Parasitol Res (2012) 111:2049–2061 DOI 10.1007/s00436-012-3052-1
ORIGINAL PAPER
Ancyrocephalidae (Monogenea) of Lake Tanganyika: III: Cichlidogyrus infecting the world’s biggest cichlid and the non-endemic tribes Haplochromini, Oreochromini and Tylochromini (Teleostei, Cichlidae) Fidel Muterezi Bukinga & Maarten P. M. Vanhove & Maarten Van Steenberge & Antoine Pariselle
Received: 17 June 2012 / Accepted: 16 July 2012 / Published online: 16 September 2012 # Springer-Verlag 2012
Abstract Lake Tanganyika is the deepest and oldest African Great Lake and of economic importance. While the diversity of its endemic cichlid radiations yielded scientific interest, a number of cichlid tribes have few representatives in the lake. Some of those, namely Oreochromini (ex-Tilapiini), Haplochromini and Tylochromini, reach higher species numbers in riverine systems. Conversely, the phylogenetic position of the monospecific and endemic Boulengerochromini is unclear. The oreochromines Oreochromis tanganicae and Oreochromis niloticus, the haplochromine Astatotilapia burtoni, the tylochromine Tylochromis polylepis and the boulengerochromine Boulengerochromis microlepis, the largest cichlid species worldwide, were surveyed for ancyrocephalid monogenean gill F. Muterezi Bukinga Section de Parasitologie, Département de Biologie, Centre de Recherche en Hydrobiologie, B.P. 73, Uvira, Democratic Republic Congo
parasites. Five new species are proposed. Cichlidogyrus gillardinae sp. n. is described from A. burtoni, Cichlidogyrus mbirizei sp. n. from O. tanganicae and Cichlidogyrus nshomboi sp. n. from B. microlepis. T. polylepis harbours Cichlidogyrus mulimbwai sp. n., Cichlidogyrus muzumanii sp. n. and a third, presently undescribed species. Four species known from outside the Tanganyika Basin were retrieved on the oreochromines. The host species are scientific models or important in the sectors of fisheries or ornamental fish trade. Moreover, their phylogenetic positions render them well-suited to help elucidate the historic relationships between riverine and lacustrine African cichlids. In this framework, their Cichlidogyrus fauna is compared to congeners known from African rivers and to the few Tanganyika representatives described. While the parasites of Oreochromis, A. burtoni and T. polylepis are reminiscent of those infecting related hosts throughout Africa, B. microlepis hosts a Cichlidogyrus morphotype typical of Lake Tanganyika. This supports its placement within an endemic cichlid radiation.
F. Muterezi Bukinga via B.P. 254, Bujumbura, Burundi M. P. M. Vanhove : M. Van Steenberge Laboratory of Biodiversity and Evolutionary Genomics, Department of Biology, KU Leuven, Charles Deberiotstraat 32, 3000 Leuven, Belgium M. P. M. Vanhove : M. Van Steenberge Ichthyology Unit, African Zoology Department, Royal Museum for Central Africa, Leuvensesteenweg 13, 3080 Tervuren, Belgium A. Pariselle (*) ISE-M, UMR5554 CNRS, UR226 IRD, Université Montpellier II—CC 063, 34095 Montpellier, Cedex 5, France e-mail:
[email protected]
Introduction Lake Tanganyika is important in terms of water, protein supply and transport to an estimated ten million people, its economic impact reaching far beyond its shores (Mölsä et al. 1999). As the oldest and deepest of the African Great Lakes (Cohen et al. 1997), it is home to around 250 cichlid species, forming the behaviourally, morphologically and genetically most diverse cichlid fauna worldwide, albeit not the most species-rich (Snoeks 2000). This cichlid assemblage includes ancestral lineages that are basal to the hyperdiverse East African radiations (Nishida 1991; Schwarzer et al. 2009). Based on Poll (1986) and Takahashi (2003), Lake Tanganyika cichlids are classified into tribes, several of which evolved into radiations
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that are endemic to the lake. Others have few Tanganyika representatives, although they sometimes display a larger species diversity elsewhere. Species belonging to these nonendemic tribes are often seen as relatively recent invaders of the lacustrine environment. This was hypothesized for Tylochromis polylepis (Boulenger 1900), the sole Tanganyika representative of Tylochromini (Koch et al. 2007) and for Oreochromis tanganicae (Günther 1894) (Klett and Meyer 2002). The latter species is the only ‘tilapiine’ present in Lake Tanganyika proper, although Oreochromis karomo (Poll 1948), Oreochromis niloticus (Linnaeus 1758), Oreochromis upembae (Thys van den Audenaerde 1964) and Tilapia rendalli (Boulenger 1897) occur in adjacent aquatic systems. Both Tylochromini and Tilapiini (sensu Poll (1986) and Takahashi (2003)) reach their highest diversity in West and West-Central Africa (Lamboj 2004). Whether or not the Tanganyika endemic Boulengerochromis microlepis (Boulenger 1899), the world’s largest cichlid, is to be considered a ‘tilapiine’ was until recently a topic of debate (overview in Klett and Meyer 2002). Takahashi (2003) erected the monospecific tribe Boulengerochromini to accommodate it. The origin of the modern Haplochromini (sensu Salzburger et al. 2005) can ultimately be traced to Lake Tanganyika cichlids, although their diversification occurred in riverine habitats (Salzburger et al. 2005). Yet, within the framework of Lake Tanganyika cichlid systematics, the