Department of Zoology and Entomology, University of the Orange Free State, PO Box 339, Bloemfontein, 9300, South Africa

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1 FOLIA PARASITOLOGICA 46: , 1999 Aspects of the morphology and a review of the taxonomic status of three species of the genus Chonopeltis (Crustacea: Branchiura) from the Orange-Vaal and South West Cape River Systems, South Africa Liesl L. Van As and Jo G. Van As Department of Zoology and Entomology, University of the Orange Free State, PO Box 339, Bloemfontein, 9300, South Africa Key words: Chonopeltis australis, Chonopeltis minutus, Chonopeltis australissimus, taxonomy, morphology, fish parasite Abstract. Comparative scanning electron microscopical studies were carried out on Chonopeltis australis Boxshall, 1976 collected from different localities in the Orange-Vaal River System in South Africa and on material of Chonopeltis minutus Fryer, 1977 and Chonopeltis australissimus Fryer, 1977 on loan from the Albany Museum, Grahamstown. This elucidates the fine structure of morphological features, which are of taxonomic importance and illustrates the significance of the copulatory structures on the legs as a taxonomic tool. It was also concluded that C. australissimus is the same as C. minutus, with C. australissimus the junior synonym. The endemic African genus Chonopeltis Thiele, 1900 comprises 14 species, which are distributed from below the bulge of Africa southwards. In the Zaïre System Chonopeltis schoutedeni (Brian, 1940), Chonopeltis congicus Fryer, 1959, Chonopeltis flaccifrons Fryer, 1960 and Chonopeltis elongatus Fryer, 1974 coexist (Fryer 1959, 1960, 1974). Chonopeltis brevis Fryer, 1961, C. schoutedeni, C. congicus, and C. flaccifrons inhabit the Great Lakes of Central Africa (Fryer 1961). Chonopeltis koki Van As, 1992 is found in the Zambesi River, whilst Chonopeltis lisikili Van As et Van As, 1996 occurs in the Okavango Delta, Botswana (Van As 1992, Van As and Van As 1996). Chonopeltis inermis Thiele, 1900 was originally described from Lake Malawi (Fryer 1956), but has recently been recorded from the Limpopo River System (Van As and Van As 1993), where it coexists with Chonopeltis meridionalis Fryer, The Olifants River in Mpumalanga, South Africa, is also inhabited by two Chonopeltis species, i.e. Chonopeltis fryeri Van As, 1986 and Chonopeltis victori Avenant-Oldewage, 1991, whilst only one species, i.e. Chonopeltis australis Boxshall, 1976 is found in the Orange-Vaal River System (Boxshall 1976, Van As 1986, Avenant-Oldewage 1991). Fryer (1977) described Chonopeltis minutus Fryer, 1977 from material collected in the Olifants River in the South West Cape, South Africa. In the same paper he also described Chonopeltis australissimus Fryer, 1977 based on museum specimens collected in 1937 from the adjacent Groot Berg River (Fig. 1). These species are closely related to C. australis and distinctly different from the northern species (Fryer 1977). In the present study additional information is provided on the morphology of C. australis from different localities in the Orange-Vaal River System. Taxonomic important morphological features of C. australis are compared to those of C. minutus and C. australissimus. Based on this it was concluded that C. australissimus is the same as C. minutus with C. australissimus the junior synonym. MATERIALS AND METHODS During fish parasitological surveys carried out at different times between 1980 and 1996 in localities in the Orange-Vaal River System (Fig. 1), specimens of C. australis were collected from Labeo capensis (Smith, 1841) and fixed in 70% ethanol. Specimens of C. minutus and C. australissimus were obtained on loan from the Albany Museum, Grahamstown, South Africa. C. minutus (labelled AML 164) was collected by Prof. Paul Skelton in 1973 from Barbus calidus Barnard, 1938 and Barbus erubescence Skelton, 1974 in the Twee River which forms part of the Olifants River, South West Cape. This jar included 16 young adult males and 22 adult females, of which 5 were egg bearing. Permission was obtained to prepare four female and three male specimens for scanning electron microscopy (SEM). Chonopeltis australissimus (labelled AML 165) collected in 1937 by