LIFE CYCLE OF CYAMUS SCAMMON! (: CYAMIDAE), ECTOPARASITE OF GRAY , WITH A REMARK ON THE ASSOCIATED SPECIES

YUK M. LEUNG Department of Biological Sciences, University of Southern California, Los Angeles

ABSTRACT

G_vamus scammoni, parasitic exclusively on gray whale, was studied under the provision of special scientific permit. Its life cycle was completed during the journey of winter migration. C. ceti and C. kessleri, messmates of C. scammoni, followed the same pattern in many respects. Significantly, the whale-lice can survive out of water for several days though other am phi pods are poorly adapted for terrestrial life. The cyamid causes certain damage to the cutaneous tissue of the host when the juvenile begins its livelihood.

INTRODUCTION

The whale-, ectoparasite of mysticete and odontocete, has been recognized ever since Oniscus ceti of the bowhead whale recorded by Linnaeus in 1758. Although scores of papers on have elaborately been published, yet many facets are still unexplored. This accounts for the fact that systematic investigation is not always feasible, not only because the population of the whale species is widely distributed in different hemispheres, but the cyamids are often discarded by the commercial whalers. Moreover, the are legally protected so that collecting is no longer available. The gray whale, Eschrichtius robustus, summers in Chukchi, Beaufort, and western Bering Seas for food, and in winter it migrates along the Californian coast to the lagoons of Baja California, Mexico, for breeding and calving. As the herd travels along a defined course in definite seasons, the life cycle of the cyamid may well be traced through a successive survey during the entire journey. Under the provision of the specific scientific permit, the author was privileged to participate the whaling expedition on several occasions, and visited the shore station at intervals to collect series of samples of which the accum­ ative data were of significance to make this study possible.

MATERIAL AND METHOD

This study was based on series of Cyamus scammoni and the associated species, C. ceti and C. kessleri, taken aboard the catcher boat off central Cali-

Sci. Rep. Whales Res. Inst., No. 28, 1976, 153-160. 154 LEU>l'.:: fornia fornia durin g 1966 -196 7 season . and in the shore s LaLion al P t. San P ablo. Cal ト f'ornia f'ornia in 1963 1964 and 1968 -1969 se ason s. Includ ed w e re bolh ind ivid ua ls mi gra tin g so uLhwa rd and homewa rd bound in th e month s of' D ece mb er co April. April. It al so cove red the m ateri al co lle cted at Pt. Barr ow. Al aska in Lh c summer m onLh s of' 1954 , 1959 and 196 1 (Leun g 1965). Some 85 male s. 200 ov ige rous females, and 250 ju ve nile s were sLU di ed . of wh ich the total len g th of eac h sta ge . and th e numb er of egg s and you ng in the the ovary and brood-pou ch wer e reco r ded. The sta ge of deve lo pmen t w as ex- amined fr om so m e 4000 indi v idua ls ta ken at P t. Ba rrow. and the livi ng spec i- me ns were s tudied at sea and at th e shore station.

LI FE HISTORY

Cyα7 九iis 8ια ?n ？九oni (Fi g . 1) is the large st spe ci es of th e family as th e male is rangin g up to 27 mm , an 仁1 th e 「e111al c to 16 111111. It s doub le cock -screw gi lls and the un evc n ly purple co loraL ion on the dor sa l so mites consti tut e uniq ue feature s of th e spe cie s. Th e d eve lo pment , alik e othe r amp h ipod s, is d i rect. The b rood wa s apparently full -grow n in summ er befor e migratin g so uthw a rds. and mating beg an when it reac h巴d sexua l m awri ty ( Fig. 2). An ov igerous female c arried a clut ch of 98 0- 1078 eggs in the brood-pouch. and the eggs. pherical. spherical. cr ea m y white, m eas urin g 325 -420 μ. we1 で「 enilizecl wh en the w ha le

Fi g. I. Cyamu s sc amm o11i Dall, male, do rsa l view (lef t) x 6, fema le , ventral v iew (ri gh t）× 10.

