BULLETIN OF MARINE SCIENCE
VOLUME 16 1966 NUMBER 2
LARVAL STAGES OF CARDIODECTES SP. (CALIGOIDA: LERNAEOCERIFORMES), A COPEPOD PARASITIC ON FISHESl
JU-SHEY HO Boston University, Boston, Massachusetts
ABSTRACT Five postembryonic stages of a fish copepod belonging to the genus Cardiodectes Wilson were recovered from pelagic snails, Janthina globosa Swainson, in the West Indies. They are probably identical with those found in Creseis sp., with those reported in Janthina exigua Lamarck in the Med- iterranean Sea, and with those recently collected from Janthina janthina (L.) in Madagascar. A comparison with adult metamorphosed females of Cardiodectes medusae us (Wilson) and Peroderma cylindricum Heller reveals that these larvae belong to Cardiodectes, a genus characterized by having only three pairs of functional swimming legs and two labial flaps encircling the mouth tube. The five stages of development are: free-swimming copepodid, chalimus I, chalimus II, chalimus III, and free- swimming adult form. Each stage is separated by one molt. Sexual dimor- phism is not observable until chalimus II.
INTRODUCTION The copepods of the group Lernaeoceriformes are some of the most eccentric and bizarre ectoparasites of marine fishes and cetaceans. They were discovered as early as the time of Aristotle but most species of the group are known only from females; nothing is known of the males. This is because of their peculiar mode of life history, in which, after copulation, only the female is capable of penetrating into the tissue of the final host (if the first host is not the final one) to carryon her parasitic life. The male dies without even attaching to the final host. Among the approxi- mately 20 known genera in the Lernaeoceriformes, a relatively complete life history is known in only one species of three different genera: Lernaeocera branchialis (L.) (Sproston, 1941), Sarcotretes scopeli Jungersen (Jungersen, 1911), and Pennella varians Steenstrup & Lutken (Rose & Hamon, 1953). Because of such incomplete knowledge of the life history and lack of knowledge about the male, the classification of this group of copepods has been rather confused by various investigators' different con-
'This study was submilted originally in partial fulfillment of the requirements for the degree of Master of Arts at Boston University. 160 Bulletin of Marine Science [16(2)
TABLE 1 NUMBERS OF DEVELOPMENTAL STAGES OF COPEPODS FROM PELAGIC SNAILS (Janthina sPP.) ------Locality Barbados, Barbados, 12°07' S 11°25' S W. Indies W. Indies 44°20' E 44°25' E --~ ---- - Call. date 9/8-9/11 7/24-8/1 8/10 10/31 1963 1964 1964 1964 Total No. of examined 41 46 35 3 125 snails infested 40 36 35 3 ] 15 Copepodid 230(62) 37(2) 8](4) 65(] ) 413(69) Chalimus I 889 74 101 89 ]153 Chalimus II 21 54 43 38 156 Chalimus III (1) 118 184 ]19 13 434 Chalimus III '? 218 256 268 7 749 Adult (1) 935(74) 625(48) 1409(181 ) 147(42) 3] 16(345) Adult '? 11 5 18 - 34 Pair 441 166 57 90 754 Total 3304 1577 2153 539 7573(414) ---- Note: The figures in parentheses indicate the number of copepods discovered in the washings (preservative). jectures and interpretations. For instance, the genus Lernaea lacks chalimus stages in its development but has been included in this group of copepods by many copepodologists on the basis of the superficial resemblance of the metamorphosed adult female to Lernaeoceriformes. This resemblance, however, is probably only the result of convergent evolution. In 1952, Rose & Hamon reported the discovery of a series of develop- mental stages of a lernaeoceriform copepod in Algerian pelagic snails, Creseis sp., but they were not able to identify the larvae. Furthermore, each developmental stage was unsatisfactorily described by them. Monod & Dollfus (1934) also discovered lernaeoceriform larvae in Janthina exigua Lamarck from Monaco, but, like Rose & Hamon (1952), they did not propose any known genus or species for them, and only a brief statement was made. Having the opportunity of obtaining pelagic snails, Janthina globosa Swainson, from the West Indies, the author was able to collect a large number of copepod larvae. This made possible a detailed morphological study of each stage. These stages were compared with those found in Janthina janthina (L.) from Madagascar. Extensive survey of the structure of the appendages of certain metamorphosed females of lernaeoceriform copepods has shown that these larvae, from the West Indies, Madagascar (Table 1), and the Mediterranean Sea, belong to the genus Cardiodectes Wilson. ] 966] No: Larval Cardiodectes 161 This work was made possible by a grant from the National Science Foundation (GB-1809) to Dr. Arthur G. Humes, to whom the author's sincere acknowledgment is extended for his most valuable advice and for providing the material from Madagascar. He also wishes to thank Dr. Richard U. Gooding for providing the material from the West Indies, and Dr. Ruth D. Turner, Museum of Comparative Zoology, Harvard Univer- sity, for the identification of the host snails.
MATERIALS AND METHODS The larvae were found either free inside the mantle cavity (free- swimming copepodid and free-swimming adult) or fixed to the gill lamellae (chalimus stages) of the snail. Therefore, in searching for the copepods, only the mantle was removed for examination. The free-swimming forms were frequently recovered from the washings (preservative). Before dissec- tion and study, the copepods were stained with chlorazol black E in lactic acid for three to five hours depending on the concentration of the stain. The wooden slide procedure (Humes & Gooding, 1964) was used to study the appendages of each developmental stage.
THE FREE-SWIMMING COPEPODID Figs. 1-] 2 The body (Fig. 1) is of the general free-swimming copepodid form found in the lernaeocerids, with the cephalothorax longer than the meta- some plus the urosome; its surface is covered with irregular dark blotches. (In all figures, the letter in parentheses indicates the scale at which the figures were drawn.) The length varies from 0.42-0.48 mm; the mean width is 145ft. The cephalothorax is oblong, of about equal width through- out its length, rounded anteriorly and nearly truncated posteriorly; it is covered with a weakly developed carapace which shows a clear ventral infolding along the latera] margins (Fig. 13). A scIerotized line showing the demarcation between the head and the rest of the cephalothorax is seen only on the dorsal surface. The two contiguous eyes are well devel- oped, and are in the center of the head beneath the cuticle. Each has a spherical lens embedded in the anterior corner of a densely pigmented blotch. The posterior part of the cephalothorax carries the first pair of legs. Behind the cephalothorax, there are four free segments, of which the last two are rather firmly united and appear as a unit. The first free segment carries the second pair of legs. The second segment is of characteristic trapezoidal shape and bears two stout spines on its posterolateral corners. The third free segment is the shortest one, representing the fourth thoracic segment and bearing no appendages at the present stage. The last free segment is subquadrate in shape, representing a combination of the genital and the abdominal segments and carrying two relatively wide caudal rami. 162 Bulletin of Marine Science [16(2)
