Tomlinsonia mclaughlinae, 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 : 288-298

Tomlinsonia mclaughlinae n. sp.

(Figs 1-6)

TYPE MATERIAL. — Philippines. Boracay, Rocky Beach, 11°57’N, 121°56’E, from shell of Drupella cornus (Röding, 1798) inhabited by ovigerous ♀ Calcinus gaimardii (H. Milne Edwards, 1848) (3.4 mm SL), 13.IV.1999, ovigerous ♀ holotype 8.15 mm max. length, 4.3 mm max. width ( USNM 1084093 ), ♂ allotype 0.71 mm ( USNM 1084094 ). — Puerto Galera, Big Lalaguna Beach , 13°30’N, 120°57’E, from shell of Peristernia incarnata (Kiener, 1840) inhabited by ovigerous ♀ C. gaimardii (3.8 mm SL), 21.VII.1997, 1 ♀ paratype with Hemioniscus ( USNM 1084095 ) ; from shell of Drupella cornus inhabited by ovigerous ♀ Calcinus minutus Buitendijk , 1937, 31.VII.1997, 1 ♀ paratype ( USNM 1084096 ) . — Puerto Galera, Coco Beach , 13°30’N, 120°56’E, from shell of D. cornus inhabited by ovigerous ♀ C. gaimardii , 12.I.1999, 1 ♀ paratype ( USNM 1084165 ; mantle on one SEM stub, cirri on separate SEM stub) . — Puerto Galera, Bayanan and Haligi Beaches , 13°29’N, 120°53’E, from shell of D. cornus inhabited by ovigerous ♀ C. gaimardii , 13.I.1999, 1 ♀ paratype ( ZRC 2006.0001 ) . — Bataan, Mabayo, 14°44’N, 120°16’E, from shell of Drupa grossularia Röding, 1798 inhabited by ovigerous ♀ C. minutus (2.85 mm SL), 21.II.1999, 1 ovigerous ♀ paratype ( ZRC 2006.0002 ) ; from unidentified gastropod shell inhabited by ♀ C. minutus (2.25 mm SL), 21.II.1999, 1 ♀ paratype ( ZRC 2006.0003 ) ; from shell of Morula granulata (Duclos, 1832) inhabited by ♀ C. minutus (2.2 mm SL), 21.II.1999, 1 ♀ paratype ( ZRC 2006.0004 ); from shell of D. grossularia inhabited by ♀ C. minutus (3.0 mm SL), 21.II.1999, 1 ♀ paratype ( USNM 1084097 ); from shell of Cantharus undosus (Linnaeus, 1758) inhabited by ♀ C. gaimardii (3.02 mm SL), 21.II.1999, 1 ♀ paratype ( ZRC 2006.0005 ); from unidentified gastropod shell inhabited by ovigerous ♀ C. minutus (2.18 mm SL), 21.II.1999, 1 ♀ paratype ( USNM 1084098 ); from unidentified gastropod shell inhabited by ovigerous ♀ C. minutus (2.82 mm SL), 21.II.1999, 1 ♀ paratype ( USNM 1084099 ); from unidentified gastropod shell inhabited by ♀ C. gaimardii (1.69 mm SL), 21.II.1999, 1 ♀ paratype ( USNM 1084100 ); from unidentified gastropod shell