Description of a New Species in the Pseudotropheus Williamsi Complex

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Copeia,2002(1), pp. 146-151

Description of a New Species in the Pseudotropheuswilliamsi Complex (Teleostei: Cichlidae), from Lake Malawi, Africa

JAY R. STAUFFER JR. AND KAREN A. KELLOGG

A new species of the cichlid genus PseudotropheusRegan (Teleostei: Cichlidae), from Lake Malawiis described. The new species is a member of the Pseudotropheus williamsicomplex from Mbenji Island. Pseudotropheuswilliamsi is the type species of the genus Pseudotropheus,which is a polyphyleticgrouping of several species of rock-dwellingcichlids from Lake Malawi.In addition to the P williamsicomplex, Pseudotropheuscontains species belonging to the P tropheops,P. elongatus,and Pseu- dotropheusaggressive complexes, as well as a group of miscellaneousforms such as Pseudotropheusfainzilberi.We predict that Pseudotropheuseventually will be restricted taxonomicallyto include only members of the williamsicomplex, but because of the lack of phylogeneticdata on manyof the miscellaneousP. forms (e.g., PRfainzilberi) we are currentlyunable to diagnose Pseudotropheusas monophyletic.

FISHES of the family Cichlidae have under- gin of the band of teeth incurved, and with a gone rapid and extensive radiation in the series of teeth on each side behind the band. lakes of East Africa, resulting in as many as 1500 Dorsal XVI-XIX 8-10. anal III 7-9. Scales den- species endemic to Lake Malawi (Stauffer et al., ticulate." 1997). Trewavas (1935) hypothesized that nine The above diagnosis did not distinguish the genera (Cyathochromis,Cynotilapia, Genyochromis, P williamsi complex, as evidenced by the fact Christyella(= Gephyrochromis),Labeotropheus, La- that Regan's new genus also included Melanoch- bidochromis,Melanochromis, Petrotilapia, and Pseu- romis auratus (Boulenger), Metriaclima zebra dotropheus) were more closely related to each (Boulenger), Pseudotropheustropheops tropheops, other than to any other genera found in Lake and Pseudotropheusnovemfasciatus (Regan). Tre- Malawi. Malawian fishermen collectively refer to wavas (1984) redescribed P williamsi and Stauf- this group as mbuna (Fryer and Iles, 1972). fer et al. (1997) diagnosed the complex based Subsequently, Oliver and Loiselle (1972) added on (1) the lack an acutely sloping ethmo-vo- Iodotropheusto this group, and recently Stauffer merine block found in the subgenus Tropheops et al. (1997) delineated Metriaclimafrom Pseu- and the Pseudotropheuselongatus complex; and dotropheus.Both morphologically and genetical- (2) a terminal mouth with a lower jaw that is ly, these 11 genera appear to more closely re- parallel to a line from the hypural plate to the semble each other than other genera that in- tip of the snout (Stauffer et al., 1997). Ribbink habit the lake (e.g., Ribbink et al., 1983; Moran et al. (1983) recognized eight distinct popula- et al., 1994; Albertson et al., 1999). Although to tions of P c.f. williamsi, but P. williamsi is the only date there has been no formal taxonomic rec- described species. The purpose of this paper is ognition of this group, they share the following to describe a new species of the P williamsi com- suite of characters: (1) large number of small plex from Mbenji Island in Lake Malawi. scales in the nape and chest region; (2) reduc- from tion of the left ovary; (3) abrupt transition MATERIALS AND METHODS large flank scales to small chest scales; and (4) possession of true ocelli (Fryer, 1959). Adult fishes were collected by chasing them Pseudotropheus williamsi was originally de- into a monofilament net while SCUBA diving. scribed by Giinther and placed in the genus All measurements were made with dial calipers Chromis.Subsequently, Regan (1922:681) desig- interfaced directly with a computer. External nated it as the type species of Pseudotropheus, counts and measurements followed Barel et al. which he diagnosed as follows: "Jaws with sev- (1977) and Stauffer (1991) except that head eral series of teeth anteriorly, the outer bicus- depth was taken along the vertical through the pid, the inner small and tricuspid, forming rath- posterior edge of the midpoint of the bran- er broad curved or travsverse bands; upper jaw chiostegal. The number of scales in the lateral with a series of conical teeth on each side pos- line series excludes scales in the overlapping teriorly, more or less sharply differentiated, portion of the lower and upper lateral lines; some or all larger than the last bicuspid teeth; pored scales located posterior to the hypural lower jaw short and broad, with the lateral mar- plate were recorded separately. Except for gill