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...JW « u l/) ~ 1966] Ho: Larval Cardiodectes 163 The first antenna (Fig. 2), usually bent ventrally and pointed postero~ laterally, is indistinctly 4-segmented. Each of the first three segments bears one seta on the anterior side close to the distal end, while the terminal segment is relatively heavily armed, with a stout aesthete projecting from the antero-subterminal portion, and 11 setae distributed around the terminal and the subterminal portions. Of these setae, the two terminal longer ones are bifurcate. Rose & Hamon (1952) described a 5-segmented first antenna, and the distribution of setae was: 0, 1, 1, 2, and 8 plus an aesthete. The different number of segments in the two cases is difficult to explain, since the segmentation of the first pair of antennae at this stage is so poorly developed that it is very difficult to tell the exact number of segments. However, the difference in the nature of the setae is noteworthy, no bifurcate seta being described by them (perhaps not observed?). The second antenna (Fig. 3) is stout and powerful, consisting of two very large first and second segments and a terminal dactylus which forms a subchelate apparatus with the distal end of the second segment and bears a seta on the base of its inner side. The mouth tube is located in a position nearly opposite to the eyes, with the opening facing downward and forward (Fig. 13). The buccal cone is formed by two parts (Fig. 4): a semicircular labium, with its gap facing anteriorly, and a pear-shaped labrum, which fits against this gap. Thus, they form a tubular apparatus and leave two openings on the basal part of the sutures for the insertion of the mandibles into the oral tube. In the distal wall of the labium, there are three sclerotic rings, which, together with the marginal membrane, form the so-called buccal tube. The distal two rings are of about the same width and complete posteriorly, but the proximal one is incomplete posteriorly, with the ends tapering off (Fig. 5). Distal to the rings, there is a thin, sclerotic band, which, at the present stage, appears as a ring made of numerous sclerotic rods. The marginal membrane is distal to this sclerotic band. Another circular mem- brane (Figs. 4, 5) is seen hanging over the sclerotic band and the most distal ring. The midanterior plaque (Figs. 4, 5) consists of three parts: a bluntly pointed median sclerite, and two bean-shaped lateral sc1erites, which help in reinforcing the buccal tube at the gap region. On the inner wall of the labrum, there is a pair of intrabuccal stylets (Fig. 4). Another pair of spatulate palps arises on the inner, anterolateral wall of the labium. These spatulate palps are situated at a right angle to the body axis, being truncated at their tips. Such palps were not observed by Rose & Hamon
~ FIGURES1-8. Free-swimming copepodid of Cardiodectes Wilson. 1, body (A); 2, first antenna, dorsal (B); 3, second antenna, lateral (B); 4, mouth tube, anterolateral (B); 5, same, posterior (B); 6, mandible and first maxilla (B); 7, second maxilla, lateral (B); 8, leg 1 (C). 164 Bulletin of Marine Science [16(2)
\ \ I I I I (
9 1966] Ho: Larval Cardiodectes 165 (1952), nor have they been mentioned by previous investigators in any known copepodids of the Lernaeoceriformes. The mandible (Fig. 6) is bluntly spear-shaped, without teeth. Rose & Hamon described the mandible as a sharply pointed, 3-segmented struc- ture. They called it 3-segmented by including the basal part which is closely fused with the base of the maxilla. Nevertheless, no segmentation in the mandible proper is detectable in the copepodids from the West Indies and Madagascar. The first maxilla (Fig. 6) is bipartite. The stout basipod inserts behind the base of the mandible and flanks the lateral wall of the labium. It carries a small exopod with a single slender seta and a large endopod tipped with two stout setae. The second maxilla (Fig. 7) has 3 segments. The first segment is the largest, the second segment is oblong, and the terminal one forms a claw with striations. This appendage was designated as the anterior maxilliped by Rose & Hamon (1952). They said that it carried a lateral tooth on the basal segment. I have examined in vain a good number of copepodids, trying to detect such a tooth on the second maxilla. All that I could see was merely an internal sclerite, which, at the present stage, never protrudes as a tooth. The postoral protuberance is situated far back from the mouth parts, having its tip touching the sternal plate of leg 1 (Fig. 11). There are two pairs of swimming legs (Figs. 8-10), with their arma- ture as follows: P 1 coxa a basis 1-0 exp II-I-3 end 7 P 2 coxa a basis 1-0 exp 1-I-3 end 6 A short spine is seen in the indentation of the outer surface of the exopods of both legs. Rose & Hamon (1952) illustrated two spines on the outer, distal end of the exopod of leg 2 (their Fig. Co. 3, P~) and mentioned nothing about leg 2 in the text. The existence of the outermost one of these spines is rather doubtful. The third pair of legs is represented by a pair of spines at the postero- lateral corners of the second free segment (Figs. 1, 12). A pair of setules is seen in the center of the genito-abdominal segment. The short, wide, caudal ramus (Fig. 12) bears four plumose setae and one very short setule. This setule was neither illustrated nor described by Rose & Hamon. The inner surface of the ramus bears a row of cilia.
ATTACHMENT AND MOLTING OF THE FREE-SWIMMING COPEPODID Figs. 13-14 The first stage described by Rose & Hamon (1952: 219-222) was a copepodid which had its attachment apparatus already developed and fixed to the host's tissue. Doubtless, this copepodid corresponds to the one that is shown in Figure 13, which is a free-swimming copepodid having just developed its attachment apparatus and ready to molt into a chalimus. By comparing the external morphology of the free-swimming copepodid (Fig. 1) with that of the attached copepodid (Fig. 13), one will find that they are identical except that the latter bears one more structure-the attachment apparatus. In my experience, an attached copepodid, when its attachment apparatus becomes detached during dissection, is indistinguish- able from the free-swimming copepodid. This implies that the molt takes place after the copepodid secures a firm attachment to its host's tissue. This assumption is further confirmed by my observation that many attached copepodids are in the process of molting, and halfway drawn out of their exuviae, and by the fact that a completely discarded exuvia (Fig. 14) is actually a template of the free-swimming copepodid. Fourteen such completely discarded exuviae were recovered free inside the mantle cavities of nine specimens of J. globosa from Barbados. The majority of free-swimming copepodids were recovered either from the sediment in the jars containing Janthina spp., or free inside the mantle cavities of the snails. Several were found holding the gill lamellae of the snail by means of their powerful, chelate second pair of antenna. In some copepodids, which had developed the attachment apparatus, the second antennae grasped this apparatus (Fig. 13). The attachment apparatus of the present copepodid is different from those described by many investigators for various species of Caligiformes, Lernaeoceriformes, and Achtheriformes. It consists of a conical strand protruding from the anteroventral face of the rostrum, becoming forked before embedding in the host's tissue (Fig. 15), where each branch termi- nates in a large, spherical swelling. It is regrettable that, insofar as the method of the larval attachment is concerned, no direct observations have been made on the larvae of the Lernaeoceriformes, although the develop- mental stages of one species of this group, Lernaeocera branchialis, has been extensively studied by various investigators. In regard to the construction of the attachment apparatus, it appears that the present copepodid, by pinching on the host's tissue with its second antennae, opens two small holes in it, and then lets the secretion from the frontal organ flow into the interior of the tissue through these openings. Thus, two slender, short strands are formed, each terminating in a small ball, the entire structure serving as an anchor for the later chalimus stages. The formation of such balls at the ends of an attachment apparatus is a 1966] Ho: Larval Cardiodectes 167 good example of parasitic adaptation. This sort of device is indispensable for a copepodid like the present one, which has its chalimus stages developed in an intermediate host where no hard structures are present to which the chalimus may attach. The time interval between the development of the attachment apparatus and molting into a first chalimus is unknown. By examining the discarded exuviae and larvae which were in the process of molting, however, it is possible to conjecture how the ecdysis has taken place. As shown in Figure 14, all the discarded skins have their anteroventral side widely opened. Doubtless, the first chalimus is released through this opening. It is presumed that shortly before ecdysis has taken place, the larva of the first chalimus, which is at the moment formed and shrunken inside the old skin, secretes a small amount of cement substance (from the frontal organs) to attach itself to the inner side of the base of the attachment apparatus. Thus, when the old skin is cast off, the newly molted larva can remain attached on the host by means of the old attachment