Drs. A. C. Harrington, K. D. Barnard and C. W. Thorn from Pseudobarbus burgi (Boulenger, 1911) in the Groot Berg River, South West Cape, included one female and two male specimens. Permission was obtained to prepare one of the male specimens for SEM. Specimens for SEM were dehydrated to absolute ethanol, critical point dried, sputter coated with gold and studied at 5 kv in a JEOL 6400 WINSEM. Measurements (in mm) of specimens were made from microscope projection drawings. Figures 2-9 are micrographs of material we collected, whilst Figs are micrographs of material which has been preserved for a long time and are therefore not of the same quality. Address for correspondence: L. L. Van As, Department of Zoology and Entomology, University of the Orange Free State, PO Box 339, Bloemfontein, 9300, South Africa. Phone: ; Fax: ; vanasll@dre.nw.uovs.ac.za 221

2 Fig. 1. Map of southern Africa showing rivers relevant to the distribution of Chonopeltis species in this region and the sampling localities where C. australis were collected. A Zambesi River; B Okavango Delta; C Limpopo River; D Orange-Vaal River System; e Vaal River; f Orange River; g Fish River; h Olifants River, Mpumalanga; J Olifants River, South West Cape; K Great Berg River. 1 Boskop Dam; 2 Vaal River Barrage; 3 Bloemhof Dam; 4 Van der Kloof Dam; 5 Wuras Dam; 6 Malibamatso River, Lesotho; 7 Hardap Dam, Namibia. Bloemfontein. RESULTS AND DISCUSSION Body measurements of males and females from different populations of Chonopeltis australis are summarised in Tables 1 and 2 and measurements of C. minutus and C. australissimus in Table 3. Chonopeltis australis Boxshall, 1976 Figs. 2-9 This species can be distinguished from other species of the genus based on the following characteristics. In some cases the characteristics are not unique, but should be evaluated in combination with other features. The anterior margin of the cephalic carapace has a broad thickened band without a medial indentation. Four chitinous supporting rods support it. The carapace length is about half the total body length (Tables 1, 2). The posterior margin extends to cover the base of the second pair of legs (Fig. 2). The maxilla is distinctly prehensile, with the last three podomeres well developed and with the combined length almost the same as that of the combined length of the first two podomeres (Fig. 3). The second podomere has a distinctive row of tooth-like scales on the posterodistal margin (Fig. 4). In the female the first pair of legs are the largest, progressively declining in size towards the forth pair. The spacing between legs is the smallest between legs 1 and 2, slightly larger between 2 and 3 and the largest between legs 3 and 4 (Fig. 2). The exopod and endopod of legs 2, 3 and 4 of males and females are more or less of the same length. They all bear a single row of long setae on the ventral side. These setae each bear a single row of setules. In the first leg the exopod is longer than the endopod. In the latter the arrangement of setae and setules is the same as those of the rami of the other legs. The exopod has two rows of setae, one row on the ventral and the other on the dorsal side. A single row of setae is also present on the dorsal side of the second podomere of the first leg. All the setae on the dorsal side of the first leg bear two rows of setules, while those setae on the ventral side of the exopod only have a single row of setules. Legs 2, 3 and 4 have no setae on the dorsal side. The natatory lobes of both sexes are undivided. In females they are broad with stout setae on the posterior margin (Fig. 5), whilst in males they are cylindrical terminating in long setae. The abdomen is short in females, less than one third and in males about one third of the total body length (Tables 1, 2). On the ventral side it is adorned with scales. The abdominal cleft is more than a third, but less than half of the abdomen length in females and about one third of the abdomen length in males. The tips of the abdomen in both sexes are straight. The spermathecae are pear-shaped and do not extend past the fused part of the abdomen. Testis of the male has smooth lateral margins and extends past the fused part of the abdomen. The first and second legs of the males are