? 2002 by the American Society of Ichthyologists and Herpetologists STAUFFER AND KELLOGG-- NEW SPECIES OF PSEUDOTROPHEUS 147

Fig. 1. Holotype (PSU 3380) of Pseudotropheusgalanos. raker meristics, all counts and measurements R williamsi (102% HL; Table 1). Pseudotropheus were made on the left side. galanos has a larger eye (vertical eye diameter Differences in body shape of 10 individuals of 27.3-32.2% HL) than R williamsi (25.5% HL). the new species and the holotype of P williamsi Similarly, the body depth as reflected in PDPA, were analyzed using sheared principal compo- ADPA, and ADP2 (Table 2) was greater in P nent analysis (SPCA) of the morphometric data williamsi than in R galanos (Table 1). The ho- (Humphries et al., 1981; Bookstein et al., 1985). lotype of P williamsi had three rows of teeth on Meristic data were analyzed using principal the lower jaw and eight dorsal fin rays, whereas component analysis (PCA) of the correlation the mode of the number of teeth rows on the matrix. lower jaw and dorsal fin rays in R galanos was four (40.0%) and nine (50.0%), respectively (Table 3). Pseudotropheusgalanos n. sp. Figure 1 Description.-Jaws isognathous; teeth on jaws in Holotype.-PSU 3380, adult male, 87.4 mm SL, 3-5 rows; majority of teeth in outer rows bicus- Mbenji Island, Lake Malawi, Malawi, Africa, 10 pid; 13 teeth in outer row of left lower jaw of March, 1996. holotype, 11-14 in paratypes. Dorsal fin with 16 spines in the holotype and 16-17 in paratypes; Paratypes.-PSU 3379, 6 (69.9-88.1 mm SL); dorsal fin rays 8-10. Pectoral fin rays 14; anal UMBC (University of Malawi, Bunda College) fin rays 8. Lower pharyngeal bone triangular in 0001, 3 (70.3-83.5 mm SL); data as for holo- outline. Scales along flank ctenoid; holotype type. with 31 lateral line scales, 31-33 in paratypes. First ceratobranchial rakers 9-11, first epibran- Diagnosis.-The absence of an acutely sloped chial rakers 2-3, 1 between epibranchial and ethmo-vomerine block and a lower jaw that is ceratobranchial (Table 3). parallel to a line from the tip of the snout to One-third of lateral dorsal portion of trunk the hypural plate clearly places this species in of males with green ground color and blue the P williamsi complex. The head depth of P highlights; ventral two-thirds blue with orange galanos (88.7-99.4% HL) is smaller than that of highlights; six faint vertical bars; belly white with 148 COPEIA, 2002, NO. 1

TABLE 1. MORPHOMETRIC VALUES OF Pseudotropheus williamsiAND Pseudotropheus galanos. Summary statistics (n = 10) include the holotype.