apparatus. Therefore, by counting the remnants of the old skins remaining on the attachment apparatus, one is able to tell how many molts have occurred, and also the stage of the larva in question. After a new chalimus secures its attachment to the base of the attachment apparatus, in some unknown way (increasing internal pressure) it makes a suture on the old skin around the base of the attachment apparatus. By continuous jerking and twitching, the newly formed larva gradually protrudes, while the old cuticle is drawn backward and eventually slips off. As to the successive molts in the later larval stages, the process is considered to be the same as the one described above. Inside the mantle cavity of a snail from Barbados, I discovered an exuvia discarded by a male chalimus III in molting into an adult, free-swimming, male. This exuvia also exhibits a very wide opening on its anteroventral surface, the same as observed in those 14 exuviae of the free-swimming copepodids. CHALIMUS I Figs. 15-23 The first molt in the mantle cavity of the snail brings about enormous retrogressive changes in the larva. The only structures which do not show any differences from the previous stage are the eyes, which remain unchanged throughout the developmental stages. The body (Fig. 15), measuring 0.42-0.46 mm, is less symmetrically formed and a little shorter than in the copepodid. The cephalothorax is now no longer about equal in width throughout its length; the widest portion, where it measures 169ft, is located at about two-thirds from the anterior end. The sclerotized line between the head and the rest of the cephalothorax has completely disappeared. As shown in Figure 15, there is a remnant of old cuticle 168 Bulletin of Marine Science [16(2) ,~ 20 \\LJ) 17 21 \ I ....,;"~ I ~ 22 1966] Ho: Larval Cardiodectes 169 remaining attached on either side of the conical, tubular part of the attach- ment apparatus. Behind the cephalothorax there are five very indistinctly separated body segments. The second segment still bears its characteristic trapezoidal shape as in the previous stage, but, instead of carrying a single spine on its posterolateral corners, there is a large protuberance bearing two terminal setae (Fig. 23). The last free segment in the copepodid is now differentiating into two segments, the anterior one of which will become the genital segment, and the posterior one the abdomen. The first antenna (Fig. 16) appears as a large, elongate palp without segmentation. The seta on each of the first three segments in the copepodid is still seen here, but only 9 setae, instead of 1], are found on the terminal segment. In addition, the aesthete curves dorsally, and no bifurcate setae were observed. The second antenna (Fig. 17) has undergone a very striking and incom- prehensible change, by transforming into a non-chelate appendage. The two large, proximal segments are still fairly well formed, but the terminal dactylus has split into three processes. The seta on the inner side of the terminal segment is retained. The mouth tube (Figs. 18, 19) has no sc1erotized rings, marginal mem- brane, or midanterior plaque. It appears that the whole tubular part of the mouth was cast off during ecdysis and only the mouth cone was retained. However, both intrabuccal stylets and spatulate palps are still seen on the inner wall of the labrum and the labium respectively. The mandible and the first maxilla (Fig. 19) have changed slightly in their appearance, but still keep the basic features of the copepodid. Like the terminal dactylus of the second antenna, the terminal claw of the second maxilla (Fig. 20) has also split into three processes and has lost its striations. Of these three processes, the median one probably repre- sents the claw proper and each of the lateral processes represents the striated portion which flanks the claw. The protopods of both leg 1 and leg 2 (Figs. 21, 22) have lost their segmentation. They appear as a shapeless single sac. All spines and setae on the legs have also become less specialized. No differentiation between spine and seta can be made; they all appear as simple non-articulated processes. The small spines, which were seen in the indentations of the lateral sides of both exopods in the copepodid, are completely missing. However, the total number of the processes on the end and the inner side FIGURES 15-23. Cha]imus I of Cardiodectes Wilson. 15, body (A); 16, first antenna, dorsal (B); 17, second antenna, lateral (B); 18, mouth tube, mandible and first maxilla, anterolateral (B); 19, mouth tube, lateral (B); 20, second maxilla, lateral (B); 21, leg 1 (B); 22, leg 2 (B); 23, urosome, ventral (C). 170 Bulletin of Marine Science [16(2) 1966] Ho: Larval Cardiodectes 171 of each ramus is equal to that in the copepodid. The sternal plates, inter- coxal plates, and the sclerites of the postoral protuberance have all disappeared. On the caudal ramus (Fig. 23), only the four longer setae are observed, and these are not articulated. The two feeble setules on the dorsal side of the abdomen are missing. Rose & Hamon (1952) did not give a detailed description of their three chalimus stages but gave three figures (their Figs. Ch. I, Ch. II, and Ch. III). Their chalimus measured 340-525ft. The former measurement is supposedly for chalimus I, which is smaller than chalimus I of my material. CHALIMUS II Figs. 24-34 Sexual dimorphism is detectable for the first time at this stage. In general body shape, the female appears a little elongate and the male rather ellip- tical. Dimorphism is also shown in the first antennae, the anlagen of the maxillipeds, the anlagen of the rudimentary fourth legs, and the number of setae on the caudal rami. On the attachment apparatus (Figs. 24, 32), two remnants of the old cuticles are seen attached on either side. For the most part, in separating chalimus II from chalimus I, I have used the form of the third pair of thoracic legs, because their difference is recognizable even under the low power of a dissecting microscope. In chalimus I, the third thoracic leg is merely a protuberance, but in chalimus II this protuberance has differentiated into a distinct protopod and a telopod. Female.-The body (Fig. 24) measures 0.45-0.48 mm; the widest part of the cephalothorax is 172ft. The cephalothorax is not well separated from the metasome. The five free body segments are still indistinctly separated. The second segment has lost its characteristic trapezoidal shape. The succeeding segment has grown larger and carries a protuberance on each posterolateral corner. These protuberances are found only in the female, where they represent the rudimentary fourth thoracic legs. In comparison with chalimus I, the genital segment has also grown larger. The first antenna (Fig. 25) shows no segmentation, and the three setae on the anterior side of the proximal part are missing. The 11 setae on the terminal portion are more filamentous than those in the male. No aesthete or bifurcate seta is discernible. FIGURES 24-30. Chalimus II of Cardiodectes Wilson, ~. 24, body (A); 25, first antenna, posterior (B); 26, second antenna, lateral (B); 27, mouth tube, an- terolateral (B); 28, second maxilla, lateral (B); 29, leg 1 (B); 30, leg 2 (B). 172 Bulletin of Marine Science 34 \ 36 \' 1966] Ho: Larval Cardiodectes 173 A chelate appendage is reforming on the second antenna (Fig. 26). Two of the three processes have completely disappeared and are replaced by a claw, but the third one still remains separate along most of its length. The seta is located on the opposite side (which is the inner side) from this separated process. The mouth tube (Fig. 27) is not much different from that of the previous stage, and no appreciable reformation was observed. The man- dible and the first maxilla also retain the same appearance as in chalimus I. The second maxilla (Fig. 28), however, has been remodeled, the two lateral processes again assuming their striated appearance. The protopods of both leg 1 and leg 2 (Figs. 29, 30) begin to show a segmentation line proximal to the insertion of the outer process. Both exopod and endopod, however, still remain I-segmented. One more terminal process is added to each ramus of leg 1 and to the endopod of leg 2, but two more to the exopod of the latter. Leg 3 (Fig. 31) is uniramous. The single ramus bears five larger processes at the end and one smaller process on the outer subterminal portion. The protopod is unisegmented and bears no process. The caudal ramus carries four long processes as in the previous stage, but they are more rigid. Male.