inhabited by ♀ C. gaimardii (2.34 mm SL), 21.II.1999, 1 ♀ paratype ( USNM 1084101 ); from unidentified gastropod shell inhabited by ♀ C. minutus (2.98 mm SL), 21.II.1999, 1 ♀ paratype ( USNM 1084102 ); from unidentified gastropod shell inhabited by ovigerous ♀ C. minutus (2.42 mm SL), 21.II.1999, 1 ♀ paratype, 1 ♂ paratype ( USNM 1084103 ); from unidentified gastropod shell inhabited by ovigerous ♀ C. gaimardii (3.31 mm SL), 21.II.1999, 1 ♀ paratype ( USNM 1084104 ; mouthparts on SEM stub); from unidentified gastropod shell inhabited by ovigerous ♀ C. minutus (2.9 mm SL), 21.II.1999, 1 ovigerous ♀ paratype 5.90 mm ( USNM 1084105 ); from unidentified gastropod shell inhabited by ovigerous ♀ C. minutus (2.54 mm SL), 21.II.1999, 1 ♀ paratype 5.9 mm max. length ( USNM 1084106 ; mouthparts on SEM stub); from unidentified gastropod shell inhabited by ♀ C. minutus (2.58 mm SL), 21.II.1999, 1 ♀ paratype 3.69 mm max. length, 2.07 mm max. width, 1 ♂ paratype 0.50 mm ( USNM 1084107 ). — Boracay , Rocky Beach , 11°57’N, 121°56’E, from shell of D. cornus inhabited by ♂ C. gaimardii (2.9 mm SL), 12.IV.1999, 1 ♀ paratype ( USNM 1084108 ), 1 ♂ paratype 0.68 mm ( USNM 1084109 ); from shell of D. cornus inhabited by ♀ C. gaimardii (3.85 mm SL), 12.IV.1999, 1 ♀ paratype ( USNM 1084110 ); from shell of Drupella rugosa (Born, 1778) inhabited by ovigerous ♀ C. gaimardii (3.5 mm SL), 15.IV.1999, 1 ♀ paratype ( USNM 1084111 ); from shell of D. rugosa inhabited by ♀ C. minutus (3.85 mm SL), 15.IV.1999, 1 ♀ paratype ( USNM 1084112 ); from shell of D. cornus inhabited by ovigerous ♀ C. gaimardii (3.7 mm SL), 15.IV.1999, 1 ovigerous ♀ paratype ( USNM 1084113 ). — Bataan, Morong, 14°41’N, 120°16’E, from shell of C. undosus inhabited by ♀ C. gaimardii , 25.IV.1999, 1 ♀ paratype with Hemioniscus ( USNM 1084114 ); from unidentified gastropod shell inhabited by ♀ C. minutus (3.0 mm SL), 25.IV.1999, 1 ♀ paratype ( USNM 1084115 ); from unidentified gastropod shell inhabited by ♀ C. minutus (3.25 mm SL), 25.IV.1999, 1 ♀ paratype ( USNM 1084116 ); from shell of D. grossularia inhabited by ovigerous ♀ C. gaimardii (3.6 mm SL), 25.IV.1999, 1 ♀ paratype ( USNM 1084117 ); from shell of C. undosus inhabited by ♀ C. gaimardii (5.2 mm SL), 25.IV.1999, 1 ♀ paratype with Hemioniscus ( USNM 1084118 ).