tribus Haplochromini has always been a mixed bag. Takahashi (2003) only retained two genera within the Haplochromini represented in Lake Tanganyika: Astatoreochromis Pellegrin 1904 and Astatotilapia Pellegrin 1904, although a third, Pseudocrenilabrus Fowler 1934, is present in adjacent systems. Astatoreochromis and Pseudocrenilabrus consist of primitive riverine haplochromine cichlids, whereas the Tanganyika representative of Astatotilapia, A. burtoni (Günther 1894), is more closely related to the Haplochromis Hilgendorf 1888 species of the hyperdiverse Lake Victoria superflock. Yet, Haplochromini sensu Takahashi (2003) are still polyphyletic as Tropheini are considered a separate tribe. This tribe originated from an early Haplochromine invasion event, and it forms the sister group to all other modern Haplochromini (sensu Salzburger et al. 2005), including the Tanganyika basin haplochromine Astatotilapia burtoni and the monophyletic (super)flocks of Lakes Victoria and Malawi that contain an estimated 1,800 species (Snoeks 2000). Tropheini have radiated within Lake Tanganyika and nowadays dominate its rocky shores. As A. burtoni is nested deep within the modern Haplochromini, a separate colonisation event that added this species to the Lake’s ichthyofauna was suggested by Genner et al. (2007). Apart from the piscivore B. microlepis, occurring in various Lake Tanganyika habitats, although it is most common in deep sandy habitats (Konings 1998), the aforementioned cichlids are benthic feeders (A. burtoni: Janssens de Bisthoven et al. 1990;
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T. polylepis: Koch et al. 2007; O. tanganicae: Konings 1998) found in the sediment-rich and vegetated areas of Tanganyika’s littoral, including swamps (Poll 1986; Brichard 1989) and river mouths (Eccles 1992). Such shores are in a way atypical to Lake Tanganyika as they are not dominated by endemic cichlids (Van Steenberge et al. 2011). T. polylepis, O. tanganicae and B. microlepis are, in view of their size, attractive fisheries targets (Konings 1998; Écoutin et al. 1994; Sinyinza et al. 2000). Swamp dwellers such as O. tanganicae are the most important species in local subsistence fisheries, providing a source of protein to the poorest of littoral households. B. microlepis is one of Lake Tanganyika’s most popular gamefish, and sport fishing is the main tourist attraction of Nsumbu National park off southern Lake Tanganyika. While it only has a minimal impact on local fish communities, it generates revenues contributing to protection of the park’s terrestrial and lacustrine biodiversity (Sinyinza et al. 2000). Because of international ornamental fish trade, the popular aquarium fish A. burtoni was able to spread into Northern Australia, where breeding populations were observed (Webb 2003; Koehn and MacKenzie 2004). Moreover, incidental introductions of this species also occurred in the Rwandese part of the Nile Basin, where it is very abundant nowadays (De Vos et al. 2001). While O. tanganicae attracts scientific attention in fields for which ‘tilapiines’ in general are seen as suitable target organisms (e.g. Cnaani and Kocher 2008 on sex determination), mostly A. burtoni is recently gaining attention as a model species in, among others, behavioural (Clement et al. 2004; Greenwood and Fernald 2004; Parikh et al. 2006), genomic (Hoegg et al. 2007; Salzburger et al. 2008; Sanetra et al. 2009) and developmental (Heule and Salzburger 2011) research. The entire cichlid family and its Tanganyika representatives in particular are important in evolutionary research (Koblmüller et al. 2008 and references therein). In this framework, the Tanganyika representatives of the above-mentioned tribes occupy an interesting position in terms of phylogeny and biogeography (see above). Additional information can be provided by the fish parasite fauna, with monogenean flatworms as an ideal target for phylogenetic and biogeographical questions, in view of their considerable species diversity and host specificity and of life history traits ensuring a close relationship with their host species. This approach has been exemplified for clariid catfishes by Barson et al. (2010) and advocated for cichlids by Pariselle et al. (2011). Africa recently saw the discovery of numerous monogenean species infecting cichlids (Přikrylová et al. 2009, 2012a; García-Vásquez et al. 2011; Vanhove et al. 2011a, b; Gillardin et al. 2012). By far the most species-rich monogenean genus on African and Levantine cichlids is the ancyrocephalid Cichlidogyrus Paperna 1960. This (probably non-monophyletic: Mendlová et al. 2010, 2012) genus comprises 78 species hitherto described (Pariselle and Euzet 2009; Vanhove et al. 2011b; Gillardin et al. 2012). While its first representatives from Lake Tanganyika were recently reported,
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the genus is best studied in tilapiines and other cichlids from rivers and small water bodies, mainly in western, but also in southern and eastern Africa. This provides the necessary background for comparatively studying the monogenean parasites of Tanganyika cichlids belonging to mostly riverine tribes. It seems a fruitful way to assess the hosts’ special phylogenetic and biogeographic position from a parasitological point of view.
