seta at base of hooked tip (Fig. 9A, B); propodi straight, medially inflated (pereopods 3-5 broader than 6 and 7), with ventral setal comb and one large stout ventral seta approximately 1/2 (pereopods 3-5) or 1/3 (pereopods 6 and 7) from distal margin and second single smaller seta near junction with dactylus (Fig. 9B); carpi of pereopods 3-7 with one stout terminal ventral seta; meri with one thin terminal ventral seta.

Pleon with five pleopods composed of basis (sympod), exopod, and endopod (Fig. 9C). Sympods with two medially directed setae bearing 3-branched tips, endopods and exopods with plumose setae (five setae each on pleopod 1, three setae on endopod of pleopod 5), with laterally directed seta shorter than other setae on exopod. Ventral abdominal lobe between first pair of pleopods with two lateral projections and median smooth concave margin (Fig. 9C). Pleotelson quadrangular, endopods approximately twice as long as exopods, basis with one distolateral seta, endopods and exopods with terminal setae (Fig. 7D).

Immature female (Fig. 7C)

Maximal body length 0.90 mm, maximal width 0.31 mm at segment 4, pleon length 0.32 mm. Similar to male in dorsal aspect, except for fused posterior four pleon segments appearing as an irregular sac posteriorly on the body and with lateral undulations indicating position of pleomeres (Fig. 7C).

REMARKS Identification of this material was hampered by the confused taxonomy of cryptoniscid isopods in general and that of barnacle parasites in particular (e.g., Nielsen & Strömberg 1965, 1973b). The following comparisons with all other species of cryptoniscoids known to parasitize barnacles were necessary to reach our conclusions.

Cryptothir Dana, 1852 (incertae sedis): the type species, C. minutus Dana, 1852 , was incompletely described and figured ( Dana 1852, 1855) from an Indo-West Pacific barnacle of the genus Creusia (material lost). It may be synonymous with Hemioniscus or at least belong to the Hemioniscidae (in which case the family would have to be called Cryptothiridae ). However, as noted by Grygier (1993), it is probably best to leave Cryptothir as incertae sedis until such time as additional material can be examined.

Liriopsis Schultz in Müller, 1864 ( Cryptoniscidae ): the new material shows no resemblance to either Liriopsis pygmaea (Rathke, 1843) or L. monophthalma Fraisse, 1878. The most obvious difference is that the females of the new species are only posteriorly degenerated, while those of Liriopsis spp. are unsegmented and form a double lobed shape. Males of the new species have only moderately long dactyli on pereopods 6 and 7, whereas those of Liriopsis spp. are exceedingly long and thin.

Hemioniscus Buchholz, 1866 (Hemioniscidae) : the males of the new species are similar to those of the type species Hemioniscus balani balani Buchholz , 1866 (see Goudeau 1967, 1970), but differ in that the coxal plates of H. balani balani have seven or eight teeth on the first plate, and four or five on posterior plates, while the new species has no teeth on any of the coxal plates. Other differences include strong cuticular striations on the anterolateral expansion of the basal antennule segment (weakly striated in H. balani balani ), considerably shorter distal teeth on the basal antennular article in H. pagurophilus n. sp., medially inflated propodi on pereopods 3-5 (distally inflated in H. balani balani ), pronounced indentation on the ventral margin near the tip of dactyli (no such indentation in H. balani balani ), and ventral median lobe between first pair of pleopods with concave margin (trilobed in H. balani balani ). Shared characters between H. balani balani and H. pagurophilus include: moderate striation of the dorsal cuticle, seven teeth on the basal article of the antennule (occasionally eight in H. balani balani ), cuticular ridges on the second article of the antennule, moderate setation on the terminal article of the antennule, eyes present, cuticular ridges on the dactyli of the first two pereopods, and moderate dorsal expansion of the meri of the pereopods. The development of the females is essentially identical to that seen in H. balani balani . All of the differences cited above between H. pagurophilus n. sp. and H. balani balani are also true when comparing H. pagurophilus n. sp. and H. balani japonica Ogawa & Matsuzaki, 1985 . The description of H. balani japonica is somewhat difficult to interpret, the line drawings are poor and Ogawa & Matsuzaki only compared their material with older descriptions of H. balani balani (e.g., Buchholz 1866; Sars 1899) and not with the more detailed studies (e.g., Goudeau 1967, 1970). Many of the purported distinguishing morphological characters between the subspecies ( Ogawa & Matsuzaki 1985: table 1) do not allow for differentiation, as their information for variation in H. balani balani is incomplete. The two taxa do show quite different coxal plate formulae, and this suggests that they represent distinct species rather than subspecies. However, in the absence of specimens of H. balani japonica , we are unwilling to make any definite opinion on the matter and retain the two taxa as subspecies for the present. The only other species ever placed in this genus was H. socialis Pérez, 1900, which is now considered a synonym of H. balani balani (Caullery 1908) . This genus is the type of Hemioniscidae Bonnier, 1900 .

