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The Tantulocaridan Life Cycle: the Circle Closed?

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The Tantulocaridan Life Cycle: the Circle Closed? JOURNAL OF CRUSTACEAN BIOLOGY, 13(3): 432-442, 1993 THE TANTULOCARIDAN LIFE CYCLE: THE CIRCLE CLOSED? Rony Huys, Geoffrey A. Boxshall, and Roger J. Lincoln ABSTRACT The discovery of a new stage in the life cycle of the Tantulocarida is reported. A sexual female, collected from a deep-sea harpacticoid copepod host, was removed from the trunk sac of the preceding tantulus larva. This female is a free-living and nonfeeding stage which pre- sumably mates with the free-swimming adult male previously described. The female comprises a cephalothorax, probably incorporating 2 limbless thoracic somites, 2 free pedigerous trunk somites, and 3 limbless trunk somites. It also possesses paired antennules, the only well-defined cephalic appendages present at any stage in tantulocaridan life history. There is a median genital aperture, the copulatory pore, located ventrally on the cephalothorax at about the level of the incorporated first thoracic somite. This is interpreted as further evidence of a sister-group relationship between the Tantulocarida and the Thecostraca. The known life-cycle stages of the Tantulocarida are now interpreted as forming two cycles, one sexual, the other parthenogenetic. Tantulocaridans are minute ectoparasitic might exist, leading to a large, free-swim- crustaceans that utilize a variety of other ming adult which would be capable of mat- crustacean groups as hosts (Bcxshall and ing with the known adult male. Huys (1991) Lincoln, 1983). The known life cycle of the interpreted the significant variation in penis Tantulocarida, as described by Boxshall and structure in known male tantulocaridans Lincoln (1987), is remarkable for the com- (Huys, 1990) as evidence in support of the plete lack of any typical crustacean molting existence of a sexual female with comple- process. The adult female described by mentary copulatory structures. He suggest- Boxshall and Lincoln (1987) has a saclike ed that there might be both parthenogenetic trunk which develops immediately behind and sexual cycles within the tantulocaridan the head; the larval trunk is sloughed, leav- life cycle. ing an abscission scar. This adult female is This paper records the discovery of the permanently attached to its host via the ad- sexual female of a tantulocaridan. A single hesive oral disc on the larval head. The fe- specimen, attached to a deep-sea harpacti- male produces relatively large numbers of coid copepod, was found in a sample of co- eggs which develop within the female's body pepods from off the Philippines. The har- and hatch directly as tantulus larvae. The pacticoid host represents a new family and life cycle is also unique in the bizarre meta- is described in a separate account (Huys, in morphosis that takes place in the develop- press). The sexual female is described in ment of the male, during which a large, free- detail and a fuller interpretation of the tan- swimming adult differentiates within the tulocaridan life cycle is presented. The phy- expanded trunk sac of the preceding tan- logenetic implications of the new informa- tulus larva. This adult male is supplied with tion on tantulocaridan morphology are nutrients via a tissue connection with the discussed. permanently attached larval head and it is after nonfeeding hatching. MATERIALAND METHODS Boxshall and Lincoln (1987) considered the relative size of the penis of male tan- A single tantulocaridan was found attached to the tulocaridans and the tantulus larva and con- exopod of the third swimming leg of a female harpac- ticoid 1993 cluded that could not take be- copepod, Styracothorax gladiator Huys, mating place (Huys, in press, fig. 1), collected during the ESTASE II tween these two stages. They therefore expedition (14 November-8 December 1984) to the suggested that fertilization might be deep waters off the Philippines on board the RV Jean achieved by injection of sperm through the Charcot (coordinators: L. D. Labeyrie and B. Metivier). wall of the saclike female. Locality: Station CP02 (14?05.40'N, 120"02.46'E) to body developing the northwest of Manila, 14 November 1984, at a depth However, they also suggested that a second, of 2,050 m. Material sorted in CENTOB, Brest (co- sexual, female developmental pathway ordinator: M. Segonzac). The specimen is stored on an 432 This content downloaded from 193.191.134.1 on Wed, 26 Nov 2014 09:36:42 AM All use subject to JSTOR Terms and Conditions HUYS ET AL.: TANTULOCARIDAN LIFE CYCLE 433 electron microscope stub in the Natural History Mu- Postcephalothoracic trunk comprising 2 seum, London: BM(NH) Reg. No. 1992.1070. somites The was for examination pedigerous (probably representing specimen prepared using third and fourth thoracic and 3 light microscopy by mounting temporarilyin lacto- somites) phenol. Observationswere made using oil immersion limbless somites (Fig. 2D), the last bearing on a Leitz Diaplan microscopewith Nomarski differ- paired caudal rami but lacking anus or anal ential interferencecontrast. Drawings