Taxonomic study of Barbus neumayeri and Barbus pellegrini from the Lake Kivu-Lake Edward region, East Africa

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1 Taxonomic study of Barbus neumayeri and Barbus pellegrini from the Lake Kivu-Lake Edward region, East Africa Chrisestom Mwatete Mlewa* Department of Biological Sciences, Pwani University College, P. O. Box 195, Kilifi, Kenya Abstract The taxonomy of the two established barbus species: Barbus neumayeri and Barbus pellegrini has presented problems due to their close relationship and pronounced character variation within and between their populations. In this study, morphomeristic methods were used to investigate Barbus specimens from several populations in the Lake Kivu Lake Edward area. Meristic and morphometric data on specimens in the RMAC collection from lakes Kivu and Edward, and the Nyabarongo and Mpanga river systems were analysed using principal component analysis in the PAST software programme. The results revealed additional morphomeristic characters useful in distinguishing the two closely related barbus species; hence, both B. pellegrini and B. neumayeri are redescribed incorporating additional characters to their respective original descriptions. Specimens from Nyabarongo river system were significantly different to warrant recognition as new species; thus, a new species B. new species is proposed and described. Meristically, the B. new species and the two established species are distinguished by lateral line scale counts; while predorsal length, head length and body depth at operculum, expressed as percentage of standard length, are the most diagnostic morphometric characters. Key words: barbus, Morphomeristics, Mpanga river, new species, Nyabarongo river system, principal component analysis Resume La taxonomie de deux especes reconnues de Barbus, Barbus neumayeri et Barbus pellegrini, pose un probleme en raison de leur proche parente et de variations tres marquees de caracteres au sein d une m^eme population et entre *Correspondence: m.mwatete@pwaniuniversity.ac.ke, mlewa2001@yahoo.com populations. Dans cette etude, nous avons utilise des methodes morphomeristiques pour etudier des specimens de Barbus issus de differentes populations de la region des lacs Kivu et Edouard. Des donnees meristiques et morphometriques obtenues sur des specimens de la collection du MRAC venant des lacs Kivu et Edouard et des systemes hydrographiques des rivieres Nyabarongo et Mpanga ont ete etudiees au moyen de l analyse en composante principale du programme PAST. Les resultats ont revele des caracteres morphomeristiques supplementaires utiles pour distinguer les deux especes de Barbus tres proches l une de l autre, et B. pellegrini et B. neumayeri sont donc decrits de nouveau en integrant les nouveaux caracteres a leur description originale respective. Les specimens du systeme hydrographique de la riviere Nyabarongo etaient significativement differents au point d inciter a les reconna^ıtre en tant que nouvelle espece; c est pourquoi une nouvelle espece de Barbus nouv. esp. est ici proposee et decrite. Au point de vue meristique, la nouvelle espece de Barbus nouv. esp. et les deux especes reconnues se differencient par le nombre d ecailles de la ligne laterale, alors que la longueur predorsale, la longueur de la t^ete et l epaisseur du corps au niveau des branchies, exprimees en pourcentage de longueur standard, sont les principaux caracteres morphometriques du diagnostic. Introduction The two species: Barbus neumayeri Fischer 1884 and Barbus pellegrini Poll 1839 (Teleostei, Cyprinidae) are closely related (Greenwood, 1962), and their taxonomy has presented problems due to their widely recognized character variation within and between populations. In his taxonomic review of some Barbus species from east, central and southern Africa, Greenwood (1962) synonymized 8 300

