Chapter 9 Parasites of Commercially Important Marine Molluscs

CHAPTER 9

PARASITES OF COMMERCIALLY IMPORTANT MARINE MOLLUSCS THE CLASS CRUSTACEA I. Class Crustacea

A. Subclass Copepoda Among the copepod crustaceans, numerous species have been reported as parasites ” or as (‘commensals ” of molluscs including several from commercially important marine species. These are reviewed in this section together with a description of each species. Since most of the earlier descriptions were rather incomplete by modern standards, there are discrepancies in the descriptions given. For an account of known copepods parasitic in all categories of molluscs, see Monod and Dollfus (1932). ((

1. Mytilicola intestinalis Steuer, 1902. (Fig. 188) (Order Cyclopoida; family Clausidiidae) Steuer (1902) described a cyclopoid copepod, Mytilicola intestinalis, from the intestine of the mussel, Mytilus galloprovincialis, in the Gulf of Trieste. Later (Steuer, 1903), he published a more detailed account of this copepod including a description of its internal anatomy. This was followed by Pesta’s (1907) description of the free-swimming nauplius, metanauplius, and first copepodid stages, and Caspers’ (1939) descriptions of the second and third copepodid stages. Cytological details of the adults have been contributed by Ahrens (1937, 1939a-c). This parasitic copepod appears to be limited to European waters. It has been reported from the Adriatic Sea (Steuer, 1902, 1903 ; Pests, 1907 ; Ahrens, 1939a), the Mediterranean (Vayssikre, 1914 ; Dollfus, 1927; Cerruti, 1932; Ahrens, 1939a; Bassedas, 1950; Monod and Dollfus, 1932) where it is primarily a parasite of M . galloprovincialis although Vayssiere (1914)has found it in M . edulis. It has been reported from Germany by Caspers (1939), from the north of France by Dollfus (1914, 1927) and Monod and Dollfus (1932), from England by Ellenby (1947), Grainger (1951), Baird et al. (1951) and Cole and Savage (1951), 286

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287

and from Ireland by Grainger (1951). According to Monod and Dollfus (1932), the species described by Dollfus (1914) as Trochicola enterica from the intestine of a marine snail along the coast of France is most probably identical with M . intestinalis. Pearse and Wharton (1938) found a single specimen identified as M . intestindis in an oyster in Apalachicola Bay, Florida, but, as

FIQ. 188. Mytilicolu intestinalis male adult, ventral view. (Redrawnafter Steuer, 1902.)

Humes (1954b) has pointed out, it is most probably not M . intestinalis but M . porrecta. The known natural hosts of M . intestinalis include Mytilus galloprovincialis, M . edulis, Ostrea edulis, Cardium edule, and the gastropods Zizyphinus zizyphinus, Gibbula cineraria and G. varia. I n addition, Hepper ( 1953) has successfully experimentally infected Mytilus edulis, Ostrea edulis, Crepidula fornicata and Paphia pullastra. Description. Male (Fig. 188) about 3 mm long ; female about 8 mm long ; body long and worm-like ; thoracic segments each with a pair of dorsolateral processes, more conspicuous in females than males ;

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abdominal segmentation incomplete ;median eye present ;first antenna of four segments, first segment with fourteen bristles, second with four, third with two, and fourth with five bristles ; second antenna of three segments, hook-shaped ; mandible short, strobiliform, always with two sharp bristles ; maxilla in form of triangular plate with lateral comb of teeth and medially located feeler ; f i s t maxilliped of female reduced to small chitinous thickening, that of male hook-shaped at same position; second maxilliped of male is only noticeable as a weak chitinous thickening ; two-jointed endopodite and exopodite of first four pairs of legs with double chitinous ring ; first four pairs of legs with short setae and spines and fine hairs along exterior margin ; fifth pair of legs reduced to short bristled pegs; genital openings paired; egg sac of female long and slender.

Life cycle. Studies on aspects of the life cycle of M . intestinalis have been contributed by Pesta (1907), Caspers (1939) and Grainger (1951). The nauplii escape into the host’s alimentary canal from within egg sacs when the latter rupture at their posterior ends. These nauplii are enclosed within a membrane. It is still not known how these nauplii escape from the enclosing membrane but in sea water cultures the nauplii escape from the egg sacs leaving this membrane behind. The nauplius and metanauplius are free-swimming. Although in laboratory cultures the first, second and third copepodid stages can be found freeswimming, Grainger (1951) is of the opinion that M . intestinalis can become parasitic during the first copepodid stage. Hepper (1953), in reporting his successful experimental infections of various molluscs, did not indicate whether i t was the first, second or third copepodid that invades the molluscs ; however, since Steuer (1902) has reported that the youngest forms found in naturally infected Mytilus galbprovincialis are 0.83 mm long and with bodies similar to that of the adult, it may be assumed that these represent first stage copepodids. Thus M . intestinalis does undergo further development, through the second and third copepodid stages to the adult, within the molluscan host. It has not yet been demonstrated how first stage copepodids enter molluscs but, since they are found within the gut, it may be assumed that they are ingested. Ecology. Various investigators have reported that the nauplius of M . intestinalis is very active and is positively phototactic. The meta-

nauplius is less active and less positively phototactic. The first copepodid, like the nauplius, is an active swimmer although its tactic response to sunlight is varied. Some are positively phototactic, others are negatively phototactic, and still others do not respond to sunlight. The varied

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responses of first copepodids, which is the invasive form, to sunlight makes it doubtful if phototaxis is an important factor involved in host-searching. Grainger (1951), as the result of his maintenance studies, has reported that crowding has a serious effect on nauplii, metanauplii and first copepodids, especially among metanauplii. If ten to twenty specimens are placed in a 4-5 in. Petri dish, they are maintained quite satisfactorily ; however, if larger numbers are thus maintained, death occurs. Grainger (1951) has also studied the distribution of M . intestinalis in naturally infected Mytilus edulis. He has found that the copepods are almost exclusively limited to the recurrent portion of the intestine and in the rectum. Moreover, the largest number can be found in that portion of the recurrent intestine embedded in the digestive gland. This would suggest that perhaps some nutritional requirements are derived from the digestive gland. Grainger has also found a significant correlation between the size of the mussel host and the number of parasites. It has been shown that the larger mussels harbor the greatest number of small copepods. Relative to seasonal fluctuations in the copepod density in naturally infected M . edulis in Ireland, Grainger has reported that there is a significant decrease in the number of copepods per mussel between November to December and May to June. Furthermore, although egg-bearing females are found all year round, the lowest number of adults in mussels of the 50-69 mm group occurs during September while during November and December the number of immature stages is highest. On the other hand, the number of immature stages is lowest during May and August. I n natural populations there is always an excess of male adults throughout the year. Since M . intestinalis has been reported to be a parasite of both Mytilus edulis and Ostrea edulis among other molluscs, Hepper (1956) studied the transmission of this parasite from mussels to oysters. It is of considerable interest t o point out that although earlier (Hepper, 1953) he was able to infect 0. edulis exposed to copepodids, when 0. edulis and M . edulis are exposed to copepodids in the same aquarium the mussels are readily infected but the oysters are not. The same phenomenon has been mentioned earlier by Bolster (1954). It would thus appear that M . intestinalis demonstrates a preference for Mytilus edulis, but if this mussel is not available as a choice it will parasitize Ostrea edulis. Physiology. What is known about the physiology of M . intestinalis has stemmed from the maintenance and culture studies of Grainger A.M.R.-5

19

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(1951) and Hepper (1953), primarily the former. Grainger has shown that eggs of M . intestinalis hatched in sea water can be satisfactorily maintained in Petri dishes without aeration. When such preparations are maintained a t 13-14"C, first copepodids will develop within 40 h and will survive up to 11 days after reaching that stage. Nauplii, metanauplii and first copepodids can be maintained in sea water that has been passed through a Berkefeld filter so that all diatoms, protozoa and other microorganisms have been removed. Grainger has concluded from such observations that the development of M . intestinalis from egg through the first copepodid is independent of ambient nutrients and derives its energy from the metabolism of nutrients stored within the body. Hepper (1953) has demonstrated that eggs of this copepod will hatch and develop to what may be assumed to be the first copepodid stage maintained in sea water a t 18°C. Pathology. It is known that LW.intestinalis has an adverse effect on Nytilus edulis and may even cause mass mortalities (Cole and Savage, 1951 ;Korringa, 1951b, 1953,1954). Cole and Savage have demonstrated that among the 5.5-5.9 cm (shell length) group of mussels there is an inverse relationship between the condition of the mussels and the mean number of parasites per mussel and the mean number of parasites over 1.5 mm per mussel. The mean weight of mussels between 5 5 - 5 9 cm long is 3.206 g among parasitized ones and 5.975 g among non-parasitized ones. Personal communications with various individuals have indicated that the adverse effect of M . intestinalis on Ostrea edulis is not as severe, although casual observations indicate that the condition of parasitized oysters is also affected to some extent. According t o Chew et al. (1963), Korringa (1950a) is said t o have reported extensive mortalities in commercial mussel beds in Europe due to parasitization by this copepod. 2. Mytilicola orientalis Mori, 1935. (Figs. 189-191) (Order Cyclopoida ; family Clausidiidae)

The second species of Mytilicola, M . orientalis, was described by Mori (1935) from the digestive tract of Crassostrea gigas (Fig. 189) and Mytilus crassitesta collected from the Inland Sea of Japan. Mori, in following Steuer, believed that this species is a member of the family Dichelestiidae, a caligoid family which includes copepods parasitic in sturgeons and marine teleosts. However) I am in agreement with Grainger (1951) that the genus Mytilicola belongs in the cyclopoid family Clausidiidae.

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201

Wilson (1938), unaware of Mori’s M . orientalis, described M . ostreae from the intestine of Crassostrea gigas which had been imported to Puget Sound, Washington, from Japan. Wilson’s description is sufficiently similar to that of M . orientalis so that Odlaug (1946) has suggested that the two species are identical. After having analyzed both descriptions and compared the original illustrations, I am in agreement with Odlaug that M . ostreae is a synonym of M . orientalis. This parasite is widely spread in Puget Sound where it occurs in Mytilus edulis, Crassostrea gigas, Ostrea lurida, Venerupis ( =Paphia) staminea

FIG. 189. Cross-section of Mytilicola intestinalis in stomach o f Crassostrea giga.8 f r o m Washington. (Slide courtesy of Dr. Kenneth K . Chew, University of Washington.)

and Crepidula fornicnta. It has also been reported in Mytilus californianus collected in Humboldt Bay, California (Chew et al., 1963).

Description. Adult female (Fig. 190), 10-12 mm in total length, 1-33 in greatest width (fourth segment), with elongate narrow body, tapering posteriorly ; head separated from thorax, wider than long, with small dorsal carapace divided longitudinally through its center ;

five thoracic segments and genital segment completely fused, with a pair of posterolateral protuberances (processes) on each of the five thoracic segments, these being more prominent than those of M . intestinalis,

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MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES

fifth pair as large as third pair, each process is triangular and extends diagonally outward and backward and with an acute tip which sometimes curves slightly forward ; genital segment enlarged a t posterior corners but without processes ; abdomen considerably narrower and thinner than genital segment, tapers slightly posteriorly, as long as genital segment, undivided and with smooth lateral margins ; caudal rami cylindrical, longer than wide, slightly divergent, with no setae ; first antenna of four segments, basal segment large and swollen, all four sparsely armed with small spines; second antenna of two segments, distal segment in form of a curved claw, divided a t center and with each half armed with a spine-like seta ; upper lip subtriangular ; mandible cylindrical, unsegmented, extremely small ; first maxilla as elliptical mamma, armed with two short spine-like setae; second maxilla of stout basal portion and a two-segmented portion with terminal segment curved and fringed with hairs ; maxilliped lacking in female ; each of four pairs of uniramous swimming legs reduced to simple pointed knob; ovisacs elongate conical, 7 mm long; eggs minute, about 200 in each sac. Adult male (Fig. 191) considerably smaller than female, total length 4 mm, greatest width 0.55 mm ; with thoracic segments more or less separated by grooves ; thoracic processes more reduced than in female but more prominent than those of M . intestinalis except for first pair which is wanting in M . orieatalis ; legs larger than in female but still as uniramous pointed knobs; abdomen unsegmented ; caudal rami enlarged and nearly parallel ; mouth parts similar to those of female but with additional pair of stout maxillipeds behind second maxillae.