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of ×100 (oil immersion, ×10 ocular) with the software LAS 3.1 and a DFC 425 Leica camera. The numbering of haptoral parts was adopted from ICOPA IV (Euzet and Prost 1981); the terminology follows Pariselle and Euzet (1995) (i.e. ‘uncinuli’ for marginal hooks) and the metrics taken are those from Pariselle et al. (2003) (Fig. 1). Measurements are in micrometers and presented as the average with the range in parentheses. Taxon and author names of fishes follow Froese and Pauly (2011).
Materials and methods Results Host cichlid fish were collected in April 2010 and May 2011 (Democratic Republic of the Congo) using gill nets or purchased from fishermen (see Van Steenberge et al. 2011 and below for location details). They were identified to species level on site by Donatien Muzumani Risasi and Joseph Lushombo Matabaro (Centre de Recherche en Hydrobiologie (CRH), Uvira, Democratic Republic of the Congo) and some ex situ by Gaspard Caporal Banyankimbona (KU Leuven/Royal Museum for Central Africa (RMCA), Tervuren, Belgium). The fish were kept alive in aerated tanks until they were sacrificed and dissected. The right branchial arches (fresh or preserved in 70 % ethanol or 4 % formaldehyde—see Justine et al. 2012) were inspected for parasites under a Wild M5 (field) or Wild M8 (laboratory) stereomicroscope. Monogenea were removed with a dissection needle. They were mounted on a slide under a cover-slip directly in a drop of ammonium picrate glycerine (Malmberg 1957). Host specimens were deposited in the RMCA and in the CRH (Uvira). Some A. burtoni hosts were purchased from a fisherman in April 2008 (Zambia) and identified by Lawrence Makasa (Lake Tanganyika Research Station, Mpulungu, Zambia) and Christian Sturmbauer (Karl-Franzens University of Graz, Austria) and stored in pure ethanol. Pictures and measurements of the hard parts of haptor and male copulatory organ (MCO) were taken based on Gussev (1962) using a Leica DM2500 microscope at a magnification
Fig. 1 Measurements used to study the new Cichlidogyrus spp. DB dorsal transverse bar: h length of dorsal bar auricle, w dorsal bar maximum width, x dorsal bar total length, y distance between auricles. A anchor: a anchor total length, b anchor blade length, c anchor shaft length, d anchor
Following Paperna (1960) and Pariselle et al. (2003), the monogenean species described below belong to Cichlidogyrus Paperna 1960. Generic diagnosis: Ancyrocephalidae. Three pairs of cephalic glands. Two posterior ocellae with crystalline lenses. Two small inconsistent anterior ocellae. Median muscular pharynx. Simple intestinal caeca joined posteriorly. Two pairs of anchors, one dorsal and one ventral. Two transverse bars, one dorsal with two auricles, one ventral curved and articulated. Fourteen uncinuli. Median posterior testis. Vas deferens at right side, not encircling intestinal caecum. Seminal vesicle present (Fig. 8E). One prostatic reservoir. MCO with penis and accessory piece, though the latter is not always present (Vanhove et al. 2011b); auxiliary plate sometimes present. Median pre-testicular ovary. Sub-median vaginal opening. Sclerotised vagina. Seminal receptacle present (Fig. 8E). Gill parasites of African and Levantine Cichlidae, Cyprinodontidae and Nandidae. Cichlidogyrus gillardinae sp. n. Type host: A. burtoni (Günther 1894) (Figs. 2 and 8). Site of infection: gills. Type locality: Nyangara wetland, Uvira, Democratic Republic of the Congo (17 May 2011, 3°20′34″ S, 29°10′43″ E).
guard length, e anchor point length. MA male apparatus: Ap accessory piece length, Pe penis total length, He heel length, U uncinuli length. VB ventral transverse bar: w ventral bar maximum width, x length of one ventral bar branch
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Fig. 2 Hard parts of C. gillardinae sp. n. MA male apparatus: Ap accessory piece, He heel, Pe penis. DB dorsal transverse bar, DA dorsal anchor, VB ventral transverse bar, VA ventral anchor, I–VII uncinuli. Scale bar030 μm
Additional localities: Kalemie fish market, Democratic Republic of the Congo (23 April 2010, 5°54′43″ S, 29°11′ 28″ E); Mpulungu, Zambia (20–21 April 2008, 8°46′1″ S, 31°6′22″) (host fish: MRAC B2.004.P.0001-0026 and B2.004.P.0027-0050). Material studied: 30 individuals. Type material: the holotype has been deposited at the Muséum National d'Histoire Naturelle (Paris) (MNHN HEL262). Paratypes have been deposited at the Muséum National d'Histoire Naturelle (MNHN HEL262-263), at the Natural History Museum (London) (NHMUK 2012.7.26.1) and at the Royal Museum for Central Africa (Tervuren) (MRAC 37697). Etymology: named after biologist Céline Gillardin, science teacher, who participated in the expedition during which most of the