A taxonomic study of sessile peritrichs (Ciliophora: Peritricha) associated with crustacean fish ectoparasites in South Africa

J.G. van As and Sophie Viljoen Research Unit for Fish Biology, Rand Afrikaans University, Johannesburg

Three new and four known species of sessile peritrichs were Introduction identified from the crustacean ectoparasites, Lernaea barnimiana (Hartman, 1870), L. cyprinacea Linnaeus, 1758 and In the course of fish parasite surveys in the Transvaal, sessile Dolops ranarum (Stuhlmann, 1891) from various fish hosts in peritrichians (Ciliophora: Peritricha) were often observed on South Africa The new species described are: Epistylis the crustacean ectoparasites Lemaea bamimiana (Hartman, cyprinaceae sp. n., E. epibamimiana sp. n. and Episty/is magna 1870), L. cyprinacea Linnaeus, 1758 and Dolops ranarum sp. n. Comparative deSCriptions of the four known species are (Stuhlmann, 1891). In some cases the growth was of given, i.e. convallaria (Linnaeus, 1758), V. microstoma Ehrenberg, 1830, Epistylis branchiophi/a Perty, 1852 and E. nym­ such an extent as to be visible to the naked eye Sessile peritrichs pharum (Engelmann, 1862). have previously been reported from different Lemaea species S. Atr. J. Zool. 1984, 19: 275-279 but were not specifically identified: Vorticella from L. haplocephala Cunnington, 1914 (Cunnington 1914), stalked Drie nuwe en vier bekende sessiele Peritricha-spesies, protozoans from L. carassi Tidd, 1933 (fidd 1933), afkomstig van die Crustacea-ektoparasiete Lernaea barnimiana from L. tortua coquae Dolley, 1940 (Dolley 1940), (Hartman, 1870), L. cyprinacea Linnaeus, 1758 en Dolops L. . Carchesium sp. from chackoensis Gnanamuthu, 1951

) ranarum (Stuhlmann, 1891) van verskillende varswatervisse in 0 Suid·Afrika is ge"identifiseer. Die nuwe spesies wat beskryf (Gnanamuthu 1951a) and L. bengalensis Gnanamuthu, 1951 1

0 word is Epistylis cyprinaceae sp. n., E. epibarnimiana sp. n., en (Gnanamuthu 1951b), clusters of colonial peritrichs from L. 2 Episty/is magna sp. n. Vergelykende beskrywings van die vier bamimiana (Hartmann, 1870) (Thurston 1969), encrustations d e t bekende spesies word gegee, nl. Vorticella convallaria of peritrichs (vorticellids, Epistylis sp.) from L. hessaragattensis a (Linnaeus, 1758), V. microstoma Ehrenberg, 1830, Epistylis d Srinivasachar & Sundarabai, 1971 (Srinivasachar & Sundarabai (

branchiophila Perty, 1852, en E. nympharum (Engelmann, 1862). r 1971) and in a recent study by Viljoen (1983) in South Africa, e S.-Atr. Tydskr. Dierk. 1984, 19: 275-279 h Epistylis sp. from L. bamimiana. s i l It is well established that a large number of sessile peritrich b u species inhabit fresh water, attached to a variety of substrates. P

e Representatives of at least four genera, Ambiphrya, Apiosoma, h t Epistylis and Scyphidia are known to be associated with fish y (Lorn 1966). Although it has not yet been determined beyond b

d any doubt whether the association of the peritrichs and the e t fish is of an ectocommensal or parasitic nature, some species n a are known to have caused severe damage and even mortalities r g amongst fish (Fischthall949; Rogers 1971). In a recent investi­ e c gation of the substrate preference of the sessile peritrichs, it n e

c was established that those occurring on fish are specific to i l piscean substrates. Peritrichs in the same habitat occurring on r e other substrates were not found on fish (Viljoen & Van As d n 1983). It is therefore of particular interest to establish whether u

y the peritrichs occurring on the fish ectoparasites, can also a settle on the piscean hosts. However, this will only be possi­ w e t ble when the comprehensive taxonomic study of fish­ a associated peritrichs, presently under way, has been G t completed. e n i In this paper, specific identifications and taxonomic b

