Haplochromis argens de Zeeuw, Westbroek & Witte

de Zeeuw, Marnix P., Westbroek, Irene, van Oijen, Martien J. P. & Witte, Frans, 2013, Two new species of zooplanktivorous haplochromine cichlids from Lake Victoria, Tanzania, ZooKeys 256, pp. 1-34 : 5-12

Haplochromis argens de Zeeuw, Westbroek & Witte sp. n. Figs 2-5, Tables 1, 2

Cheironyms used.

Haplochromis argens: Goldschmidt 1994: 179, 199-200; Haplochromis argens ; Verheyen et al. 1989: 93, 94, 96; van der Meer 1995: 26, 30-32; van der Meer and Bowmaker 1995: 232-239; Goldschmidt 1996: 164, 184-185; Hilder and Pankhurst 2003: 194; Collin et al. 2004: 769; Carleton et al. 2008.

Haplochromis “argens”; Zihler 1982: 568; Barel 1983: 384, 385, 407, 418; Witte 1984a: 604, 611; Witte 1984b: 159-161, 163; Barel 1985: chapter 1, 384, 385, 407, 418; Gottfried 1986: 1029; Witte 1987, chapter 1: 611, chapter 2: 67, 76, chapter 3: 8-13, 19; Goldschmidt 1989a: 24, 27, 29-39, 41, 42, 44, 45, 53, 55, 58, 59, 61-63, 65-69, 71-75, 77, 82, 84, 86-89, 97-101, 103, 118, 119, 148, 158, 160, 162, 166; Goldschmidt 1989b: 122-126, 129-131; Wanink et al. 1989: 25; van der Meer 1989: 52, 53; Goldschmidt and de Visser 1990: 129, 130, 132; Goldschmidt et al. 1990: 344, 346-351, 353; Goldschmidt and Witte 1990: 356-367; Barel et al. 1991: 262; Goldschmidt 1991: 181, 182, 185, 187; van der Meer 1991a: 91-94, 96; van der Meer 1991b: 3, 5, 6, 9-12, 14-22, 24-26, 28, 68, 76, 77, 83, 85-87, 89-93, 99, 101, 104; Goldschmidt and Witte 1992: 104; Kaufman 1992: 848, 849; Witte et al. 1992b: 11, 13, 17, 25, 27, 28; Barel 1993: 366; Smith and Wootton 1994: 99-103; Balshine-Earn 1995: 5; Seehausen 1995: 143, 146; Seehausen and Witte 1995: 101; van der Meer et al. 1995: 116-129; Smith and Wootton 1995: 12; Anker and Dullemeijer 1996: 4-11; de Visser and Barel 1996: 4; Seehausen 1996: 51, 55, 255, 256; Smit and Anker 1997: 9-17; Seehausen et al. 1997b: 899; Witte et al. 1997: 591; Wanink 1998: 159, 232; Rinkes 1999: 46, 47, 54, 56-58, 60, 62, 76, 77, 79, 97; de Visser 2000: 18; Tacon et al. 2000: 63; Witte and Wanink 2000: 78-81, 84; Seehausen et al. 2003: 272; Witte et al. 2005: 320; Kishe-Machumu 2012: 35; van Rijssel and Witte 2012.

H. “Argens”; Kaufman and Seehausen 1995: 148.

Haplochromis (?) “argens”; Wanink and Witte 2000: 563; Witte et al. 2000: 234, 235, 237; Witte et al. 2003: 108; Niemantsverdriet 2005: 151, 155; Witte et al. 2007a: 1153.

Haplochromis sp. “argens”; Mizoiri et al. 2008: 228, 241, 254.

Yssichromis argens ; van Staaden et al. 1995: 168; Chapman et al. 1995: 1277, 1279-1282, 1285; Huber et al. 1997: 170; Rosenberger and Chapman 2000: 498; Melnychuk and Chapman 2002: 107.

Yssichromis sp. “argens”; Mizoiri et al. 2008: 228.

Type-locality. Tanzania, Lake Victoria, Mwanza Gulf (ca 2°29'-2°36'S; 32°48'-32°54'E) and Emin Pasha Gulf (ca 2°18'-2°41'S; 31°47'-31°59' E).

Holotype. RMNH.PISC.835884, ♂, 67.3 mm SL, Tanzania, Lake Victoria, Mwanza Gulf, 8.iii.1979, HEST.