similar to those of the females and lack any projections. The posterior margin of the first podomere of leg 3 is rounded and extends to cover part of the fourth leg. The socket is situated on the dorsal side of leg 3 and consists of an elongated opening (Fig. 6). On the proximal part of the exopod of leg 4 is a rounded posterior projection of which the ventral surface is covered by scales. The peg of the fourth leg is elongated and coneshaped. It has a broad base and tapers to a straight hollow tip (Fig. 6). The peg is about half the length of the endo- and exopods. The flap of the socket covers the base of the peg, ventrally, with almost half of the peg extending past the distal margin. A collar of 7-14 scalloped extensions fringes the opening of the peg (Fig. 7). A single lobed protrusion is situated on the dorsal side below the peg opening. The tip of the peg is studded with stout scales and several short protrusions are visible on the inner fringe of the opening. The tip of the peg undergoes an interesting development from young to adult male. During the final larval moult the rudimentary hook on the outer periphery of the sucker as well as other larval characteristics such as the bristle-like setae on the postero-ventral surface between the second and third podomeres will be lost (Van Niekerk and Kok 1989). At this stage the peg of the young male is not yet fully developed. The anterio-ventral side of the tip of the peg is open and without the scalloped collar and lobed 222

3 Van As, Van As: Chonopeltis spp. from South Africa Figs Scanning electron micrographs of Chonopeltis australis. Fig. 2. Adult female, ventral view. Fig. 3. Maxilla. Fig. 4. Podomere 3 and 4 of maxilla. Fig. 5. Natatory lobes of female. Fig. 6. Legs 3 and 4 of male, dorsal view. Arrowhead indicates socket opening. Fig. 7. Fully developed peg of mature male. Arrowhead indicates lobed protrusion. Fig. 8. Peg of young male after final larval moult. Fig. 9. Peg of pre-adult male. Scale bars: Fig. 2 = 0.5 mm; Figs. 3, 5, 6 = 100 µm; Fig. 4 = 50 µm; Figs. 7-9 = 10 µm. 223

4 Table 1. Body measurements of Chonopeltis australis females from different localities in the Orange-Vaal River System, South Africa (in mm) Number of specimens measured Total body length (TBL) Carapace length (CL) CL as % of TBL Length of anterior lobe (LAC) LAC as % of CL Carapace width (CW) Width of anterior lobe (WAC) WAC as % of CW Sucker diameter (SD) SD as % of TBL Abdomen length (AL) AL as % of TBL Length of fused part (LF) LF as % of AL Length of cleft (LC) LC as % of AL Abdomen width Boskop Dam; 2 Vaal River Barrage; 4 Van der Kloof Dam; 5 Wuras Dam; 6 Malibamatso River, Lesotho; 7 Hardap Dam, Namibia. Table 2. Body measurements of Chonopeltis australis males from different localities in the Orange-Vaal River System, South Africa (in mm) Number of specimens measured Total body length (TBL) Carapace length (CL) CL as % of TBL Length of anterior lobe (LAC) LAC as % of CL Carapace width (CW) Width of anterior lobe (WAC) WAC as % of CW Sucker diameter (SD) SD as % of TBL Abdomen length (AL) AL as % of TBL Length of fused part (LF) LF as % of AL Length of cleft (LC) LC as % of AL Abdomen width Boskop Dam; 2 Vaal River Barrage; 3 Bloemhof Dam; 5 Wuras Dam; 6 Malibamatso River, Lesotho; 7 Hardap Dam, Namibia. projection (Fig. 8). In slightly larger young males the tips of the pegs resemble those of adult males, but with the top of the pegs still open (Fig. 9). This was the case in all four small specimens collected in the Malibamatso River, Lesotho. In larger specimens the tip is closed to form a hollow structure (Fig. 7). Presumably this signifies maturity. The morphology of the peg and other copulatory structures were found to be consistent characteristics of the different populations of C. australis. The relative body dimensions (Tables 1, 2) of adult specimens of both males and females from the different populations of C. australis are very similar. All the specimens collected in Lesotho were young, showing some differences in relative body dimensions to the other populations. Features of taxonomic importance 224