P williamsi P galanos Standard Counts Holotype Holotype Mean Deviation Range Standardlength, mm 84.8 87.4 80.3 6.6 69.9-88.1 Head length, mm 27.9 30.8 26.9 2.3 23.2-30.8 Percent of standardlength Head length 32.9 35.2 33.6 0.9 32.5-35.2 Snout to dorsal fin origin 36.5 37.2 37.5 0.9 36.4-39.4 Snout to pelvic fin origin 41.2 39.2 39.8 1.2 38.3-41.4 Pectoral fin length 22.4 25.4 24.5 0.9 23.3-25.6 Pelvic fin length 24.1 30.4 25.8 2.1 23.4-30.4 Dorsal fin base length 60.2 60.0 58.1 1.2 56.3-60.0 ADAA 54.7 51.9 50.7 0.9 49.5-52.1 PDPA 16.6 14.8 14.7 1.0 13.1-16.2 ADPA 64.8 62.9 61.7 1.1 59.6-63.4 PDAA 30.0 29.5 29.3 0.9 27.7-30.4 PDVC 19.1 18.3 17.3 0.7 16.3-18.3 PADC 19.9 18.7 19.4 0.5 18.6-20.2 ADP2 36.5 36.1 34.0 1.0 32.3-36.1 PDP2 49.7 54.7 53.6 1.2 51.0-54.8 Horizontaleye diameter 28.6 26.9 30.8 1.9 26.9-33.1 Verticaleye diameter 25.5 27.3 30.2 1.4 27.3-32.2 Snout length 40.8 43.8 42.5 2.2 39.7-47.6 Postorbitalhead length 41.2 40.6 41.8 0.7 40.6-42.5 Preorbitaldepth 20.1 22.7 22.4 1.3 20.7-24.5 Lower-jawlength 40.5 39.4 37.7 2.4 34.9-41.9 Cheek depth 27.8 28.3 27.3 0.9 25.6-28.4 Head depth 102.0 95.0 95.7 3.2 88.7-99.4

faint orange highlights. Head orange/brown The plot of the sheared second principal with prominent dark green spot on posterior component of the morphological data versus portion of the opercle. Ventral edge of cheek the first principal component of the meristic outlined in fluorescent blue; cheek with or- data shows that there is no overlap between the ange/brown and blue highlights. One floures- type of P. williamsi with P galanos (Fig. 2). The cent green interorbital bar. Gular region yellow. first principal component of the morphometric Dorsal fin orange with black submarginal band. data is interpreted as a size component and the Caudal fin rays black; membranes yellow with sheared components as shape, independent of blue highlights. Anal fin rays black; membranes size (Humphries et al., 1981; Bookstein et al., between rays transparent with micromelano- 1985). Size accounts for 85% of the observed phores and four orange ocelli. Pelvic fin leading variance and the second principal component edge light blue; first two rays and membranes accounts for 6%. The variables that had the black; posterior rays and membranes clear with highest loadings on the sheared second princi- orange spots. Pectoral fin rays gray with clear pal component are preorbital depth, vertical membranes. eye diameter, PDPA, and horizontal eye diame- Females green laterally with blue highlights; ter (Table 4). The first principal component of black midlateral band and second black band the meristic data explains 27% of the total var- between midlateral band and dorsal fin. Belly iance. The variables with the highest loading on white with yellow and blue highlights. Color of the first principal component are teeth rows on head similar to that of male. Dorsal fin brown the lower jaw, teeth rows on upper jaw, and with dark gray submarginal band. Caudal fin number of dorsal fin rays (Table 5). gray; anal fin gray with no ocelli. Leading edge of pelvic fin light blue; first two rays and mem- Etymology.