(Crustacea: Tantulocarida) Parasitic on a Tanaid in the Northeastern Atlantic, with Observations on M

Home , Tantulocarida

A new species ot Microdajus (Crustacea: Tantulocarida) parasitic on a tanaid in the northeastern Atlantic, with observations on M. langi Greve

Geoffrey A. Boxshall 1, Rony Huys2 and Roger J. Lincoln 1 1Department of Zoology, British Museum (Natural History), Cromwell Road, London SW7 5BD, UK eMarine Biology Section, Insatute of Zoology, State University of Ghent, K.L. Ledeganckstraat 35, B- 9000 Ghent, Belgium

Accepted for publication 27th September, 1988

Abstract

The tantulus larva of Microdajus langi is redescribed using Scanning Electron Microscopy. Thoracopods 2-5 have poorly developed but fully armed endites. Thoracopods 1-5 are biramous, with each ramus represented by a minute segment. A new species, M. pectinatus, is described from a tanaid host collected in the Rockail Trough, off the west coast of Scotland. A system of homologies for the portopodal segments of the thoracopods of the tantulus larva is proposed, Some aspects of the musculature of the adult male are described for the first time.

Introduction This account also describes a new species of Microdajus Greve parasitic on tanaids collected Tantulocarids are small, ectoparasitic in deep water in the vicinity of the Rockall crustaceans that utilize other crustaceans as Trough, off the west coast of Scotland. hosts. Six species are now known from tanaid hosts, all from high latitude localities in both northern and southern hemispheres (BoxshaU & Methods Lincoln, 1987; Grygier & Sieg, 1988). Tantulo- carids are usually found in small numbers but can Specimens were prepared for examination using be common locally. Microdajus langi Greve was light microscopy by mounting in lactophenol and found in large numbers on tanaids in Raunef- sealing with glyceel. Drawings were made using jorden, western Norway (Greve, 1965; Boxshall oil immersion on a Leitz Dialux 20 microscope & Lincoln, 1987), and has also been recorded with interference microscopy. Specimens were from Scotland (Boxshall & Lincoln, 1987), from prepared for Scanning Electron Microscopy Byfjorden, Fensfjorden, the Skagerrak and (SEM) by dehydration through graded acetone, Olsofjorden (Greve, 1988) and from Gullmarf- critical point drying, and sputter coating with jorden (Grygier & Sieg, 1988). Bulk samples palladium. SEM observations were made using a collected in Raunefjorden have recently been Hitachi S-800 electron microscope. Drawings sorted and the new material has enabled ad- were made using a camera lucida, and some ditional observations to be made using SEM. details were added from SEM photographs. 18 G.A. Boxshall et al.

Microdajm langi Greve, 1965 Remarks This SEM study of the tantulus larva of M. langi Additional description has revealed many inadequacies in the original and subsequent descriptions of this species Tantulus larva (Greve, 1965; Boxshall & Lincoln, 1987). It Cephalic shield smooth except for patches of tiny emphasises the difficulty in studying such small setules and some oblique epicuticular lamellae organisms, without dissection, using light associated with single row of 6 pores near pos- microscopy alone. The most important feature terior and ventral margins. Posterior margin of discovered using SEM is the presence of endites shield with fringe of tiny setules and 2 pairs of on thoracopods 2-5. These endites are not well larger sensillae. Posterior margin of each free developed, bulbous structures, as found in Deo- thoracic somite with similar fringe of setules (Fig. terthron (cf. Boxshall & Lincoln, 1987) and 1A) plus scattered setules over surface of tergite. Boreotantulus (cf. Huys & Boxshall, 1988). They First abdominal somite with fringe of setules are small, angular protrusions on the medial along posterior margin dorsally; ventral surface margin of a discrete praecoxal segment, and they smooth. Entire surface of second abdominal carry the typical palmate, coupling spine. These somite ornamented with long setules (Figs 1A,B). spines, as in other tantulocarids, serve to link the Caudal rami distinct, uni-segmented (Fig. 1B); members of a leg pair together during swimming. bearing a large apical seta and 2 short setae, one Other significant corrections to earlier descrip- lateral and one ventro-lateral. tions are: the presence of only one seta on the Thoracopod 1 with a bi-segmented protopod; sixth thoracopod, the presence of a third seta on first segment (syncoxa) large, lacking endite; the caudal ramus, and the recognition of the second segment (basis) small, unarmed. Each articulated bases of the setae on the thoracopods ramus represented by tiny articulating segment as representing vestigial, unisegmented rami. bearing one apical seta. Thoracopods 2-5 (Figs Additional detail of ornamentation is visible 1C,D) each with a bi-segmented protopod; first under SEM that cannot be seen using light segment (praecoxa) with poorly-developed microscopy. The setulation of the thoracic ter- endite bearing one large, palmate coupling spine gites, thoracopods and abdomen is recorded here (Fig. 1D) and 2 small setae; second segment for the first time. The ridged posterior surface of (coxo-basis) ornamented with many setules (Fig. the ramal setae on the thoracopods may enable 1C). Each ramus represented by small articulat- the setae to flex posteriorly during the recovery ing lobe bearing single apical seta. Apical seta stroke of swimming. ornamented anteriorly and laterally with tiny setules, posteriorly with regular, transverse ridges (Fig. 1C). Thoracopod 6 (Fig. 1C) com- Microdajus pectinatus n. sp. prising single protopodal segment lacking endite; bearing single apical seta inserted directly on Descrip~on segment. Tantulus larva Material examined. Two tantulus larvae and 2 Body comprising head, thorax of 6 pedigerous adult females, mounted on an SEM stub, stored somites and bi-segmented abdomen (Fig. 2A). in collections of BM(NH) Reg. No. 1988.276. Head covered with smooth cephalic shield, lack- Host. Leptognathia breviremis (Lilljeborg). ing any ornamentation of epicuticular lamellae Locality. Collected by Beyer net, from Raunef- (Fig. 2A,B). Shield with paired pores anterola- jorden, western Norway on muddy bottom at a terally, one pair of pores and one pair of fine depth of 120 m, during September 1985. setules postero-laterally (Fig. 8E). Conspicuous A new tantulocarid crustacean from a tanaid 19

