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JOURNAL OF BIOLOGY, 9(1): 126-140, 1989

NEW TANTULOCARID, STYGOTANTULUSSTOCKI, PARASITICON HARPACTICOIDCOPEPODS, WITH AN ANALYSIS OF THE PHYLOGENETICRELATIONSHIPS WITHIN THE

GeoffreyA. Boxshall and Rony Huys

ABSTRACT A new genus of Tantulocarida,Stygotantulus, is describedbased on materialfrom an an- chialine pool on Lanzarote,Canary Islands. It is the most primitive tantulocaridknown and is ectoparasiticon representativesof at least two families of harpacticoidcopepods. It is dis- tinguishedby the presenceof 7 abdominal somites in the tantuluslarva. The musculatureof the penis on trunksomite 7 of the male suggeststhat it is derivedby modificationof the seventh thoracopods.The importanceof trunk somite numbersin maxillopodansystematics is reex- aminedand an attemptis made to applythe conceptofhomology to the developmentalprocesses determiningsomite numbers.The classificationof the Crustacea,including the Tantulocarida, proposedby Starobogatov(1986), is criticizedand the validityof the developmental-functional concept of the prototagma,as used by Starobogatov,is refuted.A new scheme of phylogenetic relationshipsamong seven major maxillopodangroups is presented.

Tantulocarids are small, ectoparasitic distinctive, representingthe most primitive crustaceansfound only on crustaceanhosts. type yet found. The characters exhibited They have an unusual and highly abbrevi- promptedus to reexaminethe phylogenetic ated life cycle (Boxshalland Lincoln, 1987). relationshipsof the Tantulocaridawithin the Saclike adult females release infective tan- Maxillopoda,and to comment upon the new tulus larvae which attach directly to a new classificationof the Crustacea,including the host. Once attached, the female tantulus Tantulocarida,proposed by Starobogatov forms a trunk sac behind the cephalon and (1986). sloughs the larval trunk. The male tantulus forms a trunksac at the posteriorend of the thoraxwithin which a unique kind of meta- Subclass Tantulocarida Boxshall 1983 morphic reorganization takes place. The and Lincoln, presumed adult male differentiatesinside Family Basipodellidae the sac while being supplied with nutrients Boxshall and Lincoln, 1983 via an internaltissue connection to the lar- Stygotantulus,new genus val cephalon. Tantulocaridsexhibit no ce- Diagnosis. -Tantulus larva comprising phalic limbs at any stage of their life cycle, cephalon,6 pedigerousthoracic somites, and but their basic tagmosis and male gonopore 7-segmented abdomen. Cephalon covered location was interpreted by Boxshall and with dorsal shield ornamented with longi- Lincoln (1987) as evidence that their affin- tudinal and transverse lamellae. Oral disc ities lie with the (sensu Grygier, located anteriorly on ventral surface. Ce- 1985, 1987). phalic stylet barbed. Free thoracic somites In the presentaccount we reporton a new 1-6 each with well-developed tergite and tantulocarid collected by Prof. Jan Stock bearing pair of thoracopods. Thoracopods from an anchialine lava pool on Lanzarote 1-5 biramous, comprising unsegmented in the CanaryIslands. In the pool it is para- protopodbearing well-developed endite, and sitic on harpacticoidcopepods from at least 1- (leg 1) or 2-segmented (legs 2-5) rami. two distinct families. In the last decade Thoracopod 6 lacking endite. Caudal rami studies of the crustaceanfauna of anchialine distinct, armed with 1 short and 2 long se- habitats in the Canary Islands and else- tae. Adult male in trunk sac located pos- where have revealed a range of distinctive teriorto tergiteof sixth thoracicsomite. Male forms, such as the (Garcia-Val- cephalothoraxincorporating first and sec- decasas, 1984). The new tantulocaridis also ond thoracic somites. Thoracopods 1-5 bi- 126