samples were obtained, and one of the first people to work on Lake Tanganyika monogeneans. Diagnosis: adults 432 (281–592) long. Dorsal anchor 33 (29–38) long; guard (at 12 (9–16)) about twice as long as shaft of length c05 (4–7); regularly curved blade 23 (19–29) long; point length 7 (5–8). Dorsal transverse bar 33 (27–39) long; greatest width 6 (4–8); slightly arched; auricles 11 (8– 14) long and attached to the ventral surface; distance between auricles 12 (9–15). Ventral anchor 32 (27–37) long; guard length 10 (8–13), hence only slightly longer than shaft of length 6 (4–9); blade 28 (23–32) long; point length 8 (6– 11). V-shaped ventral transverse bar maximally 5 (3–6) wide; branch length 31 (27–35). First and third to seventh uncinuli short (sensu Pariselle and Euzet 2009, i.e. when considered in proportion to the second uncinuli which keep their larval size): pair I—11 (9–13) long, pair II—10 (8–12), pair III—15 (13–17), pair IV—17 (15–21), pair V—22 (19– 24), pair VI—21 (18–26), pair VII—14 (11–17). MCO with curved penis, 47 (42–55) long, of constant diameter, with distinct rounded basal bulb and poorly developed heel of
length 5 (4–7); straight accessory piece 35 (29–42) long, ending in a hook. Remarks: The new species has short uncinuli I and III to VII, a simple accessory piece associated with the curved penis and lacks a sclerotised vagina, as observed in: Cichlidogyrus bifurcatus Paperna 1960, Cichlidogyrus gistelincki Gillardin et al. 2012, Cichlidogyrus longipenis Paperna and Thurston 1969 and Cichlidogyrus rognoni Pariselle et al. 2003. C. gillardinae sp. n. differs from: – –
– –
C. bifurcatus by the shape of the extremity of the accessory piece (simple in C. gillardinae sp. n. versus bifurcated in C. bifurcatus) C. gistelincki by the shape of the extremity of the penis (straight in C. gillardinae sp. n. versus curved backwards in C. gistelincki) and of the accessory piece (simple in C. gillardinae sp. n. versus distal end covered by a pointed cap in C. gistelincki) C. longipenis by the length of the penis (42–55 in C. gillardinae sp. n. versus 63–79 in C. longipenis) and the presence of a developed heel (absent in C. longipenis) C. rognoni by the length of the penis (42–55C. gillardinae sp. n. versus 29–38 in C. rognoni) and the size of the auricles on the transverse dorsal bar (reduced in C. gillardinae sp. n.: 8–14 long versus well-developed and 16–26 long in C. rognoni)
Cichlidogyrus mbirizei sp. n. Type host: O. tanganicae (Günther 1894) (Figs. 3 and 8). Site of infection: gills. Type locality: Kalemie fish market, Democratic Republic of the Congo (23 April 2010, 5°54′43″S, 29°11′28″E) (host fish: MRAC B0.12.P.55-56).
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Fig. 3 Hard parts of C. mbirizei sp. n. MA male apparatus: Ap accessory piece, He heel, Pe penis. DB dorsal transverse bar, DA dorsal anchor, VB ventral transverse bar, VA ventral anchor, I–VII uncinuli, Vg vagina. Scale bar0 30 μm
Additional localities: Mugayo, Democratic Republic of the Congo (11 April 2010, 6°46′51″S, 29°33′42″E) (host fish: MRAC B0.12.P.51-54). Material studied: 25 individuals. Type material: The holotype has been deposited at the Muséum National d'Histoire Naturelle (Paris) (MNHN HEL264). Paratypes have been deposited at the Muséum National d'Histoire Naturelle (MNHN HEL264-265), at the Natural History Museum (London) (NHMUK 2012.7.26.2) and at the Royal Museum for Central Africa (Tervuren) (MRAC 37698). Etymology: named after Joseph Mbirize Ndalozibwa, technician and boat captain in the expedition during which most fish hosts where sampled. Diagnosis: adults 729 (429–1160) long. dorsal anchor 44 (37–50) long; guard of length 14 (9–17), hence longer than shaft of length c03 (2–5); blade 36 (32–42) long, regularly curved; point 12 (7–14) long. Clearly arched dorsal transverse bar of length 32 (26–44) and greatest width 7 (6–11); large auricles 15 (12–19) long and attached to ventral surface of the bar, distance between auricles 13 (9–18). Ventral anchor 46 (40–52) long; guard of length 13 (9–16), hence longer than shaft of length 3 (2–5); blade 41 (36–47) long; point length 13 (11–18). Ventral transverse bar with branches more or less straight and 32 (24–40) long; greatest width 6 (4–9). First and third to seventh uncinuli short (see above): pair I—13 (12–15) long, pair II—11 (10–12), pair III—16 (11–19), pair IV—19 (15–23), pair V—22 (19–26), pair VI—20 (18–25), pair VII—16 (14–21). MCO with very long (180 (149–204)) and thin penis and distinct heel of length 10 (7–21); rather straight accessory piece 28 (24–32) long, attached to the basal bulb of the penis, ending in rounded outgrowths. Very long, thin and spirally coiled vagina (double pitch); no valuable length measurement could be taken.