Fig. 1. M. langi tantulus larva, SEM photographs. A, Posterodorsal view, showing rear margins of thoracic tergites and posteroventrai surface of second abdominal somite; B, Abdomen of tantulus, ventral; C, Thoracopods 6 to 4, posterior surfaces; D, Endite on thoracopod 5, posterior view showing praecoxa (pc) with its enditic armature, and coxo-basis (cb). Scale-bars: 5 I~m (A-C) and 1/zm (D). 20 G.A. Boxshall et al.

Fig. 2. M. pectinatus n. sp., SEM photographs. A, Tantulus larva, dorsal; B, Head and thoracic tergites of expanded male tantulus; dorsal view showing epicuticular circlet (arrowed) surrounding pore; C, Second abdominal somite, postero-ventral view showing combs of spines and median bifid spine; D, Oral disc attached to host, frontal view. Scale-bars: 20/.~m (A, B) and 4 #m (C, D). A new tantulocarid crustacean from a tanaid 21 pair of pores present dorsally, just posterior to spine with 4 pairs of barbs (Figs 4A,B) and with rear margin of shield (Figs 2B, 8D); each sur- 2 small spinous processes. Both rami represented rounded by circlet of epicuticular ornamentation by small segments largely concealed within ter- (arrowed in Fig. 2B). Oral disc located ventrally minal concavity of protopod; each with one large at anterior margin of head. Disc about 16/.tm in apical seta. Thoracopod 6 (Fig. 3C) uniramous; diameter, attached to host integument. Oral disc comprising single, unarmed segment bearing one sheathed by short outer membrane, closely ad- long apical seta. Thoracopodal setae typically pressed onto surface of disc (Fig. 2D). Tubular smooth on anterior surface, transversely ridged structure with thick dorsal wall discernible inside along posterior surface (Fig. 4A), with scattered head leading to central pore of oral disc (Fig. lateral setules. 8D). Marked chitinous collar surrounds this tube about at midlength. Cephalic stylet visible Male metamorphosis through integument; about 20~m in length, Adult male formed in reflexed position (Fig. 4D) curved, open proximally and tapering distally. within expanded trunk sac of preceding tantulus Four glandular lobes visible posteriorly inside stage (Figs 4C, 5A). Trunk sac located posterior head. Ventro-lateral margins of cephalic shield to tergite of sixth thoracic somite; causing ven- with ridge-like folds of integument (Fig. 8E). tral deflection of larval abdomen. Tergites and Free thoracic somites each with distinct ter- limbs separated by slight thoracic expansion (Figs gite, that of first somite partly or completely 5A,B). Male inside sac connected to larval head concealed beneath posterior rim of cephalic via broad umbilical cord (Figs 5A,B). Cord shield (Figs 2A,B). Tergites smooth, lacking entering male cephalothorax mid-ventrally in conspicuous surface ornamentation. Abdomen anterior third. (Figs 2C, 3D,E) 17/xm long; first somite 1.5 times wider than long (6 × 9/xm), second somite Adult male 1.1 times longer than wide (11 × 10 p~m). First Body comprising cephalothorax incorporating somite unarmed. Dorsal surface of second somite first and second pedigerous somites, 4 free smooth, ventral surface with numerous small thoracic somites and 2 abdominal somites. spinules and well-developed combs of larger Cephalothorax covered with highly ornamented spinules near the posterior border (Figs 2C, 3D). dorsal shield (Figs 6A,B). Ornamentation con- Paired lateral combs each with 4-5 spinules, tips sisting primarily of longitudinal lameUae with of which extend beyond rear margin of caudal occasional transverse features. Dorsal surface rami. Median spinous process between combs, also bearing 7 pairs of bifid sensillae, each laterally flattened and bifid apically. Caudal rami located in its own cup-shaped depression. Cluster distinct, wider than long, armed with one long of 4 aesthetascs on each side of anterior margin and 2 short setae (Figs 3D,E). of head (Fig. 7A), presumably representing Thoracopod 1 (Fig. 3A) with bi-segmented antennules. No other cephalic appendages protopod; first segment (syncoxa) large, subrec- represented. Cephalothorax carrying 2 pairs of tangular, lacking endite; second segment (basis) thoracopods posteriorly. Ventral surface of short, unarmed. Each ramus represented by cephalothorax finely ornamented with ridges. minute, articulating segment bearing single api- Opening marking position of umbilical connec- cal seta. Thoracopods 2-5 similar (Fig. 3B); each tion simple, lacking associated structures (Fig. with large protopod bearing single endite prox- 7B). Each free thoracic somite with well- imally. Endite carried on thin-walled praecoxal developed tergite ornamented with conspicuous segment that is largely incorporated into rest of lamellae (Fig. 5A). First abdominal somite 16 × protopod; coxal portion and basis fused distally. 20/xm; tapering posteriorly; bearing penis ven- Protopod ornamented with distal row of spinules trally (Fig. 7D). Second abdominal somite (Fig. medially. Endite armed with palmate coupling 7C) 1.8 times longer than wide (40× 22/xm); 22 G.A. Boxshall et al.