2 Morphomeristic study of Barbus species from Lake Kivu and Edward areas 301 nominal species with B. neumayeri, which thus had a wide distribution in east Africa ranging from coastal streams and lakes of Kenya and Tanzania to Lake Edward and Albert in Uganda and streams and rivers flowing into Lake Victoria. The species was later reported to occur in streams and lakes in Rwanda and Burundi (de Vos & Thys van den Audenaerde, 1990). Barbus pellegrini has a relatively much less extensive range, occurring in the lakes and affluents of the central African Rift valley from Lake Albert southwards to lakes Kivu, Tanganyika and Rukwa (Seegers, 1996). However, the natural ranges of the two species clearly suggest overlap and possibilities of sympatric populations and hybridization cannot be ruled out. This study is a morpho-meristic investigation of specimens from the Lake Kivu-Lake Edward area aimed to establish whether the two Barbus species have disjunct or overlapping distribution affecting their taxonomy. Lake Edward and Lake Kivu are found on the floor of the western arm of the East African Rift Valley. The two lakes are intricately linked to other African Great Rift Valley lakes such as Lake Albert, Lake George and Lake Tanganyika (Snoeks, de Vos & Thys van den Audenaerde, 1997). Lake Edward has a northern location on the border of Democratic Republic of Congo and Uganda, whereas Lake Kivu is on the border of Democratic Republic of Congo and Rwanda to the south. Unlike most rift valley lakes which are endorheic, both Lake Edward and Lake Kivu have surface outflows of water. Lake Edward flows into to Lake Albert in the north via the Semliki River, whereas Lake Kivu flows into the River Ruzizi which flows southwards into Lake Tanganyika. Snoeks, de Vos & Thys van den Audenaerde (1997) have described the ichthyogeography of Lake Kivu and mention Barbus species among its ichthyofauna. The River Mpanga flows from the Ruwenzori mountains and empties into Lake George which is connected to Lake Edward via the Kazinga Channel, thus is part of the western rift valley lakes. Originating from the Nyungwe forest in Rwanda, the Nyabarongo River flows southwards becoming a tributary of River Kagera that flows into Lake Victoria; hence is considered part of the headwaters of Nile River system. Materials and methods Materials The material examined in this study is housed at the Royal Museum of Central Africa (RMCA) at Tervuren, Belgium. In addition, the lectoype for B. pellegrini (MNHN ) from the species type locality (i.e. Kadjudju, L. Kivu) was examined. Meristic counts Simple (unbranched) and branched fin rays on the dorsal, pectoral, ventral and anal fins. Lateral line scales (LS) up to base of caudal fin, and between the posterior edge of the occipital and the origin of the dorsal fin (OdS). Scale rows between lateral line and dorsal fin (LdS); lateral line and ventral fins, and around the caudal peduncle (CpS). Morphometric measurements Point to point measurements were taken on 18 characters to the nearest 0.1 mm using Dial Calipers as follows: standard length (SL) from the anterior end (rostral tip) of snout to caudal fin base, head length (HL) from the rostral tip to bony caudal margin of operculum, cheek length from the rostral tip to bony caudal margin of preoperculum, eye diameter horizontal diameter of orbit, interorbital width the least distance between the bony margins of interorbital space, occipital length from the rostral tip to the caudal end of the skull, predorsal length (PdL) from rostral tip to the origin of dorsal fin as in Fig. 1 of de Vos & Thys van den Audenaerde (1990), prepectoral length (PpL) from rostral tip to origin of pectoral fin, preventral length from rostral tip to origin of ventral (pelvic) fin, preanal length (PaL) from rostral tip to the origin of anal fin, PC PC 1 Fig 1 Plot of the individual scores on PC1 and PC2 on metrics as per cent of standard length of barbus specimens from L. Edward (open squares), Lake Kivu (stars), Nyabarongo river (open circles) and Mpanga River (solid squares)