Paratypes. All type specimens collected by Haplochromis Ecology Survey Team (HEST) in Mwanza Gulf, Tanzania, Lake Victoria, except where noted otherwise. Size of specimens given as standard length. RMNH.PISC.728315, ♀, 71.0 mm, 30.v.1980; RMNH.PISC.728845, 6, ♂, 74.4 mm, 31.v.1980; RMNH.PISC.73097, ♀, 71.3 mm, 27.ix.1977; RMNH.PISC.812025, ♀, 65.6 mm, 11.v.1978; RMNH.PISC.83587, ♂, 77.4 mm, 31.v.1975; RMNH.PISC.835894, ♀, 75.5 mm, 21.iv.1980; RMNH.PISC.835904, ♂, 68.2 mm, 22.iv.1980; RMNH.PISC.836064, ♂, 73.7 mm, 22.iv.1980; RMNH.PISC.836074, ♂, 65.7 mm, 15.iv.1980; RMNH.PISC.836085, ♂, 65.7 mm, 31.v.1975; RMNH.PISC.836094, ♂, 67.4 mm, 22.iv.1980; RMNH.PISC.836104, ♂, 66.2 mm, 30.ix.1977; RMNH.PISC.836114, ♂, 69.5 mm, 30.ix.1977; RMNH.PISC.836124, ♀, 71.1 mm, 30.ix.1977; RMNH.PISC.836134, ♀, 68.1 mm, 30.ix.1977; RMNH.PISC.836144, ♀, 71.9 mm, 8.ix.1977; RMNH.PISC.836154, ♂, 57.7 mm, 8.ix.1977; RMNH.PISC.836164, ♂, 70.2 mm, 19.viii.1977; RMNH.PISC.836174, ♀, 71.5 mm, 19.viii.1977; RMNH.PISC.836184, ♂, 66.1 mm, 7.ix.1977; RMNH.PISC.836194, ♂, 66.5 mm, 21.xii.1977; RMNH.PISC.836204, ♂, 65.8 mm, 10.x.1977; RMNH.PISC.836211, ♂, circa 70 mm, 30.ix.1977; RMNH.PISC.836225, ♂, 59.3 mm, 22.vi.1985, Emin Pasha Gulf; RMNH.PISC.836235, ♂, 57.2 mm, 22.vi.1985, Emin Pasha Gulf; RMNH.PISC.836245, ♂, 59.6 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836254, ♂, 58.3 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836264, ♂, 58.5 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836274, ♂, 54.3 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836284, ♂, 59.6 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836294, ♂, 55.4 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836304, ♂, 53.1 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836314, ♂, 66.8 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836324, ♂, 67.0 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836334, ♂, 60.4 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836344, ♂, 53.9 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836354, ♂, 62.6 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836364, ♂, 66.6 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836374, ♂, 69.2 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836384, ♂, 65.8 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836394, ♂, 61.3 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836404, ♂, 73.4 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836414, ♂, 64.1 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836424, ♂, 63.1 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836434, ♂, 63.7 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836444, ♂, 62.1 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836454, ♂, 64.1 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836464, ♂, 61.6 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836474, ♂, 59.8 mm, 25.viii.1981; RMNH.PISC.836484, ♂, 61.6 mm, 10.x.1977; RMNH.PISC.836494, ♂, 61.5 mm, 21.xii.1977; RMNH.PISC.836504, ♂, 57.7 mm, 6.iii.1979; RMNH.PISC.836514, ♂, 60.6 mm, 13.vii.1979; RMNH.PISC.836524, ♂, 58.0 mm, 1.ii.1979; RMNH.PISC.836534, ♂, 53.5 mm, 18.xi.1981; RMNH.PISC.836554, ♂, 61.8 mm, 14.v.1979; RMNH.PISC.836564, ♂, 59.0 mm, 27.iii.1979; RMNH.PISC.836574, ♂, 61.6 mm, 27.iii.1979; RMNH.PISC.836604, ♂, 56.8 mm, 12.iii.1979; RMNH.PISC.836614, ♂, 57.9 mm, 12.iii.1979; RMNH.PISC.836624, ♂, 59.7 mm, 14.v.1979; RMNH.PISC.836634, ♂, 58.6 mm, 14.v.1979; RMNH.PISC.836734, ♂, 55.5 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836881-3, ♂, 61.4 mm, 6.iii.1979; RMNH.PISC.836891-3, ♂, 62.2 mm, 14.v.1979; RMNH.PISC.836941, 5, ♂, 63.1 mm, 21.vi.1985, Emin Pasha Gulf; RMNH.PISC.836971, 5, ♂, 59.1 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.836981-3, 5, ♂, 61.0 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.837033, 6, ♂, 66.4 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.837041, 3, 6, ♂, 68.4 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.837051-3, 6, ♂, 67.5 mm, 23.vi.1985, Emin Pasha Gulf; RMNH.PISC.837061, 5, ♂, 68.8 mm, 27.vi.1985, Emin Pasha Gulf; RMNH.PISC.840675, 7, ♂, 72.1 mm, 15.viii.1986; AMNH 2550354, ♂, 62.2 mm, 14.v.1979; BMNH 2012.1.5.2 4, ♂, 62.8 mm, 3.v.1979; NSMT-P 1069594, ♂, 62.6 mm, 3.v.1979.