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Fig. 3. M. pecanatus n. sp. A, First thoracopod, anterior; B, Second thoracopod, anterior; C, Sixth thoracopod, anterior; D, Abdomen, ventral; E, Abdomen, lateral.

bearing mid-posterior anal slit and caudal rami. articulated setae which are bilaterally serrate Abdominal somites without ornamentation of distal to articulation. Exopod with minute first epicuticular lamellae. Caudal rami 2.5 times segment and large second segment; latter bear- longer than wide (15 × 6/zm), bearing 3 subequal ing 5 articulated setae and one outer, short, ser- setae on distal margin. rate seta. Thoracopods 3-5 (Fig. 8B) similar to Thoracopods 1 (Fig. 8A) and 2 each compris- thoracopod 1 except protopod is bi-segmented, ing large, unsegmented protopod bearing one comprising one large proximal syncoxa and one pair of brush setae proximally on medial margin, small distal basis bearing rami. Segmentation and one bi-segmented exopod and one uni-segmen- armature of rami as for thoracopod 1. Thoraco- ted endopod. Endopod just wider than long, pod 6 (Fig. 8C) uniramous, tri-segmented. First armed with single short, naked inner seta and 4 segment (syncoxa) lacking brush setae; second A new tantulocarid crustacean from a tanaid 23

Fig. 4. M. pectinatus n. sp., SEM photographs. A, Thoracopodal setae and a palmate coupling spine, posterior; B, Coupling spines on fifth thoracopod, posterior; C, Attached male tantulus with expanded trunk sac, lateral; D, Adult male removed from trunk sac, lateral. Scale-bars: 1/xm (A, B) and 50 tzm (C, D). 24 G.A. Boxshall et al.

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Fig. 5. M. pectinatus n. sp. A, Expanded tantulus containing developing male, lateral; B, Head and thoracic tergites of same; dorsal; C, Lateral view of sixth thoracic somite and abdomen, showing musculature associated with sixth thoracopod and penis (area of thin integument indicated by arrow). A new tantulocarid crustacean from a tanaid 25

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Fig. 6. M. pectinams n. sp. A, Adult male, dorsal; B, Same, lateral. 26 G.A. Boxshall et al.