This content downloaded from 193.191.134.1 on Wed, 3 Dec 2014 08:38:08 AM All use subject to JSTOR Terms and Conditions BOXSHALL AND HUYS: NEW TANTULOCARID AND RELATIONSHIPS WITHIN MAXILLOPODA 127 ramous with 1-segmented rami. Thoraco- sallydirected dorsal barb (Fig. 1B),and slight pod 6 uniramous, 2-segmented. Abdomen ventral swelling located proximal to finely 2-segmented, first somite elongate, bearing pointed tip. Tip protrudingthrough central recurved median penis ventrally. Second pore of oral disc in 1 specimen (Fig. 1B). abdominalsomite with discretecaudal rami Median striatedorgan in head appearingto carrying3 apical setae. be muscular and associated with stylet. Type-.-Stygotantulus stocki, new Quadrilobate glandular structure visible genus, new species. through integument, lobes having homo- geneous contents and leading dorsally to- Etymology.-The generic name was de- wards common median duct di- rived from the Greek anteriorly styx, stygo, meaning rected(this not traceablefurther than shown the lower and tantulus which forms world, in Fig. 1). partof the name Tantulocarida.The species of 6 free thoracic somites dis- is named for Prof. Stock who collected Tergites Jan tinct, ornamented with fine lamellae the hosts. very (Fig. 3B). Thoracopod 1 (Fig. 2A) with un- Remarks.-The new genus can be distin- segmentedprotopod bearing medial endite guished from all other genera by the 7-seg- proximally and few spinules along lateral mented abdomen of its tantulus larva. It margin. Endite armature visible only as also differs from all known genera in the spine under light microscope. Endopod complexity of the cephalic stylet. The ba- 1-segmented,bearing single short seta from sally directed, dorsal barb on the stylet is distal protrusion. Exopod 1-segmented, unique to Stygotantulus.On the basis of the bearing 2 naked setae on distal margin, in- 7-segmented abdomen, the well-developed ner longer than outer. Thoracopods2-5 bi- thoracopodal endites and rami in the tan- ramous with undivided protopod bearing tulus, and the location of the trunksac con- medial endite proximally and both rami taining the male behind the sixth thoracic distally in slight concavity (Fig. 2B). Endite tergite,the new genus is placed in the family armature visible as spinous element and Basipodellidae.We recognizethat the fam- blunt process under light microscope. En- ily is based primarily on plesiomorphic dopod apparently 2-segmented; first seg- characters,and, as such, may be paraphy- ment comprising swollen base and con- letic. It appears to be most closely related stricteddistal part,armed with 2 nakedsetae to Basipodella Becker which has a 6-seg- laterally;second segment short, bearingop- mented abdomen in the tantulus stage posablespine and toothed spatulateelement (Boxshall and Lincoln, 1983) and is also apically.Exopod 2-segmented;first segment known from harpacticoid hosts (Becker, short, unarmed;second segment bearing 1 1975; Boxshall, 1983). short and 3 long naked setae. Thoracopod 6 with simple protopodlacking endite, bear- Stygotantulusstocki, new species ing 2 tiny spinules midway along medial margin (Fig. 2C, arrowheads)and 2 apical Tantulus Larva setae. One seta located on broad base, pos- Body comprisingcephalon, 6 pedigerous sibly representingsegment of ramus, other thoracic somites, and 7-segmented abdo- seta originatingmore anteromediallyfrom men (Fig. 1A, B). Total body length 94 ,m surface of protopod. Short spinule located from tip of rostrum to end of caudal rami. near base of posterior seta. Cephalonabout 1.5 times longer than wide Abdomen length 19 atm,greatest width (43 x 29 ,m), covered with entire dorsal 11 tum.First abdominal somite with round- shieldornamented with finelongitudinal and ed posterolateralangles; second to seventh transverselamellae (precisepattern difficult somites taperinganteriorly and slightlywid- to ascertainunder light microscope).Shield er than precedingsomite. Second abdomi- with 2 pairs of pores located dorsolaterally nal somite narrowingventrally and lacking near posterior margin and pair of fine set- dorsal ornamentation;third to seventh or- ules anterolaterally.Oral disc about 9 tum namented with fine longitudinal lamellae in diameter, located anteriorly on ventral dorsally (Fig. 1A). Caudal rami wider than surface. Cephalic stylet 27 um long; with long, bearing 1 short and 2 long naked setae flared proximal opening (Fig. 3C), fine ba- apically.

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Fig. 1. Stygotantulus stocki, new genus, new species. A, tantulus larva, dorsal view; B, tantulus larva, lateral view with rami of legs not drawn.

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Fig. 2. Stygotantulus stocki, new genus, new species, tantulus larva. A, thoracopod 1, anterior; B, thoracopod 2, anterior; C, thoracopod 6, anterior.

size posteriorly, each with well-developed Adult Male tergite ornamented with fine longitudinal la- Male developing within trunk sac formed mellae. First abdominal somite elongate (34 immediately posterior to sixth thoracic ter- x 19 gm), with concave sides; second just gite of preceding tantulus stage (Fig. 3A). wider than long (22 x 23 gum),with convex All 6 tergites (Fig. 3B) separated from each sides and marked anal slit (Fig. 4C). Both other and from posterior margin of cephalic somites ornamented with fine longitudinal shield by expansion of trunk sac. Male at- lamellae. Penis situated medially at extreme tached to larval head by tissue connection posterior end of first abdominal somite; (Fig. 3A) referred to as umbilical cord by comprising swollen basal part and curved, Boxshall and Lincoln (1987). Abdomen of tapering distal part with opening at tip (Fig. preceding tantulus deflected ventrally by 4D). Extrinsic muscle originating on ventral growth of sac. surface of somite anterior to penis base and Total body length about 400 inm;com- inserting proximally on posterior wall of pe- prising large cephalothorax incorporating nis. No other internal organs associated with first and second thoracic somites, 4 free pe- penis visible. Caudal rami about 2.8 times digerous somites, and 2-segmented abdo- longer than wide (17 x 6 gim), bearing 1 men (Fig. 4A). Cephalothorax damaged short outer seta and 2 long distal setae. during removal from sac but 4 pairs of Thoracopods 1 and 2 carried posteriorly aesthetascs present anteriorly, 1 of these bi- on cephalothorax. Thoracopods 1-4 simi- fid (Fig. 4B). Rostrum small, anteriorly di- lar, each with protopod comprising broad rected. Free thoracic somites decreasing in muscular proximal segment and incom-

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Fig. 3. Stygotantulus stocki, new genus, new species. A, adult male contained within trunk sac of preceding tantulus larva, attached to anal somite of host; B, disarticulated thoracic tergites from trunk sac, dorsal view; C, attachedhead of tantulus,lateral view showing ventral surfaceof stylet. pletely fused distal segment, separated by margin. Both rami 1-segmented, exopod suture line posteriorly but not anteriorly (Fig. longer than endopod. Endopod subrectan- 5A). Armed with pair of brush setae, about gular, bearing, around distal margin, short 27 ,tm long, located proximally on medial naked seta and 4 long, articulated setae na-

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Fig. 4. Stygotantulus stocki, new genus, new species. A, adult male, lateral view with limb setae not drawn; B, tip of cephalothorax showing rostrum and aesthetascs, lateral; C, fifth and sixth thoracic somites and abdomen, dorsal; D, abdomen, lateral view showing median penis.