ADDITIONAL MATERIAL EXAMINED. — Philippines. Bataan, Morong , 14°41’N, 120°16’E, from unidentified gastropod shell inhabited by ♀ Calcinus latens (Randall, 1839) (2.2 mm SL), 28.II.1999, ♀ (JDW personal collection). — Bataan, Mabayo, 14°44’N, 120°16’E, from unidentified gastropod shell inhabited by ovigerous ♀ C. minutus (1.75 mm SL), 21.II.1999, 1 ovigerous ♀ (JDW personal collection).

ETYMOLOGY. — In honor of Patsy A. McLaughlin for her many years in pursuit of new and interesting taxa of hermit crabs, as well as for her gracious help in identifying specimens for those in need, including both of the present authors – for which we are grateful.

DISTRIBUTION. — Found in shells of Calcinus spp. hermit crabs from Aklan, Bataan, and Oriental Mindoro provinces in the central Philippines; shallow subtidally (<5 m).

DIAGNOSIS. — Female: mantle laterally compressed, muscular, oriented ventrally to aperture, conforming to spiral of the columella, body bluntly rounded at distal end toward apex or with short lobes; chitinous attachment disc with minute tubercles. Left opercular bar thin with notch on ventral side, dorsal side with shallow, rounded indentation; right opercular bar thick with flattened distal margin bordered by raised ridges along length. Opercular bar outer surfaces with dense horizontal rows of variously shaped denticules. Labrum ends of distal margin strongly produced, one broad and rounded distally and one narrow and tapered distally, medial margin subquadrate. Mandible strongly recurved. Maxilla I with acute upper spine and smaller proximoventral spine. Maxilla II an ovate plate with sparsely distributed stub setae. Cirrus I endopod and exopod of about 1/2 length protopod. Three pairs of terminal cirri uniramous with four segments; basal segment elongate, tubular, reaching to near end of second segment; second segment approximately as broad as basal segment but about 1/2 as long with protuberant “cushion” on distal inner surface, ridges on cushion with numerous regular rows of blade-like denticules; third segment narrower than basal or second, approximately as long as basal segment; fourth segment narrower than third, tapering distally, terminating in pair of bifid hooks and superior short recurved spine. Male: if present, one male per female, attached below mantle aperture. Form of stout boot with dorsal surface nearly straight, anteroventral surface domed and separated from posterodorsal surface by rounded concave area of nearly 90°, all corners rounded, ventral and posterior extensions of body subequal in length, anterolateral corner low.

DESCRIPTION

Female (Figs 1; 2A-C, E; 3-6) Maximal length 8.15 mm, maximal width (holotype) 4.3 mm (Fig. 1A). Mantle (sensu Kolbasov & Newman 2005) laterally compressed, perpendicular to the surface of gastropod shell (Figs 1; 2A, C). Flattened part of mantle (“disc”) dorsoventrally compressed, parallel to surface of gastropod shell (Figs 1; 2A, B). Chitinous attachment disc regularly rounded, oval, or irregular, depending on size of barnacle; in some larger specimens disc extends as a spiral covering the barnacle body that is exposed in this region, conforming to the shape of the shell (Fig. 2B, C), chitinous disc covered with minute tubercles. Disc lying in a plane perpendicular to sides of mantle and attaching upper part of animal with cement to wall of burrow along columella in position that orifice leads directly into mantle cavity (Fig. 2A). Aperture on columella of shell approximately straight to slightly curved, tapered slit-like opening 5.5 mm in length and 0.9 mm in width at widest point in holotype, tapering to thin extension (peduncular slit) oriented toward apex of shell (Fig. 2A, E). Mantle muscular, oriented ventrally to aperture, extending toward apex of shell, conforming to spiral of the columella, in larger specimens extending into the shell whorls, body bluntly rounded at distal end toward apex or with short lobes corresponding to shell whorls in larger individuals, burrow position shown by striae in thin layer of shell overlaying barnacle (Figs 1B, C; 2A). Orifice of mantle a narrow fissure-like opening about 1/4 length of barnacle, tapering to thin opening on ventral end with round opening at dorsal end (Fig. 2C). Left opercular bar thin with abrupt rounded end on ventral side giving the appearance of a notch, dorsal side with shallow, rounded indentation preceding connection with right opercular bar (Figs 1C; 3J, K); right opercular bar thick with flattened distal margin bordered by raised ridges along length (Figs 1A; 2C; 3A, B); right opercular bar approximately 1/3 longer than left opercular bar. Left opercular bar outer surface with dense horizontal rows of ovate denticules (some with bifid or trifid tips) (Figs 3J, L; 4E), row of long simple setae on upper margin (Fig. 3J, L), distal portion of denticule row presenting sparser area of short multifid star-shaped denticules and fewer, shorter simple setae (Fig. 3J, M); sloping region of mantle distal to notch in opercular bar with sparse area of multifid denticules similar to those seen in Figure 3M but with slightly longer shafts (Fig. 3J, N). Left opercular bar inner surface with small inner ridge bordered by dense rows of variously simple to multifid finger-like denticules, tapering towards region of mouth cirri (Fig. 3K, P), small area distal to ridge with sparse field of star-shaped multifid short denticules (Fig. 3K, O), small field of long plumose setae ventral to inner ridge (Fig. 3K; similar to those in Figure 3H on inner surface of right opercular bar), area dorsal to mouth cirri with sparse field of elongate variously simple to multifid denticules and few long simple setae (Fig. 3K, Q). Right opercular bar outer surface with sparse irregular field of simple tear-drop-shaped denticules ventral to dorsal margin and long simple setae on edge (Fig. 3A, D), below opercular bar edge dense rows of simple tear-drop-shaped denticules (Fig. 3A, C), denticules appear flat viewed head-on but are curved in lateral view (Fig. 3E). Right opercular bar inner surface with strong ridge bordered by dense rows of large multifid, foot-shaped denticules (with up to seven denticular blades), field of denticules tapering towards mouth cirri (Figs 3B, G; 4D), area dorsal to mouth cirri region with sparse rows of ovate denticules (Fig. 3B, F), distal margin with thin sparse rows of ovate denticules, mostly with bifid tips and interspersed with few short simple setae (Fig. 3B, I), area ventral to inner ridge with field of long plumose setae (Fig. 3B, H).