3 302 Chrisestom Mwatete Mlewa dorsal fin base (DfB) distance between the origin and caudal edge of dorsal fin, anal fin base (AfB) distance between origin and caudal edge of anal fin, body depth at operculum (BdO) vertical distance of body taken at the caudal edge of the operculum, body depth at dorsal fin (BdD) vertical distance of the body taken at the OdS, caudal peduncle depth at anal vertical distance of the body taken at the posterior edge of anal fin, minimum caudal peduncle depth (CdM) the least vertical distance of caudal peduncle, caudal peduncle length (CpL) distance from posterior edge of anal fin to caudal fin base. Analyses Data were explored using Principal Component Analysis (PCA) on raw metrics and all measurements (as percentage of SL) using the variance-covariance matrix to calculate the factor loadings and scores (Hammer, Harper & Ryan, 2001). The PCA was used here as an exploratory model-free and distribution free for multivariate data (Marcus, 1990). The nonparametric Mann Whitney U-test was used for univariate comparisons to evaluate differences between groups. All analyses were carried out in PAST (PAlaeontological STatistics, version 1.67: folk.uio.no/ohammer/past). Results A total of 74 specimens were examined including 38 identified as B. pellegrini, 25 identified as B. neumayeri in the RMAC collection; 10 specimens, donated by Dr. Lauren Chapman and tentatively identified as B. neumayeri from the Mpanga river drainage in Uganda; and the lectotype of B. pellegrini from the MNHN, Paris. Summaries of meristics and morphometric measurements taken on the specimens and used in the PCA analyses are shown in Tables 1 and 2. Morphometris For the initial PCA analysis, specimens were grouped into four geographical areas according to the major drainage basins of the localities they were captured. These geographical areas are the Lake Edward drainange, the Lake Kivu drainage, the Nyabarongo river system in Rwanda and the Mpanga River system in Uganda. Thus, only 40 of all the specimens examined were used in the detailed morphometric analyses. The PCA results show clear separation between the Lake Edward and Lake Kivu specimens in the negative part of the first principal component, while Nyabarongo and Mpanga river specimens were on the positive part (Fig. 1). The factor loadings in Table 3 show that the first principal component is defined mainly by PdL, HL and BdO. Whereas there is no clear separation of the polygons for the Lake Kivu and Lake Edward specimens, those from the Nybarongo and Mpanga river systems were clearly separated on the second principal component, which is mainly defined by body depth, PpL and PaL (Table 3). A subsequent PCA on the Lake Kivu and Lake Edward specimens did not result in separated polygons. When measurements of the type specimen (lectotype) were included, the PCA showed it was among the Lake Kivu specimens. For all Mann Whitney U-tests on measurements, only specimens of similar length were used so as to reduce size related bias between samples. Thus, the specimens used in the analyses ranged from (Lake Edward), (Lake Kivu), (Mpanga river) and Table 1 Meristic characters of specimens examined from various geographical areas. Frequencies are in parenthesis Character Lake Edward & Lake Kivu n = 18 Nyabarongo n = 12 Mpanga River Predorsal scales (median 11) (median 12) (median 11) Dorsal fin formula III 7 (f17), III 8 (1) III 7 (12) III 7 (12) Pectoral fin formula I 13 (2), I 14 (12), I 15 (4) I 12 (7), I 13 (3), I 14(2) I 13 (2), I 14 (7) Ventral fin formula I 7 (4), I 8 (14) I 7 (6), I 8 (6) I 7 (3), I 8 (6) Anal fin formula I 5 (1), II 5 (17) II 5 (12) II 5 (9) Lateral line scales (median 27) (median 24) (median 28) Lateral-dorsal scales 5.5 (18) 4.5 (1), 5.5(11) 5.5 (9) Lateral-ventral scales 3.5 (14), 4 (2), 4.5 (1), 5 (1) 3.5 (12) 3.5 (9) Caudal peduncle scales (1), 12 (12) 12