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Fig. 5. Stygotantulus stocki, new genus, new species, adult male. A, first thoracopod, anterior; B, fifth thora- copod, anterior; C, sixth thoracopod, anterior view showing muscles visible through integument.

This content downloaded from 193.191.134.1 on Wed, 3 Dec 2014 08:38:08 AM All use subject to JSTOR Terms and Conditions BOXSHALL AND HUYS: NEW TANTULOCARID AND RELATIONSHIPS WITHIN MAXILLOPODA 133 ked proximally and bilaterally serrate dis- since it is a compound characterinvolving tally. Exopodexpanded distally; armed with the location of the gonoporeson the correct 5 articulatedand distally serratesetae, and somite and the evolution of a median penis. short outer serrateseta. Thoracopod 5 (Fig. The penis in the new genus has at least 1 5B) similar except for complete separation extrinsic muscle and in a new species of of largeproximal (syncoxa)and small distal Microdajus(Boxshall et al., in press)several (basis) protopodal segments. Tiny spinules intrinsic muscles are present. The tantulo- present on medial margin of endopod. caridan penis appears, therefore, to repre- Thoracopod 6 (Fig. 5C) uniramous, com- sent a modification of the seventh pair of prising single protopod segment bearing 2 thoracopodsand can be considered homol- brush setae and 1-segmentedexopod. Pro- ogous with the penis ofthecostracans,which topod with indentationabout midway along is derived by medial fusion of the seventh medial margin,at level of insertion of some thoracopods(Grygier, 1987). Its possession intrinsic thoracopodal muscles. Exopod is a synapomorphy of the Tantulocarida- armed as other exopods except only 4 ar- Thecostracagrouping. The paired penes of ticulated setae present. ostracodsprobably also representmodified and the studies of Schulz Material Examined. - Holotype tantulus thoracopods, 1 male within (1976) have indicated that they originatein larva, paratype developing close to the seventh expanding trunk sac of precedingtantulus. proximity postcephalic attached to aesthetasc on anten- somite. Schulz (1976) assignedthe penes of Holotype to the sixth nule of and unidentifiable, har- Cytherella trunk somite, but damaged, out that their stron- pacticoid belonging to tisbiform group of Grygier(1984) pointed families. attached to anal gest skeletal support was derived from the Paratype ventrally seventh and somites. somite (Fig. 3A) of copepodid IV stage of eighth an undescribednew genus of canuellid har- Numbers of Trunk Somites pacticoid. Stored in collections of Zo6lo- The relationship of the Tantulocarida- gisch Museum, Amsterdam, Registration Thecostraca to other Nos. ZMA Co 102.810a and Co grouping maxillopo- (holotype) dans is because the Tantulo- 102.810b (paratype,on 2 slides). problematic, carida are now known to possess up to 13 Type Locality.-Amsterdam Expedition to trunk somites (in S. stocki) rather than the the CanaryIslands, Station 85/53, anchia- total of 11 which has previously been re- line lava pool situated 50-100 m from sea garded as diagnostic of the Maxillopoda near Playa de MontanaBermeja, Lanzarote (Dahl, 1956; Newman et al, 1969; New- x (UTM Coordinates FT61415 320395). man, 1983; Grygier, 1983). The reinterpre- Pool separatedfrom sea by ridgeof lava and tation of the abdomen of Basipodella har- pumice;tidal activity perceptiblein pool via pacticola Beckeras 12-segmented(Boxshall subterranean.connections with sea. Salinity and Lincoln, 1983) and the discovery of the of waterin pool about 27.9%o.Sample taken fossil Skaracarida(Miiller and Walossek, on 14 May 1985 by Karaman-Chappuis 1985) had already raised questions con- method. cerning the ancestral segmentation pattern of the Maxillopoda. These latter authors 12 PHYLOGENETIC AFFINITIES OF THE suggestedthat trunk somites (including the the TANTULOCARIDA the telson) may be ancestralstate for Maxillopoda. Homology of the TantulocaridanPenis The concept ofhomology is centralto the Although tantulocarids lack any recog- cladistic method, enabling charactersto be nizable cephalic appendagesat any stage of definedand compared.As currentlyapplied the life cycle, Boxshall and Lincoln (1987) to crustaceanbody segmentation,homology suggested that their affinities lie with the is a crudenumerical-positional concept and Thecostraca(sensu Grygier, 1985, 1987) be- little importance is attached to develop- cause they shared the possession of 6 pairs mental criteria.For example,the possession of thoracopods and a median penis on the of 11 postcephalic trunk somites has been seventh trunksomite of the male. This latter regarded as the main apomorphy linking characteris regardedas particularlyrobust, the Copepoda,, Thecostraca