Leponiscus Giard, 1887 (Hemioniscidae) : Giard (1887) did not select a type species from the two he included in this genus. Leponiscus anatifae Giard, 1887 was described by reference to the figures of the unnamed taxon reported by Hesse (1867), and is an available name; L. pollicipedis Giard, 1887 was accompanied by neither description nor illustration and is a nomen nudum. The type species of the genus must therefore be L. anatifae . Unfortunately, the figures of Hesse (1867) show no clear characters to distinguish L. anatifae from Hemioniscus spp. and Leponiscus must be considered inquirenda within the Hemioniscidae . Gruvel (1901) described the only other species of Leponiscus , L. alepadis , but it differs markedly from L. anatifae and appears to belong in the Crinoniscidae (see below). Gruvel (1902) also cited “ Leponiscus hessei Giard ” but as Giard never mentioned such a name, it is presumed that L. hessei is a lapsus for L. pollicipedis , which was not cited by Gruvel (1901, 1902). The conclusions of Bocquet-Védrine & Bocquet (1972) that Leponiscus Giard, 1887 is a nomen nudum, and that the taxon is valid from Gruvel (1901) (with L. alepadis as the type species) are clearly incorrect as one of the originally included species in Leponiscus Giard, 1887 is an available name. However, their statement that L. alepadis is actually allied to Crinoniscus was correct, and their suggestion that Leponiscus Giard, 1887 may be identical to Hemioniscus is a reasonable hypothesis, albeit an untestable one in the absence of lepadid cryptoniscid parasite material.

Crinoniscus Bonnier, 1900 (Crinoniscidae) :the new material does not resemble the type and sole species Crinoniscus equitans ( Pérez, 1900) , the only species currently placed in the family ( Pérez 1900a, b). Males of C. equitans lack teeth on the basal segment of the antennule and females metamorphose into a crossshaped incubatory pouch. Leponiscus alepadis Gruvel, 1901 appears more closely related to Crinoniscus than either Leponiscus or Hemioniscus as the males also lack teeth on the basal antennular segment, and the females show complete metamorphosis. However, the female body shape of L. alepadis resembles an ovoid sac with small lobes at the corners, rather than the elongate cross of Crinoniscus suggesting that L. alepadis is not congeneric with C. equitans and requires its own genus (Boyko & Williams pers. obs.). Such action is outside the scope of this work.

Gorgoniscus Grygier, 1981 (unplaced): males of the new material differ from males of sole species of Gorgoniscus , G. incisodactylus Grygier, 1981 , in the following: basal article of antennule with seven teeth (five in G. incisodactylus ) and tapered proximolateral lobe (lobe lacking in G. incisodactylus ), moderate cuticular striations on whole body (dense cuticular striations on head and first pereomere in G. incisodactylus ), and dactyli of pereopods 6 and 7 with smooth margins (notched in G. incisodactylus ). Females of G. incisodactylus are globose and lack most appendages and an obvious head, whereas immature females of the new species retain the anterior portion of the body as recognizably isopod-like. Grygier (1981) left Gorgoniscus unplaced as to family, suggesting that a new family might be required for it. This genus still remains unplaced, and no further specimens have been reported.

Scalpelloniscus Grygier, 1981 (? Hemioniscidae ): males of both S. penicillatus Grygier, 1981 , and S. binoculis (Menzies & George, 1972) differ from the new material in having toothed coxal plate formulae similar to that seen in H. balani balani , more setae on the third articles of the antennules, lack of cuticular ridges on the second article of the antennules, strongly dorsally inflated meri on the pereopods, and lack of eyes. Mature females of Scalpelloniscus are unknown. Based on the current classification scheme, Scalpelloniscus appears to belong to the Hemioniscidae rather than the Cryptoniscidae , but all the families of Cryptoniscoidea need clearer diagnoses and mature females are needed for Scalpelloniscus to determine the degree and form of their metamorphosis.

In conclusion, examination of the new species of cryptoniscid from the Tomlinsonia hosts indicates that they are best placed in the Hemioniscidae , and are rather close to Hemioniscus balani balani . There are at least as many differences between our Philippine material and H. balani balani as between Hemioniscus and Scalpelloniscus . However rather than erect a new genus for this new species, we have conservatively placed it within Hemioniscus as the males share many characters with those of the type species, and differ most obviously only in the dentition of the coxal plates, a variable feature in other cryptoniscoid families as currently defined.The females of H. balani balani and H. pagurophilus n. sp. have very similar development with nearly identical degeneration of the posterior segments into an irregularly shaped incubatory pouch, while retaining the anterior segments in unmodified form. In order to include the new species in Hemioniscus, it becomes necessary to modify Nielsen & Strömberg’s (1973b) definition of Hemioniscidae as follows: dorsal cuticular ridges relatively prominent; eyes present; basal segment of antennule with seven or eight teeth on distal margin; oral cone anteriorly directed; coxal plates with or without toothed ventral margins; posterior margin of pleotelson entire;parasitic on cirripedes. This definition is acknowledged to be a temporary one, as it is certain that future phylogenetic analyses of cryptoniscoid isopods will result in rearrangement of genera based on shared derived characters rather than shared host taxa.

ECOLOGY Of the 31 potential host barnacles examined during 1997 and 1999, three were found to harbor Hemioniscus pagurophilus n. sp. (total prevalence = 9.7%); numbers of isopods within the mantle cavity of the hosts ranged from two to six. Interestingly, numerous specimens of an unidentified species of Trypetesa from the same localities were not found parasitized by H. pagurophilus n. sp.