--The name galanos, from the Greek branes black; remainder clear with orange high- meaning blue, was chosen based on the pres- lights. Pectoral fins with gray rays and clear ence of blue highlights along the lateral sides membranes. of both males and females. STAUFFER AND KELLOGG-- NEW SPECIES OF PSEUDOTROPHEUS 149

TABLE 2. DEFINITIONOF ABBREVIATIONSFOR SELECTED ' 0.06 S0.04 MORPHOMETRICS. 0.02 0 Abbreviation Definition * P. williamsi ADAA Distance between anterior insertion of -0.04 " -0.06 P. galanos dorsal fin to anterior insertion of U -0.06 -0.08 anal fin. -0.1 PDPA • Distance between posterior insertion 0-.12 of dorsal fin to posterior insertion -0.14 of anal fin. -2 0 2 ADPA Distance between anterior insertion of PC 1 (MeristicData) dorsal fin to posterior insertion of anal fin. Fig. 2. Plot of the sheared second principal com- PDAA Distance between posterior insertion ponent (morphometric data) and the first principal of dorsal fin to anterior insertion of component (meristic data) for Pseudotropheusgalanos anal fin. and the holotype of Pseudotropheuswilliamsi. PDVC Distance between posterior insertion of dorsal fin to ventral insertion of caudal fin. terns but did not postulate as to which popula- PADC Distance between posterior insertion tions represented the species described by Guin- of anal fin to dorsal insertion of ther (1893). Konings (1995) suggested that the caudal fin. type specimen of R williamsi might have come ADP2 Distance between anterior insertion of from the population that inhabits the north- dorsal fin to anterior insertion of eastern coast of Likoma Island. It is obvious that pelvic fin. detailed morphological, genetic, and behavioral PDP2 Distance between posterior insertion data are needed to determine the relationships of dorsal fin to anterior insertion of of the many undescribed species of Pseudotro- fin. pelvic pheus. In cases where the type series consists of only one or two individuals, the details of the type locality are lacking, and when comprehen- DISCUSSION sive color notes were not recorded, it may be impossible to identify the range of many of Giinther (1893), based on a single specimen these previously described species. (BMNH 1893.1.17.6), originally described P wil- The existence of only a single specimen of P liamsi in the genus Chromis.The type locality is williamsi, prohibits us from accounting for intra- listed simply as Lake Nyasa. Ribbink et al. specific variation, when comparing the SPCA2 (1983) recognized eight distinct populations of score of P williamsi to the minimum polygon Pseudotropheusc.f. williamsi based on color pat- cluster formed by the type series of P. galanos