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(=Cirripedia/Ascothoracida/), and Ostracodawithin the Maxillopoda,yet Compound Eyes the developmental processes by which so- The distributionof compound eyes, pre- numbers are attained are very heter- sumed present in the ancestral crustacean ogeneous. primitively undergo 11 stock (Hessler and Newman, 1975), in the molts from first naupliusto adult (Boxshall maxillopodan groups provides additional et a., 1984). The last molt is definitive. The evidence of developmental heterogeneity. evolution of determinate growth in cope- The loss of compoundeyes in copepods(and pods is the result of two processes:the lim- in mystacocaridsalso) may be due to the itation of numbers of trunk somites by the simultaneouscessation of molting and pre- sudden cessation of molting, and the pre- cocious onset of sexual maturity occurring cocious attainmentof sexual maturity(pro- at a stage of development prior to the full genesis). The correlation of these separate developmentof compoundeyes. This would processescan be interpretedas evidence of explain the loss of a major sense organ as a a progenetic origin of the Copepoda as a secondary consequence of a more advan- whole (Boxshall, 1983). Assuming an an- tageous evolutionary change in basic body cestralontogeny of six naupliarstages (as in form. Compound eyes are retained in the cirripedes(Moyse, 1987)) and two cyprids thecostracan groups (and in branchiurans (as in ascothoracids (Grygier and Fratt, and also). Again this can be in- 1984)), thecostracansprimitively undergo terpretedas evidence that the shorteningof eight molts between first nauplius and the the body in thecostracanswas not brought attainment of adult body segmentation. In about by a paedomorphic event homolo- contrastto copepods,however, the last molt gous with that occurringin the copepod lin- is not definitive, since cirripedes continue eage. to molt periodically throughout adult life The compound eyes of cirripede cyprid (Darwin, 1851). Thus, there is no evidence larvae (Thecostraca),branchiurans, and os- that the evolution of a short trunk in the- tracodsvary in numbers of crystallinecone costracans is developmentally correlated cells and retinularcells, and in the config- with the earlyonset of sexualmaturity. Con- uration of the rhabdom, but they all share versely there is evidence that in ascotho- the presence of bipartite pigment cells sur- racidsthere is at least one discretepostlarval rounding the cone (Hallbergand Elofsson, stage between the attainmentof adult body 1983). The anatomy of the compound eye segmentation and the onset of sexual ma- of ascothoracidlarvae is not known in great turity (Grygier, 1984). It is probable that detail, but it appears to be closest to that the selective pressures leading to the evo- found in cirripede cyprids (Hallberg et al., lution of a short, 11-somite trunk in the- 1985). costracanswere differentfrom those affect- ing copepods, and may have involved Classificationof Starobogatov(1986) shortening of the body to enable it to be The new classification of the Crustacea completelyenclosed within a protectivecar- proposed by Starobogatov(1986) (English apace (Boxshall, 1983). The 11 trunk so- translation,by Grygier,published in 1988) of copepodsand thecostracansare ho- little resembles that summarized by Bow- mologous in a strict positional sense, but man and Abele (1982) or Schram (1986). developmentallythey are the end products The methodology employed by Staroboga- of nonhomologous processes. This inter- tov (1986) relies heavily on a refinementof pretation is reinforcedby the convergence the concept of primaryheteronomy as pro- in trunksomite numberindicated in Fig. 6. posed initially by Ivanov (1944) and later Ferrari(1988) has analyzedin detail the de- developed by Melnikov (1971). The under- velopmental patterns in numbers of ramal lying principleof primaryheteronomy holds segmentsin the swimminglegs of copepods. that metamerismexhibited by the ancestral He noted numerous similar cases of devel- stock of the Articulata (including annelids opmental convergence in which the same and )arises during embryologi- adult segmentationpatterns were produced cal development as a result of the activity by nonhomologousdevelopmental process- of 2 separateorganizing centers, one larval es. (primary)and the other postlarval(second-

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Fig. 6. Phylogeneticrelationships of the seven major maxillopodantaxa (Thecostraca,, Ostracoda. Tantulocarida,Skaracarida, Mystacocarida, and Copepoda). Numbered apomorphies refer to the characters listed in Table 1, parenthesesindicate convergence. ary). Each center follows its own rules of (1934), and by Anderson on Limnadia growth, with the former laying down so- (1967) and Tetraclita (1969) provide clear mites gradually from anterior to posterior, evidence of two such organizing centers. The the latter in the opposite direction. Manton anterior center corresponds to the function- (1949) found no such distinction in the de- al nauplius and is expressed by the virtually velopment of the Onychophora and con- simultaneous formation of the naupliar so- cluded that such heteronomy was secondary mites. The postnaupliar somites proliferate in the articulates. This conclusion was sup- from the anterior end of the telson, which ported by Anderson (1959). Heteronomy is the posterior center. Starobogatov's (1986) appears to be associated with the evolution interpretation of development is different. of specialized larvae which function early The concept of primary heteronomy is the (Manton, 1949). starting point, but, by the use of "indirect The primary heteronomy of the Crusta- data," Starobogatov arrives at a combined cea is not in question. The studies by Man- developmental-functional concept, the pro- ton on Hemimysis (1928) and Nebalia totagma. Anterior and posterior prototag-