5 Van As, Van As: Chonopeltis spp. from South Africa such as carapace length as a percentage of total length and abdominal length as a percentage of total length are the same as for those of the larger specimens from other populations. Chonopeltis minutus Fryer, 1977 Figs , 16 Chonopeltis minutus is in many respects similar to C. australis. It is however a much smaller species (cf. Tables 1, 2 with 3). Males and females of C. minutus are stout in appearance (Figs ), whilst C. australis has a slender body. The anterior carapace in C. minutus is also without a medial indentation, has supporting rods and a broad anterior margin. In adult males the carapace is more than half the total body length, with the posterior margin covering the base of the second pair of legs (Table 3). In some females the posterior margin of the carapace covers only the base of the first pair of legs, whilst in others it extends halfway between the first and second pair of legs and in some cases it covers the base of the second pair of legs. The suckers of C. minutus are much larger relative to the size of the body than is the case in C. australis. In C. minutus the diameter of the sucker is 24% of the total body length, while in C. australis it is between 12% and 17% (cf. Tables 1, 2 with 3). The maxillae of C. minutus are more robust than in C. australis, these appendages are almost twice the size of the first pair of legs. In C. australis the maxilla is not noticeably larger than the legs. The second podomere of C. minutus has similar tooth-like scales on the postero-distal margin as those found in C. australis (Fig. 4). The relative size and spacing of the legs of C. australis females is a consistent feature of this species. In C. minutus females, however, considerable variations in the relative size and spacing of legs were observed. In most cases the first legs are only slightly smaller than legs 2, 3 and 4, which are more or less the same size. In these specimens the distance between legs 1, 2 and 3 are about equal, whilst the third and fourth legs are situated slightly closer. In other specimens, including all five egg-bearing females examined, the first leg is much smaller than the rest. Leg 3 is the largest and situated very close to leg 4. In some specimens the spacing and sizes of legs were intermediate between these extremes. In specimens with wide spacing between leg 3 and 4, the appendages appeared more slender than in those with leg 3 and 4 close together. The spacing of the legs also influences the appearance of the natatory lobes. In specimens with legs 3 and 4 close together the natatory lobes are round and in those with legs 3 and 4 widely spaced, the natatory lobes are more rectangular. The abdomen length of C. minutus males is less than a third, whilst in the female it is about one third of the body length (Table 3). These dimensions are the same for C. australis. The cleft in the abdomen of C. minutus Table 3. Body measurements of females (f) and males (m) of Chonopeltis minutus (Cm) and Chonopeltis australissimus (Ca) from the Albany Museum, Grahamstown, South Africa (in mm). Cm (f) Cm (m) Ca (f) Ca (m) Number of specimens measured Total body length (TBL) Carapace length (CL) CL as % of TBL Length of anterior lobe (LAC) LAC as % of CL Carapace width (CW) Width of anterior lobe (WAC) WAC as % of CW Sucker diameter (SD) SD as % of TL Abdomen length (AL) AL as % of TBL Length of fused part (LF) LF as % of AL Length of cleft (LC) LC as % of AL Abdomen width males constitutes 25% of the total abdomen length, whilst in C. australis it is between 44% and 56%. The testis of C. minutus does not extend past the cleft, as is the case in C. australis. The spermathecae of C. minutus are oval-shaped in adult females and irregular pearshaped in young females. The ventral surface of the abdomen of both sexes in C. minutus bears scales similar to those in C. australis. The general morphology of the copulatory structures on the legs of C. minutus is very similar to those of C. australis with small, but important differences. As in the case of C. australis legs 2 are without any specialised projections. The posterior margin of the first podomere of leg 3 also covers part of the fourth leg, but appears to be larger relative to legs 3 and 4 than is the case in C. australis. There are also no differences in the morphology of the