TABLE3. MERISTICVALUES OF Pseudotropheuswilliamsi ANDPseudotropheus galanos. Summary statistics (n = 10) include the holotype.

P williamsi P galanos Counts Holotype Holotype Mode % Freq. Range Lateralline scales 31 31 31 50 31-33 Pored scales posterior to lateral line 0 2 2 40 0-2 Scale rows on cheek 4 4 4 60 3-4 Dorsal fin spines 17 16 17 80 16-17 Dorsal fin rays 8 9 9 50 8-10 Anal fin spines 3 3 3 100 3-3 Anal fin rays 8 8 8 100 8-8 Pectoral fin rays 14 14 14 100 14-14 Pelvic fin rays 5 5 5 100 5-5 Gill rakerson first ceratobranchial 10 9 10 60 9-11 Gill raker on first epibranchial 3 2 2 60 2-3 Teeth in outer row of left lowerjaw 11 13 13 40 11-14 Teeth rows on upper jaw 3 5 5 40 3-5 Teeth rows on lowerjaw 3 5 4 40 3-5 150 COPEIA, 2002, NO. 1

TABLE 4. VARIABLELOADINGS ON THE SIZE PRINCIPAL TABLE 5. VARIABLELOADINGS ON THE FIRST PRINCIPAL COMPONENTS AND SECOND PRINCIPAL COMPONENTS COMPONENTOF THE MERISTICDATA FOR Pseudotropheus (SHAPE FACTOR) OF THE MORPHOMETRICDATA FOR williamsiAND Pseudotropheus galanos. Pseudotropheuswilliamsi (n = 1) ANDPseudotropheus galanos (n = 10). PC1 Dorsal spines -0.04 Size PC2 Dorsal rays 0.48 Standardlength 0.20 0.01 Anal spines 0.00 Head length 0.20 0.10 Anal rays 0.00 Snout length 0.23 0.23 Pelvic rays 0.00 Post orbital head length 0.18 0.12 Pectoral rays 0.00 Horizontal eye diameter 0.08 0.24 Lateralline scales 0.17 Verticaleye diameter 0.09 0.48 Pored scales posterior to lateral line 0.18 Head depth 0.23 -0.13 Cheek scales 0.13 Preorbitaldepth 0.21 0.49 Gill rakerson first ceratobranchial 0.08 Cheek depth 0.21 0.15 Gill rakerson first epibranchial -0.05 Lowerjaw length 0.31 -0.07 Teeth in outer row of left lowerjaw 0.19 Snout to dorsal fin origin 0.17 0.10 Teeth rows on upper jaw 0.57 Snout to pelvic fin origin 0.18 -0.13 Teeth rows on lowerjaw 0.57 Dorsal fin base length 0.24 -0.02 ADAA 0.25 -0.18 ADPA 0.23 -0.07 PDAA 0.22 -0.00 plex and the members of the subgenus Tro- PDPA 0.26 -0.41 pheops possess an acutely sloped ethmo-vomer- PDVC 0.27 -0.23 ine block (Stauffer et al., 1997). Reinthal (1990) PADC 0.22 -0.02 showed that at least one member of the P elon- PDP2 0.22 0.22 gatus complex (P elongatus "greenback") had ADP2 0.25 -0.17 one of the smallest supraoccipital crests relative to neurocranial length, but whether this character held for other members of the complex was not discussed. The P. aggressive species (Fig. 2). Nevertheless, the fact that the variation (e.g., P. minutus Fryer) and the P. miscellaneous within P galanos is smaller than the variation group (e.g., Pseudotropheussocolofi Johnson), as between the two species, corroborates our hy- designated by Ribbink et al. (1983), lack any ap- pothesis that these two forms are heterospecific. parent common morphological character; how- Within the mbuna, Pseudotropheusis the most ever, in all of the specimens that we examined, diverse and widespread genus, and is most cer- their mouth was elevated approximately 10-20' tainly polyphyletic. Recently, Stauffer et al. above a line parallel to one hypothetically (1997) diagnosed a new genus, Metriaclima drawn from the hypural plate to the tip of the based on the following two apomorphic char- snout. The placement of P fainzilberi is problem- acters of the skull: (1) moderately sloped eth- atic. Although it superficially resembles M. zebra, mo-vomerine block; and (2) a swollen rostral tip as do many Cynotilapia spp., its mouth shape of the neurocranium compared to other Pseu- and teeth position more closely resemble Petro- dotropheusspecies. The choice of Metriaclimaas tilapa species (Staeck, 1976; Stauffer et al., the new generic name was confounded because 1997). Reinthal (1993) treated all of these Meyer and Foerster (1984) had earlier pro- groups as genera, with the exception of P. fain- posed the name Maylandia as a subgenus of zilberi in his distribution analysis. Thus, Pseudo- Pseudotropheus,with Pseudotropheusgreshakei as tropheusis certainly a polyphyletic genus and we the type species. The use of Maylandia as a pro- hypothesize that eventually members of the P posed subgenus of Pseudotropheuswas not ac- tropheops,P elongatus,and P aggressive complex- companied by either a diagnosis or a descrip- es will be placed in separate genera, based on tion; thus Maylandia is a nomen nudum (Stauf- apomorhic morphological characters. We also fer et al., 1997; Konings and Geerts, 1999). predict that Pseudotropheuswill only contain In addition to the P williamsi complex, Pseu- members of the P williamsi complex, but be- dotropheusnow contains species belonging to the cause of the lack of phylogenetic data on many subgenus Tropheops(Trewavas, 1984), P elonga- of the groups, we are currently unable to diag- tus complex, P "aggressive" complex, and nose monophyletic groups into which all species "miscellaneous" group (Ribbink et al., 1983) asP. currently included in Pseudotropheusshould be well as P fainzilberi. Both the P elongatus com- placed. STAUFFER AND KELLOGG-- NEW SPECIES OF PSEUDOTROPHEUS 151