Life cycle. The life cycle of M . orientalis is not known although it is most probably of the same pattern as that of M . intestinalis. Ecology.* I n their paper in which was reported the occurrence of this copepod in Mytilus californianus, Chew et al. (1963) also reported that although the average number of copepods per mussel is not significantly different in Ostrea lurida (2*4),Mytilus edulis (2-3),and M . californianus (2.5), those in Ostrea lurida are larger, averaging 6-3 mm in length, than those in the two species of mussels, with those in mussels ranging from 3-0 to 4.0mm. Examination of these copepods has revealed that the smaller specimens (3.0-4.0 mm) are males while the larger ones (6.0 mm and longer) are females. Although their samples included only fifty-two 0. lurida (9.6% infected), twenty-four M . edulis (5893% infected) and twenty M . californianus (65yo infected), their finding of proportionally more males in 0. lurida may be significant.

* See note

011

p. 390.

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9. T H E CLASS CRUSTACEA

Pathology. Odlaug (1946) has demonstrated that Olympia oysters, Ostrea lurida, when infected with M . orientalis, have a lower condition index (a measurement of fatness) than uninfected ones. Similarly, Chew et al. (1964) have shown that M . orientalis reduces the condition index in Crassostrea gigas." I n the area of histopathology, Sparks (1962) has shown that metaplasia occurs in the gut of Crassostrea gigas when parasitized by this copepod (see Chapter 4, Section 11, A, 6).

2

FIGS.190-193. Mytilicola spp. (190) Adult female M . orientalis, ventral view; (191) adult male M . orientalis, ventral view (redrawn after Mori, 1935); (192) adult female M . porrecta, ventral view; (193) adult male M . porrecta ventral view (redrawn after Humes, 1954b).

3. Mytilicola porrecta Humes, 1954. (Figs. 192 and 193) (Order Cyclopoida; family Clausidiidae) The third species of Mytilicola, M . porrecta, is also known to be a parasite of commercially important molluscs. It was described by * See note on p. 390.

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MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES

Humes (195413) from the intestine of the quahaug, Mercenaria mercenaria, the recurved mussel, Brachidontes recurvus ( =Mytilus recurvus), and the ribbed mussel, Modiolus demissus granosissimus, collected near Grand Isle and Grand Terre, Barataria Bay, Louisiana.

Description. Adult female (Fig. 192) reddish to brownish orange ; egg sacs whitish to greenish blue (depending on age of embryos) ; total length of body (from anterior end to tips of rami) 4.017-5.850 mm (average 4.875 mm), width 0.343-0.414 mm (average 0.377 mm) a t anterior border of somite bearing second pair of legs; five pairs of dorsolateral thoracic projections of subequal length ; abdomen elongate and slender, terminating in two small caudal rami which extend posteriorly and bear four small spines ; no distinct cuticular division between thoracic and abdominal somites but segmentation suggested by arrangement of internal muscles ; first antenna with four segments, each of three distal ones armed with an aesthete and several setae or spines, basal segment large with scattered spines and a group of fine spinules along anterior border ; second antenna of four segments, the terminal one in the form of a chitinized hook curving slightly towards midline of body ; mandibles absent ; first maxilla as circular base from which two setae arise ; second maxilla with three podomeres, basal one elongated and largest, middle one short, distal one spatulate and fringed with row of slender setae ; maxillipeds lacking but with chitinous thickenings a t their positions ; head 0.342 mm long x 0.418 mm wide ; ratio of length to width is 0.924; all four pairs of swimming legs biramous; first leg with rami of two podomeres, expanded on their outer margins to form a wide lamella, first exopodite podomere with single seta on outer distal corner, secondexopodite podomere with three terminal setae, endopodites unarmed ; second leg similar to first but with outermost terminal exopodite reduced in size ;third and fourth legs with only two terminal setae; fifth leg absent; openings of oviducts strongly chitinized and with transverse rod across aperture ; egg sacs 1.28 mm x 0.15 mm, contain about forty-five to fifty-five eggs, extend beyond ends of caudal rami. Adult male (Fig. 193) reddish to brownish orange but paler than female ; total length 2.379-2.574 mm (average 2.472 mm), width, measured as in female, is 0.272-0.340 mm (average 0.319 mm) ; dorsolateral thoracic processes reduced to indiscernible humps ; abdomen elongate, without distinct segmentation, terminates in caudal rami as in female ; first and second antennae and first and second maxillae like those of female ; mandibles absent ; maxilliped well developed, consisting of large subtriangular basal podomere and terminal podomere

TABLEXVI. A COMPARISONOF

DIAGNOSTIC CHARACTERISTICSOF Mytilicola spp. After Humes, 1954b.

THE

~~

M . intestinalis Steuer Female Caudal ramus : Posterior corners of head :

M . porrectu Humes ?

Elongated (237p) and widely divergent Smoothly rounded

Dorsolateral thoracic projections : Short and rather stout Ratio of length of head to width : 0.647 Egg sac : Long, reaching far beyond caudal rami Male Dorsolateral thoracic projections : Well formed Claw of maxilliped :

M . orientalis Mori ( = M . ostreae Wilson)

~

Elongated, not strongly hooked

Elongated (233p) but not widely divergent With a pair of slender processes Long and tapering 0.782 Long, 2.74 mm, reaching far beyond caudal rami Well formed but absent on 1st leg-bearing somite according to Mori (1935) Elongated, not strongly bent

Short ( 9 6 p ) and not divergent Smoothly rounded Short and rather stout 0.924 Short, 1.28 mm, reaching only short distance Reduced to almost undiscernible humps Short, stout, hooked

strongly

c3

i

Q

F

kiR

8 kM +-

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in shape of recurved hook ; four swimming legs resemble those of female except for setal armature ; endopodites of legs bear long terminal setae ; second and third legs similar ; fifth leg as erect lobe with three terminal setae and one on outer margin; sixth leg as flat rounded lobe with two setae, located on posterior area of ventral surface of sixth thoracic somite. Humes’ ( 195413) table comparing the distinguishing characteristics of the three species of Mytilicola found in commercially important molluscs is reproduced in Table XVI. Life cycle. Although the various stages in the life cycle of M . porrecta have not been found, the nauplius, metanauplius, and most probably the first copepodid stages undoubtedly are free-swimming as they are in the two related species. Parasitization of the molluscs most probably occurs when first copepodids invade these hosts. Ecology. According to Humes (1954b), the pelecypods in which M . porrecta are found occur in water with a salinity of 25 %,,. Modiolus demissus granosissimus is the most frequently infected (42 yo)followed by Brachidontes recurvus (18%). Only one Mercenaria mercenaria was examined and it was infected. Humes also has noted that 400 Crassostrea virginica were examined from the area but none was parasitized. This suggested that perhaps as in the case of M . intestinalis, the invasive first copepodid stage is selective for certain pelecypods. The largest number of M . porrecta in a single Modiolus was fifteen (five males and ten females) but the average number was 2.75. Pathology. Although pathological changes in pelecypods harboring M . porrecta have not been studied, the fact that both M . intestinalis and M . orientalis are known to cause injury suggests that this species may also be injurious. 4. Panaietis haliotis Yamaguti, 1936. (Figs. 194 and 195) (Order Cyclopoida; family Clausidiidae) Panaietis haliotis was described by Yamaguti (1936) based on one male and three females found in the mouth cavity of the abalone Hccliotis (Sulculus) gigantea from “ the Pacific coast ” of Japan. Description. Adult female (Fig. 194) with elongate body, 7.4-7-6 mm long, tapering posteriorly ; head broadened posteriorly, 0.92-0.98 mm long x 1-6-1.7 mm broad a t posterior end, with nearly truncate frontal margin 0.62-0.7 mm broad ; five thoracic segments distinct, with rounded sides, gradually narrowed posteriorly, 2.8-3.0 mm long in combined length ; genital segment 0-5-0.6 mm long x 1.2-1.8 mm broad, with prominent sides ; egg strings 2-25-2.7 mm long x 0.4-0.5

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297

mm broad ; eggs large, rounded, in several longitudinal rows ; abdomen of four segments, nearly cylindrical, 2.1-2.2 mm long, first through third segments broader than long but fourth segment is longer than broad ; caudal rami 0.83-0.85 mm long, each tapering slightly toward distal end which has one subterminal and four claw-like terminal spines ; first antenna of seven segments, 1.06-0.1 mm long, 0.25 mm wide a t base, narrowed distally, with not very numerous small spiniform setae ; terminal segment with four short setiform claws at tip and four setae on posterior margin ; second antenna stout, of three segments, first segment with a seta a t distal end, second segment with a shorter pedunculate seta on inner margin, third with a group of three small spines on inner margin and four terminal claws, one of which is stout and the others are two-segmented; mandible terminating as pointed blade with about twelve sharp teeth of which the two basal ones each have an accessory tooth and a long spiniform ramus fringed with spines on inner margin and four terminal claws, one of which is stout seta, the latter with a very small spine on each side of its base, and three spines close together near inner end; second maxilla comparatively short, with four teeth on distal inner margin and two small mediodorsal spines near base ; maxilliped with rudimentary spine at its bluntly pointed end ; first four legs biramous, each with three-segmented rami ; proximal and middle podomeres of first through fourth endopodites with short spine a t outer end of each pectinate distal margin, corresponding podomeres of exopodites with three similar spines and a comb on each outer margin; each distal podomere of endopodites of first through fourth legs with eight to nine spines, of which the outer ones form three groups of two each with a comb a t each base and the inner ones are longer, pectinate, and isolated ; corresponding podomere of exopodites with eleven to twelve spines of which the outer ones form four groups of two each and a comb a t each base and the inner ones are longer, pectinate and isolated; fifth leg uniramous, digitiform, not reaching posterior end of genital segment, with one seta and one spine a t tip and two short subterminal spines, each of which is provided with a comb a t the base. Adult male (Fig. 195) 4.1 mm long, resembling female in general shape but with differing maxilliped and genital segment ; head 0.75 mm long x 1.2 mm wide; thorax 1.75 mm long, tapering gradually posteriorly, 1 . 1 mm broad a t first segment, 0-67 mm broad a t fift,hsegment ; genital segment nearly quadrangular, 0.40 mm x 0.625 mm, with a pair of ventral prominences bearing two setae on each posterior edge ; abdomen of four segments, 1.5 mm long, first through third segments broader than long, fourth segment longer than broad; caudal rami

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0.67 min x 0.15 mm ; basal and distal segments of maxilliped subequal in length with terminal claw which is slender and 0.2 mm long, armed with a small spine on inner side of base ; fifth leg reaching to posterior end of genital segment, with one seta and two spines a t tip, and one subterminal spine on outer margin.

FIGS.194-197. Clausidiid copepods from Japan. (194) Adult female Panaietis haliotis, dorsal view; (195) adult male P . haliotis, dorsal view (redrawn after Yamaguti, 1936): (196) adult female Philoconcha amygdalae, dorsal view; (197) adult male P . amygdalae, dorsal view (redrawn after Yamaguti, 1936).

