Enteromius yardiensis, Englmaier & Tesfaye & Bogutskaya, 2020

Englmaier, Gernot K., Tesfaye, Genanaw & Bogutskaya, Nina G., 2020, A new species of Enteromius (Actinopterygii, Cyprinidae, Smiliogastrinae) from the Awash River, Ethiopia, and the re-establishment of E. akakianus, ZooKeys 902, pp. 107-150 : 107

Enteromius yardiensis sp. nov. Figs 6 , 7 , 8 , 9A , 10A

Material examined.

Holotype (Fig. 6A ). BMNH 2018.10.10.1, holotype, 40.2 mm SL (voucher specimen for CO1: MN747019), side channel of the Awash River at Kada Bada, north of the bridge on the way to Herto Bouri (site 2; 10°13'53"N, 40°34'43"E; 565 m a.s.l.), Afar Region, Ethiopia, 28.01.2018, coll. G.K. Englmaier, G. Tesfaye, P. Meulenbroek and H. Waidbacher.

Paratypes. BMNH 2018.10.10.2-4, 3, 35.6-38.8 mm SL, same date and locality as holotype. BMNH 2018.10.10.5-24, 20, 17.9-26.2 mm SL, same date and locality as holotype. NMW 99232, 1, 34.1 mm SL, same locality as holotype, 21.05.2018, coll. G.K. Englmaier and G. Tesfaye. NMW 99233, 18, 23.1-41.0 mm SL, same date and locality as NMW 99232. NMW 99234, 16, 24.9-31.2 mm SL, four voucher specimens for CO1 (MN747015, 29.5 mm SL; MN747016, 27.2 mm SL; MN747017, 24.3 mm SL; and MN747018, 22.8 mm SL), two vouchers for cytb (MN747022, 29.5 mm SL; and MN747023, 27.2 mm SL) and three C&S specimens in a separate jar (23.4-29.0 mm SL), all same date and locality as holotype. NMW 99235, 21, 17.4-24.1 mm SL, same date and locality as holotype. NMW 99259, 13, 24.4-33.4 mm SL, three C&S specimens in a separate jar (25.6-37.6 mm SL), same date and locality as NMW 99232. NMW 99487, 25, 20.4-42.2 mm SL, Awash River at Aditu [Adayitu], downstream of the bridge (site 3; 11°7'46"N, 40°45'52"E; 465 m a.s.l.), Afar Region, Ethiopia, 12.03.2019, coll. G.K. Englmaier, G. Tesfaye, P. Meulenbroek and H. Waidbacher. NMW 99488, 13, 20.9-32.6 mm SL, two voucher specimens for cytb (MN747024, 32.9 mm SL; and MN747025, 28.4 mm SL), same date and locality as NMW 99487. NMW 99493, 17, 26.2-33.8 mm SL, Awash River at Dubti (site 4; 11°41'50"N, 41°7'22"E; 375 m a.s.l.), Afar Region, Ethiopia, 13.03.2019, coll. G.K. Englmaier, G. Tesfaye, P. Meulenbroek and H. Waidbacher. NMW 99494, 8, 17.2-33.9 mm SL, two voucher specimens for cytb (MN747026, 41.0 mm SL; and MN747027, 42.8 mm SL) same date and locality as NMW 99493. NMW 99500, 4, 8.0-22.2 mm SL, western shore of Lake Gamari (site 5; 11°30'54"N, 41°38'57"E; 342 m a.s.l.), Afar Region, Ethiopia, 14.03.2019, coll. G.K. Englmaier, G. Tesfaye, P. Meulenbroek and H. Waidbacher. NMW 99501, 5, 8.9-23.2 mm SL, two voucher specimens for cytb (MN747028, 36.5 mm SL; and MN747029, 43.1 mm SL), same date and locality as NMW 99500. NMW 99639, 1, 28.7 mm SL, eastern shore of Lake Yardi (site 1; 10°14'41"N, 40°32'44"E; 565 m a.s.l.), Afar Region, Ethiopia, 21.05.2018, coll. G.K. Englmaier and G. Tesfaye. NMW 99640, 5, 30.3-42.9 mm SL, same date and locality as NMW 99487. NMW 99641, 8, 31.9-46.7 mm SL, same date and locality as NMW 99493. NMW 99642, 2, 25.6-52.9 mm SL, same date and locality as NMW 996500.