1 dissected to describe oral jaws; 2 dissected to describe pharyngeal jaws; 3 dissected to count gill filaments; 4 proportional measurements taken (Table 1); 5colour picture available; 6colour picture of anal fin available; 7 specimen of which Dr E. Verheijen, Royal Belgian Institute of Natural Sciences, has taken a tissue sample for DNA analysis.

Diagnosis.

Small sized (<8 cm SL), slender (BD <31% SL), micrognathic (LJL <45% HL) zooplanktivorous Haplochromis species with slightly curved to straight dorsal head profile. Relatively long and slender, mainly bicuspid, teeth in oral jaws. Premaxillary dentigerous area extending almost to caudal end of dentigerous arm. Both males and females silvery with conspicuously ivory-white lips. Three to five, generally faint vertical stripes on flank; faint traces of a dark mid-lateral band occasionally present. Males with yellow to greenish sheen on flank.

Description.

Proportional measurements of type material given in Table 1.

Habitus. See Fig. 2. Body slender. Dorsal head profile straight to slightly curved, occasionally moderately curved. Premaxillary pedicel slightly prominent. Mouth oblique. Lips not thickened. Medial part of premaxilla slightly expanded. Caudal part of maxilla not bullate. Vertical through caudal tip of maxilla running through iris, just rostral to pupil. Lateral snout outline isognathous and obtuse, in larger specimens slightly prognathous. Jaws equal anteriorly or lower jaw slightly protruding. Mental prominence slightly pronounced. Retro-articular processes of right and left mandible touching each other, interrupting ventral body outline. Eye approximately circular and medium to large. Generally an aphakic aperture present in pupil. Cephalic lateral line pores not enlarged.

Scales. Cheek, gill cover and rostral part of dorsal head surface covered with cycloid scales. Nape and rostral part of dorsum with mixture of cycloid and weakly ctenoid scales. Chest with ctenoid, weakly ctenoid and some cycloid scales. Scales on remaining part of body mainly ctenoid. Scales on chest smaller than those on ventral and ventro-lateral part of body; size transition gradual. Small elongated scales on basal quarter to half of caudal fin. Three to seven (mode 6) scales between upper lateral line and dorsal-fin origin, four to eight (mode 6) between pectoral- and pelvic-fin bases.

Fins. Pelvic fins just reaching or slightly surpassing rostral-most point of anal-fin origin. Pelvic fins with first soft rays slightly produced in both sexes, in males occasionally filamentous. Caudal tip of anal fin not reaching caudal-fin origin. Caudal-fin outline truncate to slightly emarginate.

Gill apparatus. Description based on lateral gill rakers and lateral hemibranch of first gill arch. Number of gill rakers on lower part of gill arch 11-12. Lower two to three rakers reduced (= very short), next one to two short, followed by two to six slender and longer ones. Remaining rakers hooked, bifid, trifid or quadrifid. Rakers generally closely set, viz. touching each other over major part of length. Number of gill filaments 94 to 106.

Viscera. Ratio between intestine length and SL: 1.0-1.4 (n = 25).

Oral jaws. (Fig. 3 A–C) Premaxillary ascending arm equal to or longer than dentigerous arm (asc./dent. arm ratio 1.0 to 1.1). Angle between the arms 77° to 81°. Symphyseal articulation facet not present. Lower jaw slightly more elongated than generalized type (length/height ratio 2.3 to 2.5). Upper half of dentary with distinct outwardly directed flare. Mental prominence slightly pronounced.