Sc i. R ep . Whales Re s 目 Ill s!., No. No. 28, 1976 . LIF E CYC L E OF CYA M US SC AM 1¥4QN, 155

Fig. Fig. 2 . C. ceti, ma tin g on side of th e jaw of the ho st. x 10 arri ved in ce n tral Ca li fo rnia in O c tober. A ltho ugh the fema le c arried a co n- iclerable siclerable num ber of eggs in a clutch , on ly 450 -76 0 (a bo ut 60 %) w e re fertil ize d. The youn g, me asuring about 0.5 mm , re se mbled the parent ex c ept that the g ill s, i nstead of double and spira ll y co il ed, we re si ngle and knob shapecl , and there was no trace of genita l appe nd ages in bot h male and fem ale ( Fig. 3). B ein g not not a free- sw immin g amphipo d . the vul nerable you n g reta ined in the bro od- pouch 「or two to thr ee mont hs unt il it reac hed the stage of miniature adul t. Tho se arri vin g in D ece mber and .J an 凶 ry the juve nile s had been relea se d from the the broo d-po uch to ma inta in lif e independ ent ly. T h巴 free ju ve nile , measuri ng 1.0 -1. 5 mm, fa s tened it se lf w i th peavey hook -lik e un gul ae in th e so ft s kin ti ss ue of of the belly of the hos t (F ig. 4 a nd 5) , or s hielded itse lf in the sca r 01 ・ori 自ce o[ the endem ic cirrip eてI (C γyptolev αsr α chianecti) along both ja, .vs of the w ha le. Subsequcntly. Subsequcntly. the yo ung wa s able to cover itse lf fo r pr otect ion again st th e tu rbule nt c urrent (Fi g.6 ). .-¥ft er remainin g in the re cess of the cor ium o「the h ost and crev i ce o「the cirrip c: d fo r some tim e. the ju ve 凶 c bega n t o s et foot on thec uti cle of th e hos t ''ith it ss trong pera eopoded claw s. At this st age, the k nob- shap ed g il ls began to expa nd and cur v巴 in. and bifur ca te w h en the yo un g att ain ed 4・ mm in length: at ful l gro wt h the n umber of co il s of the sec ond bran ch was almo st do uble the number of the first one. When the in- div id u al m eas ur ed about 6 mm . th e oos teg ites of the female proje ct ed inw ar dl y on the gill-be aring so m ite s (31 てl and 4 th bod y s egment s), an 仁l the purple co lor- a tion of both mal 巴 and female app ear ed gradual ly on the dor sum . In F 巴bruar y w hen the h ost was ret urni ng to the habit atf ro m th 巴 so uth. the m ini at ur e male ad ult at tained 8- 10 111 111 , and the fema le from 6 8m m ; th e m ale ac cesso ry gi ll s (a bsent in femal e) and th e gen it al app endag es began to appear; the pa i red

Sci. Sci. R ep. Whale s R es .I ns t. , No. No. 28, 1976 156 156 LEUNG .. 、

fi g. 3. Micrograph of a juv eni le C. scammo11i, ve ntral view , sho wing th e knob- sh aped gills befor e bi fur cating. x 45. Note th e unn amed chonotrichous ciliates infe st in g th e ventra l surfac e of th e body. gen it al va l ves on the 5th so mi tc or the female could be traced. In Mar chm ost of the indi vidua ls reac hed maturi ty m eas urin g 14- 18 mm in ma le, and 10 - 12 mm in femal e, the gi ll s, accessory gills and the gen ital appendages of the male we re fu ll y developed; w her eas the oostegites of the female had shaped to form a brood-po uch, of wh ieh the poste ri or pl ates extended over th e an teri or one s. T he elaborate ove rlappin g arrangemen t of the oo steg ite ss heltered the eggs and th e yo un g in th e broo d-po uch thr oughout th 巴 incubation period, but

Sci. Sci. R e戸 Wha les R es . In st ., No . 28, 1976.

No . . 28, 1 976.

Sci. R e p. W ha l es R es . . In st . . .

but but the la s t t matur e d m d o r e e e arli e r r s in ce ce the the egg s s w e re h at c h e d b d c ror e e th e e

n C. i11wn i i α th e e co unt e r part o f i f t s s m SC ess ce t mat i i C . . es . . ¥¥"a C k . . S S ess l eri. and and

est im ated ated that i t t underw e nt e i g ht t o o n i n e e m o n th s s c omp l e te the lir e e to cy cl e.

d e ,・cl o ped ped upon upon th e a e iri va l l o r r t h e e w h al e e in the the s umm e r r habitat , , and and it w as

in c re as e e to i t s s fu ll ca pac i t y y art e r r so m e e tim e . . Fina ll y . . th e e br oo d w d as ru l l y y

350 depo - 380 s i t t e gg s s in th e e bro o d - pouch pouch h o m e war d s . . and and t he he numb e r r wou l d d

i t t wa s s automat i ca ll y y op e ne d d w h e n n t he he y oung oung I fu l l-grown. l-grown. A A e m alc might might ¥l"a S S ・

Fi g. T h e e o ut e rm os t t s 5. kin ti ss u e e h e avil y y dama ge d d by y o un g g C. x 2 5 5 sca mm o ni

Fig . . Y o un g g 4 . . b o rin g g h o l es on the C b . . e ll y y of the sc am h mo11i os t. x x 2 5.