were made using operculum. Pedigerous and limbless so- a cameralucida. After light microscopy,the specimen mites without defined sur- was washed in alcohol to remove the lactophenoland tergites, lacking transferredto 50% acetone ready for preparationfor face ornamentation. Caudal rami (Fig. 2G) Scanning Electron Microscopy (SEM). It was dehy- elongate, about 100 Atmin length by 10 ,tm drated through graded acetone, critical-point dried, in width; ornamented with numerous irreg- mountedon a stub,and sputter-coatedwith palladium. ular rows of denticles. Each ramus Observationswere made a HitachiS-800 FSEM. bearing using 2 distal in The pore pattern nomenclaturefollows Boxshall and setae, set a concavity formed by Vader (in press). dorsal and ventral marginal membranes with serrated edges. Caudal setae curved at tip DESCRIPTION and provided with serrated membrane along concave surface. Sexual Female Legs 1 and 2 biramous, similar in seg- Body comprising large cephalothorax, 2 mentation; protopod 2-segmented, com- free pedigerous somites and 3 limbless so- prising small coxa and large basis separated mites (Fig. 1A). Body cuticle weakly chitin- by well-developed articulation; both rami ized. Body length measured around curved 1-segmented. Leg 1 (Fig. 2E) slightly larger dorsal surface, about 435 ,tm from frontal than leg 2; coxa unarmed, basis unarmed margin of cephalothorax to rear margin of but ornamented with few denticles. Exopod caudal rami. Cephalothorax without de- and endopod both elongate, each armed with fined dorsal shield; with conspicuous, paired, single seta distally; posterior margins of both lateral zones of longitudinally folded cuticle rami bearing toothlike spinous processes. (Figs. 1A, 3C). Surface of cephalothorax en- Setae curved at tip, irregularly serrate along tirely lacking integumental pores and sen- posterior margin. Leg 2 (Fig. 2F) with un- silla (Fig. 4A). No epicuticular ornamenta- armed coxa, basis unarmed but ornamented tion apparent on cephalothorax, although 2 with several surface denticles. Rami each transverse furrows (arrowed in Fig. 3D) armed with single seta distally, with base of present posteriorly, possibly representing seta protected anteriorly by marginal mem- vestigial boundaries marking position of in- brane with serrated edge. Posterior margin corporated first and second thoracic so- of both rami ornamented by numerous den- mites. Frontal margin of cephalothorax ticles; setae irregularly serrate along posterior bearing paired antennules (Figs. 1B, 4A), margin, more slender than those of leg 1. located dorsal to large median aperture into which umbilical cord passes (Fig. 1D). Cephalothorax bearing median aperture, Tantulus Larva referred to here as copulatory pore, posteri- The adult female was contained, in the orly on ventral surface (Fig. I E, G). Copula- reflexed position typical for adult males, tory pore surrounded by fine cuticular ridg- within the expanded trunk sac of the pre- es, arranged radially (Fig. 4C, D); pore ceding tantulus larval stage (Fig. 3A). The extending internally, via short cuticle-lined postcephalic trunk of the tantulus had al- duct, into poorly defined sac. Most of space ready been sloughed, leaving an abscission inside cephalothorax occupied by 14 eggs, scar (Figs. 1D, 2B, C, 3B). about 32 Atmin diameter. Dorsal shield of tantulus larva (Figs. 2A, Antennules unsegmented, anteriorly di- C, 3B) slender, tapering anteriorly; shield rected; fused together basally and fused to length about 58 ,tm, maximum width about frontal margin of cephalothorax (Fig. 1C). 30 tm; about 1.9 times longer than wide. Antennule armed with 5 setal elements, 1 Cephalic shield with 13 pairs of pores and located dorsally about at midlength, 1 sub- 2 unpaired median pores: pore formula apically, and 3 around distal margin. Each AI_V,Di_IV, LI-_I,, M. Pores Ai, DI and L, all seta with parallel sides and brushlike apex sensillate. Median pores (M) arranged (Figs. 1B, 4B). asymmetrically, on either side of midline, This content downloaded from 193.191.134.1 on Wed, 26 Nov 2014 09:36:42 AM All use subject to JSTOR Terms and Conditions C D M~S. S : 2 a : E F I I c.p. Cj B/ -D Fig. 1. Itoitantulusmisophricola, sexual female. A, lateralview; B, anteriormargin of cephalothorax,lateral; C, same, dorsal; D, anterior part of tantulus sac, showing umbilical cord leading to sexual female, lateral; E, cephalothorax, showing eggs and copulatory pore, lateral; F, same, dorsal; G, ventral surface of cephalothorax, showing copulatory pore. [Abbreviations: c.p. = copuiatory pore, f.c. = folded cuticle, s. = abscission scar, t.s. = tubular structure, u.c. = umbilical cord.] This content downloaded from 193.191.134.1 on Wed, 26 Nov 2014 09:36:42 AM All use subject to JSTOR Terms and Conditions HUYS ET AL.: TANTULOCARIDAN LIFE CYCLE 435 / y/||^?y p / \ A u '~B o50 20 /u o ^ (Ii '''N1E\ E V\ (Al V11VP, v~ ~ i LL~ ~ ii~ A/ A \ Fig.~Itotnuu 2.iohioa ,cpai hedo atuu,dra;B neirpr fatce atls veta;C,sm,lterl D, seua feaewti rn a fpeeigtnulssae eta;E ishrcpd lateralhrcpd F,scnaea;G adlrms aea iwwt ro niaigdra ufc.[b breviations:~s.=asisinsa.
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