Diagnosis.

Enteromius yardiensis sp. nov. belongs to a phenotypic group characterised by small size and the last unbranched dorsal-fin ray thickened and serrated. The new species is readily distinguished from its Ethiopian congeners by three unique specialisations: the absence of the anterior barbel, the absence of the medial branch of the supraorbital cephalic canal and few, 1-3, commonly two, scale rows between lateral line and anus. It further differs by posterior barbel usually shorter than half eye diameter; eye large, its diameter 24-34 % HL; snout short and pointed; lateral line complete and strongly curved; scales in the lateral series 32-35; few transversal scale rows between lateral line and pelvic-fin base (1-3); scale rows between dorsal- and pelvic-fin origins 7-10; often four unbranched dorsal-fin rays; few branched pectoral-fin rays, commonly 12 or 13; 17 or 18 abdominal vertebrae; 10-12 predorsal abdominal vertebrae; and 6-9 vertebrae between first pterygiophores of dorsal and anal fins.

Description.

Morphometric and meristic characters of the holotype are in Tables 2 , 4 - 5 . The general appearance of E. yardiensis is shown in Figs 6 , 7 , dorsal fin in Fig. 8 , sensory canals in Fig. 9A , axial skeleton in Fig. 10A and relative measurements of the holotype and paratypes are given in Table 2 and Suppl. material 1, Table S3. Variations in 14 meristic characters and numerically coded types of posterior barbel length are provided in Table 4 , and data on the number of serrae on last unbranched dorsal-fin ray in Table 5 .

Longest examined specimen 52.8 mm SL (NMW 99642, Fig. 6B ). Body markedly compressed. Dorsal head profile slightly concave, its transition to back smooth, slight nuchal hump only present in few larger individuals (more than 35 mm SL). Head commonly longer than body depth at pelvic-fin origin.

In most specimens, predorsal back outline steeply rising to dorsal-fin origin. Postdorsal back outline slightly convex or straight to end of caudal peduncle. Head depth at nape not exceeding HL. Snout pointed and relatively short, its length not exceeding eye horizontal diameter. Mouth terminal, tip of mouth cleft on about level of middle of eye, mouth cleft straight. Posterior barbel short (coded length 2), shorter than half eye diameter. Anterior barbel absent in all specimens (17.9-52.8 mm SL) but foramen for its nerve present in maxillary (examined in six C&S specimens). Eye large, its horizontal diameter greater than snout length but shorter than lower jaw length. Eye diameter negatively correlated with SL (R = -0.72 Spearman’s rank correlation, N = 39). Interorbital width is commonly less than eye horizontal diameter.

Dorsal fin with three or four unbranched and eight branched rays. Last unbranched ray moderately thickened and densely serrated. Serration extending over more than 76 % of ray non-segmented part (range 62-86 %) and lower non-serrated part relatively short and not strongly thickened (Table 2 , Fig. 8 ). Number of serrae ranging from 10 (<25 mm SL) to 27 (> 50 mm SL) and positively correlated with size (R = 0.96, Spearman's rank correlation). In case of four unbranched rays (in 32 % of examined specimens, Table 4 ), first ray often small and only visible in radiographs or in C&S individuals (Fig. 8 ). Predorsal body long and dorsal-fin origin placed behind origin of pelvic fin. Dorsal-fin depth slightly shorter than HL. Anal fin with three unbranched and six branched rays, reaching to about middle of caudal peduncle. Pelvic fin with one unbranched and commonly seven branched rays (Table 3 ), commonly reaching behind anus and rarely to anal-fin origin. Pelvic splint variable in length but relatively short (19-32 % of pelvic-fin length). Pectoral fin with one unbranched and commonly 12 or 13 branched rays (Table 4 ), commonly not reaching pelvic-fin origin. Pectoral, pelvic and anal fins of about similar length (Table 2 ). Caudal fin forked with 2+17 principal rays (commonly eight in upper lobe and seven in lower lobe). Upper procurrent rays 7 (11), 8 (17) or 9 (1), lower procurrent rays 6 (2), 7 (25) or 8 (2).