Remarks: The new species has a long, thin, non-spirally coiled penis, such as Cichlidogyrus arthracanthus Paperna 1960, Cichlidogyrus bychowskii (Markevich 1934) Paperna 1960, Cichlidogyrus cirratus Paperna 1964, Cichlidogyrus inconsultans Birgi and Lambert 1986 and Cichlidogyrus nandidae Birgi and Lambert 1986. It can be distinguished from all these species (except C. cirratus) in having short uncinuli I (which are long in the other species). C. mbirizei sp. n. is easily distinguished from C. cirratus by the shape of the accessory piece of the MCO: absence of a long expansion at mid-length (versus presence in C. cirratus) and of a hook at the distal extremity (versus rounded outgrowths in C. cirratus). Also, the shape of the vagina (spirally coiled (double pitch) in C. mbirizei sp. n. versus sinuous in C. cirratus) is distinctive. Cichlidogyrus mulimbwai sp. n. Type host: T. polylepis (Boulenger 1900) (Figs. 4 and 8). Site of infection: gills. Type locality: Mulembwe, Democratic Republic of the Congo (9 April 2010, 6°07′10″S, 29°16′18″E) (host fish: MRAC B0.12.P.0075-0078). Additional locality: Moba, Democratic Republic of the Congo (14 April 2010, 7°02′30″S, 29°46′28″E). Material studied: 12 individuals. Type material: The holotype has been deposited at the Muséum National d'Histoire Naturelle (Paris) (MNHN HEL266). Paratypes have been deposited at the Muséum National d'Histoire Naturelle (MNHN HEL266-267) and at the Royal Museum for Central Africa (Tervuren) (MRAC 37701). Etymology: named after biologist Théophile Mulimbwa N’sibula, scientific director of the CRH (Uvira) who participated in the expedition during which most fish hosts were sampled.
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Fig. 4 Hard parts of C. mulimbwai sp. n. MA male apparatus: Ap accessory piece, He heel, Pe penis. DB dorsal transverse bar, DA dorsal anchor, VB ventral transverse bar, VA ventral anchor, I–VII uncinuli. Scale bar030 μm
Diagnosis: adults 796 (666–1042) long. Dorsal anchor 36 (32–42) long; guard three times longer than shaft (guard length 12 (10–15) versus shaft length 4 (3–5)); regularly curved blade of length 29 (25–34); point 10 (9–12) long. Large dorsal transverse bar of length 44 (38–52) and greatest width 6 (5–7); small auricles, 7 (6–9) long, located on anterior convex side of bar; distance between auricles 11 (9– 12). Ventral anchor 35 (31–40) long; guard two times as long as shaft (guard length 10 (7–13) versus shaft length 5 (4–6)); blade 32 (28–35) long; point 10 (9–12) long. Thin Vshaped ventral transverse bar with long straight branches of length 37 (33–44) and maximal width 5 (4–6); extremities sharply curved. First uncinuli and pairs III to VII short (see above): pair I—15 (13–16), pair II—12 (11–13), pair III— 18 (17–19), pair IV—19 (18–21), pair V—22 (20–23), pair VI—19 (17–21), pair VII—17 (16–20). Short penis of length 41 (35–46), slightly spiralled, ending in a sharp extremity distal to the aperture. Long heel of length 9 (8– 13). Accessory piece 36 (31–40) long, not linked to the penis, pierced by the copulatory tube. Remarks: This new species resembles its three congeners already described from Tylochromis Regan 1920 hosts (Cichlidogyrus berrebi Pariselle and Euzet 1994, Cichlidogyrus kothiasi Pariselle and Euzet 1994 and Cichlidogyrus pouyaudi Pariselle and Euzet 1994) in having small auricles of the dorsal transverse bar (‘two small, hollow outgrowths on the anterior convex face’: Pariselle and Euzet 1994) and a spirally coiled penis. Moreover, the accessory piece of the MCO is not connected to the base of the penis. This phenomenon is, within Cichlidogyrus spp., unique to the three abovementioned species described from Tylochromis jentinki (Steindachner 1894) (this feature was not explicitly mentioned in the original descriptions).