a descriptions are presented of the sessile peritrichs occurring S J.G_ Win As· and Sophie Viljoen on the crustacean ectoparasites, collected from a variety of y b Research Unit for Fish Biology, Rand Afrikaans University, host fish and localities in South Africa Other crustacean d p.o. Box 524, Johannesburg, 2000 Republic of South Africa e ectoparasites occurring on the skin and fins of fish, such as c u ArgulU5 japonicus Thiele, 1900 and Chonopeltis australis d *To whom correspondence should be addressed o Boxshall, 1976 were also collected and examined but did not r p Received 31 August 1983; accepted 23 March 1984 e host any sessile peritrichs. R 276 S.-Afr. Tydskr. Dierk. 1984, 19(4)

Material and Methods this collection are provided. Sessile peritrichs were removed from the carapace and appen­ dages of crustaceans ectoparasitic on fish, mounted in a drop Vorticella Linnaeus, 1767 of pond water on a microscope slide and studied live under a compound microscope. The slides were then air dried, stained YorticellJl convallaria (Unnaeus, 1758) (Figures 1a, 1b and 8A) with Harris' hematoxylin and used for further microscopic Specimen reference number: Slide 82/4/10 - 3 investigations. Host: Lemaea cyprinacea Linnaeus, 1758 from Oreochromis Systematic descriptions are based on live as well as hema­ mossambicus (peters, 1852). toxylin-stained specimens. All measurements are in micro­ Locality: Hartbeespoort Dam (25°45'S127°50'E), Transvaal. metres and were obtained from stained specimens. Minimum Dimensions: Length of body 27 - 72 (49,1 ± 7,0; 24), diameter and maximum values are given, followed in parenthesis by the of body 25 -65 (47,8 ± 11,5; 22), diameter of stalk 2-6 (4,4 arithmetic mean, standard deviation and number of specimens ± 1,0; 19), diameter of macronucleus 3 - 6 (4,8 ± 0,8; 13). measured. Body length is measured from the junction of zooid Remarks: Conforms to the description of V. conva/lana by and stalk to the peristomial disc, and body diameter at the Noland & Finley (1931) and Viljoen & Van As (1983). The widest part of zooid. latter authors found representatives of this species attached to Type specimens of new species described are deposited in a variety of plant, animal and inanimate substrates in an im­ the fish parasite collection of the Department of Zoology of poundment in the Transvaal. the Rand Afrikaans University, Johannesburg. Specimen reference numbers are indicated at the relevant descriptions. YorticellJl microstoma Ehrenberg, 1830 (Figures 2a, 2b and 8B) In the case of comparative descriptions of known species, Specimen reference number: Slide 83/4/20-14 specimen reference numbers of microscope slides deposited in Host: L. cyprinacea from O. mossambicus. I , -,','..

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c Figures 1-7 (1) Vorticella convallaria: (a) expanded, (b) contracted. (2) Vorticella microstoma: (a) expanded, (b) contracted. (3) Epistylis nympharum' u (a) expanded, (b) contracted, (c) stalk. (4) Epistylis branciophila' (a) expanded, (b) stalk. (5) Epistylis cyprinaceae: (a) expanded, (b) contracted microzooid, d o (c) contracted rnacrozooid, (d) stalk. (6) Epistylis epibarnimiana' (a) expanded, (b) contracted, (c) stalk. (7) Epistylis magna' (a) expanded, (b) contracted, r

p (c) stalk. Scales in all cases indicate 8 11m for Figures (a), Figures (b), (c) and (d) not drawn to scale. e R S. AfT. 1. Zool. 1984. )9(4) 277

Locality: Lowveld Fisheries Research Station, Marble Hall convex. Peristomiallip does not open as wide as body. Infundi­ (24°55'S129°2O'E), Transvaal. bulum curved, extending to middle of body. Contractile Comparative description: Solitary. Body oval-shaped, length vacuole situated near peristomiaJ lip. Food vacuoles disuibuted 29-46(36,3 ± 6,J; 14), ctiameter20-38 (30.5 ± 5,8; 14). I hroughoul body. Macronucleus ribbon-like, diameter 2 - 5 Pellicular striations present but inconspicuous. Sralk contrac­ (3,5 ± 0,9; 9). tile, diameter 3 - 4 (3,5 ± 0,5; 10). Peristomial disc roundly Remarks: Not previously reoorded from South Africa. Con-