Lateral line complete (in all specimens with well-preserved scales) and clearly downwardly curved on the body going along midline on posterior half of caudal peduncle. Total lateral series with 32-35, commonly 33, scales (Table 4 ). Circumpeduncular scale rows 12-14 (mode 13 (6), N = 11). Back, belly and chest fully scaled. Short axillary scale present at pelvic-fin base.

Five infraorbital bones (io) but io4 often fragmented into two. Bones io3 to io5 wide, covering most surface of cheek in front of preoperculum; io5 as wide as deep or wider as deep (in larger specimens, Fig. 9A ).

Supraorbital canal complete lacking medial branch of supraorbital canal in all specimens (Fig. 9A ). Infraorbital and supratemporal canals complete. Preoperculo-mandibular canal complete between lower jaw and preoperculum and not communicating with postocular commissure of infraorbital canal; preopercular section of this canal terminating at upper margin of preoperculum or continuing into suprapreopercular segment fused to antedorsal process of operculum terminating by free pore over its upper margin or somewhat below.

Total vertebrae few, 33 (most commonly, Fig. 10A ) or 34; other vertebral counts given in Table 4 . Supraneurals 5-6, first three or four square-shaped and two or three in front of dorsal fin deeper and elongated.

Gill rakers in outer row of first gill arch 10 (5), 11 (4) or 12 (1), with eight or nine on lower limb and two on upper limb. Pharyngeal teeth thin and slightly hooked, not serrated, 2.3.5-5.3.2.

In four examined specimens (23.4-29.1 mm SL), length of digestive tract (not stretched) about 82-107 % of SL. Intestine folded in simple loop before reaching anus.

Mature females were observed during mid of dry season at sizes less than 40 mm SL (36.7-39.4 mm SL, N = 4). Early stage of maturation (the developing phase of the reproductive cycle according to Brown-Peterson et al. (2011)) in females was found between 28.9-29.5 mm SL (N = 2).

Colouration.

In life (Fig. 7 ), overall silvery, with greenish brown back. Greenish iridescence especially at nape and upper eye. Fins pale, base of pectoral, pelvic and anal fins sometimes faintly pinkish, caudal-fin base brownish. No stripe or blotches. Most ethanol-preserved specimens (Fig. 6A ) overall silvery with much shine at midline, ventral and opercular regions. Other body parts brownish orange or silvery grey. Fins pale, base of caudal fin and, often, anterior part of dorsal-fin base ash-grey. Formalin (initial fixation) and later transferred to 75 % ethanol (Fig. 6B ) specimens creamy to yellowish, formalin-deposited whitish. Back greyish brown, posterior head brownish black. Narrow black mid-lateral stripe usually of increasing intensity at caudal peduncle but not reaching caudal-fin base. Ventral body (especially bases of pectoral and anal fins) often yellowish. Fins pale, anterior part of dorsal-fin base brownish. Sparse melanophores on rays of dorsal, caudal and anal fins.

Distribution and habitat.

The new species was found so far only in the Lower Awash River and interconnected lakes (Fig. 1 ). The altitude ranges from 565 m a.s.l. (10°14'41"N, 40°32'44"E) to 342 m a.s.l. (11°30'54"N, 41°38'57"E). This wetland area is a part of the extensive Afar lowland which is a geological depression caused by the Afar Triple Junction, connected in the south to the north-eastern segment of the Main Ethiopian Rift ( Beyene and Abdelsalam 2005).

Specimens were abundant in shallow shoreline habitats of the main channel (low flow velocity), deep (max. 1.5 m) stretches of side channels, stagnant water bodies of the adjacent floodplain, and the shoreline of lakes (Fig. 11 ). A preference for structured habitats with aquatic plants, woody debris, dense river bank vegetation and fine substrate (sand and finer fractions) was noted. A pronounced difference between wet and dry season is characteristic for the area. The water was usually turbid (suspended solids). Water temperature ranged from 26.1 °C to 31.9 °C.

Gut contents examined from type locality (N = 15) contained unidentifiable fine organic detritus and remains of planktonic crustaceans (exuviae of Phyllopoda ( Cladocera ), Copepoda , Rotatoria) but also nematodes, remains of terrestrial arthropods (beetles), diatoms, larger plant material (e.g., leaf parts), seeds, and wood debris, and some non-organic material (sand grains).