Labrum very large, inner edge partially covered by minute denticules and row of long setae proximal to margin along whole length of labrum, ends of distal margin of labrum unequal but both strongly produced, one broad and rounded distally and one narrow and tapered distally (Figs 5C; 6B), both with groups of typically three short simple setae (Fig. 5C inset), medial margin subquadrate (Figs 5C; 6B). Mandible strongly recurved, distally as acute projection, no accessory spines (Figs 5D; 6C). Maxilla I smaller than mandible with acute upper spine and smaller proximoventral spine (Figs 5E; 6C), with rows of five or six tapered denticules along inner margin (Fig. 6E). Maxilla II (maxillule) an ovate plate with rows of tiny setae on mesiodistal edge and a strong stout seta near mediomesial edge (Figs 5E; 6C), with sparsely distributed stub setae, more abundant at the base (Fig. 6D).

Four pairs of cirri. Cirrus I (mouth cirrus) biramous; protopod elongate and tubular, naked; endopod and exopod of about 1/2 length of protopod; exopod bearing more long plumose setae on surface and tip than endopod (Figs 5B; 6A, B). Three pairs of terminal cirri (IV-VI) widely separated from mouth cirrus, uniramous with four segments (Figs 4F, G; 5A); basal segment elongate, tubular, with row of long setae along inner surface, reaching to near end of second segment; second segment approximately as broad as basal segment but only about 1/2 as long, with protuberant “cushion” on distal inner surface (Fig. 4H), ridges on cushion with numerous regular rows of small tapered, blade-like denticules (Fig. 4H and inset); third segment narrower than basal or second, approximately as long as basal segment, narrow setae along lateral margins; fourth segment narrower than third, tapering distally, terminating in pair of bifid hooks and single superior short recurved spine (Figs 4F inset; 5A inset, bottom) (one specimen with three bifid hooks plus superior spine, see Fig. 5A inset, top), two very long setae positioned subterminally.

Male (Figs 1A; 2D, F, G)

Length 0.71 mm (allotype). One male present maximally per female, attached below mantle aperture of female (Fig. 1A). Form of stout boot with dorsal surface nearly straight, anteroventral surface domed and separated from posterodorsal surface by rounded concave area of nearly 90°, all corners rounded, both ventral and posterior extensions of body subequal in length (Fig. 2D, F), anterolateral corner low and rounded. Lateral surface with distinct median bulge (Fig. 2G). Penis not observed. Ganglion on vesicular seminalis connected by nerve to small dark eyespot (Fig. 2D, F, G).

REMARKS

Tomlinsonia Turquier, 1985 was proposed for the preoccupied genus name Alcippoides Turquier & Carton, 1976 (non Strand, 1928) (see Turquier 1985; Tomlinson 1987), and the type species is still known from only a single female specimen. The form of the protuberant “cushion” or “button” on the second segment of cirri IV-VI of female trypetesid specimens has been described as “transversely wrinkled by fine, distinctly crenated ridges of unknown function” (Nilsson-Cantell 1978). In fact, these “wrinkles” are composed of regular rows of minute tapered and bladelike denticules and possibly serve a function in feeding (Fig. 3H). As indicated by Turquier & Carton (1976), these “cushions” were suggested to be vestigial endopodites ( Darwin 1851), although the complexity of the denticules on the surfaces does not fit well with a vestigial designation.