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d Figu~ 8 PholOmicrographs of hemaloxyUn-stained (A. E. F. H) and Uve (8, C, D. G) sessile perilrichians from crustaeean fish ectoparasiIC:S. (A) Vor· o

r /iceJlD convallarla. (8) Verlice/la micros/emil. (q Epislylis nympharurn. (0) £pisly/is nympharum on appendages of Dolops ranorum. (E) £pis/ylis bl"tl,,­ p C"hiophila. (F) £pis/y/is c:yprinacene. (G) Episrylis ep/bQmimiana. (Hl £pwylis maglUJ. e R 278 S.-Afr. lYdskr. Dierk. 1984, 19(4)

forms to the descriptions by Noland & Finley (1931) and Green Type host: L. cyprinacea from O. mossambicus. (1974). This species is considerably smaller than, and differs Type locality: Hartbeespoort Dam (25°45'S127°20'£), significantly in the shape of the zooid from V. convallaria. Transvaal. The macronucleus, although ribbon-like, is relatively short. Description: Colonial. Many zooids per colony. Zooids of two Vorticella microstoma corresponds in overal dimensions to V. distinct sizes. Zooids roundish-oval. Microzooid, length 19 - 33 Iymnaearum Viljoen & Van As 1983, but differs significantly (27,9 ± 3,9; 18), diameter 21 - 26 (22,3 ± 1,3; 18), macro­ in the shape of the zooid, diameter of the peristomiallip when zooid, length 45-48 (46,4 ± 1,5; 6), diameter 51-54 (52,1 expanded, and shapes of both macronucleus and contracted ± 1,4; 6). Pellicle not striated. Stalk branched extensively, zooid. diameter 3 -4 (3,5 ± 0,5; 16). Macronucleus horseshoe­ shaped, mostly situated in adoral region of zooid, in micro­ Epistyfis Ehrenberg, 1838 zooid, diameter 3-5 (3,7 ± 0,7; 11), and in macrozooid, Epistylis nympluuum (Engelmann, 1862) (Figures 3a, 3b, 3c, diameter 3 - 5 (3). 8c and 8D) Remarks: A second population of this species was found on Specimen reference number: Slide 83/4/30 - 2 L. cyprinacea from Labeo rubropunctatus Gilchrist & Thomp­ Host: Dolops ranarum (Stuhlmann, 1891) from Oreochromis son, 1913 from Glen Alpine Dam (23°20'S128°4O'E), mossambicus. Transvaal. The two populations correspond in morphological Locality: Roodeplaat Dam (25°5'S128°30'£), Transvaal. characteristics, differing only slightly in overall dimensions. The Comparative description: Frequently solitary, sometimes paired mean dimensions of the Glen Alpine Dam population are on bifurcated stalk or colonial. Zooid cylindrical and elongated, given below. Microzooids, length 22,4; diameter 19,3. Macro­ length 61-157 (112,9 ± 23,3; 31), diameter 24- 98 (55,9 ± zooids, length 39,2; '4iiameter 37,8. Stalk diameter 3,4. Macro­ 20,9; 31). Divided into two regions by circular groove. Upper nucleus in microzooid 1,8 and in macrozooid 3,0. region about twice the length of lower region. No pellicular Viljoen & Van As (1983) found an unidentified Epistylis sp. striations observed. Stalk bifurcated in colonial fonns, short, on the thoracical appendages of a freshwater crab in an im­ less than one third of zooid length, diameter 5 -18 (8,3 ± 3,6; poundment in the Transvaal, of which the morphological 24). Peristomial lip opens as wide as body. No vacuoles ob­ characteristics of the zooids confonn to the present species. served. Macronucleus sausage-shaped, centrally placed, It differs however in overall dimensions, as well as the absence diameter 5 - 12 (7,7 ± 1,8; 36). of micro- and macrozooids. Mention of micro- and macro­ Remarks: First record of this species in South Africa. Con­ moids in a single Epistylis colony was made by Matthes & forms to the descriptions of E. nympharum by Nenninger Scheubel (1970) in which case the size differences of moids