This content downloaded from 193.191.134.1 on Wed, 3 Dec 2014 08:38:08 AM All use subject to JSTOR Terms and Conditions 136 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 9, NO. 1, 1989 mata togethercomprise the larvalsegments, are presumablyplaced in this by anal- and are separated by a third prototagma ogy, since they do not show this character. comprised of postlarval segments derived Reference to the original data on the de- from a growth zone. The classification of velopment of Derocheilocaris (see Dela- the Crustacea produced by Starobogatov mare-Deboutteville, 1954; Hessler and (1986) is based on the relationshipbetween Sanders, 1966) clearly shows that there is these prototagmataand adult tagmosis and no deviation in the orderlysequence of so- segmentationpatterns, type of carapace,and mite separationfrom the telson. Somites are degreeof heteronomyof the trunk append- progressivelybudded off the anteriorend of ages. the telson in the typical crustacean ana- The Tantulocaridaare placed by Staro- morphic manner. The only deviation is in bogatov (1986) in the Class Ascothorac- the rate of development of the appendages, ioides. This groupis diagnosedby the com- thoracopod 3 becoming functional before position of the middle and posterior thoracopod2 in D. typicusPennak and Zinn prototagmata;the middle prototagmacon- andD. remaneiDelamare-Deboutteville and sists of three somites and the posterior of Chappuis.In D. katesae Noodt, however, it five to eight includingthe anal segment.The is thoracopod4 that appearsbefore thorac- class includes the Ascothoracida, Mysta- opods 2 and 3 (McLachlan, 1977). The in- cocarida,and Copepodaas well as the Tan- direct method of determining boundaries tulocarida.The last three taxa are placed in between prototagmatais clearly unreliable the subclass Cyclopiones, diagnosed by when species within a singlegenus can show "carapacenot flexedalong dorsomedial line, differences in "prototagmosis."We inter- but in all known forms to some extent re- pret this heterochronyas evidence of mor- duced, first antennae used for floating or phogeneticplasticity within the genus in re- swimming." The Tantulocarida(as the su- sponse to particular functional needs. perorderBasipodelliformii) are then placed Similar functional heterochronyis seen in in the infraclassCalanioini together with the other .For example, in the deca- gymnopleancopepods. The Calanioiniis di- pod Palaemon serratus (Pennant), pereio- agnosed by the location of the major body pod 5 becomes functionalbefore pereiopod articulationbehind the sixth trunk somite. 4 (see Fincham, 1983), but both belong to This classification scarcely deserves se- the same prototagmain Starobogatov'ssys- rious consideration. It is based on an ex- tem. It is apparentto us that developmental tremely small number of characterscom- criteriaare very important in assessing ho- paredto a modem cladistic classificationof mology of body somites (as discussed the same and relatedtaxa (see Grygier,1983, above), but we find no evidence that the 1987, for example). Functional analysis is eventual role of an appendagein the adult not used as a method of understandingand has any effecton the patternof proliferation delimiting characters,but function itself is of the postcephalic somites. Any hetero- used as a character.Virtually no attempt is chrony in the sequence of appendage de- made to assess the homology of structures velopment can readily be attributedto the or to assess the plesiomorphic-apomorphic functional specializationof the larvae con- polarityof characterstates. Rather than list cerned.We thus concludethat the basic con- other deficiencies in methodology it seems cept of the prototagmaas a developmental- most instructive to examine the "indirect functional entity is invalid. method" of which identifying prototagma of is centralto Starobogatov'ssystem. The in- PhylogeneticRelationships direct method uses deviations in the se- Tantulocarida quence of somite formationof definitive so- Grygier's (1987) recent study of maxil- mites and appendages(Starobogatov, 1988, lopodan phylogeny was completed before in letter to Grygier).The identification of the new information on the tantulocaridan the prototagmaboundaries in the Ascotho- penis and trunksegmentation was available. racioidesis based on the appearanceofthor- The primaryaim of that study was to assess acopod 3 before thoracopod 2 in the de- the systematic position of the Facetotecta velopment of Derocheilocaris. The in relationshipto other thecostracans.Our copepods, ascothoracids,and tantulocarids aim is to determinethe position of the Tan-

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Table 1. Characterset for analysis of relationshipsamong maxillopodantaxa.