Fig. 7. M. pectinatus n. sp. Adult male, SEM photographs. A, Anterior part of cephalothorax, ventral view showing aesthetascs; B, Same, showing opening (arrowed) where umbilical cord enters male; C, Abdomen, dorsal; D, Abdomen, postero-lateral view showing curved distal part of penis (arrowed), and caudal rami. Scale-bars: 20/~m (A, C, D) and 5 p.m (B). A new tantulocarid crustacean from a tanaid 27 segment (basis) short, unarmed; third segment and posterior group of 4 muscles. Former ap- (exopod) carrying one outer serrate seta and 4 pears to insert anterior to basal foramen of articulated, distally serrate setae. thoracopod and presumably act as promotors; Penis (Figs 5C, 8C) located medially with base latter insert posterior to foramen and act as fused to ventral surface of first abdominal somite. remotors producing swimming power stroke. Distal part (arrowed in Fig. 7D) curved and pos- Three other muscles, lying anteriorly within tero-ventrally directed; separated from base by syncoxa, may also be regarded as extrinsic mus- indistinct suture; area of thin integument cles. These have widely divergent attachments (arrowed in Fig. 5C) present just proximal to distally on wall of syncoxa and one common suture; longitudinal membrane present along proximal attachment, apparently to ventral body- concave ventral surface of penis. Slight subapi- wall adjacent to foramen of limb. These muscles cal swelling on ventral margin with 3 tiny probably represent continuations of extrinsic spinules. Penis with large apical opening. promotors, passing into limb via intermediate attachments. Musculature There are 3 intrinsic muscles. One pair of Some muscles can be seen through the in- flexors originates postero-medially in syncoxa, tegument and are described here although it has passes obliquely towards exopod and appears to not been possible to identify precisely all the sites insert laterally on its rim. These muscles flex of origin and insertion. exopod away from mid-line and may also move Trunk muscles. Paired longitudinal trunk mus- brush setae on syncoxa. Single short double- cles present dorsally and ventrally. Dorsal trunk stranded muscle originates high on postero- muscles originate in rear half of cephalothorax, lateral wall of syncoxa and inserts medially on close to mid-line. Each muscle comprises 3 rim of exopod. This muscle opposes lateral strands at its origin. Muscles pass posteriorly flexors. through all free thoracic somites, attaching Thoracopod 6 (Figs 5C, 8C) has fewer muscles anteriorly in each somite. In second free thoracic but shows same basic pattern. There is one sin- somite 2 strands fuse resulting in each dorsal gle-stranded promotor and one similar remotor, muscle becoming double stranded. They insert each with a continuation inside syncoxa. Sin- on anterior rim of first abdominal somite. There gle short intrinsic muscle originates laterally on are no dorsal trunk muscles in abdomen (Fig. syncoxa and passes distally. Its insertion may be 5¢). on basis or on exopod. Ventral trunk muscles also originate in pos- Penis musculature. Penis is bi-segmented, with terior part of cephalothorax close to mid-line. first segment fused to genital somite. Single They pass posteriorly through all free thoracic broad band of muscles (Fig. 8C) originates on somites before inserting ventrally on rim of first ventral surface of proximal penis segment and abdominal somite. Intermediate attachments of inserts on the ventral surface of distal segment ventral muscles in free pedigerous somites could about one third along its length (Fig. 5C). These not be confirmed. Ventral muscles continue into intrinsic muscles can flex distal part of penis abdomen (Fig. 5C), attaching on rim of second ventrally; flexure being facilitated by area of thin abdominal somite before inserting mid-way along integument proximal to suture line. somite. Ventral trunk muscles are double-stranded near their origin, but become single-stranded Material examined. Holotype male tantulus at their insertion. containing developing adult male within expan- Thoracopodal muscles. Thoracopods 1 to 5 each ded trunk sac; 20 males and three tantulus larvae have a similar musculature (Fig. 8B). Extrinsic paratypes. Material collected by Scottish Marine muscles originate on dorsal body-wall and form 2 Biological Association and found by Dr Graham functional groups, anterior group of 3 muscles Bird (Nottingham University). Stored in the col- 28 G.A. Boxshall et al.