-The body (Fig. 32), rather stubbier than the female, measures 0.43-0.47 mm; the widest part is 226p.. The third free body segment is not as well developed as in the female, and does not carry the rudimentary third pair of legs. The caudal ramus bears five processes. The first antenna (Fig. 33) appears to be better developed than in the female, showing some traces of lines of segmentation, which indistinctly divide the antenna into four segments. The setae are shorter, but there are two more than in the female. On the ventral side of the cephalothorax, a little posterior to each second maxilla, there is a pair of protrusions (Fig. 34) which are the anlagen of the maxillipeds. These anlagen are found only in chalimus II which are destined to be males. Other features are as in the female. CHALJMUS III Figs. 35-51 The elongate appearance of the female (Fig. 35) is more accentuated than in the previous stage by increasing the relative length of the cephalo- ~ FIGURES31-37. Chalimus II and chalimus III of Cardiodectes Wilson. (Fig. 31, chalimus II c;>; Figs. 32-34, chalimus II 5; Figs. 35-37, chalimus III C;>.) 31, leg 3 (B); 32, body (A); 33, first antenna, posterior (B); 34, mouth tube, first maxillae, second ma.xi!laeand anlagen of maxillipeds (D). 35, body (A); 36, first antenna, anterior (B); 37, second antenna, lateral (B). 174 Bulletm. 0f Marine SClen. ce [16(2) 43 ~ 44 \ 1966] Ho: Larval Cardiodectes 175 thorax and the genital segment. The cephalothorax is characteristically spindle-shaped, with the widest portion about one-third from the posterior end. In the male (Fig. 45), however, the cephalothorax is rather squarish and has no alate protrusions such as seen in the female. Inside the male genital segment a pair of spermatophores is forming, and a pair of fairly well developed maxillipeds is seen, having their "elbows" protruding beyond the edges of the cephalothorax. Although the segmentation of the thoracic segments in both sexes is better defined than in chalimus II, the boundary between the genital and the abdominal segments is nevertheless not well formed. As to be expected, both sexes of the present stage carry three remnants of the old cuticles attached on both sides of the attachment tube. The mouth tube of the present stage is noteworthy not only in differ- ing from the previous stages, but also in showing sexual dimorphism. Further consideration of this will be given in the following sections where more detailed accounts of each appendage are given for both sexes. Female.-The body (Fig. 35) measures 0.47-0.54 mm; the widest part of the cephalothorax is 212JL. The first antenna (Fig. 36) still shows no trace of segmentation. However, from the mode of armature, it appears to be 4-segmented. If this is so, then the distribution of the setae would be 2, 1, 3, and 10 without discernible bifurcate setae or aesthete. The second antenna (Fig. 37) has completely regained its chelate appearance, but is not yet well sclerotized. In the wall of the labrum (Figs. 38, 39) close to the tip, the midanterior plaque, which disappeared in the previous two stages, is reformed, and shaped similarly to the one that was observed in the copepodid stage. In the wall of the labium (Figs. 38, 39), for the first time in the course of development, two contiguous flaps are produced. Although these labial flaps are here completely embedded inside the labium, the striations on them are discernible. The intrabuccal stylets, spatulate processes, mandibles, and the first maxillae are all similar to those of the previous stage. Two strong hooks are formed on the anterior side of the basal segment of the second maxilla (Fig. 40). The outer one is larger than the inner one. In other respects, the maxilla is not much different from that in the previous stage. All three pairs of thoracic legs (Figs. 41-43) are close to their adult form. The segmentation lines on the protopods and all rami are nearly complete. The adult number of spines and setae on each ramus is repre- ~ FIGURES 38-44. Chalimus III of Cardiodectes Wilson, ~. 38, mouth tube, lateral (B); 39, same, posterior (B); 40, second maxilla, lateral (B); 41, leg 1 (B); 42, leg 2 (B); 43, leg 3 (B); 44, urosome, dorsal (D). 176 Bulletin of Marine Science [16(2) 48 .--..- ~ '.-.~--..,--;-,..... ,...... •~... . -.. ,~ -' , 51 1966] Ho: Larval Cardiodectes 177 sented by processes of various lengths. The number of processes on each leg is as follows: P 1 coxa o basis 1-1 exp 1-1, 7 end 0-1, 7 P 2 coxa o basis 1-0 exp 1-1, 7 end 0-1, 7 P 3 coxa 0 basis o exp 0, 6 Leg 4 (Fig. 44) is represented by a pair of short protuberances tipped with a setiform process which is not seen in the previous stage. The setae on the caudal ramus become a little longer. Male.-The body (Fig. 45) measures 0.47-0.52 mm. In the following description, only those characters which are different from the female are given. The first antenna (Fig. 46) is indistinctly 4-segmented. The dis- tribution of elements is 2, 3, 4, and 11. The three elements on the antero- distal portion of the terminal segment are thicker; they probably represent the aesthete and the two bifurcate setae found in the adult. The wall of the labium (Figs. 47, 48), instead of containing two labial flaps as in the female, shows three sclerotic rings, reformed like those observed in the free-swimming copepodid. The sclerotic band and the marginal membrane are also formed distal to the uppermost ring. In this chalimus III, the whole newly reformed mouth tube is embedded in the wall of the labium, but, conceivably, after molting the whole mouth tube will be exposed. The second maxilla (Fig. 49) still retains the general form as in the previous stage, but no hooks are developed on the first segment. The ring of cilia, seen in the copepodid on the inner surface of the distal half of the second segment, occurs here also. The rudimentary fourth thoracic legs are not developed in the male. The caudal ramus carries five setae, which is one more than in the female. THE FREE-SWIMMING ADULT MALE Figs. 52-63 The body (Fig. 52) measures 0.58-0.64 mm, larger than reported by Rose & Hamon (1952). The cephalothorax is rather squarish and a little shorter than one-half of the body length. Its anterior end bears a large, well developed rostrum, which is located between and dorsal to the first pair of antennae. The cephalon occupies about the anterior one-third of ~ FIGURES 45-51. Chalimus III of Cardiodectes Wilson, ~. 45, body (A); 46, first antenna, anterior (B); 47, mouth tube, anterolateral (B); 48, same, posterior (B); 49, second maxilla, lateral (B); 50, maxilliped, ventral (B); 51, urosome, dorsal (D). 178 Bulletin of Marine Science [16(2) / \ \'-' 55 , ( / { I 53 >1 ., , ~.,~,\ ) \ ./ I . ~ \ I 1966] Ho: Larval Cardiodectes 179 the cephalothorax, and is separated from the remaining part of the cephalo- thorax by two scIerotized lines running obliquely on the anterior part of the carapace. Two other shorter sclerotized lines are seen in the anterior portion of the cephalon, in front of the centrally placed eyes. The posterior end of the cephalothorax is truncate, and flanked with an obtuse lobe on each side. Behind the cephalothorax there are five segments. The first three represent three thoracic segments, with each of the anterior two carrying one pair of swimming legs, and the last one being legless. As observed in the copepodid, the fourth thoracic segment is more or less firmly fused with the succeeding genital segment, in which a pair of kidney-shaped spermatophores is seen. On the ventral surface of the genital segment (Fig. 63) two oblique ridges run from the center to both posterior corners. The last free body segment is the abdomen, a single segment which is not well separated from the genital segment, and is armed with two small setules on its dorsal surface. The color of most adult males is light amber, but some of them were stained deep purple with the "ink" secreted by the host. The first antenna (Fig. 53) is 4-segmented. The setae on the first three segments are restricted to the anterior surface only, and they also tend to occur near the distal end of each segment. The distribution of setae is 7, 8, 5, and 11 (with 2 bifurcate) plus one aesthete. The pattern of armature on the last segment is identical with that of the copepodid. This has already been pointed out by Kabata (1961: 245) in Lernaeocera branchialis. Rose & Hamon (1952) did not satisfactorily describe or illustrate the first antenna. They stated that it was 5-segmented, but, according to their Figures Ml, M2, and M3, they obviously considered the attachment area of the antenna as a segment. Although they did not fully illustrate the distribution of setae, still, by comparing their Figure Ml with my Figure 53, one sees that the basic pattern of the distribution of setae is identical. Since they did not mention the number of setae, there is no way to compare the setal formula. The second antenna (Fig. 54) is a subchelate, powerful appendage. In spite of having undergone many changes during the chalimus stages, it has the same construction as that of the copepodid. The only difference observed is in the second segment, which is elliptical rather than rec- tangular. The main construction of the mouth tube (Fig. 55) is also similar + FIGURES52-57. Free-swimming adult of Cardiodectes Wilson, t. 52, body (A); 53, first antenna, ventral (B); 54, second antenna, lateral (B); 55, mouth tube, anterolateral (B); 56, mandible and first maxilla (B); 57, second maxilla, lateral (B). 