Oral teeth shape. (Fig. 3 A–C) Generally teeth in outer row of both premaxilla and lower jaw bicuspid or weakly bicuspid, with some unicuspid or tricuspid teeth interspersed. In specimens over 65 mm SL, weakly bicuspids and unicuspids may dominate. Major cusp of bicuspids isoscelene to subequilateral, protracted and acutely pointed. Flange generally absent, when present very small. Minor cusp weakly developed to distinct, relatively short compared to major cusp. Cusp gap wide. In labial view, neck slender to moderately slender, crown not or slightly expanded. In lateral view, crown compressed. Outer-row teeth in both premaxilla and lower jaw recurved. Inner rows in both jaws with mainly tricuspid or weakly tricuspid teeth.

Oral teeth size. Outer-row teeth relatively long and slender, gradually decreasing in size from rostral to caudal.

Dental arcade and tooth band. (Fig. 3B) Rostrally dental arcade rounded. Outer row generally occupying almost total length of dentigerous arm of premaxilla, in two specimens (RMNH.PISC.83697 and RMNH.PISC.83621; Fig. 3B) edentulous part about 25% of arm. Outer row in lower jaw not, or just, reaching coronoid wing in most dissected specimens. In one case caudal-most tooth relatively high on coronoid wing. One or two inner rows in rostral part of both jaws, decreasing to zero in caudal part.

Teeth counts and setting. Outer row of upper jaw (l+r premaxilla) with 30-52 teeth. In both jaws outer-row teeth regularly set, their placement wider rostrally than laterally.

Tooth implantation. Outer-row teeth of premaxilla rostrally erect. Inner-row teeth recumbent. Outer-row teeth of lower jaw slightly procumbent, inner-row teeth erect.

Lower pharyngeal element. (Fig. 3 D, E) Lower pharyngeal element relatively small and slender (length/width ratio 1.2-1.3). Dentigerous area slightly broader than long (length/width ratio = 0.7-0.9). Suture straight.

Pharyngeal teethcounts. Caudal-most transverse row with about 30-38 teeth, medial longitudinal rows with eight to 11 teeth.

Pharyngeal teeth shape. Teeth in caudal-most transverse row hooked, major cusp only slightly incurved, blunt to slightly acute. Other teeth bevelled or pronounced. All teeth relatively fine and slender, medial teeth not coarser than other teeth.

Vertebrae. Total number of vertebrae in 57 specimens: 30 (12), 31 (39) or 32 (6), comprising 13-14 abdominal and 16-19 caudal vertebrae.

Live colouration males. (Fig. 4 A, B). Sexually active males with ivory to grey snout and cheek. Lips remarkably ivory-white with no or few pigment spots. Eye with grey outer ring and silver to golden inner ring. Lower jaw and interoperculum whitish. Gill cover silver, sometimes with grey to dusky flush. Dorsal head surface, dorsum and flank silvery-grey, dorsum with bluish to purplish sheen, flank with yellow to greenish sheen. Chest, belly and ventral side silvery-white.

Pelvic fins black; in specimens of Emin Pasha Gulf, medial side sometimes red. Anal fin rostrally faintly to distinctly red, rest of fin hyaline. One to two dark yellow to orange egg dummies with hyaline ring present on caudal part of anal fin. Caudal fin orange-red to wine-red. Dorsal fin hyaline with red streaks and spots. Lappets hyaline or reddish, rostral lappets sometimes dusky.

Dark grey to blackish markings: Nostril-, interorbital-, and supraorbital stripes, sometimes rather distinct. Lachrymal stripe distinct, but relatively short (i.e. small blotch at caudal end of lachrymal generally not reaching caudal tip of maxilla), sometimes extending over iris. Irregular preopercular vertical bar generally present. Opercular blotch distinct. Three to five, generally faint vertical stripes on flank. Traces of dark-grey mid-lateral band occasionally present.

Live colouration females. Live females basically with same colours as males, lacking bluish-purplish and yellow-greenish sheens and distinct red colouration in fins, but sometimes with faint red flush in caudal fin. In females upper lip usually with more pigment than in males. Of markings on head, only lachrymal stripe and opercular blotch distinct. Mid-lateral band sometimes more distinct than in males, vertical stripes faint.

Preserved colouration of males and females. (Fig. 5) Body light brown, dorsally darker than ventrally. Snout, lips and lower jaw coloured as old ivory. Fins hyaline and light grey-brown in both sexes, except for black pelvic fins in adult males. Same markings, but slightly more distinct, as in live specimens.

Distribution.

Haplochromis argens is only known from the Tanzanian part of Lake Victoria. Specimens were caught in the Mwanza Gulf (from entrance of Stuhlmann Sound to entrance of gulf in north), in the south-western part of the Speke Gulf (near its entrance), in the area around Kome Island, and in the Emin Pasha Gulf (Fig. 1).