5 . Philoconcha amygdalae Yamaguti, 1936. (Figs. 196 and 197)

(Order Cyclopoida; family Clauuidiidae) Philoconcha amygdalae, the genotype, was described by Yamaguti (1936) based on two mature males, one gravid female, and some immature specimens found in Tapes semidecussata from Tiba Prefecture, Japan. Their exact location within the pelecypod was not reported. Description. Adult female (Fig. 196) up to 6.6 mm long, with greenish digestive tract ; head approximately triangular, with strongly convex sides, sharply demarcated from first thoracic segment in immature specimens but more or less fused in adults and measuring 1.2 mm wide a t its somewhat prominent posterolateral corners ; frontal margin prominent, with rostrum projecting ventrad between

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299

bases of first antennae ; nauplius eye 0-2-0.27 mm from frontal margin ; cephalothorax and free thoracic segments arched dorsally and turned over ventrally, with latter segments projecting onward beyond former, measuring 0.75 mm x 1.85 mm, 0.91 mm x 2.1 mm, and 0.9 mm x 1.9 mm respectively ; fifth segment markedly narrower, 0.33 mm long x 0.7 mm wide, with a small rounded protuberance on each side in young, with uneven but nearly parallel sides in adults ; genital segment very short, 0-225 mm long x 0.6 mm broad, with somewhat convex sides ; abdomen almost cylindrical, three- or four-segmented, 1-25 mm x 0-5-0.6 m m ; caudal rami short, cigar-shaped, 0-66-0.66 mm x 0.21-0.23 mm, each with a fine seta on outer margin behind its middle and five similar terminal setae, of which three are close together in the middle ; eggs small, rounded, 0.060-0-080 mm in diameter, multiseriated ; first antenna tapering gradually towards distal end, about 0.3 mm long, of seven segments, armed with few setae, tipped with a medianlengthed and a few shorter setae; second antenna of five segments, first segment enlarged, second the longest and with a spine on inner margin, third short and with two setae a t distal end of inner margin, terminal claw about 0.1 mm long ; first maxilla with two setae ; second maxilla stout a t base, distal segment terminating in two setiform pectinate rami, with a seta on inner margin ; maxilliped swollen, with a digitiform process and two setae a t tip; first four legs biramous, each basipodite comprised of two segments, with a seta on inner margin of proximal segment, each ramus of three segments except endopodite of fourth leg which consists of two ; fifth leg uniramous, plump, slightly curved inward, tipped with a blunt spine-like inner process and a simple outer seta. Adult male (Fig. 197) with narrow body, 2.7-2.8 mm long, grayish white, semi-transparent ;head subtriangular, with convex sides, 0.61mm wide a t posterior end, wall fused with first thoracic segment, frontal margin prominent, with rostrum projecting ventrad between bases of first antennae; nauplius eye about 0.13 mm from frontal margin; cephalothorax and free segments projecting ventrally on each side but less conspicuously than in female ; first fused segment only slightly narrower than head, wider than second ; second through fourth segments diminishing in width posteriorly, measuring 0.20-0.21 mm x 0.51 mm, 0.18-0.19 mm x 0.41-0-42 mm, and 0.225 mm x 0.338 mm respectively ; fifth segment strongly constricted off from fourth, fused with genital segment; genital segment 0.34-0-4 mm x 0-4-0-21 mm, with convex sides ; abdomen nearly cylindrical, of three segments, 0.65 mm long; first segment rounded, 0.2 mm long x 0.3 mm wide, second segment rounded but shorter, third segment 0.3-0.31 mm x 0.24-

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MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES

0.25 mm, with parallel sides; caudal rami cigar-shaped, 0.45 mm x 0.12-0.13 mm, armed as in female; maxilliped of four segments, terminal claw 0.12-0.138 mm long, with slender basal spine measuring 0.010 mm long ; legs armed with spines and setae except endopodite of

fourth leg which may sometimes possess a rudimentary seta on its basal podomere. 6 . Myocheres major Williams, 1907. (Fig. 198)

(Order Cyclopoida ; family Clausidiidae) This copepod was originally described by Williams (1907) as Lichomolgus major based on male and female adults collected from the

FIG. 198. Adult female Myocheies major, dorsal view. (Redrawn after Williams, 1907.)

mantle cavity of M y a arenaria, Mercenaria mercenaria and Mactra solidissima a t Wickford and Matunuck on Narragansett Bay, Rhode Island. It was transferred to the genus Myicola by C. B. Wilson (1932) who also gave a short redescription. Later, M. S. Wilson (1950) erected Myocheres with this species as the genotype. Although Wilson placed it in the family Lichomolgidae and Pearse (1947) placed it in the family Myicolidae, in following Humes and Cressey (1958) I am assigning i t to the family Clausidiidae.

9. T H E CLASS CRUSTACEA

301

Description. Adult female (Fig. 198) with fairly transparent body of uniform grayish or pinkish color ; total length 1-1-1.3 mm ; metasome cylindrical ; head fused with first segment and about as wide as long ; second, third, and fourth segments slightly tapered, fifth segment abruptly reduced to half the width of the fourth segment, but about the same length ; urosome as long as metasome, tapered posteriorly ; caudal rami a little longer than anal segment, six times as long as wide; first antenna of six segments of which second segment is the longest ; second antenna of four segments the terminal one of which is tipped with two stout curved claws and three long, nearly straight setae ; labrum ending in an acute, backwardly directed spine ; labium with apparently movable terminal claw with hemispherical pad at base beset with recurved bristles ; second maxilla of two joints with one bristle midway on its posterior edge ; maxilliped absent ( 2 ) ; first four swimming legs with both rami of three podomeres, distal margin of basipodite of second leg and outer margins of both rami of first leg fringed with stout triangular spines ; fifth leg of two segments with the distal segment three times as long as wide and with long apical and two stout outer serrate spines and a stalked filiform seta on dorsal surface near tip. Adult male much larger than female, 1.75-1-9 mm in total length ; of same general shape as female; genital segment swollen and with fringe of spines and single seta on each lateral margin; antennae, mouth parts, and swimming legs as in female except that a pair of two-jointed maxillipeds is present ; maxilliped with second segment swollen and armed with two rows of tubercles and two setae on inner surface, sickle-shaped apical claw, enlarged a t base where thereis a small bristle, and serrated on inner margin. Other informahon. Although this copepod is undoubtedly usually found in the mantle cavity, on one occasion I found a single female in the stomach of a specimen of M y a arenaria collected in Narragansett Bay, Rhode Island. M. S. Wilson (1950) has reduced Myicola spinosa, described by Pearse (1947) from the gills and mantle of Tagelus gibbus, Dosinia discus and Mercenaria mercenaria from Beaufort, North Carolina, to synonymy with M . major. 7 . Other Clausidiids

I n addition to the clausidiids given above, Humes and Cressey (1958) have described five additional species from the mantle cavities of marine pelecypods from West Africa. Since these molluscs are presently of

302

MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES

limited commercial importance, information on their copepods wilI not be reviewed in this paper. However, since these pelecypods are of potential commercial importance, these parasites are briefly mentioned a t this point. Humes and Cressey have described Conchyliurus torosus from Mactra glabrato from Pointe-Noire, Congo ; C. lobatus from Cardita ajar dredged near Freetown, Sierra Leone ; Conchyliurus sp. from Cardium ringens dredged in the harbor of Accra, Ghana ; Myocheres scobina from Tellina nymphalis buried in the muddy sand a t Loango, 19 km north of Pointe-Noire, Congo ; and M . dentata from Macoma cumana dredged from mud in the bay of Accra, Ghana. 8 . Ostrincola gracilis Wilson, 1944. (Figs. 199 and 200) (Order Cyclopoida; family Ergasilidae)

Adults of Ostrincola gracilis were originally described by Wilson (1944) from specimens removed from the mantle cavity of Crassostrea virginica taken at Beaufort, North Carolina, and deposited in the U.S. National Museum. This species was redescribed by Humes (1953) based on specimens from the mantle cavity of C. virginica, Modiolus demissus gmnisissiwzus, Brachidontes recurvus (= Mytilus recurvus) and Mercenaria mercenaria collected fsom the Barataria Bay region of Louisiana. Description. Adult female (Fig. 199) colorless except for dark reddish-black median eye and brownish intestine : total length (from anterior end to tip of caudal ramus) averages 1-083mm, greatest width 0.274 mm ; abdomen three-segmented ; minute spines on ventral surfaces of genital segment and abdomen, dorsal surfaces without spines ; caudal ramus bears three terminal setae and three along outer edge ; first antenna of seven segments and several aesthetes, arrangement of setae on distal segment suggests a subdivision but there is no articulation ; second antenna with notch-like interruption on inner margin of claw; mouth parts greatly reduced; first, second, third, and fourth swimming legs biramous, with spine and setal formula as follows : Leg 1 exp end 1st podomere 2ndpodomere 3rdpodomere

1:0 1:l 8

0:l 0:l 6

Leg 2 exp end

Leg 3 exp end

1:0 1:l 9

1:0 1:1 8

0:l 0:2 6

0:1 0:2 6

Leg 4 exp end 1:0 1:l 8

0:l 0:2 5

9. T H E CLASS CRUSTACEA

303

fifth leg with two podomeres, basal one small, with single outer seta, distal one expanded as broad inwardly concave disk with four marginal setae ; egg sacs attached dorsoventrally, each containing about seven eggsAdult male (Fig. 200) resembles females in color; total length averaged 0-760 mm, greatest width 0.200 mm ; abdomen of four segments ; ventral surfaces of genital segment and abdomen bear minute spines ; caudal rami similar to those of female ; first antenna of seven segments, with all but basal one having an aesthete ; second antenna

FIQS.199-202. Ostrincola spp. (199) Adult female 0. gracilis, dorsal view; (200) adult male 0. gracilis, dorsal view (redrawn after Humes, 1953); (201) adult female 0. clawator, dorsal view; (202) adult male 0. clavator, dorsal view (redrawn after Humes, 1958b).

like that of female ; four pairs of swimming legs identical with those of female ; fifth leg with two podomeres, basal one with single outer seta, second podomere longer, not expanded, with more or less parallel margins, and with four marginal setae ; sixth leg consists of two setae a t posterior corner of genital segment. Other information. Humes (1953) has reported that from one to eleven copepods are found in each of the 157 parasitized Crassostrea virginica, one to seven in each of the eighty-nine parasitized Modiolus

304

M A R I N E MOLLUSCS AS HOSTS FOR SYMBIOSES

dernissus, one to two in each of the seven Brachidontes recurvus, and the single specimen of Mercenaria mercenaria examined was parasitized and it harbored two copepods. 9. Ostrincola clavator Humes, 1958. (Figs. 201 and 202) (Order Cyclopoida; family Ergasilidae) Ostrincola clavator adults were described by Humes (1958b) from the mantle cavity of the oyster, Ostrea sp., clinging to rocks off the coast of Madagascar on the island of Nossi-BB. Description. Adult female (Fig. 201) body cyclopoid, transparent, eye brown or black, total length (from anterior end to tip of caudal ramus) 1.068-1.152 mm (average 1.098 mm), greatest width 0.3000.348 mm (average 0-318 mm) ; base of first leg indistinctly separated from head by transverse suture ; several bristles dispersed on dorsal surfaces of head and thorax; posterior margins of thoracic segments rounded ; genital segment distinct, not very swollen, slightly longer than wide, approximately 0.148 mm x 0.151 m m ; ovigerous sacs attached dorsolaterally on anterior portion of segment, each with two very small spinous processes ; ventral surface of genital segment with two transverse groups of spines, two short rows on posterolateral regions and a transverse row of very smaIl spines along posterior margin; abdomen of three segments measuring 0-070, 0-050 and 0.036 mm respectively ; transverse row of very small spines along posterior borders of first and second abdominal segments and several small spines on posterolateral borders of third ; ovigerous sac not seen ; first antenna of seven segments, measuring (from base to tip) 0.024, 0.036, 0.010, 0.012, 0.023, 0.13 and 0.016 mm in length respectively; a sensory organ on each of three basal segments; second antenna of three joints, third segment elongate and slightly curved, with short seta on medial edge, recurved hook a t terminal, and shorter bifurcated process, with small lateral spine, abutting hook ; first through fourth swimming legs biramous ; formula for spines and setae is as follows :