180 Bulletin of Marine Science [16(2) ? 1966] Ho: Larval Cardiodectes 181 to that of the copepoclid. The only structure which is missing in the adult male is the pair of spatulate palps on the inner wall of the labium. These labial palps were already missing at the chalimus III stage. Of the three sclerotic rings, the most proximal one is still incomplete posteriorly. The rings, however, are not as slender as in the copepodid. The sclerotic band, which serves as the base of the marginal membrane, is made of many fine, sclerotic studs like those described and illustrated by Kabata (1962: 313; Figs. 1, 3) for L. branchia/is. The intrabuccal stylets are 2-segmented as in the copepodid stage. The midanterior plaque also resembles that of the copepodid, except that it appears larger in the adult male. The man- dible and the first maxilla (Fig. 56) are closely attached to each other. The former, which is lanceolate in shape and distinctly 2-segmented, enters the mouth tube through a lateral slit in the wall of the mouth cone. No teeth were observed on this appendage. The first maxilla is bipartite, with a rather swollen basipod carrying a tiny exopod bearing a weak seta, and a comparatively larger endopod with two large setae. The second maxilla (Fig. 57) is 3-segmented. The first segment is the largest and the best sc1erotized; the second segment is elongate and bears a ring of cilia on its inner distal half; and the third segment is the smallest, with striations on both sides. The maxilliped (Fig. 58) is two-segmented, very strong, and powerful. The first segment is robust, with a strong, well sc1erotized spur on the inner surface close to the base. The second segment is slender, curves slightly inward, and bears two spines, of which the distal one is about three times as long as the proximal one. The distal part of the segment tapers off gradually beyond a swelling and terminates as a large obtuse spine. The postoral protuberance (Fig. 62) has a considerably different shape from that of the copepodid, and also appears to be much less scJerotized. This structure was completely suppressed throughout the chalimus stages. There are only three pairs of swimming legs (Figs. 59-61), with their armature as follows: P 1 coxa 0 basis 1-1 exp I-I, U-5 end 0-1, 7 P 2 coxa 0 basis 1-0 exp I-I, 1-6 end 0-1, 7 P 3 coxa 0 basis 0 exp 0, 1-5 The first and the second pair of swimming legs described by Rose & ---~- +- FIGURES58-63. Free-swimming adult of Cardiodectes Wilson, ~. 58, maxilli- ped, ventral (B); 59, leg 1 (C); 60, leg 2 (C); 61, leg 3 (C); 62, postoral protuberance and coxal regions of leg 1, leg 2, and leg 3, ventral (D); 63, urosome, ventral (D). 182 Bulletin of Marine Science [16(2) 64 69 \ 65 ) 68 1966] Ho: Larval Cardiodectes 183 Hamon (1952) are different from the present ones in that the first seg- ments of both exopods lack an outer spine, the second segment of the first exopod has only one spine, and there is no seta on the posterior surface of the first basis. These three spines are not only so small, but usually so closely adhered to the exopod along their length that they are hardly to be detected. It is suspected that they were overlooked by Rose & Hamon. The caudal ramus (Fig. 63) is short and wide, and carries five plumose setae arranged in two groups. The outer group contains two short setae, and the inner group consists of one very long, one moderately long, and one short seta. The inner surface of the ramus is fringed with cilia. THE FREE-SWIMMING IMMATURE ADULT FEMALE Figs. 64-74 The adult females from Janthina, with spermatophores attached, are here considered to be immature, inasmuch as none carried egg strings. This follows the opinions expressed by Sproston (1941: 455) and Dudley (1964: 24). As illustrated in Figure 64, the adult female is much more slender and elongate than the male; it measures 0.60-0.72 mm. The cephalothorax is oblong, rounded anteriorly and truncated posteriorly; and on both sides, a little posterior to the middle, there is a slight protuberance. The rostrum is large and conical. The cephal on is fairly well demarcated from the rest of the cephalothorax. The eyes are located a little anterior to the center of the cephalon. Underneath the rostrum, the anterior end of the cephalo- thorax produces a wide plate (Fig. 70), which is rounded anteriorly with an incision at the center, and protruded posterolaterally. This plate is located between the first and the second pair of antennae and also serves as their attachment. There are five segments behind the cephalothorax. The first three represent the thoracic segments and each carries one pair of legs. The fourth segment is a long slender genital segment with striations on its surface. Ventrally, at about the middle of the length, there are two small projections (Fig. 74, showing only the one on the right side) which are not observed in the male or in any chalimus stages. On the posterior corners of the genital segment, there are depressions indicating the female genital openings. In 14 females having a pair of spermatophores attached to this area, a tiny conical projection from the spermatophore is seen ~ FIGURES64-69. Free-swimming adult of Cardiodectes Wilson, immature 9. 64, body (A); 65, first antenna, dorsal (B); 66, second antenna, lateral (B); 67, mouth tube, anterolateral (B); 68, same, posterior (B); 69, second maxilla, lateral (B). 184 Bulletin of Marine Science [16 (2) Iv 70 ,;. - " I f ~- ., '. \ \ 71 74 SCALE E 0.1 nlm f------~ 1966] Ho: Larval Cardiodectes 185 inserted into this genital opening (Fig. 74). The single-segmented abdomen is not well separated from the genital segment; it bears a pair of short and wide caudal rami, and a pair of small setules on the dorsal surface. The color of the body is either light amber or light purple with scattered irregular dark brown blotches. The first antenna (Fig. 65) is very short, about half as long as that of the male. Judging from its arma- ture, it could be 4-segmented, and the distribution of setae would be 5, 2, 4, and 9 plus an aesthete, with only one bifurcate seta on the terminal segment. Most of the setae are extremely long, even longer than twice the length of the antenna. The setae on the proximal three segments tend to occur on the anterodistal portion, as in the male. The second antenna (Fig. 66) is similar to that in the male, except that the second segment is rectangular rather than elliptical. The mouth tube (Figs. 67, 68) is mainly composed of the buccal cone. The buccal tube is represented only by two labial flaps, which made their appearance in the last stage. These two labial flaps, one on each side of the labium, bend over the opening of the mouth tube, but do not meet each other at the center. There is left between them an elongate, oval space over the mouth opening, this space being closed posteriorly but gaping in the front, where it is blocked by the midanterior plaque. The spatulate labial palps, which persisted throughout the chalimus stages, are missing. Both midanterior plaque and intrabuccal sty lets resemble those of the male. The labial flap is crescent-shaped, being a comparatively thick membrane reinforced with numerous branching, scierotized lines arising from the base. In the wall of the labium, considerably internal to the rim of the labium, there is an incomplete sclerotized ring. No sexual dimorphism is shown in the mandible or the first maxilla. The second maxilla (Fig. 69) appears quite different from that of the male. It is 3-segmented, but the first segment is enormously swollen and armed with two large, strong spines on the anterior surface, and a small spine on the posterior surface. Of these two anterior spines, the outer one is larger and appears as an outgrowth of a sclerite without articulation with the segment proper; the inner one, however, is distinctly articulated with the segment. The small spine on the posterior surface also is an extension of a sclerite. The second segment is much smaller than the first segment and does not bear a ring of cilia, but the terminal segment is much the same as in the male. ~ FIGURES 70-74. Free-swimming adult of Cardiodectes Wilson, immature ~. 