C. mulimbwai sp. n. can be easily distinguished from all these species in having its penis going right through the accessory piece which does not span the penis’ entire length. Cichlidogyrus muzumanii sp. n. Type host: T. polylepis (Boulenger 1900) (Figs. 5 and 9). Site of infection: gills. Type locality: Mulembwe, Democratic Republic of the Congo (9 April 2010, 6°07′10″S, 29°16′18″E) (host fish: MRAC B0.12.P.0075-0078). Additional locality: Moba, Democratic Republic of the Congo (14 April 2010, 7°02′30″S, 29°46′28″E). Material studied: 17 individuals. Type material: The holotype has been deposited at the Muséum National d'Histoire Naturelle (Paris) (MNHN HEL268). Paratypes have been deposited at the Muséum National d'Histoire Naturelle (MNHN HEL268-269) and at the Royal Museum for Central Africa (Tervuren) (MRAC 37699). Etymology: named after biologist Donatien Muzumani Risasi (Democratic Republic of the Congo), researcher from the CRH (Uvira) who participated in the expedition during which most of the fish hosts were sampled and who identified many of the fish hosts. Diagnosis: adults 516 (321–608) long. Dorsal anchor 51 (44–58) long; guard of length 18 (14–22) three times longer than shaft of length 6 (4–8); regularly curved blade of length 36 (30–40); point 10 (9–12) long. Dorsal transverse bar 54 (45–62) long and maximally 9 (7–14) wide, with rounded extremities and small auricles (14 (10–19) long) on its anterior convex side; distance between auricles 17 (13– 21). Ventral anchor 42 (37–47) long, smaller than dorsal, with guard (length 6 (4–9)) slightly longer than shaft (length
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Fig. 5 Hard parts of C. muzumanii sp. n. MA male apparatus: Ap accessory piece, He heel, Pe penis. DB dorsal transverse bar, DA dorsal anchor, VB ventral transverse bar, VA ventral anchor, I–VII uncinuli. Scale bar030 μm
4 (3–6)); blade 41 (35–46) long; point 11 (9–13) long. Thick ventral transverse bar attains greatest width of 8 (5–10) at mid-length of branches; branches 53 (47–63) long, slightly curved at the extremities. First uncinuli large and III to VII equal in size and short (see above): pair I—24 (20–27), pair II—12 (12–13), pair III–VII—21 (18–24). MCO composed of a penis 63 (57–68) long, starting in a considerable bulb, with broad and thick-walled spirally coiled tube, not very prominent heel of length 5 (4–7) and an accessory piece 19 (17–20) long, not attached to the penis. Remarks: Once again, this new species from Tylochromis possesses reduced auricles on the anterior surface of the dorsal transverse bar, a spiralling tubular penis and an accessory piece not linked to the base of the penis (features characteristic of Cichlidogyrus spp. from Tylochromis spp.). Fig. 6 Hard parts of Cichlidogyrus sp. ‘T. polylepis 3’. MA male apparatus: Ap accessory piece, He heel, Pe penis. DB dorsal transverse bar, DA dorsal anchor, VB ventral transverse bar, VA ventral anchor, I–VII uncinuli, Vg vagina. Scale bar030 μm
C. muzumanii sp. n. differs from all other species found on Tylochromis hosts in having a reduced accessory piece, not encircling the penis nor pierced by the penis. A single specimen was recovered from a species closely resembling C. muzumanii sp. n., differing in: – – – – –
A bigger accessory piece, including a rather fine portion A clearly visible sclerotised vagina A shorter and less spiralling penis Smaller haptoral anchors and transverse bars Relatively smaller first uncinuli (see above), in contrast to the well-developed first pair in C. muzumanii sp. n. and C. kothiasi
For want of a sufficient number of specimens, no formal description is provided of this species, hereafter referred to as C. sp. ‘T. polylepis 3’ (Figs. 6 and 9).
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Cichlidogyrus nshomboi sp. n. Type host: B. microlepis (Boulenger 1899) (Fig. 7 and 9). Site of infection: gills. Type locality: Mulembwe, Democratic Republic of the Congo (9 April 2010, 6°07′10″S, 29°16′18″E) (host fish: MRAC B0.12.P.0072). Material studied: 24 individuals. Type material: The holotype has been deposited at the Muséum National d′Histoire Naturelle (Paris) (MNHN HEL270). Paratypes have been deposited at the Muséum National d'Histoire Naturelle (MNHN HEL270-271), at the Natural History Museum (London) (NHMUK 2012.7.26.3) and at the Royal Museum for Central Africa (Tervuren) (MRAC 37700). Etymology: named after biologist Dr. Venant Nshombo Muderhwa, general manager of the CRH (Uvira) and involved as senior scientist in the organisation of the expedition yielding most of the host fish for this study. Diagnosis: adults 613 (428–928) long. Dorsal anchor 62 (47–70) long; guard (length 20 (12–27)) two and a half times longer than shaft (length 8 (3–12)); regularly curved blade of length 46 (42–54); point 12 (10–15) long. Dorsal transverse bar simple, 59 (49–71) long and at most 11 (9–15) wide; auricles 17 (14–23) long, closely resembling those from Tylochromis parasites (short and attached to the anterior surface of the bar), planted relatively far apart at a distance of 23 (18–30). Ventral anchor 49 (45–54) long; blade length 46 (43– 50); shaft 8 (4–12) and guard 13 (10–16) long; point length 14 (12–17). V-shaped, thick (maximal width 10 (6–14)) and large ventral transverse bar; branches straight and 55 (48–63) long. First pair and pairs III to VII of the uncinuli long and thin (see above): pair I—29 (27–32), pair II—12 (11–12), pair III—24 (22–25), pair IV—25 (23–27), pair V—29 (26–31), pair VI—27 Fig. 7 Hard parts of C. nshomboi sp. n. MA male apparatus: Ap accessory piece, He heel, Pe penis. DB dorsal transverse bar, DA dorsal anchor, VB ventral transverse bar, VA ventral anchor, I–VII uncinuli. Scale bar030 μm
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(25–30), pair VII—26 (23–28). MCO with short and relatively thin straight penis, 25 (23–28) long, its distal external wall exhibiting a spirally coiled thickening; large basal bulb, very long heel of length 22 (18–25) (nearly as long as the penis); long and straight accessory piece of length 20 (18–23) with a rounded expansion near its distal extremity. Remarks: This new species is very reminiscent of Cichlidogyrus centesimus Vanhove et al. 2011b in having (1) a very long heel, (2) a short and straight penis with its distal external wall marked with a spirally coiled thickening and (3) short auricles attached to the anterior surface of the dorsal transverse bar (a feature not mentioned in the original description of C. centesimus). There are, however, differences in haptoral hard part morphology: C. centesimus is unique within Cichlidogyrus in having large uncinuli I and long uncinuli III to VII, whereas the latter are medium in size and length in C. nshomboi sp. n. Apart from this different relative uncinuli size, C. nshomboi sp. n. is easily distinguished from C. centesimus by the presence of an accessory piece (which is lacking in C. centesimus) associated with the penis in the MCO. Other monogenean species were recovered during our survey, from: –
–
O. tanganicae (MRAC B0.12.P.55-56): Cichlidogyrus halli (Price and Kirk 1967) (new host and locality (Kalemie)); Scutogyrus gravivaginus (Paperna and Thurston 1969) (new host and locality (Kalemie)) O. niloticus: C. halli (new locality (Nyangara wetland)); Cichlidogyrus sclerosus Paperna and Thurston 1969 (new locality (Nyangara wetland)) and Cichlidogyrus thurstonae Ergens 1981 (new locality (Nyangara wetland)). These species are often reported from this host species in various parts of Africa (see Pariselle and
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Euzet 2009; Akoll et al. 2012) and introduced with their host in South America (Cohen and Kohn 2008) and Asia (Ferdousi and Chandra 2002 (see comments in Pariselle and Euzet 2009); Wu et al. 2007).