1st podomere 2ndpodomere 3rd podomere

Leg 1 exp end

Leg 2 esp end

Leg 3 exp end

1:0 1:l 8

1:0 1:l 9

1:0 1:l 8

0:l 0:1 6

0:l 0:2 6

0:1 0:2 6

Leg 4 exp end 1:0

1:l

0:l 0:2

8

5

first leg with medial spine on basipodite, with three spines on lateral surface of basal podomere of exopodite, exopodite also with a semigladiate terminal spine and four plumose medial bristles ; second leg

305

9. THE CLASS CRUSTACEA

without medial spines on basipodite, with three lateral spines on basal podomere of exopodite, one terminal spine, and five medial setae, also with three lateral spines and three medial setae on basal podomere of endopodite ; third leg similar to second leg but with only two lateral spines on basal podomere of exopodite and a seta on basal podomere of endopodite which transforms into a plumose seta along its basal portion but becomes blade-like distally ; fourth leg with three lateral spines and four medial setae on basal podomere of exopodite, with four spines and one medial plumose seta on basal podomere of endopodite ; fifth leg with distal podomere flattened, 0.072 mm x 0.036 mm, with a seta (0.023 mm long) on its medial border, three setae (0.018, 0-018 and 0.020 mm long) at its tip, and with small spines scattered along it ; sixth leg absent ; caudal ramus elongate, 0.093 mm x 0.017 mm, with flattened dorsal seta and remaining setae relatively strong and claviform including one slightly dorsal to midline of ramus, three long setae a t tip (longest measuring 0-024 mm), and three short setae near base. Adult male (Fig. 202) with body shape and color similar to female ; total length 0.612-0-696 mm (average 0.645 mm), greatest width 0.1680-192 mm (average 0.183 mm); base of first leg distinctly separated from head; genital segment almost as long as wide, 0.18 mm x 0.112 mm, with posteroventral suture ; ventral surface with a transverse band of spines near midlength and with row of small spines at each posterolateral margin ; two spermatophores visible, each approximately 0.090 mm x 0-042 mm; abdomen of four segments measuring (from base to tip) 0.036, 0.031, 0,024 and 0.018 mm respectively; with transverse rows of small spines along posteroventral margin of segments except the posteriormost segment which has a group of small spines near the base of each caudal ramus ; first antenna of seven segments measuring (from base to tip) 0.018, 0.024, 0.007, 0.011, 0.017, 0.011 and 0.017 mrn respectively; large sensory organ on third and fourth segment; small sensory organ on fifth and two on basal segment; second antenna like that of female ; first through fourth legs like those of female ; fifth leg with flattened distal podomere, 0.042 mm x 0.014 mm, with four setae measuring (from base to tip) 0.016, 0.016, 0.014 and 0.022 mm ; sixth leg composed of two setae, 0.018 mm and 0.017 mm long ; caudal ramus like that of female. 10. Ostrincola simplex Humes, 1958. (Figs. 203 and 204)

(Order Cyclopoida; family Ergasilidae) Ostrincola simplex adults were described by Humes (1958b)from the mantle cavity of oysters, Ostrea sp., off the coast of Madagascar on the island of Nossi-BB. A.M.D.-5

20

306

MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES

Description. Adult female (Fig. 203) total length (from anterior terminal to tip of caudal ramus) 0.696-0.852 mm (average 0.766 mm), greatest width 0.216-0.264 mm (average 0.230 mm) ; genital segment a little wider than long, 0.108 mm x 0-128 mm, with smooth dorsal surface but with several lateral spines ; ventral surface with two transverse rows of spines across anterior half of segment and with a row of small spines along its posterior border; abdomen of three segments, 0.045, 0.057 and 0.024 mm long, without spines dorsally but with a row of small spines ventrally along posterior border of first segment; first antenna with seven segments, measuring (from base to tip) 0.024, 0.029, 0.013, 0.010, 0.022, 0.011 and 0.019 mm respectively; a sensory organ on each of three basal segments ;second antenna of three segments, third segment long and slender, with a sensory organ and a row of indistinct bristles along interior border, a row of small spines along basal portion of exterior border, and three thin setae and large recurved claw a t its apex ; segments of first through fourth swimming legs like those of 0. cluvutor ; spines and setae of exopodites like those of 0. clavator ; terminal spine on endopodite of first leg semi-gladiate, with a row of bristles along interior margin; terminal podomere of endopodite of second leg with a short gladiate spine on external surface, a long semi-gladiate spine with bristles along internal border, and four plumose setae exteriorly ; terminal podomere of endopodite of third leg with three spines and three setae ; terminal podomere of fourth leg with three external spines, a gladiate seta on its distal half, and a plumose seta on its medial surface ; terminal spines on podomeres very long and large, that on terminal podomere of exopodite of fourth leg, for example, measures 0.056 mm long; second podomere of fifth leg flattened, 0.098 mm x 0.078 mm, with single spine, 0.022 mm long, on distal border of external edge and three spines on medial edge measuring 0.011, 0.024 and 0-014 mm respectively; edge of middle podomere without spines but with small sclerified denticles along medial surface ; groups of long spines on both edges of basal podomere ;sixth leg absent; caudal ramus, 0.096 mm x 0.017 mm basally, 0.096 mm x 0.006 mm distally, with dorsal seta 0.012 mm long and lateral seta about 0.030 mm long, lateral subterminal seta 0.005 mm long, three terminal setae 0.006, 0.013 and 0.010 mm long ; egg sacs slightly orange, 0.132 mm x 0.070 mm, containing about fifty-five eggs. Adult male (Fig. 204) with body outline like that of female ; total length 0.540-0.648 mm (average 0.602 mm), greatest width 0.1440.192 mm (average 0.160 mm); first podomere of first leg distinctly separated from head ; genital segment somewhat rounded, 0.092 mm x 0.093 mm, posteroventrally divided, with group of small spines at

9. THE CLASS CRUSTACEA

307

border of division and another group of small spines tranversely arranged in posterior half of segment; abdomen of four segments measuring 0.030, 0.034, 0.036 and 0.016 mm respectively ; posterior borders of first and second abdominal segments each with a group of small spines; dorsal surface of genital segment without spines; two spermatophores present ; first antenna with seven segments measuring (from base to tip) 0.033, 0.042, 0.015, 0.022, 0-041, 0.026 and 0.030 mm long respectively ; two large sensory organs on fourth segment and one little one on each of three basal segments ; second antenna as in female ; first through fourth legs liks those of female but medial seta of coxo-

FIGS. 203-206. Ost?%COh and Myicola. (203) Adult female 0. simplex, dorsal view;

(204) adult male 0. simplex, dorsal view (redrawn after Humes, 1968b); (206) adult female M . rnetisiensis, dorsal view; (206) adult male M . metisienais. dorsal view (redrawn after Wright, 1886).

podite of fourth leg much longer than that of female ; distal podomere of fifth leg much finer than that of female measuring 0.042 mm x 0.012 mm, seta on its external border 0.025 mm long while the terminal setae measure 0.019, 0.016 and 0.032 mm long respectively; sixth leg includes two setae, 0.015 and 0.013 mm long; caudal rami like those of female. Other information. Humes (1958b) has noted that these copepods will live in a glass container in the laboratory and will swim capriciously when disturbed.

308

MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES

11. Myicola metisiensis Wright, 1885. (Figs. 205 and 206)

(Order Cyclopoida; family Myicolidae) Myicola metisiensis, the genotype, was originally found and described by Wright (1885) between the gill lamellae of M y a arenaria collected a t the village of Little Metis, Quebec, on the Gulf of St. Lawrence. It was redescribed by Wilson (1932) from the mantle cavity of the same host collected a t Wellfleet, Massachusetts, and placed in the family Lichomolgidae. Wright had placed this species in the no longer recognized family Corycaeidae. However, in following Pearse (1947), I am placing it in the cyclopoid family Myicolidae. Description. Adult female (Fig. 205) averaging 3 mm long, first four thoracic segments subequal, broader than long ; fifth segment smaller than first abdominal segment ; double genital segments nearly as long as remaining three abdominal segments; furcal segments as long as last two abdominal segments, with six setae of which three are apical and one subapical ; rostrum shield-shaped ; anterior antennae as long as head, with first, second, and fifth segments being the longest ; second antennae directed downwards, shorter than first pair ; labrum with lateral borders denticulated and posterior border emarginated ; mandible with two setose lobes and two setose filaments; maxillae with three setae of which the middle is the longest; two basal joints of first maxillipeds tumid, with two converging oblique patches of spines, distal joint of first maxilliped with strong seta and terminating in two curved setose filaments of which the more slender is attached like a palp ; first through fourth legs biramous ; basipodite of first leg with a row of strong spines on ventral surface which decrease in rigidity on the second and third legs and are absent from the fourth ; fifth leg uniramous, of three podomeres, two basal ones each with a seta while the distal podomere has two apical setae and a group of subequal spines ; egg sacs cylindrical, 1.0 mm x 0.5 mm. Adult male (Fig. 206) very similar to female, smaller, measuring 1-75 mm or less in length ; thoracic segments gradually decreasing in breadth anteroposteriorly ; posterior borders of genital and two subsequent abdominal segments denticulated ; second maxilliped with basal joint denticulated ; spermatophores subpyriform, 0.2 mm x 0.1 mm. Life cycle. The stages in the life cycle of this species are not known. Relative to the mode of infection of the soft clam, Wright (1885) has stated : I have found some in the suprabranchial chambers, which would seem to indicate entry through the cloaca1 siphon, while I have found others, head

9. THE CLASS CRUSTACEA

309

upward, in the gill-tubes, which would appear to argue an entry while still in the nauplius-stage, through the inhalant siphon and the water-pores of the gill-plates. Ecology. According t o Wright, female copepods found in clams during June carry egg sacs enclosing eggs a t various stages of development, but by August they have lost their egg sacs. Males have been reported to be much faster swimmers than females when teased out of their hosts. Pathology. The only information available on the effects of M . metisiensis on its host is that reported by Wright who has stated : No considerable irritation appears to be set up by the presence ofthe parasite in the gill-tubes. The claws of the posterior antennae and the setae of the various appendages are often invested by a yellowish film undoubtedly derived from the blood of the host, but no greater exudation resulting in the formation of a cyst round the foreign body is to be observed. . . . The granular contents of the intestine of the copepod have a bluish-green tint, which is most readily noticed in the wider rectum, but I must leave undecided whether these are derived from the blood of the host. 12. Pseudomyicola ostreae Yamaguti, 1936. (Pig. 207) RADGL~FF~ (Order Cyclopoida; family Pseudomyicolidae) Pseudomyicola ostreae, the genotype, was described by Yamaguti (1936) based on two female specimens recovered from the branchial cavity of Ostrea denselamellosa cultured a t the Hutami oyster bed in Hy6go Prefecture, Japan. I n following Humes and Cressey (1958), I am assigning it t o the family Pseudomyicolidae.