ACKNOWLEDGMENTS Pseudotropheusdu lac Malawi avec des remarques sur le complexe Pseudotropheus-Melanochromis(Pisces, We thank the University of Malawi and espe- Perciformes, Cichlidae). Rev. fr. Aquariol. 10:107- cially A. Ambali for including us under the Uni- 112. I. AND P. N. REINTHAL.1994. versity of Malawi's collecting permit. R. Ruffing MORAN,P., KORNFIELD, Molecular systematicsand radiation of the haplo- aided in data analysis. The project was complet- chromine cichlids (Teleostei: Perciformes) of Lake ed under 00R107-00 issued approved IACUC by Malawi. 1994:274-288. the Institutional Animal Care and Use Commit- Copeia OLIVER,M. K., ANDP. V. LOISELLE. 1972. A new genus tee at Penn State This was University. project and species of cichlid of the mbuna group (Pisces: funded in part by a Fulbright Research Award Cichlidae) from Lake Malawi.Rev. Zool. Bot. Afr. to JRS in 1994. 855:309-320. REGAN, C. T. 1922. The cichlid fishes of Lake Nyasa. Proc. Zool. Soc. Lond. (for 1921):675-727. LITERATURECITED REINTHAL,P. N. 1990. Morphological analyses of the neurocranium of a group of rock-dwelling cichlid ALBERTSON,R. C., A. MARKERT,P. D. DANLEY,AND J. fishes (Cichlidae: Perciformes) from Lake Malawi, T. D. KOCHER.1999. of a rapidly evolving Phylogeny Africa. Zool. J. Linn. Soc. 98:123-139. clade: the cichlid fishes of Lake Malawi, East Africa. 1993. Evaluatingbiodiversity and conserving Proc. Natl. Acad. Sci. 96:5107-5110. •-.Lake Malawi'scichlid fish fauna. Conserv. Biol. 7: VAN AND BAREL,C. D. N., M. J. P. OIJEN,F. WITTE, E. 712-718. L. M. WITTE-MAAs.1977. An introduction to the RIBBINK, A. B. A. MARSH, A. C. MARSH, A. C. RIB- and of the J., taxonomy morphology haplochromine BINK,AND B. J. SHARP.1983. A preliminarysurvey Cichlidae from Lake Victoria. Part A. Text. Neth. J. of the cichlid fishes of the rocky habitats in Lake Zool. 27:333-389. Malawi.S. Afr. Sci. 18:149-310. HUMPOH- J. BOOKSTEIN,F. L., B. CHERNOFF,R. ELDER,J. W. 1976. einer G. ANDR. 1985. STAECK, Ergebnisse ichtyologischen RIES, SMITH, STRAUSS. Morphomet- Sammelreise zum Nordende des Das rics in The of Nat- Nyannasees. evolutionarybiology. Academy 10:486-492. ural Sciences of Philadelphia.Speci. Publ. 15. Phil- Aquarium STAUFFERJR., J. R. 1991. Description of a facultative adelphia, PA. cleanerfish (Teleostei: Cichlidae) from Lake Mala- FRYER,G. 1959. The trophic interrelationships and of some littoral communitiesof Lake wi, Africa. Copeia 1991:141-147. ecology Nyasa N. K. A. AND K. with reference to the fishes, and a discus- , J. BOWERS, KELLOGG, R. special McKAYE.1997. A revision of the blue-black Pseudo- sion of the evolution of a of group rock-frequenting from Cichlidae. Proc. Zool. Soc. Lond. 132:153-282. tropheus zebra (Teleostei: Cichlidae) complex Lake Malawi, Africa, with a of a new -9, ANDT. D. ILES.1972. The cichlid fishes of the description and ten new Proc. Acad. Nat. Sci. GreatLakes of Africa.T.F.H. Publications, genus species. Neptune, Philo. 148:189-230. NJ. fishes of A. 1893. Second on the ba- TREWAVAS,E. 1935. A synopsisof the cichlid GiJNTHER, report reptiles, Lake Ann. Nat. Hist. 16:65-118. trachians,and fishes transmittedto Mr.H. H. Nyasa. Mag. John- -. 1984. Nouvel examen des et sous- ston, C. B., from British CentralAfrica. Proc. Zool. genres Soc. 1893:616-628. genres du complexe Pseudotropheus-Melanochromis du lac Malawi.Rev. fr. 10:97-106. HUMPHRIES,J. M., F. L. BOOKSTEIN,B. CHERNOFF,G. Aquariol. R. SMITH,R. L. ELDER,AND S. G. Poss. 1981. Mul- tivariatediscrimination by shape in relation to size. (JRS) PENNSYLVANIASTATE UNIVERSITY,SCHOOL Syst. Zool. 30:291-308. OF FOREST RESOURCES, UNIVERSITY PARK, A. 1995. Malawi cichlids in their natural KONINGS, PENNSYLVANIA16802; AND (KAK) SKIDMORE habitat. 2d ed. Cichlid Press, St. Leon-Rot, Germa- COLLEGE,ENVIRONMENTAL STUDIES PROGRAM, ny. SARATOGASPRINGS, NEW YORK 12866. E-mail: --, AND M. GEERTS.1999. Comments on the re- Send to vision of Pseudotropheuszebra. Cichlid News, January: (JRS) [email protected]. reprint requests 18-26. JRS. Submitted: 12 Sept. 2000. Accepted: 3 MEYER,M. K., AND W. FOERSTER.1984. Un nouveau Aug. 2001. Section editor: S. A. Schaefer.