Discussion The Cichlidogyrus fauna is reported of the oreochromines O. niloticus and O. tanganicae, of Lake Tanganyika’s only tylochromine T. polylepis, of the boulengerochromine B. microlepis and of the haplochromine A. burtoni, proposing five species new to science. This is the first mention of helminth parasites of the Tanganyika endemics among them (i.e. all but Fig. 8 Micrographs of the hard parts of newly described Cichlidogyrus species. A C. gillardinae sp. n.: haptor. B C. gillardinae sp. n.: MCO. C C. mbirizei sp. n.: haptor. D C. mbirizei sp. n.: vagina. E C. mbirizei sp. n.: MCO. F C. mulimbwai sp. n.: haptor. G C. mulimbwai sp. n.: MCO
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O. niloticus), except for the quadrigyrid acanthocephalan Acanthogyrus (Acanthosentis) tilapiae (Baylis 1948) reported from O. tanganicae by Prudhoe (1951). The same fish species harbours the ergasilid copepods Ergasilus kandti van Douwe 1912 and Ergasilus flaccidus Fryer 1965, as well as the argulid branchiuran Argulus striatus Cunnington 1913 (Fryer 1965). The host species under study are of economic importance in fisheries and the ornamental fish sector (see above). Moreover, their phylogenetic position within Cichlidae renders them of scientific interest (late colonization of Lake Tanganyika by Oreochromini and Tylochromini, questioned origin of Boulengerochromini, cradle function of the lake and multiple recolonisation in Haplochromini). What does their Cichlidogyrus gill parasite fauna tell us in this respect?
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C. muzumanii sp. n., C. mulimbwai sp. n. and C. sp. ‘T. polylepis 3’ show clear morphological affinities with the Cichlidogyrus fauna hitherto known from Tylochromis cichlids in possessing a dorsal transverse bar with small auricles and an MCO with spiralling tubular penis and without connection between accessory piece and the base of the penis. The only species retrieved from O. tanganicae, C. mbirizei sp. n., compares to congeners parasitising cichlids belonging to Tristramella Trewavas 1942 and Tilapia Smith 1840 (C. arthracanthus), Hemichromis Peters 1857 (C. bychowskii), Sarotherodon Rüppell 1852 (C. bychowskii and C. cirratus) and Oreochromis Günther 1889 (C. cirratus) and the nandid Polycentropsis abbreviata Boulenger 1901 (Pariselle and Euzet 2009). While the evolutionary position of Cichlidogyrus Fig. 9 Micrographs of the hard parts of newly described Cichlidogyrus species. A C. muzumanii sp. n.: haptor. B C. muzumanii sp. n.: MCO. CC. ‘T. polylepis 3’: haptor. D C. ‘T. polylepis 3’: vagina. E C. ‘T. polylepis 3’: MCO. F C. nshomboi sp. n.: haptor. G C. nshomboi sp. n.: MCO
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species infecting nandid fishes is unknown, it is remarkable that the other host genera are all cichlids belonging to the ‘primitive’ tribes Hemichromini and Tilapiini. It should be noted, however, that the latter tribe has recently been split in view of its paraphyly with regard to the East African cichlid radiations by Schwarzer et al. (2009), classifying the aforementioned ‘tilapiines’ under Oreochromini and Boreotilapiini. In any case, it appears that both Tylochromini and Oreochromini, a meagre number of which have colonised Lake Tanganyika at a relatively late stage, have retained a Cichlidogyrus parasite fauna reminiscent to that of the respective primarily riverine cichlid tribes/genera (Figs. 8 and 9). Conversely, C. gillardinae sp. n., in the configuration of its haptoral uncinuli, the lack of a sclerotised vagina and the
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structure of its MCO, is comparable to C. bifurcatus (known from different Haplochromini s.l. species and Oreochromis aureus (Steindachner 1864)), C. rognoni (known from O. niloticus), C. longipenis (from Astatoreochromis alluaudi Pellegrin 1904) and C. gistelincki from the tropheine ‘Ctenochromis’ horei (Günther 1894). With this species as well as with the Tropheini parasites Cichlidogyrus steenbergei Gillardin, Vanhove, Pariselle, Huyse and Volckaert 2012 and Cichlidogyrus irenae Gillardin et al. 2012, it also shares small uncinuli, an asymmetry between dorsal and ventral anchors, and well-developed, albeit normal-sized dorsal bar auricles. Except for C. rognoni, these are all parasites of cichlids belonging to the Haplochromini s.l. (Pariselle and Euzet 2009). Although we could conclude that several representatives of the Tropheini and other haplochromine cichlids hence yield similar