Males of Tomlinsonia mclaughlinae n. sp. differ markedly from those reported for Trypetesa species in that their sides form a vaguely equilateral triangle with one concave margin and lack either the elongated penis containing lobe of Trypetesa lampas (Hancock, 1849), Trypetesa habei Utinomi, 1962 , and Trypetesa spinulosa Turquier, 1976 or the deeply concave margins of Trypetesa nassarioides Turquier , 1967. The male of Trypetesa lateralis Tomlinson, 1953 has never been figured or adequately described but was said by Tomlinson (1953, 1969) to lack a penis. Although we have found no evidence of a penis in Tomlinsonia mclaughlinae n. sp., we have only seen five specimens.The apparent absence of a penis is not likely due to immaturity of the specimens (they lack the antennules which are characteristic of immature males) (see Turquier 1971). However, the majority of males in many acrothoracican species may appear to lack penes as these organs can develop relatively late in the life of the male ( Tomlinson 1969). Only after examination of large series of males, as done by Tomlinson (1969) for Trypetesa lateralis , should any conclusions about presence or absence of penes in acrothoracican species be made.

The only acrothoracican previously reported from the Philippines was Trypetesa lampas ( Rosell 1981) . Study of Rosell’s (1981) description and illustration leaves no doubt that he was dealing with a Trypetesa species , but his description could apply to any species in the genus and the illustrations, particularly of the mandible, strongly suggest that this was not T. lampas , but perhaps an undescribed species. The so-called “caudal appendage” cited by Rosell (1981) is the sixth pair of terminal cirri; there are no caudal appendages (= furca) on apygophoran acrothoracicans.

The present finding of a Tomlinsonia species in the Philippines extends the distribution of the genus considerably from the type locality of T. asymetrica in Madagascar and represents the first report of this genus in the northern hemisphere. Such an amphitropical distribution is also seen in Trypetesa and may reflect a relictual distribution of the entire family (cf. Newman 1979).

The proportions of the terminal cirri segments in Tomlinsonia mclaughlinae n. sp. are quite different from those reported in T. asymetrica . In T. mclaughlinae n. sp. the first two segments are subequal in width and the distal two segments are much thinner, while the first and third segments are nearly as long as each other with the second and fourth segments being approximately 1/2 the length of first and third. In T. asymetrica , the first three segments are all about as wide and as long as each other, while only the fourth segment is shorter (although not 1/2 as long) and thinner. The existence of a pair of bifid terminal hooks and superior spine (Fig. 5A) has not been previously reported in trypetesids.

The shape of the labrum differs between the two species of Tomlinsonia with T. asymetrica having a gently rounded medial margin between the terminal produced lobes while the same area in T. mclaughlinae n. sp. is subquadrate. In T. asymetrica the thinner terminal lobe is longer than the broader lobe, whereas in T. mclaughlinae n. sp. the broader lobe nearly extends as far as the thinner one.

There are also some differences between the mouthparts of the two Tomlinsonia species. The mandible of T. mclaughlinae n. sp. is more acutely tapered than that of T. asymetrica and lacks the distal small spine; maxilla II of T. mclaughlinae n. sp. is also more acutely tapered than that of T. asymetrica , while the maxilla I is more regularly ovate and possesses a stout inner setae that is lacking in T. asymetrica .

It is difficult to compare the various denticules on the inner and outer opercular bars of T. mclaughlinae n. sp. with those of T. asymetrica , as Turquier & Carton (1976) described and figured only those from certain portions of the opercular bars. However, the basic form of ovate denticules with simple to multifid tips can be seen in both species. The dense rows of denticules found on the inner opercular bars dorsal to the ridges are similar to those reported for Trypetesa spinulosa Turquier, 1976 (see Turquier 1978: pl. 3, fig. 4) but are more densely packed and with typically four or five denticular blades on a single shaft as compared to typically two or three in T. spinulosa .