4 Morphomeristic study of Barbus species from Lake Kivu and Edward areas 303 Table 2 Morphometric measurements of specimens examined from various geographical areas. Standard deviation in parenthesis Lake Edward n = 11 Lake Kivu n = 6 Nyabarongo River n = 10 Mpanga River Mean (SD) Range Mean (SD) Range Mean (SD) Range Mean (SD) Range Standard length (SL) in mm 60.2 (10.2) (11.8) (7.2) (9.2) Head length%sl 25.4 (0.5) (1.0) (0.9) (1.0) Predorsal length%sl 52.9 (1.2) (0.8) (1.5) (1.0) Prepectoral length%sl 26.9 (1.2) (1.3) (1.0) (0.8) Preventral length%sl 49.5 (1.2) (1.4) (1.0) (1.0) Preanal length%sl 70.9 (1.8) (1.6) (1.2) (0.7) Dorsal fin base%sl 12.8 (1.8) (0.6) (1.1) (0.4) Anal fin base%sl 8.4 (0.6) (1.1) (0.6) (0.5) Body depth at 22.6 (0.7) (0.7) (1.2) (0.6) operculum%sl Body depth at dorsal 27.1 (1.8) (0.8) (1.6) (1.5) fin%sl Caudal peduncle depth 14.7(0.5) (1.2) (0.8) (0.6) (anal)%sl Caudal peduncle 12.8 (0.6) (0.7) (0.7) (0.5) depth (min.)%sl Caudal peduncle 21.7 (1.0) (1.8) (1.3) (0.8) length%hl Head length (HL) in mm 15.3 (2.5) (2.6) (3.1) (1.7) Snout length%hl 29.2 (1.2) (2.2) (1.9) (1.0) Cheek length%hl 70.9 (1.2) (2.2) (1.7) (1.5) Eye diameter%hl 29.4 (1.1) (2.7) (1.4) (1.5) Interorbital width%hl 34.7 (1.9) (1.2) (1.4) (1.6) Occipital length%hl 74.4 (2.6) (2.1) (2.8) (3.2) (Nyabarongo). The Mann Whitney U-test results showed that Lake Edward and Lake Kivu populations were relatively similar in their morphometry showing no significant differences in only two of the 17 characters examined in this study (Table 4). Both these populations however showed significant differences when compared to specimens from Nyabarongo and Mpanga River systems (P < to P < 0.005). Lake Edward specimens differed significantly in nine and eight metrics when compared to Mpanga and Nyabarongo specimens, respectively. Lake Kivu specimens had seven significant differences compared with Nyabarongo and eight compared with Mpanga river specimens. The highest character difference observed in this study was between Mpanga and Nyabarongo specimens which differed significantly in eleven characters, of which five (i.e. PdL, PpL BdO, AfB and minimum caudal peduncle depth) were highly significant (P < 0.005). Meristics A first PCA on the raw meristics (excluding invariable ones between groups) of all specimens resulted in a clear separation of Nyabarongo specimens in the negative part of the first principal axis (Fig. 2). Mpanga river specimens are partially separated on the extreme positive side. The factors contributing mostly to variation on both the first and second principal components are lateral line scales, pectoral fin rays and predorsal scales (Table 5). Mann Whitney U-tests showed differences in these characters between Nyabarongo and all other specimens were highly significant (P < 0.001). A subsequent PCA without the Nyabarongo specimens resulted in a near complete separation of the Mpanga river specimens on the first principal component defined mostly by the number of lateral scales. A Mann Whitney test showed highly significant difference (P = ) in

5 304 Chrisestom Mwatete Mlewa lateral line scales between the Mpanga river and both L. Kivu and L. Edward. All other meristics were not significantly different (P > 0.05). Table 3 Loadings of the per cent standard length metrics on the first and second principal components of Lake Edward (n = 12), Lake Kivu (n = 6), Nyabarongo (n = 12) and Mpanga river () specimens examined. Most significant loadings are in bold Discussion Lake Edward and Lake Kivu specimens showed least character variation, differing significantly in only two [i.e. DfB width and CpL (Table 1)]. The PCA on meristics could not separate specimens from lakes Kivu and Edward as well. Lake Kivu is the type locality of B. pellegrini, and there has been no record of B. neumayeri in that lake (Seegers, 1996). Thus, these differences perhaps reflect PC 1 PC 2 Head length%sl Predorsal length%sl Snout length%hl Cheek length%hl Eye diameter%hl Interorbital width%hl Occipital length%hl Prepectoral length%sl Preventral length%sl Preanal length%sl Dorsal fin base%sl Anal fin base%sl Body depth (operculum)%sl Body depth (dorsal fin)%sl Peduncle depth (anal)%sl Peduncle depth (minimum)%sl Peduncle length%sl PC PC Fig 2 Plot of individual scores on the first and second principal components of raw meristics of all specimens examined in the study. Open circles = Nyabarongo, solid triangles = Lake Kivu, open squares = Lake Edward, solid squares = Mpanga river Table 4 P-values of the Mann Whitney U-test on the morphometric data of the Lake Edward (Ed), Lake Kivu (Kiv), Nyabarongo (Nyb) and Mpanga river populations. NS = not significant Ed v. Kiv n = 11 v. n = 6 Ed v. Mp n = 11 v. Ed v. Nyb n = 11 v. n = 10 Kiv v. Mp n = 6v. Kiv v. Nyb n = 6v.n= 1 Mp v Nyb v. n = 10 Head length %SL NS <0.001 <0.001 <0.005 <0.005 NS Predorsal length %SL NS <0.005 <0.001 <0.05 <0.005 <0.001 Prepectoral length %SL NS <0.001 NS <0.05 NS <0.001 Preventral length %SL NS <0.005 <0.05 <0.05 NS <0.05 Preanal length %SL NS NS NS NS NS NS Dorsal fin base %SL <0.05 <0.05 NS <0.005 <0.05 <0.05 Anal fin base %SL NS <0.05 NS <0.05 NS <0.005 Body depth (operculum) %SL NS <0.005 <0.001 <0.005 <0.005 <0.005 Body depth (dorsal fin) %SL NS NS <0.05 NS <0.005 <0.05 Peduncle depth (anal) %SL NS NS NS NS NS <0.05 Peduncle depth(minimum) %SL NS NS NS NS NS <0.005 Peduncle length %SL <0.05 <0.05 NS NS NS NS Snout length %HL NS NS <0.05 NS NS <0.05 Cheek length %HL NS NS <0.05 NS <0.05 <0.05 Eye diameter %HL NS <0.05 NS <0.05 NS NS Interorbital width %HL NS NS NS NS NS NS Occipital length %HL NS NS <0.005 NS <0.05 NS

6 Morphomeristic study of Barbus species from Lake Kivu and Edward areas 305 Table 5 Loadings of the individual raw meristics on the first and second principal components. The most significant loadings are in bold PC 1 PC 2 Branched dorsal rays Branched pectoral rays Branched ventral rays Lateral line scales Lateral-dorsal scales Lateral-ventral scales Caudal peduncle scales Predorsal scales % variance geographical variation among B. pellegrini population. The little geographical variation in characters between the Lake Kivu and Lake Edward B. pellegrini populations could partly attributed to the fact that until recently the two lakes were linked by the northward flowing Rutshuru river. The clear separation on the first principal component in Fig. 1 likely reflects morphometric differences between the two species with B. pellegrini being in the negative part and B. neumayeri in the positive. These differences were confirmed by the Mann Whitney U-test and are summarized in the species character synopses. The complete separation on the second principal component of the B. neumayeri groups may as well reflect geographical variation in this species. However, Mann Whitney tests showed that their significant character differences were of higher magnitude than those between B. pellegrini in Lake Edward and either of the B. neumayeri groups. On this basis, it appears that each B. neumayeri group warrants recognition as distinct taxon at the species level. Following the synonymization by Greenwood (1962), B. neumayeri comprise a large and morphologically diverse group. Greenwood s work basically expanded the taxon to include specimens with fewer lateral line scales than was originally described for the species [30 31 (Fischer, 1884)]. Thus, as currently described in the literature, B. neumayeri have lateral line scales (Greenwood, 1962; de Vos & Thys van den Audenaerde, 1990). Therefore, based on this meristic, both the Nyabarongo and Mpanga river specimens examined in this study are within this range (Table 1). However, at least two groups that are well separated are clearly evident in PCA of their meristics (Figure 2). One group (the Nyabarongo specimens) has a significantly lower number of lateral line scales (26 or fewer), while the other (the Mpanga specimens) has a higher number (more than 26). The morphometric and meristic differences between the Nyabarongo and Mpanga river specimens revealed in the present study warrant separation at the species level. The question would then be which of the two is the real B. neumayeri? Although I was not able to examine the type specimen (housed in Humberg Museum), Boulenger (1911) in his catalogue of Freshwater Fishes of Africa noted that the type specimen at the Humberg Museum has scales. Thus, on the basis of this, it would be logical that the Mpanga group with the higher number of scales would be the real