parasites as A. burtoni, the oreochromine host records of C. rognoni and C. bifurcatus form an important exception here. The limited information available suggests that haptor configuration (on the scale of larger lineages) and genital structure (on the scale of closely related species) are systematically informative (Pouyaud et al. 2006) but do not necessarily reflect host choice (Vignon et al. 2011). Indeed, representatives from various Cichlidogyrus lineages seem to infect hosts within Haplochromini s.l. (Gillardin et al. 2012). As genetic data are missing for most Cichlidogyrus spp., it cannot be inferred at present whether these patterns stem from host-switching events or whether the morphological similarities result from convergent evolution. At the very least, both C. gillardinae sp. n. and C. mbirizei sp. n., as well as the species retrieved on T. polylepis, represent Cichlidogyrus morphotypes previously observed in the respective cichlid tribes and widely found in African riverine systems. Their hosts being secondary invaders of Lake Tanganyika that occur in atypical habitats, not dominated by endemic cichlids, it is not surprising that their gill parasite community shows no proof of typical Tanganyika elements. This cannot be said of C. nshomboi sp. n. The spirally coiled wall of the penis of this species reminds of C. centesimus, found on Ophthalmotilapia Pellegrin 1904, belonging to the endemic Lake Tanganyika tribe Ectodini. A similar structure was found in yet undescribed congeners infecting other Ectodini, as well as Perissodini and Bathybatini (nobis). Within Cichlidogyrus, this feature hence seems to be unique to Lake Tanganyika (while also observed in Thaparocleidus Jain 1952 parasites of Eurasian siluriforms (Pariselle et al. 2001)). While the host of C. nshomboi sp. n., the boulengerochromine B. microlepis, colonised the lake independently from O. tanganicae, the timing of this event is undetermined (Salzburger et al. 2002). Recent findings did, however, identify B. microlepis as a primitive member of the clade containing the East African radiations, which are all grouped within the Austrotilapiini (Schwarzer et al. 2009), supporting its placement in a separate tribe, outside the Tilapiini, by Takahashi
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(2003). Whether the fish originated in Lake Tanganyika or not, it is clear that it harbours a parasite lineage typical and apparently endemic to the Lake. The unusual MCO morphology of C. nshomboi sp. n. serves as an additional argument against considering B. microlepis a tilapiine cichlid. More intensive Cichlidogyrus sampling in Lake Tanganyika and its tributaries is needed to infer the phylogenetic relationship between the parasite fauna of riverine and lacustrine cichlids and the events giving rise to the parasite communities observed. A comparison with genetic analyses is recommended (for an example on catfishes, see Přikrylová et al. 2012b). It can at present not be invoked which morphological character states are to be considered ancestral—though the ‘simple’ features of the Cichlidogyrus spp. on Tylochromis might reflect their hosts’ primitive position within African cichlids. In view of the current results, a combination of colonisation within or from Lake Tanganyika together with the presence of ‘ancient’ lineages seems likely, not unlike suggested for the host cichlids, or for the gyrodactylid monogenean Gyrodactylus von Nordmann 1832 from Lake Tanganyika (Vanhove et al. 2011a). Acknowledgments T. Huyse, F.A.M. Volckaert, J.A.M. Raeymaekers (KU Leuven), J. Snoeks, G. Caporal Banyankimbona (KU Leuven/ RMCA), C. Sturmbauer (Karl-Franzens University of Graz, Austria), C. Gillardin (ZAVO), L. Makasa (Lake Tanganyika Research Station, Mpulungu, Zambia), V. Nshombo Muderhwa, T. Mulimbwa N’sibula, D. Muzumani Risasi, J. Mbirize Ndalozibwa, V. Lumami Kapepula and J. Lushombo Matabaro (CRH, Uvira, Democratic Republic of the Congo) are gratefully acknowledged for scientific and logistical contributions to this work. M.P.M.V. and M.V.S. are Ph.D. fellows of the Research Foundation—Flanders (FWO—Vlaanderen). Fieldwork was partly funded by two travel grants from the Research Foundation—Flanders (to M.P.M.V.) and two from the King Leopold III Fund for Nature Conservation and Exploration (to M.P.M.V. and M.V.S.). F.M.B. received financial support from IRD (BEST) for a training session in France, during which this manuscript was elaborated.
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