socket structure on leg 3 (cf. Figs. 6 and 14). The peg in C. minutus (Fig. 14) is also coneshaped and tapers towards a straight hollow tip, similar to the peg of C. australis. The opening of the tip shows some significant differences, which were found to be a consistent feature in all the specimens of these two species examined. In C. australis a collar consisting of a single row of scallops, with a single lobed protrusion on the dorsal side, fringes the opening (Fig. 7). In the case of C. minutus the peg opening is fringed by a double row of much longer scallops, without any projections (Fig. 16). The peg structures in young males of C. minutus undergo similar development as in C. australis, where the tips of the pegs are open in young and closed in mature males (Figs. 8, 9). 225

6 Figs Microscope projection drawings of Chonopeltis minutus females. Fig. 10. Dorsal view. Fig. 11. Ventral view. Scale bar = 0.5 mm. Figs Microscope projection drawings of Chonopeltis minutus males. Fig. 12. Dorsal view. Fig. 13. Ventral view. Scale bar = 0.5 mm. 226

7 Van As, Van As: Chonopeltis spp. from South Africa Figs Scanning electron micrographs of Chonopeltis minutus and Chonopeltis australissimus. Fig. 14. Legs 3 and 4 of C. minutus male, dorsal view. Fig. 15. Legs 3 and 4 of C. australissimus male, dorsal view. Fig. 16. Tip of peg, C. minutus. Fig. 17. Tip of peg, C. australissimus. Scale bars: Figs.14, 15 = 100 µm; Figs. 16, 17 = 10 µm. Chonopeltis australissimus Fryer, 1977 Figs. 15, 17 Fryer (1977) separates C. minutus and C. australissimus by the following features: Legs 3 and 4 of the females of C. minutus are very close together while those of C. australissimus are well spaced. The spacing of the single specimen of C. australissimus examined in this study corresponded to Fryer s description. Among the 22 females of C. minutus which we examined we found a whole range of variation, including specimens where legs 3 and 4 were well spaced, as well as specimens with these legs close together. Some of the females of C. minutus resemble the female described by Fryer as C. australissimus. This also applies to the single specimen of C. australissimus we examined. Fryer (1977): The legs of C. australissimus are more slender than those of C. minutus. Within the sample of C. minutus we examined, we also found specimens with slender appendages. Fryer (1977): In C. minutus the rami of legs are approximately similar in length while in C. australissimus the exopod of leg 1 is longer than the endopod. The exopod bears long setae on the dorsal side. In all the specimens of C. australis, C. minutus and C. australissimus we examined, the exopods were longer and long dorsal setae were present. In all cases these setae bore a double row of setules unlike those on the ventral side, which only have a single row. The function of these setae is most likely to clean the respiratory areas on the lateral carapace. In comparing the scanning electron micrographs of the copulatory structures of males of C. minutus (Figs. 14, 16) with C. australissimus (Figs. 15, 17) no reason can be found to separate them as different species. The details of all the morphological features are identical. The specimens of C. minutus and C. australissimus, examined in this study, have been preserved for more than 20 and 60 years respectively and there is a time gap 227

8 of more than 40 years between the collection of these specimens. Despite this, there can be no doubt as to the similarity of the fine structure of the peg opening of these two specimens shown in Figs. 16 and 17. The taxonomic importance of the fine structure of the peg has been demonstrated in other Chonopeltis species, i.e. C. fryeri (Van As 1986), C. koki (Van As 1992), C. inermis (Van As and Van As 1993), C. victori (Luus- Powell and Avenant-Oldewage 1996) and C. lisikili (Van As and Van As 1996). The precise function of the peg is still unknown, though we suspect that it may play a role in sperm transfer (Van As and Van As 1993). The variation in some characters in females, is most likely the result of postlarval development, which continues after the final larval moult. In males, such changes are, for example, the continuing development of the peg structure as