The lowland fish fauna of the Awash River is dominated by cyprinids ( E. yardiensis sp. nov., Garra makiensis (Boulenger, 1903) (in Boulenger 1903b), G. dembeensis ( Rüppell, 1835), Labeobarbus intermedius ( Rüppell, 1835) and introduced Cyprinus carpio Linnaeus, 1758 but also includes Micropanchax antinorii (Vinciguerra, 1883), Oreochromis niloticus (Linnaeus, 1758), Coptodon cf. zillii and Clarias gariepinus (Burchell, 1822) ( Golubtsov et al. 2002; Englmaier 2018).

Etymology.

The species name yardiensis refers to Lake Yardi, where the new species is abundant.

Comparative remarks.

Our data confirm the assumption that E. yardiensis sp. nov. belongs to the group of E. paludinosus -like smiliogastrin barbs. Based on data from Greenwood (1962) and Golubtsov and Berendzen (2005) (the latter for E. kerstenii from Lake Chamo-Abaya basin), the new species is different from the E. kerstenii complex by the absence of an orange or yellow blotch on the operculum (vs. presence) and 32-35 total lateral-series scales (vs. 23-27 in the lateral line that equals to lateral series in case lateral line is complete).

Enteromius yardiensis sp. nov. clearly differs from all examined species (Tables 2 - 5 ) and still unidentified forms (or undescribed species) in the group of E. paludinosus -like fishes by the absence of the anterior barbel, the absence of the medial branch of the supraorbital cephalic canal and few, 1-3, commonly two, scale rows between lateral line and anus.

Comparison of E. yardiensis sp. nov. with Ethiopian congeners. Besides the characters mentioned above, E. yardiensis sp. nov. is readily distinguished from the E. pleurogramma syntypes (Lake Tana basin, Upper Blue Nile) by a set of characters: commonly seven branched pelvic-fin rays (vs. eight); 33-34 total vertebrae (vs. 35); 17-18 abdominal vertebrae (vs. 19-20); 6-9, commonly seven, vertebrae between first pterygiophores of the dorsal and anal fins (vs. 8-9, commonly nine); 32-35, commonly 33, total lateral-series scales (vs. 34-36); and 1-3, commonly two, scale rows between the lateral line and the pelvic-fin origin (vs. four) (Table 4 ).

Literature data confirm the distinctiveness of the new species and E. pleurogramma from Lake Tana which is characterised by 7-9, commonly eight, branched pelvic-fin rays; 34-36, commonly 35, total vertebrae; 32-37, commonly 35, total lateral-line scales; and 4-6 scale rows between the lateral line and the pelvic-fin origin ( Dejen et al. 2002; Golubtsov and Berendzen 2005).

Enteromius yardiensis sp. nov. can be further distinguished from E. akakianus (including the holotype of the latter species, Fig. 12A ) by 12-14, commonly 13, branched pectoral-fin rays (vs. 16); 33-34 total vertebrae (vs. 35-37, Fig. 10B ); 17-18 abdominal vertebrae (vs. 20-21); 6-9, commonly seven, vertebrae between first pterygiophores of the dorsal and anal fins (vs. 10-11); 32-35, commonly 33, total lateral-series scales (36-37); and posterior barbel coded length 1-2 (vs. 3-4) (Table 4 ).

Enteromius akakianus (Akaki River, Upper Awash drainage) is similar to the CMER combined sample (Fig. 12B, C ) by most characters (Tables 3 - 5 ).

Enteromius yardiensis sp. nov. differs from the CMER Enteromius by 12-14, commonly 13, branched pectoral-fin rays (vs. 12-16, commonly 15); 33-34 total vertebrae (vs. 34-37); 17-18 abdominal vertebrae (vs. 19-20, commonly 20); 6-9, commonly seven, vertebrae between first pterygiophores of the dorsal and anal fins (vs. 8-12, commonly 10); 32-35, commonly 33, total lateral-series scales (vs. 34-37, commonly 35); posterior barbel coded length 1-2 (vs. 2-4, commonly 3) (Table 4 ). Enteromius yardiensis sp. nov. is further distinguished from the CMER samples by a wider than deep io5 (vs. deeper than wide, Fig. 9B ).