B. neumayeri. Consequently, a new species status hereby designated B. New species is therefore proposed for the Nyabarongo population whose lateral scale counts are much lower than those reported for the real B. neumayeri. Based on the findings of the present study, the two established species (B. neumayeri and B. Pellegrini) are redescribed as follows: Barbus neumayeri Fischer 1884 (Mpanga specimens): number of lateral line scales to the base of caudal fin (median 27). More posterior location of dorsal fin located along horizontal profile, PdL , HL , and BdO in SL. Barbels generally shorter; with anterior rarely extending beyond mid eye and posterior one usually reaching just beyond the edge of the posterior edge of the eye orbital. Body colour pattern variable. Barbus pellegrini Poll 1939 (Lake Kivu and Lake Edward specimens): number of lateral line scales to the base of caudal fin (median 27). PdL in SL; HL in SL; and Bdo in standard. Barbels generally longer; with the anterior reaching posterior edge of eye orbital (or slightly beyond); and the posterior one usually reaching beyond the preopercle. Body colour pattern variable. It is noteworthy that of the two established species examined in the present study, the B. new species appears more closely related to B. neumayeri. However, in addition to the above distinguishing morphological characters, the B. new species can be distinguished from B. neumayeri as it possesses a narrower AfB ( % SL), longer PpL ( % SL), more elongate (BdD fin ( % SL) and caudal peduncle depth ( % SL). On meristics, the Barbus new species has higher number of lateral line scales (median 28) and pectoral fin rays. A full taxonomic description of the proposed new species is as follows:

7 306 Chrisestom Mwatete Mlewa Barbus new species (Type locality: Nyabarongo drainage): number of lateral line scales to the base of caudal fin (median 28). PdL in SL. A longer and more pointed head, HL , and BdO in SL. Barbels generally longer with anterior one reaching posterior edge of eye orbital (or slightly beyond), while the posterior barbel usually reaching beyond the preopercle. Body colour pattern variable. Conclusion This study has provided additional morpho-meristic characters useful in distinguishing the two established species B. neumayeri and B. pellegrini. Specimens from the Nyabarongo drainage were morpho-meristically different as to warrant recognition as a different species; thus, a new species status B. new species whose type locality would be the Nyabarongo drainage is proposed. Acknowledgements Data in this work were collected during the FishBase and Fish Taxonomy 2007 training course at the Royal Museum of Central Africa (RMCA) through an RMCA scholarship. I am grateful to Dr. Mark Hanssens for guidance on morpho-meristic data analysis and comments on an earlier draft of the manuscript. I acknowledge the assistance of Prof. Jos Snoeks (the Scientist incharge of training) and the Fishbase Scientists, Gert Boden and Tobias Musschoot, for gentle introduction and help in using FishBase. References Boulenger, G.A. (1911) Catalogue of the Fresh-Water Fishes of Africa, Volume 2. Brit. Mus. (Nat. Hist.), London Greenwood, P.H. (1962) A revision of certain Barbus species (Pisces, Cyprinidae) from east Central and South Africa. Bull. Br. Mus. Nat. Hist. (Zool.) 8, Hammer, Ø., Harper, D.A.T. & Ryan, P.D. (2001) PAST Palaeontological Statistics Software Package for Education and Data Analysis. Electronica 4, Palaentol, 9. Marcus, L.F. (1990) Traditional morphometrics. In: Proc. of the Michigan Morphometrics Workshop (Ed. F.J. Rohlf and F.L. Bookstein). Special Publication Number 2. Ann. Arbor, MI: The Mich. Mus. Zool Seegers, L. (1996) The fishes of the Lake Rukwa drainage. Ann. Mus. R. Afr. Centr. Sci.Zool. 278, Snoeks, J., de Vos, L. & Thys van den Audenaerde, D.F.E. (1997) The ichthyogeography of Lake Kivu. S. Afr. J. Sci. 93, de Vos, L. & Thys van den Audenaerde, D.F.E. (1990) Petits Barbus (Pisces, Cyprinidae) du Rwanda. Rev. Hydrobiol. Trop. 23, (Manuscript accepted 02 September 2012) doi: /aje.12074