Character Plesiomorphicstate Apomorphicstate 1. Antennule biramous uniramous 2. Trunklimbs 15 pairs 7 pairs 3. Trunk somites includingtelson 16 13 maximum 4. Male gonopores trunksomite 8 trunksomite 7 5. Tapetalcells of naupliuseye absent present 6. Trunksomites includingtelson 13 12 maximum 7. First trunklimb unmodified modified as maxilliped 8. Endite on thoracopods2-6 present absent 9. Carapace present absent 10. Compoundeyes present absent 11. Male trunklimb 7 unmodified modified as penis 12. Female trunklimb 7 present absent 13. Trunklimb exopod 3-segmented 1 or 2-segmented 14. Trunklimbs 2-6 present absent 15. Caudalrami 1-segmented 3-segmented 16. Trunksomites 12 or 13 11 17. Antennaryexopod in adult 14 segments 9 segmentsmaximum 18. Mandibularexopod in adult 13 segments 7 segmentsmaximum 19. Antennulesegments 9 or more 8 or less 20. Trunklimbs 2-5 biramous buds 21. Gonopores(male) on trunk somite 7 on trunksomite 5 22. Intercoxalsclerites on thoracopods2-6 absent present(as couplers) 23. First trunksomite free fused to cephalon 24. Maxilliped biramous uniramous 25. Cephalicappendages present absent 26. Oral disc absent present 27. Antennaryexopod in adult 14 segments 2 segments 28. Bipartitepigment cells in compound eye absent present 29. Naupliarcarapace absent present 30. Trunklimbs 3-6 present lost 31. Lateralgut caeca in carapace absent present 32. Antennularyattachment device absent present 33. Poison spine absent present 34. Postmaxillularylimb buds in nauplius present absent 35. Frontalfilaments not associatedwith associatedwith compoundeye compound eye tulocarida and we present a phylogeny (Fig. This analysis relies on relatively few char- 6) incorporating all the major taxa previ- acters and many of these are unsatisfactory, ously attributed to the Maxillopoda. The since they cannot be scored for all taxa. This was used as the out-group in is due in part to the great diversity exhibited accordance with the scheme of maxillopo- by maxillopodans. For example, some have dan origins proposed by Newman (1983). no cephalic appendages but a full comple- The phylogenetic scheme was generated by ment of trunk limbs, while others have all hand and the characters used are given in the cephalic limbs but only a single pair of Table 1. The plesiomorphic states for char- trunk limbs. The only limb common to every acters 1-5, 9-12, and 15 are based on the maxillopodan is the first postcephalic trunk out-group. Those for characters 6-8, 13 and limb. Also, it is difficult to find characters 14, and 16-35 are determined by in-group that are equally applicable to both fossil and analysis, in which it is assumed that evo- recent taxa. However, despite its prelimi- lution has proceeded largely by oligomer- nary nature and the considerable conver- ization (Boxshall et al., 1984; Hessler and gence evident within the group, this analysis Newman, 1975). Transition series of 3 or indicates that there are two main lineages more states of any given character (for ex- within the Maxillopoda: the lineage leading ample, characters 3, 6, and 16 in Table 1) to the Copepoda (comprising Copepoda, are treated in discrete steps rather than as Mystacocarida, and Skaracarida) and that multistate characters. leading to the Thecostraca (comprising The-

This content downloaded from 193.191.134.1 on Wed, 3 Dec 2014 08:38:08 AM All use subject to JSTOR Terms and Conditions 138 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 9, NO. 1, 1989 costraca, Branchiura, Ostracoda, and Tan- the caudal rami are 3-segmented. This is tulocarida). The former is best character- treated in Table 1 as an apomorphic char- ized by the modification of the first trunk acter state for the Skaracarida, because the limb as a maxilliped, the latter by the mod- out-group, the Malacostraca, and the ma- ification of the male seventh trunk limb as jority of other maxillopodans have 1-seg- a penis (presumed to have been lost sec- mented caudal rami. However, it is possible ondarily in the Branchiura). The Tantulo- that it is a plesiomorphy, since evolution carida share the loss of the compound eyes within the Crustacea is presumed to proceed and carapace with the copepod lineage, but typically by oligomerization (Hessler and are placed at the base of the thecostracan Newman, 1975; Boxshall et al., 1984). Some lineage on the presence of the penis, the loss cirripedes have multisegmented caudal ap- of the female seventh trunk limb, and the pendages on the abdominal rudiment (New- 2-segmented state of the thoracopodal ex- man et al., 1969), but this may be the result opods. The cladogram presented by Grygier of secondary annulation, as found in the (1987) contains fewer taxa, but the Theco- thoracopodal cirri. We have regarded the straca, Branchiura, and Copepoda are in the ascothoracidan 1-segmented condition as same relative positions as in Fig. 6. the plesiomorphic state of the Thecostraca. Relationships between maxillopodan taxa Other characters of skaracarids are difficult were also analyzed in Schram (1986), a work to interpret because of their general "pa- completed prior to the publication of new laeozoic" appearance. The antennae, for ex- data on the Skaracarida (Miiller and Wal- ample, appear to have 14 exopodal seg- ossek, 1985), Tantulocarida (Boxshall and ments but these may not be true segments, Lincoln, 1987), and Facetotecta (Grygier, separated proximally and distally by joints 1987). Schram's cladogram (1986, fig. 43- containing arthrodial membrane. In Skara 6) divides the Maxillopoda into an unre- annulata Miiller and Walossek there are solved trichotomy. The Tantulocarida form more "joints" on the posterior side of the one branch. The second branch groups the antennary exopod than on the anterior side thecostracan taxa together and places the (Miiller and Walossek, 1985). This suggests Copepoda as the sister group of the The- that these "joints" on skaracarid limbs may costraca on the possession of 4 or more nau- not be homologous with the segments of pliar stages, a character state that we inter- recent maxillopodans. There are similar dif- pret as plesiomorphic. The third branch ferences in the subdivision of the protopods comprises the Branchiura, Mystacocarida, of the postmandibular limbs which make and Ostracoda. These are linked by the the identification ofhomologies with recent reappearance of the mandibular palp and maxillopodans extremely difficult. Despite the possession of less than six thoracic so- these problems we consider that it is more mites. We interpret the possession of the informative to bring such fossil taxa into an mandibular palp as plesiomorphic to the exploratory analysis of this sort rather than Maxillopoda on the basis of in-group anal- to ignore them. ysis. The presence in the Cytherella of paired penes, derived from the thoraco- ACKNOWLEDGEMENTS pods of trunk somite 6, 7, or 8 (see above), The material was collected during a guest-profes- indicates that a thorax of less than six so- sorship of Prof. Dr. J. H. Stock at the University of mites cannot be used as an of La Laguna(Tenerife) under a contractwith the Com- apomorphy isi6n Asesora de Investigaci6neCientifica y Technica this lineage. Schram shows the Branchiura (CAICYT),Madrid. We are gratefulto Prof. Stock for and Mystacocarida as sister groups but makingthe materialavailable for study.We would also specifies no synapomorphy. The differences like to thank Dr. Mark Grygierfor many improve- between 6 and the of Schram ments suggested.This paper is Part 00 of the Stygo- Fig. cladogram fauna of the Islands. (1986) can be attributed to differing inter- Canary pretation ofhomology, polarity of character LITERATURECITED states, and new data unavailable to Schram. We have reservations about the position Anderson,D. T. 1959. The embryologyof the poly- of the Skaracarida in 6. This ex- chaeteScoloplos armiger. -Quarterly Journalof the Fig. group MicroscopicalSociety 100: 89-166. hibits many basic features that differ from 1967. Larvaldevelopment and segmentfor- the recent maxillopodan taxa. For example, mation in the branchiopodcrustaceans Limnadia