LIFE LIFE CYC LE LE OF OF C YAM US US SC AMMO N ! ! 1 57 57 158 LEUNG

Fi g. 6. ju ven il es embedding in th e cleft s of th e endem ic cir riped s on on the side or the low er jaw . x 25 .

se aso nal mi g rati on began. Of 392 1 C. kessleri tak en at Pt. B arr o "・ in .Jul y and Augu st. 3534 were ju¥・enile s. on ly 387 adu lt s. 』¥I hen the host m ig ra tcd so uthw~川l pass in g ce ntral Ca li fornia in mid .J anuary , so me of th e female s had alr eady been deposit in g egg s in the brood-p ou ぐIi. During the co urse of returnin g north wa rd in late Ma rch, the new generation atta in ed full maturity as as among 58 fem a les exam in ed. 25 w ere ca rryi ng eggs . 18 wi th ju venile s in the brood-pou ch. and 15 ha vin g release d their young . An ovigerous C. kessleri ca rr ied 215-300 eggs . on ly 150 -260 (about 75 -80 % ) were fer tili zed. whe r eas C. ceti ceti carr ied 154 -242 embryo s. but 13 1- 146 (about 70 -75 %) were fertili zed. Obv iously. the numb er of emb r yos produced is va ri ed acco rdin g to the spe c ies and th e si ze o f th e female. Th ere is spee u lat ion as to the number of in sta r$ of C . sc α m,m,oni and the assoc i ated spec i es as the numb er o f ec cly sis is untra cea bl e. H ow eve r, it see m s li kely ther that e ma y be at lea st seve n or eight sta ges as far as the range of size and the d eve lopment of th e m orphologi ca l stru ctur es are co ncern ed . Fur- thermore, it is probable that the cyc le overlap s by 閃 aso n that so me juveni ! es are are alway s pr ese nt on each co l ony.

GENE R AL CONS ID ERAT ION

De sp ite the cya mid belong s to the same group w i th the ca prellid (Ca prel lidea), it ha s diverged fr o m the ge ne ra l pl an to a great ext e nt in as mu ch as th e mod i- 自eel structure of the peraeop ods and the pos sess ion of accesso ry gi ll s are ex tra- ord inar y in amphip o d. Po ssessing the se unique stru ct ure s, the wha le-l ouse is, so far as is known , the only tru e para siti c form among th e am phi pod s. Th e

Sc i. R ep . ~~・hales R es . In st ., No. 28, 1976. LIFE CYCLE OF CYAMUS SCAMMON! 159 cyamids, particularly those of infesting larger mysticetes, have rigid host speci­ ficity and site restrictiveness (Leung l 970a) as C. scammoni occurs habitually either on the delicate skin tissue of the belly or on the scar of the endemic cirriped along both jaws of the whale; C. ceti, being received at the same table occasionally with C. sca11imoni, is found generally on the creases of the lips, flippers and flukes; whereas C. kessleri localizes only on the umbilicus, genital opening and anal aperture of the host. During the whaling seasons, nine whales had been inspected aboard the catcher boat and in the shore station, and all were heavily infested with cyamids of different stages. Among the three species, C. scammoni exceedingly predominated over the other two. The cyamids breathe by means of gills, however, it is remarkable that they are able to exist beyond the environmental condition. At the shore station it was not uncommon to see the whale-lice crawling for many hours after the whale drawn from the sea. While cruising on the catcher boat, it was curious to observe three individuals of C. scammoni reposing on a steel cable of the winch in the late afternoon as no whale was taken during the day. Obviously, these individuals had survived from the catch of the previous day. Further surprising evidence was afforded by G.]. B. Ross of the Snake Parks and Ocea­ narium of S. Africa (per. comm.) who reported that the cyamids could outlive for three days on a stranded south at Algoa Bay in 1971. Integu­ mentary respiration of the whale-lice is of considerable significance, because they were able to survive for several days divorced from the aquatic environ­ ment even though the amphipods are poorly adapted for terrestrial life. The mouth parts of the cyamid are for piercing. There is some likelihood that whale-lice are omnivorous feeding on the algal filaments and the outer­ most layer of skin tissue of the host. However, the bill of fare seems to be the cutaneous tissue of the host as the young customarily encases itself by piercing the delicate skin tissue or embedding itself in the cleavages of the sessile cirriped when it begins to maintain its livelihood. Since the host pro­ vides favorable sites and adequate food supplies, opportunity of building up large population is eminent. On the other hand, the small streamlined odontocete furnishes neither adequate accommodation nor profuse provisions, and the survival rate is therefore in a reverse direction (Leung l 970b ). Three species of cyamids occur on the gray whale. With the exception of C. scammoni, the systematic status of C. kessleri and C. ceti have long been bewildered. Although C. kessleri was recorded by E. Wosnessensky in 1864 at Metschigmensky in the vicinity of the Bering Strait, yet the host had not been identified. It did not come to light until 1954 when Mohr (Hurley and Mohr 1957) collected a few hundred individuals of this species from a gray whale killed by the Eskimos off Pt. Barrow, Alaska, and the host proper was finally justified. C. ceti was described from the bowhead or the Greenland right whale, but the association with the gray whale is poorly known. Since the bowhead and the gray whale inhabit in Arctic waters, the possibility of