Description. Female (Fig. 207) 2.1-2-43 mm long, uniformly grayish in alcohol-preserved specimens ; head 0.45-0.51 mm x 0.525-0.625 mm, abruptly narrowed anteriorly, with setae on each side as in first thoracic segment ; head indistinctly demarcated from thorax ; thorax 0.9-1.25 mm long, with first four segments almost uniformly broad, 0.67 mm in maximum breadth; fifth thoracic segment about half as long as and much narrower than fourth but slightly broader than genital segment ; genital segment 0.225-0.260 mm x 0.28 mm, with two transverse rows of spines and scattered setae on ventral surface ; egg strings not seen; abdomen of three segments, first segment 0.12-0.13 mm x 0.20.21 mm, with about ten setae on ventral side near posterior margin, second segment 0.10-0.11 mm x 0-175 mm, third segment 0.0880.1 mm x 0.14-0.15 mm, with numerous small spines on ventral and outer sides near posterior end; caudal rami narrow, 0.16-0.18 mm x 0.035-0.04 mm, each with two spines on outer margin, three a t tip and

310

MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES

numerous smaller ones on ventral side ; first antenna of six segments, about 0.3 mm long, basal half enlarged, basal segment with slender, slightly curved spines, measuring 0.051 mm long, a t anteromedial corner and four setae a t distal anteroventral part, second segment incompletely segmented from third, approximately triangular in ventral aspect, with about twelve simple setae, third segment with nine setae one of which is on dorsal surface, fourth segment with four setae, fifth with three setae, sixth with one subterminal and six terminal

FIGS.207-209. Pseudomyicola spp. (207) Adult female P. ostreae, dorsal view (redrawn after Yamrtguti, 1936); (208) abdomen of adult female P. glabra, dorsal view; (209) abdomen of adult male P . glabra, dorsal view (redrawn after Pearse, 1947).

setae, with one much longer than others; second antenna of three segments with basal segment stout, middle segment about 0.225 mm long, arcuate, with one basal and three terminal setae, and covered with numerous minute spines ; terminal claw comparatively short with a false joint near middle; mandible terminating in two pectinate blades ; first maxilla with four setae of which the outermost is long and the two inner are difficult to see; basal segment of second maxilla armed with numerous spines along posteroventral margin of its larger proximal portion, terminal blade fringed with eight spines on inner

9. THE CLASS CRUSTACEA

311

side ; maxilliped knoblike, behind base of second maxilla ; first four legs biramous, each ramus of three segments which are fringed with spines on outer margin; each basipodite of two indistinct segments and with a seta and a row of two to five minute spines on outer side and a seta on inner side, spines also occur along posteroventral margin between bases of both rami ; basipodite of first leg with a stout pectinate spine and a group of smaller simple spines at its posteromedial corner ; fifth leg uniramous, of two podomeres, basal podomere with one seta at dorsal distal terminal, terminal podomere about twice as long as broad, with marginal setae a t distal portion, a row of four to ten setae on inner margin, and a few oblique rows of spines on ventral surface. Male unknown. 13. Pseudomyicola gbbra Pearse, 1947. (Figs. 208 and 209)

(Order Cyclopoida; family Pseudomyicolidae) This species was described by Pearse (1947) based on male and female specimens removed from the gills and mantle cavities of Modiolus demissus, Crassostrea virginica, Atrina rigida, Aequipecten irradians, Noetia ponderosa and Mytilus edulis collected at Beaufort, North Carolina. I n following Humes and Cressey (1958), it is being assigned to the family Pseudomyicolidae. Description. Adult female (Pig. 208) 2.23 mm in total length, 0.53 mm wide; head separate from first thoracic segment; second through fifth thoracic segments become narrower posteriorly, urosome half as long as metasome ; caudal rami more than twice as long as anal segment, slender, tapering, with two short terminal setae and two on the lateral and dorsal surfaces ; genital segment with five little ridges on sides near posterior margin ; anal segment with minute spinules around posterior margin ; first antenna with sharp strong spine projecting posteriorly from basal segment, entire ant,enna of six segments, the basal being the longest and the basal three being wider than distal three ; second antenna with basal segment widest, second segment shortest, and third segment longest, narrowest, and recurved, strong terminal claw present; swimming legs all biramous with each ramus being three-segmented ; fifth leg of two podomeres, broad, flat, and thickened along one margin, with four distal setae, two rows of seven and eight denticles along middle of thin margin, and eleven spines across anterior surface ; egg strings, each measuring 0.33-0.55 mm long, contain five to twelve eggs arranged in linear groups. Adult male (Fig. 209) similar to female but smaller; total length 1-78 mm, width 0.47 mm; fifth legs relatively smaller, about half as long as those of female, of two podomeres and with five denticles on

312

MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES

medial distal angle of terminal segment ; lobes of genital segment with a small seta on posterior margin ; denticles in posterior margin of anal segment longer than those on female. 14. Other Pseudomyicoliids I n addition to the pseudomyicolids given above, Humes (1958b) described Pseudomyicola mirabilis from the mantle cavity of Arca decussata collected a t Nossi-Bk, Madagascar. Later, Humes and Cressey (1958) reported finding the same copepod in A . senilis collected at Somone, Senegal, in Ostrea tulipa from the same locality, and in Pitar tumens a t Haan, Senegal. Since these pelecypod hosts are of limited commercial importance, P. mirabilis is being briefly recorded herein. 15. Tisbe celata Humes, 1954. (Figs. 210 and 211) (Order Harpacticoida; family Tisbidae) The genus Tisbe includes twenty-seven recognized species and several doubtful ones. Among these, only two, T . wilsoni and T . celata, have been found as symbionts, possibly parasites, while two others, T . elongata and T . furcata, which are usually free-living, have been found in association with other invertebrates. Specifically, T . wilsoni was described by Seiwell (1928) as a " commensal " from Amaroucium a t Woods Hole, Massachusetts, and T . celata, the species under consideration, was described by Humes (1954a) from the mantle cavity of Mytilus edulis collected a t St. Andrews, New Brunswick, Canada. T . elongata was recorded by Gurney (1933) and Leigh-Sharpe (1935) on the gills of Homarus vulgaris, and T . furcata was found by Aurivillius (1885, 1887) in the tunicate Molgula ampulloides. Relative to T . celata, Humes (1954a) is of the opinion that it is a parasite of Mytilus edulis. Description. Adult female (Fig. 210) colorless except for bright red eye and pale orange egg sac ; total length (from tip of rostrum to tip of caudal rami) 0.929-0.979 mm (average 0.961 mm); greatest width, a t level of first thoracic segment, 0.415 mm ; genital segment, 0.641 mm long, distinctly divided dorsally and laterally by transverse furrow; first four thoracic segments and genital segment each with minute slender seta, 0.010 mm long, located near posterolateral margin in addition to a pair of similar setae in front of transverse furrow; abdomen of three segments ; anal operculum as a smooth flap ; rostrum, 0.028 mm long, broadly rounded, with two minute setae; second thoracic segment 0.115 mm long; third thoracic segment 0-103 mm

9. THE CLASS CRUSTACEA

313

long, fourth thoracic segment 0.080 mm long, fifth thoracic segment 0.064 mm long, sixth thoracic segment 0.136 mm long; genital and abdominal segments each armed with a row of minute spines along posteroventral margin but unarmed dorsally ; caudal ramus, 0.029 mm x 0.025 mm, slightly wider than long, with longest terminal seta, which may be partially retracted, measuring 0.336 mm ; two additional setae present on ramus; egg sac dorsoventrally flattened, 0.290 mm long x 0.270 mm wide x 0-120 mm thick, reaching bases of caudal

FIGS.210 and 211. Tisbe celutu adults. (210) Female, dorsal view; (211) thorax and abdomen of male, dorsal view. (Redrawn after Humes, 1954a.)

rami, contains about forty-five eggs, each about 0-054 mm in diameter ; first antenna of eight segments measuring 0.038, 0.060, 0.044, 0.027, 0.015, 0.014, 0.010 and 0.028 mm long respectively; fourth segment with aesthetask, 0.125 mm long, extending well beyond tip of antenna; second antenna with four segments of endopodite somewhat indistinctly separated ; first swimming leg with exopodite shorter than endopodite, bent at an angle so as to cross behind endopodite, endopodite podomeres measure 0.082, 0.081 and 0.007 mm respectively, exopodite podomeres measure 0.045, 0.045 and 0.020 mm respectively ; second,

314

MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES

third and fourth pairs of legs similar except for certain differences in armature, stronger inner basipodite spine absent and outer basipodite spine slender in all three legs ; leg spine and setal formula as follows :

1st podomere 2ndpodomere 3rd podomere

Lag 1 exp and

Leg 2 exp and

Leg 3 exp end

1:0 1:l 6

1:l 1:l 7

1:l 1:l 8

0:l 0:l 2

0:l 0:2 5

0:l 0:2 6

Lag 4 exp end 1:l 1:l

0:l 0:2

8

5

fifth leg with three slender setae on inner expansion of basal podomere, middle seta 0.115 mm long, two shorter setae subequal, about 0.048 mm long; single seta, 0.044 mm, a t outer corner of podomere; distal podomere 3.1 times longer than wide, averaging 0.097 mm x 0.031 mm, with four terminal setae, three subequal in length (0.046-0*051 mm), fourth member of quartette, next to innermost, longer (0.067 mm), fifth seta, 0.073 mm long, on outer edge of podomere at junction of distal two quarters, with small spines along both edges of podomere ; sixth pair of legs visible on anteroventral part of genital segment, represented by three setae on either side of oviducal opening. Adult male (Fig. 211) resembles female in color and body form; total length 0.705-0-800 mm (average 0-781 mm), greatest body width 0.328 mm, a t level of first thoracic segment ; abdomen of four segments ; rostrum 0.025 mm long ; head plus somite of first leg 0-223 mm long, second, third, fourth, fifth and sixth legs measure 0.070, 0.083, 0.064 0.057 and 0.061 mm long respectively ;caudal ramus, 0-020mmlong, like that of female ;first antenna subprehensile, with nine segments measuring 0.030, 0.048, 0.023, 0.006, 0.029, 0.009, 0.021, 0.022 and 0.032 mm respectively, aesthetask on fifth segment measures 0.109 mm long ; second antenna similar to that of female ; second through fourth legs like those of female ; distal podomere of fifth leg, 0.042 mm x 0.018 mm, shorter than that of female, with few minute spines on slightly convex broad outer surface, with middle spine, 0.043 mm long, broad and with fine hair-like tip; inner expansion of proximal podomere less pronounced than in female, with two setae, one long (0.057mm) and one short (0.017 mm); sixth leg as broad lobe bearing spinose, distally naked setae, a row of small spines near bases of two inner setae ; spermatophore, 0.070 mm x 0.030 mm with slender neck.

9. THE CLASS CRUSTACEA

315

Other information. Humes (1954a) has stated that : T . celata would seem t o be a parasite of Mytilus edulis rather than a freeswimming species accidentally introduced into the mantle cavity, since it occurs only in the mussel and then in relatively large numbers, and since the presence of immature stages indicates it probably breeds in the mussel. 16. Lichomolgid Copepods Humes and Cressey (1958) described three species of the family

Lichomolgidae from the mantle cavities of pelecypods of limited commercial importance in West Africa. These are briefly mentioned a t this point. They described Anthessius sp. from Pinna rudis taken a t a depth of 1 m at Pointe-Noire, Congo; Modiolicola injlatipes from Mytilus perna attached to rocks a t Pointe-Noire ; and Lichomolgus arcanus from Ostrea tulipa collected at Joal, Senegal, and from Pitar tumens collected at Hann, Senegal.