70, anterior cephalosome, ventral (D); 71, leg 2 (E); 72, leg 3 (E); 73, postoral protuberance and coxal regions of leg 1, leg 2, leg 3, and rudimentary leg 4, ventral (D); 74, urosome, carrying a pair of spermatophores, lateral (D). 186 Bulletin of Marine Science [16(2) 75 / I -::"):) I J ."' / E ( E M 0 '~~:f ( .; , l:- ,'\,"-, ... ~A f- ~...• ,- •.. ' u / ! '1' Vl I " I to / I ~< ( '-- ( I J7', 'f-/ I ( \ \~ / /')~ I 1 78 ~:t I-J / (f J~v 76 / I , - " ~. ,,7 ;/ \ "L)- ~-c,"'- . ., -/"- / /1 <~- , ..••....•./' / / _/ 77 --- 1966] Ho: Larval Cardiodectes 187 The armature of the first three pairs of legs is a little different from that of the male in that the outermost seta on the terminal segment of the second (Fig. 71) and the third (Fig. 72) exopod is plumose on one side and membranous on the other side, and the outer setae on the first and the second basis are much longer than those in the male. All three pairs of legs are less sc1erotized than in the male. The fourth pair of legs (Figs. 73, 74) is considerably degenerated, represented merely by a small palp armed with a plumose seta. A palp about the size of leg 4 projects downward from the ventral surface of the fourth thoracic segment. This palp may be considered as a degenerated fourth sternal plate, which is completely missing in the male (where the fourth pair of legs has disappeared also). The caudal ramus carries only four plumose setae, and the inner surface is naked. The setae are arranged in two groups: two outer and two inner. Rose & Hamon (1952) described five setae on the caudal ramus of their female specimens, but I failed to find the fifth one in the present material. The female "larves evoluees" described by Rose & Hamon (1952) were larvae which had not yet detached from their attachment apparatus. Six such females were found in the present material. They resemble the free- swimming adult female in every way except that they still keep the attach- ment filament. Many males are also found to have the free-swimming type of body construction, but are still fixed to the host tissue by their attach- ment apparatus. All such attached adult males and females are classified as free-swimming adult males and females respectively in the present study. The first antenna of Rose & Hamon's (1952) "larves evoluees" is 5-segmented and has a smaller number of setae. The numbers of setae given by them in their three figures, F2, F3, and F4, are different from each other, and in the text (p. 224), they said: "les premiers avec une a quatre soies breves; l'avant-dernier avec une longue soie externe; Ie dernier avec six grandes soies," which is still quite different from the condition in the female studied by me. The base of the mandible, by which this ap- pendage attaches to the first maxilla to form a unit, is again treated by them as a distinct segment and they described the mandible as 3- segmented. The armature of the first and the second legs described and illustrated by them is also different from that in my females. In their Figure F3 (p. 225), the mouth tube was illustrated as having neither +- FIGURES75-78. Larvae and adults of Cardiodectes Wilson. (Figs. 75, 76, amplexus in the larvae. Figs. 77, 78, ovigerous PAIRING AND COPULATION Figs. 75, 76 The male member in amplexus is invariably a mature adult, but the female is represented by the larvae oE every developmental stage from the attached copepodid through the immature adult (Table 2). In Figure 75, which was drawn from a pair in which the female was chalimus III, the adult male holds the female dorsally by means of his second antennae and maxillipeds. The second antennae are used to grasp the female's rostrum and the maxillipeds to hook on both lateral edges of her carapace. However, it appears that the second pair of antennae are the main appendages employed in holding the female, because in most cases, only the second pair of antennae was observed to hold on the female, with the maxillipeds remaining in their resting position. In those pairs where the female is younger than chalimus III, such as chalimus n, chalimus I, and attached copepodid, the manner of pairing does not differ from that described above. It is my opinion that, by the time the female accomplishes her fourth molt and becomes an immature adult female, still remaining attached to the snail's tissue, the male changes his hold from her rostrum to her "waist" (the fourth thoracic segment) and thus is ready for copulation. Only two pairs of such examples were found, one of them being shown in Figure 76. It is fairly plausible that copulation has taken place before the female leaves the snail to search for her final host, and probably the action is done before the female detaches herself from her attachment apparatus. The exact manner of copulation is entirely unknown. However, from the manner of their amplexus, it could be that the male, keeping his hold on her fourth thoracic segment, bends his urosome downward and then forward to bring his genital openings close to those of the female, thus introducing the spermatophores into the vulva. After this, the male releases his hold on the female and retires, but the female will remain inside the snail for a while and then make her journey to the fish. Among 34 individuals of immature adult females, 14 of them carried a pair of spermatophores, and were found free in the spaces between the gill lamellae. Of the remaining 20 individuals not carrying spermatophores, 6 of them were found attached to the snail's gills with their attachment apparatus, and the remaining 14 were either clinging to the gill with their 1966J Ho: Larval Cardiodectes 189 TABLE 2 NUMBERS OF FEMALE MEMBERS IN AMPLEXUS AT DEVELOPMENTAL STAGES Stage Chalimus Chalimus Chalimus Adult Total Locality Copepodid I II III ----- Barbados, W. Indies 59 180 5 195 2 441 Barbados, W. Indies 23 47 9 87 166 12° 07' S 44° 20' E 4 15 2 36 57 11° 25' S 44° 25' E 21 38 14 17 90 Total 107 280 30 335 2 754 ------second pair of antennae or free in the spaces between the gill lamellae. From the above observations and the facts that the adult female is not yet as well sclerotized as in the male and that no adult females were discovered in washings of the snails, it seems probable that the female does not leave the snail right after accomplishing her fourth molt, or even copulation, but remains there for a while until she is better prepared to launch out for her final host. Sproston (1941: 156), in her study on the developmental stages of L. branchialis, stated that: "Copulation takes place immediately the male comes along, even though the female has barely finished molting," and on p. 457, she gave a short description of copulation, which was strictly hypothetical and is considerably different from the one given here by me. Sproston's conjecture regarding copulation is rather unacceptable, in that she was not fortunate enough to come across paired examples. Capart (1948: 173, & Fig. 14) found an adult male holding on to a fixed adult immature female in a manner like the pair shown in Figure 76. This pair he discovered in the esophagus of a specimen of Pleuronectes f1esus. No pairing was mentioned by Rose & Hamon (1952), but this could be because they observed paired examples but simply neglected their signif- icance. I myself committed the same mistake. At the beginning of the examination of the larvae in Janthina, I considered that their pairing was strictly accidental and did not pay much attention to them, until I came across an immature adult female carrying a pair of spermatophores. She was clinging to the snail's gill by means of her second pair of antennae, and beside her there lay an atrophied male. I think that it was this atrophied male who gave her the pair of spermatophores. Such atrophied males were also discovered in washings of the snails. Although these still keep their external features like those of an active male, they have lost their light amber color, dark blotches, and proper arrangement of internal organs, and thus appear semitransparent. 