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stanleyanaKing (Conchostraca)and Artemiasalina of the Maxillopoda.-Ph.D. thesis, University of (L.) (Anostraca).-Australian Journalof Zoology 15: Californiaat San Diego. Pp. 1-417. 47-91. 1985. Comparativemorphology and ontog- .1969. On the embryologyof the cirripede eny of the Ascothoracida,a step towardsa phylogeny crustaceansTetraclita rosea (Krauss), T. purpuras- of the Maxillopoda.-Dissertation AbstractsInter- cens (Wood), Chthamalusantennatus (Darwin) and national 45(8): 2466B-2467B. Chamaesiphocolumna (Spengler) and some consid- . 1987. New records, external and internal erationsof crustaceanphylogenetic relationships.- anatomy,and systematicposition of Hansen'sy-lar- PhilosophicalTransactions of the Royal Society of vae (Crustacea:Maxillopoda: Facetotecta).-Sarsia London,Series B, BiologicalSciences 256: 183-235. 72: 261-278. Becker, K.-H. 1975. Basipodella harpacticola ,and D. B. Fratt. 1984. The ascothoracidcrus- n.gen.,n.sp. (Crustacea, Copepoda).-Helgoliinder tacean Ascothoraxgigas: redescription,larval de- wissenschaftlicheMeeresuntersuchungen 27: 96-100. velopment, and notes on its infestationof the Ant- Bowman,T. E., and L. G. Abele. 1982. Classification arctic ophiuroid Ophionotus victoriae.-Antarctic of the Recent Crustacea.--In:L. G. Abele, ed., The ResearchSeries 41: 43-58. biology of Crustacea,vol. 1, pp. 1-27. Academic Hallberg,E., and R. Elofsson. 1983. The larvalcom- Press, New York and London. pound eye of .-Journal of CrustaceanBi- Boxshall,G. A. 1983. A comparativefunctional anal- ology 3: 17-24. ysis of the major maxillopodangroups.- In: F. R. , and M. J. Grygier. 1985. An ascotho- Schram,ed., Crustaceanphylogeny. Pp. 121-143. A. racid compound eye (Crustacea).-Sarsia 70: 167- A. Balkema,Rotterdam. 171. , F. D. Ferrari,and H. Tiemann. 1984. The Hessler, R. R., and W. A. Newman. 1975. A trilo- ancestralcopepod: towardsa consensus of opinion bitomorphorigin for Crustacea.--Fossilsand Strata at the First InternationalConference on Copepo- 4: 437-459. da.-Crustaceana, Supplement7: 68-84. ,and H. Sanders. 1966. Derocheilocaristypicus ,R. Huys, and R. J. Lincoln. (In press.) A new Pennak & Zinn (Mystacocarida)revisited. -Crus- species of Microdajusparasitic on a tanaid in the taceana 11: 141-155. northeasternAtlantic, with observationson M. langi Ivanov, P. P. 1944. The primaryand secondaryme- Greve.-Systematic Parasitology. tameryof the body.-Zhurnal ObshcheyBiologii 5: , and R. J. Lincoln. 1983. Tantulocarida,a 61-95. [In Russian with Englishsummary.] new class of Crustaceaectoparasitic on other crus- McLachlan,A. 1977. The larval development and taceans.-Journal of CrustaceanBiology 3: 1-16. populationdynamics of Derocheilocarisalgoensis. - ,and . 1987. The life cycle of the Tan- ZoologicaAfricana 12: 1-14. tulocarida(Crustacea). -Philosophical Transactions Manton, S. M. 1928. On the embryologyof a mysid of the Royal Society of London, SeriesB, Biological crustaceanHemimysis lamnornae.-Philosophical Sciences 315: 267-303. Transactionsof the Royal Society of London, Series E. 1956. Some crustacean B, BiologicalSciences 216: 363-463. Dahl, relationships.-In: - K. G. ed., Bertil Hanstr6m,zoological 1934. On the embryologyof Nebalia bipes. Wingstrand, the of in honourof his sixty-fifthbirthday, Novem- PhilosophicalTransactions of Royal Society papers Sciences223: 168-238. ber20, 1956.Pp. 138-147. ZoologicalInstitute, Lund, London,Series B, Biological Sweden. 1949. Studieson the OnychophoraVII. The of and some Darwin,C. 1851. A monographon the sub-classCir- earlyembryonic stages Peripatopsis gen- with of all the The eral considerationsconcerning the morphologyand ripedia, figures species. Lepadi- of the dae;or pedunculatedCirripedes. -Ray Society,Lon- phylogeny Arthropoda.-Philosophical don. 1-400. Transactionsof the Royal Society of London, Series Pp. Sciences 233: 483-580. C. 1954. Le development B, Biological Delamare-Deboutteville, Melnikov,0. A. 1971. Primaryheteronomy of body postembryonairedes Mystacocarides.-Archives de in Articulata.-Zhurnal 32: 597- et G6enrale91: 25-34. ObshcheyBiologii Zoologie Exp6rimentale 612. [In Russian with Englishsummary.] D. 1988. in num- Ferrari,F. Developmentalpatterns Moyse,J. 1987. Larvaeoflepadomorph barnacles.- bersoframal segmentsof copepodpost-maxillipedal In: A. J. Southward,ed., Barnaclebiology. Pp. 329- legs.-Crustaceana 54: 256-293. 362. Crustaceanissues 5, pp. 1-364. A. A. Balkema, Fincham,A. A. 1983. Larvaldevelopment of British Rotterdam. prawnsand shrimps (Crustacea:Decapoda: Natan- Muller, K. J., and D. Walossek. 1985. Skaracarida, tia)4. Palaemon(Palaemon) serratus (Pennant, 1777) a new orderof Crustaceafrom the Upper Cambrian and functionalmorphology of swimming.-Bulletin of Vastergotland,Sweden.-Fossils and Strata 17: of the British Museum (Natural History), Zoology 1-65. 44: 125-161. Newman, W. A. 1983. Origin of the Maxillopoda: Garcia-Valdecasas,A. 1984. Morlockiidaenew fam- urmalacostracan ontogeny and progenesis.-In: F. ily of Remipedia (Crustacea)from Lanzarote(Ca- R. Schram,ed., Crustaceanphylogeny. Pp. 105-119. nary Islands).-Eos 60: 329-333. Crustaceanissues 1, pp. 1-365. A. A. Balkema,Rot- Grygier,M. J. 1983. Ascothoracidaand the unity of terdam. Maxillopoda.-In: F. R. Schram, ed., Crustacean ,V. A. Zullo, and T. H. Withers. 1969. Cir- phylogeny.Pp. 73-104. Crustaceanissues 1, pp. 1- ripedia.-In: R. C. Moore, ed., Treatise on inver- 365. A. A. Balkema,Rotterdam. tebratepaleontology, Part R (Arthropoda1), vol. 1, 1984. Comparativemorphology and ontog- pp. R206-295. Geological Society of America and eny of the Ascothoracida,a step towardsa phylogeny University of Kansas Press, Lawrence,Kansas.