It . (1948) and Green (1974). has a relatively large zooid and were ascribed to different stages of the reproductive cycle. In )

0 has a characteristic groove which is more distinct than in other the present study the presence of micro- and macrozooids was 1

0 species of this genus. It has previously been found on Chiron­ a constant feature of all observed colonies and it is clearly a 2 omidae by Nenninger (1948), on cladocerans and insect lar­ distinct species from those observed by the above-mentioned d e t vae by Green (1974) and Cyclops spp. by Foissner & Schiff­ authors. a

d mann (1974). During contraction, the zooid maintains its cylin­ ( Epistylis epibamimiana sp. n. (Figures 6a, 6b, 6c and 8G) r drical shape, the base of the zooid has a wrinkled appearance e h and the peristomial lip is drawn together rather than inward Type specimens: Holotype slide 83/4120 - 3, paratype slide s i l as in the case of Vorticella species. 83/4/20-2 b u Type host: Lemaea bamimiana from Labeo capensis (Smith, P Epistylis branchiophi/a Perty, 1852 (Syn: E. formosa Nen­ 1841). e

h ninger, 1948) (Figures 4a, 4b, and 8E) t Type locality: Wuras Dam (19°0'8/26°151£), Orange Free

y Specimen reference number: 82/5/3-1 State. b

d Host: L. cyprinacea from O. mossambicus. Description: Colonial. Up to 20 zooids per colony. Zooids oval, e t Locality: Hartbeespoort Dam (25°45'S127°50'£), Transvaal. length 41-98 (57,3 ± 11,5; 21), diameter 44-69 (53,8 ± 5,3; n a Comparative description: Colonial. Large colonies with many 20). No pellicular striations observed. Stalk irrigularly r g

zooids per colony. Zooid cylindrical to inverted bell-shaped, branched, diameter 4-11 (7,4 ± 2,1; 17). Peristomial disc flat. e c length 48-94 (69,6 ± 11,2; 22), diameter 51-84 (64,0 ± 8,0; Peristomiallip opens as wide as body. Food vacuoles situated n e 22). Pellicle striated. Stalk, dichotomously branched, diameter centrally. Macronucleus sausage-shaped, centrally placed, c i l

5 -14 (8,9 ± 2,6; 19). Peristomial disc convex. Peristomial diameter 4-6 (5,2 ± 1,0; 19). r e lip opens as wide as body. Infundibulum curved, extending Remarks: This species is the only sessile peritrich thus far found d n past middle of body. Contractile vacuole and food vacuoles on Lernaea bamimiana, an indigenous crustacean copepod ec­ u

y situated in upper body region. Macronucleus sausage-shaped, toparasite of fish in Africa. A distinctive characteristic of this a short and thick, diameter 5-9 (7,2 ± 1,0; 21). peritrich is the orientation of the macronucleus in relation to w e t Remarks First record of E branchiophila in South Africa. The the body axis, the shape of the zooid and the irregularly a branched stalk. Although individual colonies do not consist

G shape and dimensions of zooids as well as branching of stalk t of many zooids, large clusters were found on the cephalothorax e conforms to the description by Nenninger (1948) and Biegel n i (1954) who however makes no mention of the colony size. This of L. bamimiana, visible to the naked eye. b a species differs significantly from the other known Epistylis S species as well as those described in the present study, with Epistylis magna sp.n. (Figures 7a, 7b, 7c and 8H) y b reference to the large colony size and relative long main stalk. Type specimens: Holotype slide 82/5/3 - 1, paratype d e 82/5/3-2 c u Epistylis cyprirwceae sp.n. (Figures 5a, 5b, 5c, 5d and 8F) Type host: L. cyprinacea from O. mossambicus. d o Type specimens: Holotype slide 83/4/20-5, paratype slide Type locality: Hartbeespoort Dam (25 ° 45'S127 °20'£), r p