190 Bulletin of Marine Science [16(2) 80 / \ ,~ I " I 83 ,\ \ \ I 81 \ \ \ I 84 86 :J ;:\\~-.·l\c~ v \ \ '-0 82 \../ r, .,i r l .'.'. V" <..:. : - \ \ , / '\, I, \ 85 1966] Ho: LarvaL Cardiodectes 191 There remains at least one more question about the copulation of these larvae from Janthina, i.e., whether the male, who grasps the female at the very beginning of her attached copepodid stage, will continue to hold on to her, and is the one who finally copulates with her. If this is the case, then in order to have a male in amplexus with a female, the time required for the male development must be shorter than for the female. Since no live material was available for carrying out an experimental study, and since the snails obtained were not collected regularly at the same locality for at least one season, these questions very regrettably can not be solved at present. The holding in amplexus is not very firm. As a matter of fact, many pairs have been separated while dissecting the copepods from the snail's gill lamellae. The members of pairs which have become separated are not listed in Table 1 as "Pair" but are included in the developmental stage to which they belong. Therefore, the paired examples among the present material are more than 754, as indicated in Table 1. IDENTIFICATION OF THE LARVAE From the preceding descriptions, one can conclude without the slightest difficulty that the copepods from Janthina represent a series of the post- embryonic developmental stages of a lernaeoceriform copepod, stages similar to the copepod larvae discovered in Creseis from Algeria by Rose & Hamon (1952). To identify these larvae, the author made a detailed study of the generic diagnoses of all known genera of the Lernaeoceriformes. Only two genera, Cardiodectes Wilson and Peroderma Heller, were found to possess three pairs of well developed and functional legs, which is the most characteristic feature of the larvae from Janthina and Creseis. Consequently an extensive comparison between the appendages of the free-swimming immature adult female from Janthina and the type species of these two genera was carried out. In connection with this study, the author is deeply indebted to Mr. Gordon C. Hewitt, Department of Zoology, Victoria University, Welling- ton, New Zealand, for providing three ovigerous specimens of Cardiodectes medusaeus (Wilson), each attached to a specimen of Lampanyctus Leucopsarum (Eigenmann & Eigenmann), collected from the San Pedro Basin, off the California coast, and Mr. P. Sam Bennet, Central Marine Fisheries Research Substation, Kozikode, India, for the courtesy of placing FIGURES 79-86. Cardiodectes medusae us (Wilson), ovigerous ~. 79, second antenna (B); 80, rostrum (E); 81, mouth tube (D); 82, labial flaps (F); 83, second maxilla (F); 84, leg 1 (E); 85, leg 2 (E); 86, leg 3 (E). 192 Bulletin of Marine Science [16(2) 88 / f I \ 87 I .,;N I W ..J ~ FIGURES 87-92. Peroderrna cylindricurn Heller, free-swimming copepodid. (Figs. 89-92, ovigerous S>.) 87, body (A); 88, first antenna (B); 89, first antenna (D) (with some setae broken); 90, second antenna (H); 9], mandible and first maxilla (D); 92, second maxilla (H). 194 Bulletin of Marine Science [16(2) 95 I J ) ,[ 100 1966] Ho: Larval Cardiodectes 195 It is possible to conclude here that the larvae developing in Janthina are attributable to the genus Cardiodectes. The following evidence reveals their affinity: 1) the similarity of the setation on the first antenna is not only exhibited on the terminal segment, but is also expressed on the first three segments; 2) the well developed, large rostrum in the immature adult female from the pelagic snails is reminiscent of the prominent rostrum (Fig. 80) found in the ovigerous female in close association with the two pairs of antennae [the relative position of the rostrum and antennae in the ovigerous female has been illustrated by both Wilson (1917: pI. III, Fig. 17) and Shiino (1958: Fig. 2C)]; 3) the elements in the construction of the mouth tube are the same both in the ovigerous female and the immature adult female, the presence of two labial flaps in both of them being especially convincing, and 4) the form of the second antenna, mandible, first and second maxilla, and the first three pairs of legs of the immature adult female is in each case a template of the append- age in the metamorphosed, ovigerous female. The Ovigerous Peroderma cylindricum Heller, 1865 (Figs. 87-100).- Although many reports have been made on this species, a complete account of its appendages is nevertheless not seen in the literature. So far as I am aware, there are only two reports which have given rather adequate illus- trations and descriptions of some of the appendages, i.e., Candeias' report (1952: 6; pI. I, Figs. 3a, 3b, & 3c) on the three pairs of thoracic legs, and Nunes-Ruivo's report (1954: 6; Figs. 4b, 4c, & 4e) on the cephalic appendages. An accurate observation on the mouth tube, however, has never been made. Since my observation on the Indian specimen revealed certain fine features which have not been described or illustrated in the above mentioned two reports, and which were overlooked by Bennet (1962), all appendages are here illustrated again and accompanied with the following brief notes. The first antenna (Fig. 89) is indistinctly 4-segmented; the number of setae appears to be 4,2,2, and 8 (with one bifurcate) plus one aesthete. The second antenna (Fig. 90) is chelate, powerful, and 3-segmented. The base of the terminal segment bears a setule on the inner side. The dorsodistal corner of the second segment, which produces a catch for the chelate construction, is denticulate. The mouth tube (Figs. 93, 94) lacks sclerotic rings. The marginal membrane is upright and fringed with cilia; another circular membrane is seen hanging proximally from the distal end ~ FIGURES93-100. Peroderma cylindricum Heller, ovigerous Q. 93, mouth tube (D); 94, same, lateral (D); 95, leg 1 (A); 96, leg 2 (A); 97, leg 3 (A); 98, posterior part of body, dorsal (G); 99, same, ventral (G); 100, setae on caudal ramus (A). 196 Bulletin of Marine Science [16(2) of the labium. Both the midanterior plaque and intrabuccal stylets are as usual. The mandible (Fig. 91) is lanceolate, 2-segmented, and without teeth. The first maxilla (Fig. 91) is bipartite, with a large endopod armed with two stout setae and a very small exopod bearing a feeble setule. The second maxilla (Fig. 92) is 3-segmented. The first segment is the largest, with two blunt spines on its anterior surface; the second segment is also provided with a blunt spine on the distoventral surface, and the terminal segment is uncinate, with striations. The armature of the legs is as follows: P 1 coxa 0 basis 1-] exp 1-] , U-5 end 0-] , 7 P 2 coxa 0 basis 1-0 exp I-I, 1-1-5 end 0-1, 7 P 3 coxa 0 basis 1-0 exp 0, 1-1-4 There are denticles on the external surfaces of all rami of the three pairs of legs, and in leg 1 and leg 2 also on the internal surfaces of the basis. The posterior margins of the intercoxal plates of leg 1 and leg 2 arc fringed with a denticulate membrane. No intercoxal plate is seen in leg 3. Leg 4 is absent, and the caudal ramus (Fig. 100) is armed with four setae. It is very evident that the larvae taken from Janthina and Creseis are not assignable to Peroderma. The fine structural differences on the second antenna, mouth tube, second maxilla, and three pairs of legs are all very convincing. However, the copepodid, which was artificially hatched by Bennet from the egg-strings of a specimen of P. cylindricum from India, differs from those from the pelagic snails only in the size and the armature of the first antenna (Fig. 88). The copepodid of P. cylindricum (Fig. 87) is much larger, measuring from 0.64-0.67 mm, which is even a little larger than the adult females from the pelagic snails. The classification within the genus Cardiodectes is, as in the other genera of the 1ernaeoceriform copepods, based