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Schram,F. R. 1986. Crustacea.-Oxford University of Starobogatov(1986) by M. J. Grygier,including Press, New York, London. Pp. 1-606. additionalnotes by Starobogatov.] Schulz, K. 1976. Das Chitinskelettder Podocopida (Ostracoda,Crustacea) und die Frageder Metamerie RECEIVED:31 May 1988. dieser Gruppe.-Ph.D. thesis, University of Ham- ACCEPTED:14 July 1988. burg.Pp. 1-167. Starobogatov,Ya. I. 1986. Systematics of Crusta- Addresses:(GAB) British Museum (NaturalHisto- cea.-Zoologicheskiy Zhurnal 65: 1769-1781. [In ry),Cromwell Road, London SW7 5BD, England;(RH) Russian,with Englishsummary.] Marine Biology Section, Institute of Zoology, State 1988. Systematicsof Crustacea.-Journalof Universityof Ghent, K.L.Ledeganckstraat35, B-9000 CrustaceanBiology 8: 300-311. [Englishtranslation Ghent, Belgium.

ANNOUNCEMENT

The following applicationhas been received by the InternationalCommission on Zoo- logical Nomenclatureand has been publishedin the Bulletin of ZoologicalNomenclature, volume 45, part 3 (23 September 1988). Comment or advice on this applicationis invited for publication in the Bulletin and should be sent to the Executive Secretary,ICZN, % BritishMuseum (NaturalHistory), CromwellRoad, London SW7 5BD, United Kingdom. Case 2622. Pleuromma princeps Scott, 1894 (currentlyGaussia princeps; Crustacea, Copepoda):proposed conservation of the specific name.

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