B. Subclass Malacostraca Among the malacostracans, a number of decapods are known to live symbiotically with commercially important marine molluscs, a t least during one phase of their life cycles. Specifically, certain species of crabs of the family Pinnotheridae are known t o live within the mantle cavities of oysters and other pelecypods. Although the relationships between these crabs and their hosts are not clearly understood, a t least certain species are believed to be parasitic (see Chapter 4, Section 11, A, 6). Since the nature of the relationship between pinnotherid crabs and their hosts is a t best uncertain, the following information is limited primarily to the more common species, especially those which have been incriminated as being true parasites. For detailed information on the entire family, the monographs of Rathbun (1918) and Sakai (1965) should be consulted. 1. Pinnotheres ostreum Say, 1817. (Figs. 212-215)

(Order Decapoda; suborder Reptantia; section Brachyura; superfamily Brachyrhyncha; family Pinnotheridae) The adults and post-planktonic stages of Pinnotheres ostreum, the oyster crab, are found primarily in the mantle cavity of the American oyster, Crassostrea virginica, but they can also occur in Aequipecten and Anomia simplex (Christensen and McDermott, 1958) and in Mytilus edulis (McDermott, 1961). They need not always be associated with pelecypods since Gray (1960, 1961) has reported finding them occasionally in Chaetopterus tubes. P. ostreum is a New World species with its known range extending from Massachusetts to Santa Catarina, Brazil

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MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES

(Williams, 1965). According to Williams, its synonyms include P. depresseum Say, 1817 and P. depressus Rathbun, 1918. The combined contributions of Birge (1882), Hyman (1924), Stauber (1945), Sandoz and Hopkins (1947) and Christensen and McDermott (1958) have made this the best understood of all the species of Pinnotheres. Due t o space limitations, it is not possible to give an exhaustive treatment of all that is known about P. ostreum. Interested readers are referred t,o the original papers cited for details.

Description of stuges in mollusc. The excellent comparative chart given by Christensen and McDermott (1958))in which the distinguishing characteristics of the stages which may be encountered in molluscs are listed, is reproduced in Table XVII. In addition, the descriptions of the mature female and so-called hard-shell male are given below. Mature female (Fig. 212) whitish or salmon pink, with carapace subcircular, 4-15 mm wide, surface mostly glabrous, smooth, shiny, membranous, yielding to touch, convex from front to back and with a broad, shallow, longitudinal depression at each side of cardiac and gastric areas ; lateral margins thick and bluntly rounded ; posterior margin broad ; front rounded, slightly produced, covering and concealing eyes ; orbits small, subcircular, anteriorly placed ; antennule large ; antenna small, flagellum not as long as diameter of orbit ; buccal mass roughly quadrangular but bent into broad crescentic arch, short anteroposteriorly ; outer maxilliped with ischium and merus fused ; TABLEXVII. POST-PLANKTONIC DEVELOPMENTAL STAGES OF Pinnotheres ostreum Data based on observations by Stauber (1945) and Christensen and McDermott (1958). (After Christensen and McDermott, 1958.)

Stage of development

Range in carapace Most important external width morphological characteristics (mm)

Invasive stage 0-69-0.73 Flattened carapace and (First crab stage) pereiopods. Posterior margins of pereiopods thickened, 3rd and 4th pairs have plumose swimming hairs. Two small, white spots on carapace and on sternum. Carapace hard around these spots

Biological factors

Free-swimming until invasion of host. After invasion it is found in all parts of waterconducting system of the host

317

9. THE CLASS CRUSTACEA

TABLEXVI1.-continued

Stage of development

Range in carapace Most important external width morphological characteristics (mm)

Pre-hard stages

Male 0*75*-2.7* Female 0.75*-2*7*

Hard stage (stage I of Stauber, 1945)

Male 1.4-4.6 Female 1.3-2.7

Stage I 1

1.3*-3.1

Stage I11

2.6-4.4

Stage I V

3.6-84

Stage V (Mature female)

4.4-15.1

* Approximate measurements.

Rounded carapace. Thin, flexible exoskeleton. Slender pereiopods. No swimming hairs. Large females practically indistinguishable from 2nd stage crabs Carapace flattened and very hard. Flattened pereiopods with posterior margins thickened and with plumose swimming hairs on 3rd and 4th pair. Two large, white spots on carapace and on sternum. Males larger on the average than females Rounded carapace. Thin flexible exoskeleton. Slender pereoipods. No swimming hairs. Abdomen wholly contained in sternal grove. No hairs on pleopods Edges of abdomen extend beyond depression in sternum. First two pairs of pleopods clearly segmented and supplied with a few hairs Relative width of abdomen larger than in preceding stage, just reaching coxae of pereiopods in most cases. Pleopods almost fully developed and well supplied with hairs Abdominal edges covers coxae of pereiopods. Pleopods fully developed. The orange gonads may be seen through the thin carapace

Biological factors

Found in all parts of the water-conducting system of the host

Found free-swimming and in all parts of water-conducting system of the host. Copulatory stage. Males die in this stage

Never free-swimming. Predominantly, possibly always, found only on the gills of the host Only found on the gills of the host

As in 3rd stage

As in 3rd stage

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MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES

carpus (first article) of palp short and oblong ; propodus elongate with rounded terminal ; dactyl inserted behind middle of propodus, minute and slender ; chelipeds small ; merus and carpus slender ; palm some-

FIQS.212 and 213. Pinnotheres ostreum. (212) Adult female, dorsal view; (213) adult male, dorsal view. ( R e d r a m after Williams, 1965.)

what flattened inside, swollen outside, widened from proximal toward distal end, then narrowed ; width across base of fingers less than width of palm ; fingers stout, not gaping, tips hooked past each other, with minute teeth on opposing edges and a larger tooth near base of each ;

9. THE CLASS CRUSTACEA

319

walking legs slender, subcylindrical, last two articles with thin fringe of hair; second and third legs subequal in length but with first leg slightly stouter ; abdomen large, extending beyond carapace in all directions. Hard-shell male (Fig. 213) and female dark or brownish with two large almost circular pale white spots on both carapace and sternum ; with dorsal spots on brachial regions and ventral spots flanking abdomen and medial to first pair of legs ; with well-calcified carapace, 1.4-4.6 mm wide in males, 1.3-2.7 mm wide in females, flat dorsally, subcircular in outline, with truncate front more advanced than in mature female ; posterior margin straight ; lateral margin thin, sharply bent from dorsal side, margin marked by a raised band of short dense hair ; eyes well developed ; buccal mass crescentic, arched, broad from side to side but short anteroposteriorly ; cavity completely closed by external maxillipeds; chelipeds stout; merus and carpus not slender as in mature female ; palm slightly flattened inside, swollen outside, with both margins convex ; hands with bands of pubescence on upper and outer surfaces of palm and outer surface of immovable finger ; fingers stout, toothed proximally, tooth fitting between two protuberances on immovable finger when closed; both fingers with stiff hairs on gripping edges ; walking legs flattened, with posterior margin thickened and with plumose swimming hairs on second and third pairs; abdomen narrow, confined to sternal depression ; copulatory stylets of male well developed, first pair blade-like and hairy, second pair rodlike and almost hairless. Life cycle. The pre-symbiotic larval stages of P. ostreurn occur in the plankton. These include four zoeae followed by one megalops. Descriptions of the first zoeal stages have been given by Birge (1882) and redescribed by Hyman (1924) while descriptions of all the planktonic stages have been given by Sandoz and Hopkins (1947). The planktonic larval stages do not possess dorsal or lateral spines on the carapace. The time required from hatching to molting of the megalops to give rise t o the first crab stage is 25 days. The symbiotic (parasitic?) stages have been studied by Stauber (1945) and Christensen and McDermott (1958). The so-called '' invasive stage '' is the first crab stage (Figs. 214 and 215). It is this form that invades oysters. Six additional developmental stages ensue in the case of females, including the mature adult stage. Males do not develop beyond the hard stage. I n both sexes it is the hard stage which is the specialized stage a t which copulation occurs. The males leave their hosts a t this stage to search for females in another host. It is only during this stage that the crab is free-swimming. After copulating

320

MARINE MOLLUSCS AS HOSTS BOR SYMBIOSES

with one or more females, which usually takes place in June or July, the males disappear. Thus males only become 1 year old or less. Females become ovjgerous in their first summer but do not attain maximum size before their second summer. Some do not attain this until their third summer. Fully grown ovigerous females measure from 9.4 to 10.8 mm in width. These carry from 7 957-9 456 eggs. The

P

FIGS.214 and 215. Stage I (hard stage) Pinnotheresostreurn. (214)Female, dorsal view; (215) female, ventral view. (Redrawn after Stauber, 1945.)

exact period for which the eggs are carried is not known but it is believed to be from 3 t o 5 weeks. Females only produce one batch of eggs during the first year but may produce two batches during the second and third years. Ecology. Again, interested readers are referred to the detailed ecological observations by Stauber (1945) and Christensen and McDermott (1958). It is known that in Delaware Bay, and presumably also in other temperate regions, invasion of oysters by P. ostreum is

32 1

9. THE CLASS CRUSTACEA

seasonal. Few invasions occur before 1 August. It should be noted that the peak of oyster setting occurs during July in Delaware Bay ; thus by the time the f i s t crab stage commences to invade in large numbers, the oyster spat has grown to sufficient size to harbor one or two crabs. A single young oyster measuring 4.2 mm long may harbor two crabs while larger ones may harbor up to seven crabs. The crab appears to prefer spat (76.7% infestation) over yearling oysters (54.6 yoinfestation) and older ones (21.5% infestation), but the survival rate of crabs is better in yearlings and older oysters. Although the first crab stage (invasive stage) of P. ostreum can be found in oysters all winter, growth and development stop in Delaware Bay a t the beginning of November when the ambient water temperature begins to drop below 15°C. Pathology. During the feeding of P. ostreum in oysters, two types of gill erosions are secondarily effected. These pathological changes are discussed in an earlier section (Chapter 4, Section 11,A, 6). Resulting from a study designed to determine the effect of P. ostreum on the gross physical condition of Crassostrea virginica, Haven (1959) has demonstrated that oysters harboring crabs contain less soft tissues (meat) per unit of shell cavity volume than those without crabs but the water contents of oysters with and without crabs are not significantly different. Another aspect of crab-associated change in oysters has been postulated by Christensen and McDermott (1958). These investigators believe that P. ostreum may influence the sex ratio among oysters during their second spawning season if they retain their crab " parasites '' from the first year. Their postulation is based on the earlier finding by Awati and Rai (1931) who found that among 794 uninfested Ostrea cucullata, 41.7% were males, 56.4% were females, and 2.9% werc hermaphrodites. On the other hand, among eighty-six oysters harboring Pinnotheres s ~ . 82.6% , were males, 10.4% were females, and 7.0% were hermaphrodites. Since females can be induced to change sex in the laboratory by simple starvation, Awati and Rai concluded that the crab probably interferes sufficiently with food intake of the oyster so that it produces sperm instead of the more " expensive " eggs. That the change in sex is due to reduction in food intake and is not chemically stimulated by some crab-secreted substance appears to be supported by the findings of Amemiya (1935) and Egami (1953), who have shown that the experimental removal of a part of the gill in Crassostrea gigas will cause the number of males to far exceed that of females during the breeding season, provided that the operation is performed no later than the previous October. A.P.B.-6

21

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MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES

2. Pinnotheres maculatus Say, 1818. (Figs. 216 and 217)

(Order Decapoda; suborder Reptantia; section Brachyura; subsection Brachygnatha; superfamily Brachyrhyncha ; family Pinnotheridae) Pinnotheres maculatus, the mussel crab, is the second New World species which is known t o be a symbiont of various marine invertebrates, including several commercially important molluscs. Its range,

FIQS.216 and 217. Pinnotheres maculatus. (216) Adult female, dorsal view; (217) adult male, dorsal view. (Redrawn after Williams, 1965.)

according to Williams (1965), extends from off Martha’s Vineyard, Massachusetts, to Mar del Plata, Argentina. Both fully developed males and females have been reported in the mantle cavities of a large number of pelecypods including Mytilus edulis, Modiolus modiolus, M . americanus, Mya arenaria, Aequipecten irradians, A. gibbus, Placopecfen magellanicus, Atrina serrata and oysters (species unspecified).