mainly on the nature of the frontal processes and the body shape of the ovigerous female. Thus, a further consideration of the species to which these larvae belong is impossible, since among the seven known species other than the type species, namely anchorellae Brian & Gray, bellotii (Richiardi), cristatus Shiino, frontosus Schuurmans-Stekhoven, hardenbergi Markewitsch, longi- cervicus Shiino, and rubosus Leigh-Sharpe, no detailed account of the appendages has ever been made. Moreover, until the actual metamorphosis of these larvae on the fishes is observed, a precise identification of them down to the species level is impossible. The identity of the larvae found in Creseis sp. and J. exigua from the Mediterranean Sea with the present material can not be assured without examining the specimens. However, even with the incomplete description and illustration made by Monod & Dollfus (1934) and Rose & Hamon 1966] Ho: Larval Cardiodectes 197 (1952), it is still higWy probable that the larvae from the Mediterranean Sea also belong to Cardiodectes. In 1951, Gnanamuthu reported three larvae of two chalimus stages taken along with Cardiodectes anchorellae from Stolephorus (Engraulis) indicus. He claimed that they were larvae of C. anchorellae, in spite of so many differences existing in their appendages. According to the description given by him on pp. 247-251 and Figures 8-12, it can be recognized without the slightest difficulty that his larval specimens are two character- istic chalimus stages found in the caligiform copepods (especially the caligids), and not in the Lernaeoceriformes. In his remarks on the larval stages (pp. 250-251) he stated: "The absence of other copepod parasites on the host fishes, the adult parasites bearing eggs, as well as the site of infection being the same, indicate that these are larvae of Cardiodectes anchorellae." These indications have much less significance, however, than the fundamental differences in the appendages exhibited between those chalimus stages and the adult ovigerous C. anchorellae. Their coexistence on S. indicus probably means nothing more than that they happen to have the same host preference. Furthermore, Gnanamuthu also described a pair of maxillipeds for his Indian C. anchorellae (female). This can hardly be accepted for copepods of the Lernaeoceriformes in which the maxillipeds are not developed in the female. SUMARIO ESTADOSLARVALESDE Cardiodectes SP. (Caligoida: Lernaeoceriformes), UN COPEPODOPARASITODE PECES Una serie completa de los estados del desarrollo postembrionario de un copepodo lernaeoceriforme, un ectoparasito de peces marinos, se encontr6 en un caracol pelagico, Janthina globosa Swainson, en las lndias Occidentales. Las larvas fueron encontradas bien libres en la cavidad del manto a fijas a las lamelas de las branquias del caracoI. Se identificaron cinco estados del desarrollo: copepodito libre, chalimus I, chalimus II, chalimus III y adulto libre. Cada estado separado por una muda. Aunque la copulaci6n ocurre en el ultimo estado, el amplexus se observa tan temprano como en el chalimus I cuando la larva apenas ha logrado fijarse en la lamela de la branquia del caracol y aun no ha desarrollado dimor- fismo sexual observable. Se hizo una comparacion con las larvas en Creseis sp., en Janthina exigua Lamarck en el Mar Mediterraneo y en Janthina janthina (L.) de Madagascar. En los copepodos lernaeoceriformes, se han reportado dos generos con especies que poseen solo tres pares de patas funcionales, 0, adem as, un cuarto par de patas rudimentarias. Ellos son Cardiodectes Wilson y Pero- derma Heller. El examen de la especie tipo de Cardiodectes-C. medusaeus 198 Bulletin of Marine Science [16(2) (Wilson), y Peroderma-P. cylindricum Heller revel a que los copepodos encontrados en los caracoles pelagicos son larvas de copepodos parasitos de peces pertenecientes a Cardiodectes y no a Peroderma. Es imposible un estudio mas amplio de las especies a las cuales pertenecen estas larvas, ya que la c1asificaci6n en el genero Cardiodectes se basa principalmente en la naturaleza de los procesos frontales y la forma del cuerpo de la transformada hembra ovigera. Las larvas de Cardiodectes anchorellae Brian y Gray reportadas por Gnanamuthu (1951) son de Caligiformes y no de Lernaeoceriformes. LITERATURE CITED BENNET, P. SAM 1962. Peroderma cylindricum Heller, a copepod parasite of Sardinella albella. J. Mar. bioI. Ass. India, 3: 70-74. CANOE lAS, A. 1952. On Peroderma cylindricum (Heller) on Sardina pilchardus (Walb.) from the Atlantic. Notas Est. Inst. bioI. Marit., No.4, 10 pp. CAPART, A. 1948. Le Lernaeocera branchialis (Linne 1767). La Cellule, 53 (2): 159-212. 1953. Quelques copepodes parasites de poissons marins de la region de Dakar. Bull. Inst. franc;. Afr. Noire, 15 (2): 647-671. DUDLEY, P. L. 1964. Some gastrodelphid copepods from the Pacific coast of North Amer- ica. Amer. Mus. Novit., No. 2194, 51 pp. GNANAMUTHU, C. P. 1951. Studies on a lernaeid copepod Cardiodectes anchorellae Brian and Gray. Proc. zool. Soc. London, 121 (2): 237-252. HELLER, C. 1865. Crustaceen der Novara-Expedition. Reise der osten. Fregatte Novara. Zoo!. Theil, 2 (3): 1-280. HUMES, A. G. AND R. U. GOODING 1964. A method for studying the external anatomy of copepods. Crusta- ceana,6 (3): 238-340. JUNGERSEN, H. F. E. 1911. On a new gymnoblastic hydroid (lchthyocodium sarcotretis), epizoic on a new parasitic copepod (Sarcotretes scopeli) infesting Scope/us glacialis (Rhdt.). Vidensk. Medd. dansk. naturh. Foren., 64: 1-33. KABATA, Z. 1961. Lernaeocera branchialis (L.) a parasitic copepod from the European and the American shores of the Atlantic. Crustaceana, 2 (3): 244- 249. 1962. The mouth and the mouth-parts of Lernaeocera branchialis (L.), a parasitic copepod. Crustaceana, 3 (4): 311-317. MONOD, T. AND R. PH. DOLLFUS 1934. Des copepodes parasites de mollusques. Ann. Paras it. hum. comp., 12 (1): 309-321. NUNES-RUlVO, L. 1954. Resultats des campagnes du "Prof. Lacaze-Duthiers." 1. Algerie 1952. Copepodes parasites de Poissons. Vie et Milieu, Supp!., No.3: 115-138. 1966] Ho: Larval Cardiodectes 199 ROSE, M. ANDM. HAMON 1952. Sur un copcpode parasite de certains moIlusques ptl~ropodes theco- somes. Ann. nat. Zool., 14 (11): 219-230. 1953. A propos de Pennella varians Steenstrup & Lutken, 1861 parasite des branchies de Cephalopodes. Bull. Soc. Hist. nat. Afr. Nord, 44 (5/6): 172-183. SHIINO,S. M. 1958. Copepods parasitic on Japanese fishes. 17. Lernaeidae. Rep. Fac. Fish. Pref. U. Mie, 3 (1): 75-100. SPROSTON,N. G. 1941. The developmental stages of Lernaeocera branchialis (Linn.). J. Mar. bioI. Ass. U. K., 25 (3): 441-466. WILSON,C. B. 1908. North American parasitic copepods; A list of those found upon the fishes of the Pacific coast, with description of new genera and species. Proc. U. S. nat. Mus., 35: 431-481. 1917. North American parasitic cope pods belonging to the Lernaeidae with a revision of the entire family. Proc. U. S. nat. Mus., 53: 1-150. ADDITIONAL REFERENCES The development of the Lernaeoceriformes is not well known and for those who are particularly interested in this group, the foIlowing additional references are listed: BRIAN,A. 1912. Copepodes parasite des poissons et des echinides provenant des campagnes scienti£iques de S. A. S. Ie Prince Albert Iec de Monaco. Res. Camp. Sci. Monaco, 38: 1-58. BRIAN,A. ANDP. GRAY 1928. Morphologie ext erne et interne d'un nouveau copepode parasite Cardiodectes anchoreIlae, n. sp. trouve a Madras. Boll. Mus. Zool. Anat. compo U. Genova, 8 (20/27): 1-10. HAMON, M. 1952. Un nouveau Lernaeide, parasite larvaire du poisson Serranus cabrilla L. Ann. Sci. Nat. Zool., 14 (2/3): 207-218. KABATA,Z. 1963. The free-swimming stage of Lernaeenicus (Copepoda Parasitica). Crustaceana,5 (3): 181-187. KIRTISINGHE,P. 1950. Parasitic copepods of fish from Ceylon. III. Parasit., 40 (112): 77-86. LEIGH-SHARPE,W. H. 1934. The Copepoda of the Siboga Expedition. 2, Commensal and parasitic Copepoda. Siboga-Exped., 29b, 43 pp. MARKEWITSCH,A. P. ] 936. Cardiodectes hardenbergi, ein neuer parasitischer Copepode aus der Java See. Treubia, 15 (4): 407-411. RICHIARDI,S. 1876. Intorno al Peroderma cylindricum dell' Heller, e sopra 2 nuove specie del gen. Philichthys. Atti Soc. Tosc. Sci. nat., Pisa, 2 (2): 189-201. SCHUURMANS-STEKHOVEN,H. J. 1937. Crustacea parasitic a, in Resultats Scientifiques des Croiseres du Navire-:Ecole BeIge "Mercator". Mem. Mus. roy. Hist. nat. Belgique, (2) 9: 11-24.