illustrated in Figs In the five egg-bearing specimens of C. minutus examined in this study, legs 3 and 4 are close together and the spermathecae oval-shaped (most likely filled with sperm). Other specimens showing differences in the spacing of legs or other minor differences in the shape of the abdomen and natatory lobes are most likely not yet fully developed. Based on the morphological information provided above there can be little doubt that C. australissimus is the same species as C. minutus with the former the junior synonym. Chonopeltis species appear to have a narrow host range, restricted to a few closely related host species. Chonopeltis minutus was originally collected from two barb species in the Olifants System and C. australissimus from the adjacent, but isolated Groot Berg River, occurring on another barb species, endemic to this river. This isolation was one of the reasons why Fryer separated the two species. In our opinion, C. australis and C. minutus originated from a common ancestor. The present C. minutus radiated after the southern rivers became isolated from the Orange River System. Distribution from the Olifants River to the Groot Berg River could have occurred before these two systems became isolated. Alternately, C. minutus could have distributed across the watershed after the two rivers were isolated. The headwaters of these two rivers are in close proximity and in times of exceptionally heavy rain translocation of fish and their parasites could conceivably have taken place. At least two examples of such translocation of Chonopeltis species have been recorded. Chonopeltis brevis crossed a watershed from the Tana River to Lake Victoria and C. inermis from Lake Malawi to the Limpopo River (Fryer 1968, Van As and Van As 1996). In both cases they are found on different hosts, after crossing the watershed. Acknowledgement. The authors thank the staff of the Albany Museum for making the Branchiura material available. REFERENCES AVENANT-OLDEWAGE A. 1991: A new species of Chonopeltis (Crustacea: Branchiura) from the Kruger National Park, southern Africa. Rev. Zool. Afr. 105: BOXSHALL G.A. 1976: A new species of Chonopeltis (Crustacea: Branchiura) from southern Africa. Bull. Br. Mus. Nat. Hist. Zool. 30: FRYER G. 1956: A report on the parasitic Copepoda and Branchiura of the fishes of Lake Nyasa. Proc. Zool. Soc. Lond. 127: FRYER G. 1959: A report on the parasitic Copepoda and Branchiura of the fishes of Lake Bangweulu (Northern Rhodesia). Proc. Zool. Soc. Lond. 132: FRYER G. 1960: Studies on some parasitic crustaceans on African freshwater fishes with description of a new copepod of the genus Ergasilus and a new branchiuran of the genus Chonopeltis. Proc. Zool. Soc. Lond. 133: FRYER G. 1961: The parasitic Copepoda and Branchiura of the fishes of Lake Victoria and the Victoria Nile. Proc. Zool. Soc. Lond. 137: FRYER G. 1968: The parasitic Crustacea of African freshwater fishes: their biology and distribution. J. Zool. (Lond.) 156: FRYER G. 1974: Une nouvelle espèce de Chonopeltis (Crustacea: Branchiura) parasite d un poisson congolais. Rev. Zool. Afr. 88: FRYER G. 1977: On some species of Chonopeltis (Crustacea: Branchiura) from the rivers of the extreme South West Cape region of Africa. J. Zool. (Lond.) 182: LUUS-POWELL W.J., AVENANT-OLDEWAGE A. 1996: Surface morphology of the fish parasite Chonopeltis victori Avenant-Oldewage, 1991 and aspects of the histomorphology. Kudu 39: VAN AS J.G. 1986: A new species of Chonopeltis (Crustacea: Branchiura) from the Limpopo System, southern Africa. S. Afr. J. Zool. 21: VAN AS J.G. 1992: A new species of Chonopeltis (Crustacea: Branchiura) from the Zambesi River System. Syst. Parasitol. 22: VAN AS L.L., VAN AS J.G. 1993: First record of Chonopeltis inermis Thiele 1900 (Crustacea: Branchiura) in the Limpopo River System with notes on its morphology. Syst. Parasitol. 24: VAN AS L.L., VAN AS J.G. 1996: A new species of Chonopeltis (Crustacea: Branchiura) from the southern Rift Valley with notes on larval development. Syst. Parasitol. 35: VAN NIEKERK J.P., KOK D.J. 1989: Chonopeltis australis (Branchiura): structural development and functional aspects of the trophic appendages. Crustaceana 57: Received 27 October 1998 Accepted 25 February