9. THE CLASS CRUSTACEA

323

It has also been found in the tubes of Chaetopterus variopedatus, from

Molgula robusta, in the pharynx of Bostrichobranchus pilularis and on Asterias vulgaris. It was originally described by Say (1818) as inhabiting " the muricated Pinna of our coast." Descriptions. Mature female (Fig. 2 16) with suborbicular carapace, 13.7 mm long, 14.3 mm wide, thick and firm but not hard, convex; surface uneven, covered with short and deciduous tomentum ; gastrocardiac area higher than and separated by depressions from branchiohepatic area ; front slightly advanced, approximately one-fifth width of carapace, subtruncate in dorsal view, slightly bilobed ; orbits small, subcircular ; eyes spherical ; antenna longer than width of orbit ; antennule large, obliquely transverse ; buccal mass roughly quadrangular, crescentic, much broader than long ; ischium and merus of external maxilliped united ;propodus larger than carpus ; dactyl narrow, curved, spatulate, attached near middle of propodus, reaching to near extremity of propodus ; chelipeds moderately stout, articles subcylindrical, more or less pubescent ; carpus elongate ; palm thick, blunt edged, increasing in size distally ; fingers stout, fitting closely together with tips hooking past each other ; immovable finger nearly horizontal ; dactyl with tooth near base fitting into sinus with tooth at either side on immovable finger ; walking legs slender, hairy above and below ; second pair longest but shorter than chelipeds ; first three dactyls falcate, shorter than propodi; last leg shortest, turned forward and upward, with long dactyl of same length as propodus. Obscure brown in color, Young females resemble dark-colored males except in shape of abdomen and characteristics of appendages ;free-swimming,measuring up to 6.2 mm in length. More mature females symbiotic with hosts (usually pelecypods) ; light colored, measuring from 3.3 mm in length ; long hair persists on such small- and medium-sized females. Mature male (Fig. 217) with flat subcircular carapace, 9.1 mm long, 8.7 mm wide, harder than female ; regions superficially defined, more by color than by structural prominence, light areas mostly elevated, usually allowing pubescence to wear ; gastric, cardiac, and branchial regions separated by broad, shallow confluent indentations ; front broad, prominent, depressed, slightly lobed, approximately one-third width of carapace ; orbits subcircular, eyes large ; antenna somewhat longer than width of orbit; chelipeds shorter than in female, hands stouter ; walking legs wider, especially propodal articles of first three legs ; posterior surface overlaid with thin fringe of hairs attached near upper margin ; last leg relatively shorter than in female, not reaching propodus of third leg, dactyl more like third leg than in female;

324

MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES

abdomen at middle, approximately one-third width of sternum, gradually narrowing from third to seventh segment, sides of third convex, sides of seventh obtusely rounded ; sutures between segments of abdomen and sternum with narrow lines of dark pubescence. Strikingly light dorsal color pattern of bare spots on a background of dark pubescence consisting of a median stripe constricted on middle and behind, a subtriangular spot on each side in front of middle, and a linear spot on each side behind; chelipeds with dark pubescence on inner and upper surface of carpus, a bit on upper surface of merus and inner side of palm proximally, otherwise scattered flecks on hands and walking legs. Some males resemble mature females in coloration and structure of legs, ranging in length from about 4 mm upwards. Such males are symbiotic. Life cycle. Accounts of the life cycle of P. maculatus have been contributed by Pearce (1964) and Costlow and Bookhout (1966). As in the case of P. ostreum, the zoeal and megalopal stages are planktonic. Myman (1924)has described the first zoeal stage which, unlike that of P. ostreum, has well-developed spines in the carapace. According to Costlow and Bookhout, who have reared the larval stages from hatching to the crab stage under laboratory conditions there are five zoeal stages followed by the megalops stage. Thus, in addition to morphological differences,which have been given in detail by Costlow and Bookhout, P. maculatus differs from P. ostreum in its number of zoeal stages, the former with five and the latter with four. It may be noted that thenumber of zoeal stages is known to vary among the Pinnotheridae. For example, Lebour (1928b),working with material from the plankton, has reported two zoeal stages in the life cycle of P. veterum; Hart (1935), who has reared P. taylori, has also reported two zoeal stages in this species ; and Irvine and Coffin (1960) have reported four zoeal stages in the life cycle of Pabia subquadrata. According to Pearce (1964), ovigerous females of P. maculatus occur from late May to mid-June in the Woods Hole, Massachusetts, area. By early August the eggs are hatched and the zoeal and megalopal stages are planktonic. The megalopal stage molts during mid-September to give rise to the first true crab stage. It is at this stage that P. maculatus invades the mantle cavity of Mytilus edulis. Within the host, the crab undergoes several molts with each succeeding instar being somewhat larger but morphologically similar to the preceding. By mid-October, the crabs measure approximately 3.3 mm in carapace width. A molt follows, resulting in an anomalous juvenile with a well calcified exoskeleton (thus compamble to Christensen and McBermott’s hard stage). It is

9.

THE CLASS CRUSTACEA

325

at this stage that hard stage males and females leave their host and engage in copulatory swimming in open water. After this, females reinfest mussels and undergo four post-hard molts with each instar possessing unique characteristics but all with soft and poorly calcified exoskeletons. Male crabs in the hard stage are said to spend more time in open water during and after copulatory swimming and hence are more subject to predation; however, a few males are found in hosts following swimming. It is of interest to point out that Pearse has reported that juvenile (hard stage) females which enter hosts already inhabited by mature females beome retarded in their development and do not reach the sexually mature stage V instar. All crabs are believed to over-winter in the first post-hard (stage 11)instar, but with the advent of higher water temperatures in May the precociously inseminated crabs undergo the remaining three post-hard molts and attain the adult form (stage V).

Pathology. Detailed accounts of damage inflicted in molluscs by P. maculatus are not yet available. It may or may not damage its host's gills like P. ostreum and P. pisum although it is suspected that it does. Ecology. The seasonal periodicity manifested in the appearance of ovigerous females varies through the range. Rathbun (1918) has indicated that such females occur in January at St. Thomas, Virgin Islands, in March in Jamaica, from May to November in Florida, from June to January in North Carolina, from July to September in Rhode Island and Massachusetts (although Pearce has stated that they only occur from late May to mid-June at Cape Cod), and in June in Brazil. Relative to the swimming velocity of P. maculatus larvae, Welsh (1932) has reported that it is greatly influenced by temperature and light intensity. At temperatures between 20" and 25"C, the maximum swimming velocity is attained at light intensities between 10 and 25 meter-candles. When maintained a t different constant temperatures, it is known that there is a change in the relationship of velocity to light intensity, with the maximum possible velocity occurring at each constant temperature during the initial period of exposure to higher temperatures. Furthermore, the light intensities will bring about a marked effect on general activity. 3. Pinnotheres poisum Linnaeus, 1767. (Figs. 218-221)

(Order Decapoda; suborder Reptantia; section Brachyura; subsection Brachygnatha ; superfamily Brachyrhyncha; family Pinnotheridae) The pea crab, Pinnotheres pisum, is the common symbiont of pelecypods in northern European waters. It appears t o be most

326

MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES

frequently found in Mytilus edulis although it has been reported from Cardium edule, Ostrea edulis (Orton, 1920) and Cardium norwegicum

FIGS.218 and 219. Pinnotheres pisum. (218) First crab stage (invase stage); (219) prehard stage. (Redrawn after Christensen, 1959).

(Smith and Weldon, 1904). It has been known since the days of the Pharaohs and has been the subject of many colorful, although not quite accurate, legends (see Calman, 1911).

9. THE CLASS CRUSTACEA

327

Descriptions of stages I-IV females have been given by Atkins (1926) (Figs. 218-221).

FIQE.220 and 221. Pinnotheres pisum. (220) Hard stage female, dorsal view; (221) stage III female, dorsal view. (Redrawn after Atkins, 1926).

Descriptions. Adult female between 9 and 18 mm wide, carapace soft, wider than long, often quadrilateral in shape, generally without conspicuous color pattern ; front very narrow, about one-fifth width of

328

MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES

carapace, hardly visible from dorsal surface ; eyes feebly developed, very small and not visible from above; abdomen large, overlaps basipodite of legs laterally, completely covers mouth parts anteriorly, reaching immediately posterior to eyes ; last abdominal segment bent inwards rather sharply while feeding so that mouth is uncovered; abdomen deeply hollowed ; thorax hollowed ; numerous long hairs on edges of abdomen and sternum, between bases of cheliped and on pleopods. Smallest ovigerous female with carapace 7.5 mm wide ; numerous eggs carried in cavity formed by hollowed thorax and deeply hollowed abdomen ; space between sides of abdomen and thorax very small, well guarded by long fringing hair ; exopodite of second pair of pleopods long and blade-like, fringed with long and numerous hairs, fits along inside of gap as far forward as fifth abdominal segment and gives protection to eggs. Hard-shelled male with carapace almost circular, 1.9-6.3 mm wide, for the most part glabrous, light gray or fawn in color, with a conspicuous pattern of pale yellow areas outlined with darker yellow or yellowish orange ; in larger specimens the yellow areas increase in size and fuse to cover the greater part of dorsal surface of carapace ; pigmented lines and areas also occur on chelipeds and legs, including symmetrically placed yellow spots on their ventral surfaces ; frequently numerous black, occasionally red, chromatophores scattered over body ; chelipeds hairy, with broad and swollen palms; two rows of setae beneath chela, with one reaching from base of palm to tip of finger and other extending on inner surface only slightly beyond immovable finger, both rows converging distally ; large tooth present near base of dactylus, fits into slight notch, with small tooth a t both ends, in propodia1 finger; both biting surfaces bear stiff setae, with closely set spines towards tips of fingers; small teeth of propodial finger and curved spines from both fingers absent in some ;walking legs somewhat flattened, extremely hairy, with hairs being plumose ; second leg slightly longer than third, both extremely hairy; first leg shorter than third, fourth leg shortest ; short curved dactyli terminate in horny tips ; abdomen narrow and tapering ; two small transversely ridged chitinous nodules on fifth thoracic somite which fit into two pockets on sixth abdominal segment ; copulatory organs large, first appendage bladelike and hairy, with closed groove along inner surface, with numerous rosette glands around lower portion of groove, second appendage rodshaped with swollen base, with distal stylet almost hairless and without glands. Atkins (1958) has reported the occurrence of thin- or soft-shelled males. She states : " The thin-shelled male has a normal male abdomen,