Sci. Rep. Whales Res. Inst., No. 28, 1976. 160 LEUNG accidental transfer by bodily contact is not unlikely to happen. However, it is seemingly not the case as our colleague, Dr. F. E. Durham, a bowhead bio­ logist, reported that he found neither C. scammoni nor C. kessleri but C. ceti on the bowhead (per. comm.). For this reason, the likelihood of interchange seems unlikely. Virtually, C. ceti is akin to C. monodontis of the narwhal which Lutken (1873) described it as a "peculiar dwarf-form" of C. ceti. In view of C. ceti of the gray whale, there is reason to speculate that it may fall within the original description from the bowhead, and a concept of specific independent species has been conceived. Consequently, both species should be thoroughly reviewed. There are various unnamed species of chonotrichous ciliates (Chonotricha) infesting the ventral surface of the young cyamids (Fig. 4). It is of interest that these collar ciliates, alike the cyamids, demonstrate an extraordinary mode of that shares on other congeners to occupy the same community, and the occurrence of interchange is uncommon even though the messmates are colonized at the adjoining locality. Accordingly, it is suggested that it may be a contributing factor to identify the whale-lice and the cetaceans in the presence of the ciliates. Finally, the whale-lice cause certain damage to the whale skin when the young begin to maintain their livelihood, and the injury is a result of piercing the tissue in which they shelter for safety and for food. As a matter of fact, the outermost layer of whale skin is extremely thin and delicate in structure, hence it is no wonder that the unwelcome guests frequent these haunts for living. ACKNOWLEDGMENT I am grateful to Mr. Dale W. Rice and Mr. Allen A. Wolman of the National Marine Fisheries Service for their pertinent information and facilities; to Del Monte Fishing Co. for permission to make observation in the factory ; and particularly to the skipper and his crew members of the catcher boat " Allen Cody" for their full cooperation to make this study possible. The use of the library and laboratory of Allan Hancock Foundation is gratefully acknowledged.

REFERENCES HcRLEY, D. E, and J. L. MOHR, 1957. On whale-lice (Amphipoda: Cyamidae) from the Cali­ fornia gray whale E. glaucus. ]. Parasitol., 43(3): 352-357. LEC'W, Y. M., 1965. A collection of whale-lice (Cyamidae: Amphipoda). Bull. Soc. Calij. Acad. Sci., 64(3): 132-143. LEC:-IG, Y. M., 1970a. Cyamus orcini, a new species of whale-louse (Cyamidae, Amphipoda) from a killer whale. Bull. de Inst. Fundamental D'Afrique Noire, Universite de Dakar, T32, ser A, N'3: 669-675. LEU'.'iG, Y. M., 1970 b. First record of the whale-louse genus Syncyamus (Cyamidae, Amphipoda) from Western Mediterranean, with notes on the biology of obontocete cyamids. In: In­ vestigation on II. Univ. of Berne, Swirzealand, pp. 243-247. LUTKEN, C. F., 1873. Bidrag til kundakab om arterne af slaegten Cyamus Latr. eller Hval­ lusene. Vidensk. Selsk. Skr., (5) 10(3) :t 229-284.

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