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Fig. 8. M. pectinatus n. sp. A, First thoracopod of male, posterior; B, Somite bearing fourth thoracopod of male, posterior view showing thoracopodal musculature (posterior muscles omitted from right side; C, Abdomen and sixth legs, ventral view showing associated musculature; D, Head of expanded tantulus, dorsal view showing internal organs; E, Same lateral. A new tantulocarid crustacean from a tanaid 29 lections of the BM(NH), Reg. Nos. 1988.277 3 Cephalic shield about as long as wide; cephalic (hototype) and 1988.278-287 (paratypes). stylet 14 t~m long ...... M. langi Host. An as yet undescribed new species of - Cephalic shield 1.2 times longer than wide; Tyl~lotanais, referred to as Typhlotanais sp. D cephalic styler 30 tzm long ...... M. gaelicus (in part) from stn. 6 in the BIOGAS report of Holdich & Bird (1985: 445). This is one of three Homology of protopodal segments of the thoraco- species found in the area that closely resembles T. sandersi Kudinova-Pasternak. pods Loca~ty. Holotype and 20 paratypes parasitic on The protopodal part of the thoracopods of both a single Typhtoumais sp. D collected at Station ES218 (57022 ' N 10024 ' W) at a depth of 2175 m, tantulus and adult stages has a maximum of two segments in any known species of tantulocarid. on 3 August 1982. One paratype parasitic on a second Typhlomnais sp. D from the same local- However, the distribution and structure of these ity. One paratype parasitic on a Typhlotanais sp. segments suggests that the basic protopodal D from each of two stations: ES10 (56°37'N structure of the adult male is tri-segmented 11004 ' W), at 2540m on 4 July 1973, and ES197 (Huys & Boxshall, 1988). A similar analysis can be undertaken using the tantulus thoracopods. (57°21'N 10°29'W), at 2200m on 19 August There are three different types of tantalus 1981. Etymology. The specific name is derived from thoracopods known. In the first type, as found in the Latin pectinis meaning a comb, and refers to Deoterthron, there is a single protopodal segment the ventral combs of spines on the abdomen of bearing an endite originating at its proximal rim. the tantulus. The praecoxal derivation of the endite is shown in the second type, found in BoreotanUdus (Huys & Boxshall, 1988), in which the endite-bearing Rema~s praecoxa is separate from the rest of the protopod. The third type, as found in the first leg of The new species cl~ly belongs to Micmdajus. It M. pectinatus, also has two segments but the has the tagmosis, cephalic shield ornamentation distal segment is much smaller and probably and reduced thoracopods, in the tantulus stage, represents the basis. The large proximal segment, typical of this genus and the adult male is very although lacking an endite, represents a syncoxa, similar to that of M. langi described by Boxshall derived from praecoxa and coxa. It is, therefore, & Lincoln (1987). There are now four species in suggested that the basic protopod of both larval Microdajus, M. langi, M. gae//cus Boxshail & and adult tantulocaricts comprised praecoxa, with Lincoln, M. aln~rosus Grygier & Sieg and M. or without an endite bearing coupling spines pectinatus n. sp. The latter is the only species (tantulus) or brush setae (adult male), coxa and known to possess the combs of spines on the basis. ventral surface of the second abdominal somite. The four species can he distinguished by means of the following key: Acknowledgements 1 Sixth thoracopod with two setae ...... M. aporosus We would like to thank Dr Graham Bird (Uni- - Sixth leg with one seta ...... 2 versity of Nottingham), who found the new 2 Ventral surface :of second abdominal somite of Microdajus material and advised us on the iden- tantulus with pair of prominent spine combs . tity of its host, and Lita Greve Jensen (University ...... M. pecanatus of Bergen, Museum of Zoology), for providing This somite without such combs ...... 3 information and literature. 30 G.A. Boxshall et al.

References tulocarida) parasitic on an Antarctic tanaidacean, and a range extension of M. langi Greve. Journal of Natural History 22, 1495-1505. Boxshall, G.A. & Lincoln, R.J. (1987) The life cycle of the Holdich, D.M. & Bird, G.J. (1985) A preliminary report of Tantulocarida (Crustacea). Philosophical Transactions of "dikonophoran" tanaids (Crustacea). In: Laubier, L. & the Royal Society of London, Series B, 315, 267-303. Monniot, C. (Eds), Peuplements profonds du Golfe de Gas- Greve, L. (1965) A new epicaridean from western Norway, cogne campagnes BIOGAS. Brest: Institut Fran~ais de parasitic on Tanaidacea. Sarsia, 20, 15-19. Recherche pour l'Expioration de la Mer, pp. 441-447. Greve, L. (1988) Litt om klassen Tantulocarida (Crustacea) - Huys, R. & Boxshall, G.A. (1988) A new genus and species en gruppe orsma krepsdyrparasitter. Fauna, Oslo, 41, 12- of tantulocaridan (Crustacea: Tantulocarida) parasitic on a 15. harpacticoid copepod from the Skagerrak. Sarsia, 73, Cn'ygier, M.J. & Sieg, J. (1988) Microdajus (Crustacea: Tan- 205-211.