Habitat.

Haplochromis argens is a pelagic species from the littoral and sub-littoral zone. At night the species is virtually restricted to the two upper metres of the water column ( Witte 1984b, Goldschmidt et al. 1990). By day, the highest densities were found at two to three metres from the surface, but individuals of this species were also caught with bottom trawls over sand and mud bottoms, and in gill nets and traps near rocks ( Goldschmidt et al. 1990, Witte et al. 1992b).

Abundance.

During 1979-1982, Haplochromis argens was present in 70% of the bottom-trawl tows by day and in 100% of the surface trawl tows at night; the mean numbers of individuals per tow ranged from 6.2 to 18.3, respectively (Table 2). In 1987-1988, it occurred in 3% of the bottom trawl tows and the mean number of individuals per tow was 0.03; the species was absent in surface trawls. Thirty-four bottom-trawl tows in 1990-1999 captured no Haplochromis argens . From 2001 to 2011 more than 150 bottom-trawl tows contained about 15 individuals of Haplochromis argens , corresponding to a decline in catch per unit effort of more than 50 times compared to the 1979-1982 captures; no individuals were caught with surface trawls.

Food. Before the ecological changes in Lake Victoria,the diet of Haplochromis argens comprised mainly zooplankton during the day; Chaoborus larvae were important at night ( Goldschmidt et al. 1990). The current diet is unknown, but all the studied resurgent species in the Mwanza Gulf changed their diet (e.g. van Oijen and Witte 1996, Katunzi et al. 2003, Kishe-Machumu et al. 2008).

Breeding. Haplochromis argens is a female mouth brooder. Spawning sites are located at depths <9 m ( Goldschmidt and Witte 1990).

Etymology.

In reference to the silver male colouration, Haplochromis argens was given the nickname “argens” under the false assumption it was Latinized Greek for silver. Since this species is well known under its cheironym, we think it is best to upgrade the nickname to the species’ epithethon.

Comparisons.

The zooplanktivorous species Haplochromis (Yssichromis) laparogramma Greenwood & Gee, 1969, Haplochromis (Yssichromis) pyrrhocephalus Witte & Witte-Maas, 1987 and Haplochromis (Yssichromis) heusinkveldi , Witte & Witte-Maas, 1987, have shorter bicuspid teeth in the oral jaws than Haplochromis argens , and generally the premaxillary dentigerous arm is edentulous over the caudal 1/4 -1/3 versus the dentigerous portion extending almost to the caudal end of the dentigerous arm. The dental features of the zooplanktivorous/insectivorous Haplochromis tanaos van Oijen & Witte, 1996 and Haplochromis thereuterion van Oijen & Witte, 1996, are more or less similar to those of Haplochromis argens , but the former two species have more unicuspids. Haplochromis argens is further distinguished from these and other species by its colouration. Sexually active males of Haplochromis tanaos are dark blue, the females silvery with a distinct mid-lateral band and slightly less distinct dorso-lateral band. Sexually active males of Haplochromis thereuterion are black, the females coloured like females of Haplochromis tanaos ( van Oijen and Witte 1996). The body of Haplochromis argens is less slender (BD 26.0-30.7% of SL, mean 28.2%, Table 1) than that of Haplochromis tanaos and Haplochromis thereuterion (22.1-27.1% and 24.4-27.6% of SL, respectively; Tables 3 and 7 in van Oijen and Witte 1996). Live Haplochromis argens is similar to (juvenile) Haplochromis cassius in colouration and general habitus. However, Haplochromis cassius has a broad, well defined mid-lateral band ( Greenwood and Barel 1978), more and distinctly longer unicuspid teeth, more curved and more widely set teeth, and thicker lips than Haplochromis argens . The maximum size of Haplochromis cassius (99.0 mm SL) is larger than that of Haplochromis argens , but when comparing similar size ranges (see material and methods) Haplochromis argens has: a smaller head (ratio HL/SL: 31.0 - 35.6%, mean 32.9% versus 35.0 - 36.0%, mean 35.5% in Haplochromis cassius ); a shorter snout (ratio SnL/HL: 23.6 - 29.7%, mean 26.6% versus 29.8 - 32.6%, mean 31.2% in Haplochromis cassius ); larger eyes (ratio EyL/HL: 30.9 - 39.0%, mean 35.7% versus 26.8 - 28.8%, mean 28.3% in Haplochromis cassius ). For comparison with Haplochromis goldschmidti sp. n., see below.