9. THE CLASS CRUSTACEA

329

only slightly wider in relation to the width of the thorax than that of the thick-shelled male. . . thin-shelled males (measure) 1-9-6.3 mm.” Life cycle. P. pisum, like P. ostreum, includes four zoeal stages and a single megalops. The first zoea has been described, but not very effectively, by Thompson (1835) and later redescribed in detail by Lebour (1928a,b). What may have been the second zoea has been described by Lebour (19288). All of the stages, including the prezoea, first through fourth zoeae, and megalops, have been described in detail by Atkins (1955). The zoeal and megalopal stages are planktonic. The most recent and complete accounts of the life cycle of P. pisum are those given by Christensen (1959, 1962). Prior to this, Thompson (1935) had briefly described male and female adults. He stated that the males are hard-shelled while the females are soft-shelled. This concept was held until Orton (1920) demonstrated the existence of hard-shelled females which resemble males in all respects except for their genital apertures and pleopods. Atkins (1926) has described the molting stages of P. pisum in Mytilus edulis but followed Orton (1920) in designating the hard-shell stage as the first crab stage (which obviously does not correspond to the first crab stage of P. ostreum as given by Christensen and McDermott (1958)). Later Atkins (1954, 1955) realized her error and abandoned the concept that the hard stage is the first crab or invasive stage. Atkins (1955) has described the postembryonic development of P. pisum and still later (1958) has recorded the occurrence of thin-shelled males which resembles stage I1 females. Actually soft-shelled males had been found by Mercier and Poisson (1929) but these French workers failed to realize that this is a normal form. They were of the opinion that the soft-shelled condition had resulted from parasitism by an entoniscid parasite. Although Atkins (1958) has advanced our understanding of the stages in the life cycle of P. pisum by definitely demonstrating the soft-shelled males, she did not grasp their significance. She expressed the opinion that males altered between the hard- and soft-shelled forms during growth. It is now clear that the hard-shelled form, or hard stage, precedes the softshelled stages. Investigators prior to 1959 had consistently failed to find the prehard stages of P. pisum in Mytilus edulis, and it was for this reason that Atkins (1926) was originally of the opinion that the hard stage represents the first crab or invasive stage. Christensen (1959), however, has been able to correct this misinterpretation with the discovery that P. pisum changes hosts at the hard stage and hence this is the youngest form found in mussels. He has also found the true first crab or invasive stage of P. pisum in Spisula solida. Although Christensen (1962, and personal

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MARWE MOLLUSCS AS HOSTS FOR SYMBIOSES

communication) later found an ovigerous female in S. solida and informed Houghton (cited in Houghton, 1963) that he had also found what is possibly a pre-hard stage of P. pisum in a mussel at Roscoff, he considers these to be exceptions. Thus it would appear that although the symbiotic (parasitic) stages of P. pisum are comparable to those of P. ostreum (see Table XVII), its life cycle differs in that two hosts are involved, with the second being invaded by the hard stage. It is of interest to note that Christensen (personal communication) has reported that the ovigerous female found in Spisula solida was only about 4 mm in carapace width and was obviously retarded in its growth but not its development.

Ecology. As the result of field studies in Langstone Harbour, near Portsmouth, England, and at Conway, Wales, Houghton (1963) has reported that the larger crabs are found only in Iarger mussels ;furthermore, this crab is found more frequently in the larger mussels which occur in greater numbers lower along the shore. Houghton has also reported that “ the percentage of infestation differs from one locality to another a t the same tidal level and that it increases from the middle shore to the sublittoral zone for any given size-group.” Since Christensen (cited in Houghton, 1963) has found that the first crab stage, which is the invasive stage, is photonegative, it is unlikely that it will invade a, primary host high up on the shore line or near the water surface. It thus follows that the hard stage escaping from the primary host is more likely to enter Mytilus edulis living from the middle shore to the sublittoral zone where the primary host is found. Other information. Orton (1920) has observed the feeding habits of P. pisum in Mytilus edulis through a window cut in one of the host’s valves. He has reported a feeding habit similar to that observed by Stauber (1945) in P. ostreum (see Chapter 4, Section 11,A, 6). It should be noted, however, that Orton did not observe the pea crab to inflict any injury to Mytilus edulis comparable to that observed by Stauber in Crassostrea virginica invaded by P. ostreum. Nevertheless, the presence of P. pisum in mussels is known to cause certain physiological changes. Specifically, Berner (1952) has noted that there is a partial or even complete cessation in the production of gametes in those mussels infected with P. pisum measuring 10 mm or more in carapace width. Mussels harboring smaller crabs are very seldom affected in this manner. This change in sex in Mytilus edulis is most probably the result of starvation as is the case of Ostrea ceccullata infested by Pinnotheres sp. (Awati and Rai, 1931) and not due to some crab-secreted substance.

9. THE CLASS CRUSTACEA

331

4. Pinnotheres pholadis de Haan, 1835. (Figs. 222 and 223) (Order Decapod&; suborder Reptantia; section Brachyura; superfamily Brachyrhyncha; family Pinnotheridae) This species, originally described by de Haan (1836), has been reported but not redescribed since then by Tesch (1918))Balss (1922))

i'

FIQS.222 and 223. Pinnotheres pholudia. (222) Adult female, dorsal view; (223) adult male, dorsal view. (Redrawn after Sakai, 1965.)

Yokoya (1928,1933)and Sakai (1934,1936,1939, 1963)from a number of marine pelecypods including Chlarnys nipponensis, Mytilus edulis, Crassostrea gigas, Meretrix lusoria, Tapes japonica and Mactra sulcataria. According to Sakai (1966))who redescribed both the male and female of P . pholudis, P . cardii, described by him (Sakai, 1934))is a synonym.

332

MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES

Description. Adult female (Fig. 222) with soft exoskeleton, carapace rounded quadrangular, 12-13 mm in length and width, with markedly deflexed front; with four pairs of ambulatory legs, with the second being the longest ; row of long hair on carpi and propodi in very young specimens, disappears in full-grown ones ; dactyli of all legs very short and uniformly hook-shaped ; dactylus of external maxilliped styliform with tip exceeding that of propodus. Adult male (Fig. 223) smaller than female, with well-calcified body ; carapace circular, about 9 mm in length and nearly 9 mm in width ; dorsal surface strikingly convex, frontal edge thick, produced anteriorly, slightly emarginated in middle ; of four pairs of ambulatory legs, the second is longest; carpi with an oblique row of very long, featherlike hairs ;propodi with a row of similar hairs along anterior border ;dactylus of external maxilliped styliform as in female. Other information. According to Sakai (1965), during the mat,ing season, which occurs in early summer in Japan, both the male and female are usually seen together within the same mollusc's mantle cavity. This would suggest that unlike the three species of Pinnotheres discussed previously, neither the male nor both the male and female leave the pelecypod. 5 . Other Pinnotherid Grabs

Rathbun (1918), in her definitive treatise of the grapsoid crabs of America which includes the Pinnotheridae, has listed twenty-seven species of the genus Pinnotheres. Of these, she lists seven which are " commensals " of commercially important pelecypods (Table XVIII). No host is listed for ten other species, while the remaining ten are listed as " commensals '' of other types of invertebrates. Among the four species of Fabia listed, one is noted as a " commensal '' of Tapes and other pelecypods, while another, F . subquadrata, is listed as a " commensal " of " bivalved molluscs ". Of the five species of Parapinnixa and seven species of Dissodactylus, she lists none to be associated with a pelecypod. Of the twenty-six species of Pinnixa, she lists two species as being " commensals '' of commercially important molluscs (Table XVIII). The monotypic genera Xcleroplax, Tetrias and Pinnotherelia are reported not to include symbionts as is the case among the three species of Pinnaxodes. The single species of Opisthopus, 0. transversus, is said to be a " commensal of Mytilus edulis ". The relationships between the eleven species of pinnotherid crabs listed by Rathbun as occurring in the mantle cavities of commercially important molluscs have not been investigated. If futuro studies should

TABLE XVIII.

SPECIESOF PINNOTHERID CRABSREPORTED BY RATEBUN(1918) AND SAKAI(1965) COMMERCIALLY IMPORTANT MOLLUSCS “Oysters” M y t i h

Pinnotheres ostreurn P . geddesi P . politus P . angelicus P . maculatus P . margarita P . guerini P . sinensis P . boninewis Fabia lowei Pinnixa faba P . littoralis Opisthoptm tranaveraua Ostracotherea subquudratwr

+ + + + + + + +

+ + +

Mya

+

+ +

+

Aequipecten Pinna Margaritifera

+

+

Tapes

TO BE

SYMBIOTIC IN

“Clams” Gaatropods

+

i

+ +

+

+*

* Schizothaerus.

W

w

w

334

MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES

reveal metabolic dependency, as is suspected in the case of Pinnotheres ostreum, P. maculatus and P. pisum, then these pinnotherids should be considered as parasites. For further information, especially the descriptions of these species, Rathbun’s monograph should be consulted. Sakai (1965), in his monograph on the crabs of Sagami Bay, has listed those species of pinnotherid crabs commonly found in commercially important molluscs in the Far East. These are also included in Table XVIII. References to the descriptions of these species, along with notes on their natural history, can be found in Sakai’s monograph. Since the appearance of Rathbun’s monograph, several authors have reported the occurrence of immature Pinnixa fuba and P. littoralis associated with various species of pelecypods, including some commerically important ones. Although the relationship between these two species of crabs and their molluscan hosts has not been demonstrated to be a parasitic one, such accounts are being briefly mentioned for those interested in crabs associated with commerically important marine molluscs. Pearce (1966a) has reported that the adults of both P. faba and P . littoralis are sympatrically distributed with their clam host, Tresus capax, in Puget Sound, State of Washington, but are never associated with the closely related clam T . nutalli. Furthermore, he has confirmed the observations of others that immature specimens of both of these crabs are found within the mantle cavities of a number of pelecypods. Specifically, Pearce has confirmed Rathbun’s (1918) report that immature P. faba and P. littoralis have been found in Mya arenaria, Tapes, Saxidomus, Macoma nasuta and “ cockles ”, and Wells’s (1928, 1940) reports that the young of P. littoralis can occur in Macoma nasuta, M . inquinuta, M . indentata, M . secta, Mya arenaria, Saxidomus giganteus and Clinocardium nuttalli. It should be mentioned that in addition to immature specimens, Wells (1940) has also reported the occurrence of both P.faba and P. littoralis adults in small specimens of Macoma, Mya and Cardium on rare occasions. It would appear from such observations that both P. faba and P. littoralis may undergo a change in host as is the case with Pinnotheres pisum. In another paper (Pearce, 1966b), it has been reported that the post-planktonic stages of Fabia subquadrata occurs in the mantle cavity of the horse mussel, Modiolus modiolus, collected from the San Juan Archipelago in the State of Washington. Pearce not only has given a detailed description of the ecology, mating habits, and growth of this crab, but also has considered it a true parasite, basing his opinion on the fact that F. subquadrata causes extensive damage to the gills, palps, and mantle of its host.

9. THE CLASS CRUSTACEA

335

6. Other Crabs Associated with Pelecypods Crabs of the family Xanthidae, commonly known as mud crabs, are known to include certain species which are predators of the American oyster, Crassostrea virginica, and other pelecypods. For example, according to McDermott (1960), both Chestnut (unpublished) and Smith and Richards (unpublished) have shown that mud crabs, probably Panopeus herbsti, prey on Crassostrea virginica in New Jersey waters. It has been reported that a single crab will destroy thirty oysters in a month under laboratory conditions. McDermott and Flower (1952) have reported that Panopeus herbsti is an active predator of 1- or 2-year-old oysters. Similarly, Menzel and Hopkins (1956) have reported that another xanthid crab, Menippe mercenaria, preys on oysters, and Landers (1954) has reported that in Rhode Island another species, Neopanope texana preys on young Mercenaria mercenaria. McDermott (1960) has reported that Panopeus herbsti, Neopanope texana sayi and Eurypanopeus depressus will all prey on Crassostrea virginica in nature and that under laboratory conditions Panopeus herbsti will destroy 1- to 2-year-old oysters at the rate of 0.15 oyster per crab per day. He has also demonstrated a selectivity on the part of this crab for the smaller, thin-shelled specimens. The predatory xanthid crabs are being briefly mentioned here to emphasize that these are not parasites sensu strictu but are of importance to the shellfisheries industry. For a listing of the literature pertaining to the ecology of xanthid crabs, the paper by Ryan (1956) should be consulted.