e 82/5/3-3 Transvaal. R S. Afr. J. Zool. 1984, 19(4) 279

Description: Colonial. Four to eight woids per colony. Zooids GNANAMATHU, C.P. 1951a. l-ernaea chakoensis n. sp.: A copepod inverted bell-shaped when expanded, round when contracted, parasitic on two Madras fishes. Parasitology 41: 143 -147. length 83 -166 (130,6 ± 22,8; 15), diameter 82-145 (117,7 GNANAMUTHU, C.P. 1951b. Lernaea bengalensis sp. nov.: A copepod parasitic on Channa punctatus. Rec. Indian Mus. 54: 5. ± 18,3; 15). No pellicular striations observed. Stalked, main GREEN, J. 1974. Parasites and epibionts of Cladocera. Trans. Zool. stalk short, bifurcated, sometimes with three branches, Soc. Lond. 32: 417-515. diameter 7 - 21 (13,2 ± 4,1; 10). Peristornial disc protruding LOM, J. 1966. Sessiline peritrichs from the surface of some distinctly when expanded. Peristomiallip does not open as wide freshwater fish. Folia Parasitol. 13: 36 - 60. as body. Infundibulum not spiralled, extending to middle of MATTHES, D. & SCHEUBEL, J. 1970. Epistylis galea, Ehrenberg, body. Food vacuoles situated in upper body region. Macro­ ein polyrnorphes Peritrich. Arch. Protistenk. 112: 30 - 64. nucleus sausage-shaped and curved, situated adorally, diameter NENNINGER, URSULA. 1948. Die Peritrichen der Umgebung von Erlangen mit besonderer Beriicksichtigung ihrer Wirtsspezifitiit. 11-20 (13,8 ± 3,1; 9). Zool. Jahrb. Abt. Syst. Oekol. Geogr. Tiere. 77: 169 - 266. Remarks: This species is the largest sessile peritrich occurring NOLAND, L.E. & FINLEY, H.E. 1931. Studies on the taxonomy of on crustacean fish ectoparasites found in the present study. the genus Vorticella. Trans. Am. Microsc. Soc. 59: 80-123. It is also relatively large in comparison to other species of the ROGERS, W.A. 1971. Disease in fish due to the protozoan Epistylis genus. (Ciliata: Peritricha) in the Southern U.S. Proc. Annu. Con! South-east. Assoc. Game. Fish. Comm. 25: 493 -498. References SRINIVASACHAR, H.R. & SUNDARABAI, A. 1971. A new cope­ BIEGEL, MARIA. 1954. Beitrag rur Peritrichenfauna der Umgebung pod parasite, Lemaea sp. nov., on a cyprinodont fish, Lebistes Erlangens. Arch. Protistenk. 100: 153 -182. reticulatus (Peters). Curro &i. 40: 453 - 455. CUNNINGTON, W.A. 1914. Zoological results of the Third THURSTON, J.P. 1969. The biology of Lernaea bamimiana Tanganyika Expedition, conducted by Dr W.A. Cunnington, (Crustacea: Copepoda) from Lake George, Uganda. Rev. Zool. 1904-1905. Report on the parasitic Eucopepoda. J. of Zool. Bot. Afr. 80: I - 2. 819-829. TIDD, W.M. 1933. A new species of Lernaea (Parasitic Copepoda) DOLLEY, T.S. 1940. A new lernaean (parasitic copepod) from min­ from the goldfish. Ohio. J. Sci. 33: 465 - 469. nows in Lafayette county, Mississippi. Trans. Am. Micros. Soc. VILJOEN, B.C.S. 1983. 'n Seisoenstudie van die visektoparasiet Ler­ 59: 70-77. naea (Crustacea: Copepoda) in Boskopdarn, Transvaal. M.Sc. FISCHTHAL, J.H. 1949. Epistylis, a peritrichous protozoan on Dissertation, Rand Afrikaans University, Johannesburg, South hatchery brook trout. Prog. Fish-Cult. II: 122 -124. Africa, 210 pp. FOISSNER, W. & SHIFFMANN, H. 1974. Vergleichende Studien an VILJOEN, SOPHIE & VAN AS, J.G. 1983. A taxonomic study of argyrophilen Strukturen von vierzehn peritrichen Ciliaten. Protisto­ sessile peritrichians of a small impoundment with notes on their logica. 10: 489 - 508. substrate preferences. J. Limnol. Soc. Sth. Afr. 9(1) 33 - 42.

. ) 0 1 0 2 d e t a d ( r e h s i l b u P e h t y b d e t n a r g e c n e c i l r e d n u y a w e t a G t e n i b a S y b d e c u d o r p e R