ECOLOGY The prevalence of Tomlinsonia mclaughlinae n. sp. ranged from 0.45 to 7.94% in the samples from the Philippines (overall prevalence = 3.2%, n = 981 hermit crabs collected during 1997 and 1999). The species is known to be associated with the three most common species of hermit crabs ( Calcinus gaimardii [n = 14], C. latens [n = 16], and C. minutus [n = 1]) from the coral reef areas sampled in the Philippines ( Williams 2002). Of the 31 Tomlinsonia mclaughlinae n. sp. specimens examined all but one was found associated with female hermit crabs; 15 of these females were ovigerous (50%). Although the sex-ratios of the hermit crabs did not significantly differ from 50:50 (χ2 [n = 325] = 1.63, P = 0.2, df = 1], the distribution of the barnacles among the two most common hermit crabs was significantly different than predicted values (χ2 [n = 14] = 10.29, P = 0.001, df = 1; this and previous χ2 test based on a subset of the 1999 collections for which the sex of all hermit crabs was recorded). Tomlinsonia mclaughlinae n. sp. has been found in six species of gastropod shells (most commonly Drupella cornus ). No shells were found to harbor more than one Tomlinsonia individual, although other species of boring barnacles (such as members of the genera Trypestesa and Weltneria Berndt, 1907 ) were found in the same shells as those occupied by T. mclaughlinae n. sp. The position of the barnacle in the columella and general body shape of T. mclaughlinae n. sp. are similar to that of T. asymetrica and Trypetesa nassarioides Turquier, 1967 in conforming to the helical spiral of the columella. The aperture of T. mclaughlinae n. sp. is oriented so that the ventral, tapered end of the slit is facing the apex of the gastropod shells, often too far inside the shell to be detected until cracked. Tomlinsonia mclaughlinae n. sp. is apparently an obligate commensal of hermit crabs and is the seventh known species of extant trypetesid associated with hermit crab hosts ( Williams & McDermott 2004). Additional trypetesids are known from the fossil record based on their borings in shells ( Lambers & Boekschoten 1986; Baluk & Radwánski 1991).

The feeding biology of Tomlinsonia and Trypetesa remains largely unknown. Tomlinson (1987) suggested the reduced cirri of the barnacles could not be extended outside the aperture and were only used for feeding on small particles brought in by pumping action of the thorax. However, Williams (1999, 2002) reported that an unidentified species of the genus Trypetesa was found to ingest the eggs or developing embryos of host hermit crabs from the Philippines. Based on its position within the shell and proximity to eggs or embryos attached to the pleopods of host hermit crabs (similar to that seen in Trypetesa sp. from the Philippines), Tomlinsonia mclaughlinae n. sp. may also be an egg predator. Among the present samples of T. mclaughlinae n. sp. there is no direct evidence (e.g., egg corions from host hermit crabs identified within the stomach of the barnacles) for this behavior. However, the body of some specimens contained material that was the same coloration as host hermit crab eggs and the barnacles were found predominately with female hermit crabs. Since gonadal tissue of the barnacles could be confused with ingested eggs or embryos of the hosts, histological examination of newly collected specimens needs to be completed to determine if the new species is an egg predator. The barnacles might also gain food in the form of dropped food particles by the crab, materials brought in by the respiratory currents, and/or fecal material of the crab ( Baluk & Radwánski 1991; Williams & McDermott 2004), or even the consumption of other symbionts or their offspring in gastropod shells inhabited by hermit crabs. Although egg predation would in large part explain the blind gut of trypetesids, how they are able to capture host eggs and what they feed on while inhabiting shells with male hermit crabs remains unknown.

Tomlinsonia mclaughlinae n. sp. produce fairly large broods of eggs (estimated at c. 100+ eggs) that are 186 ± 5 µm in length and 145 ± 7 µm in width (n = 10). The eggs appear to hatch as nauplii as evidenced by this stage found in the mantle cavity of some specimens of Tomlinsonia mclaughlinae n. sp.