We did not examine specimens from the Didessa River (tributary of the Blue Nile), the White Nile and the Omo River and refer to published data ( Golubtsov and Berendzen 2005) for a comparison. These populations are identified as E. paludinosus ( Golubtsov and Berendzen 2005) or as a member of the E. pleurogramma complex ( Mina et al. 2017). Enteromius yardiensis sp. nov. can be readily distinguished by the absence of the anterior barbel (vs. always present); 12-14 branched pectoral-fin rays (vs. 13-17); 33-34, commonly 33, total vertebrae (vs. 33-36, commonly 34-35); predorsal length 53-58 % SL (vs. 46-55 % SL). Data on cytb located Didessa Enteromius close to E. pleurogramma but as a still distant (p-Euclidean distance 6.6-6.8 %) and well supported clade (Fig. 3 , Suppl. material 1, Table S4).

Comparison of E. yardiensis sp. nov. with East African congeners outside Ethiopia. All morphological analyses of the type series of E. paludinosus and E. longicauda (both are from the Lower Zambezi) revealed their closest morphological affinities. This brings additional support to Greenwood’s (1962) and Seegers’ (1996) synonymisation of the two species, with priority to the name paludinosus . Enteromius yardiensis sp. nov. differs clearly from E. paludinosus samples (which combine the type specimens of E. paludinosus and E. longicauda ) (Fig. 13 ) by the absence of the anterior barbel (vs. presence) and a set of counts (Table 4 ), including fewer, 1-3, mean 2.2, transversal scale rows between the lateral line and the pelvic-fin base (vs. 3-4) and between the lateral line and the anus, 1-3, mean 2.1 (vs. 4-5); fewer total vertebrae, 33-34, mean 33.2 (vs. 34-36, mean 34.3); and a higher number of predorsal abdominal vertebrae, 10-12, mean 10.9 (vs. 9-10, mean 10.0). The ranges of number of lateral-series scales largely overlap (32-35, mean 33.3 vs. 33-37, mean 34.5), but the highest count, 36 and 37, recorded in E. paludinosus were not found in the new species. A character distinguishing the two species is also the structure of the last unbranched dorsal-fin ray: in E. yardiensis sp. nov., the lower (non-serrated) part of the ray is short (less than one-third of the entire unsegmented part of the ray) (Fig. 10A ) vs. a markedly longer (much longer than one-third) lower non-serrated part of the ray in E. paludinosus (Fig. 10C ). Respectively, in E. yardiensis sp. nov., the upper serrated part is commonly longer than 75 % of the entire unsegmented part of the ray (vs. 59 % and less in E. paludinosus ).

Enteromius amphigramma (Nairobi River, Kenya [Nairobi River, Kilimanjaro]), E. loveridgii (Amala River, Kenya), E. macropristis (Lake Victoria), E. macropristis meruensis (Mount Meru, Tanzania) and E. vinciguerraii (Wembere River, Tanzania) are currently synonymised with E. paludinosus. The type series of these nominal species examined in the present study showed that they are different from E. yardiensis sp. nov., first of all, by the presence of the anterior barbel, which is well-developed in all species including small-sized E. vinciguerraii .

Enteromius yardiensis sp. nov. shares with E. macropristis meruensis and E. vinciguerraii such characters as a high number of predorsal abdominal vertebrae (10-12) and a lower number of vertebrae between the first pterygiophores of the dorsal and anal fins (6-9). However, the new species is well distinguished from the two by fewer vertebrae: 33-34 total and 17-18 abdominal (vs. 35-36 and 19, respectively) and the absence of a small distinct dark spot at the end of the caudal peduncle (vs. presence).

Within the group of small-sized African smiliogastrin barbs with a thickened and serrated last unbranched dorsal-fin ray outside Ethiopia, a very short or vestigial anterior barbel was reported in E. apleurogramma (Boulenger, 1911) from Lake Victoria, E. amboseli (Banister, 1980) from the Middle Athi River in Kenya ( Boulenger 1911, Banister 1980, Schmidt et al. 2018), and specimens identified as E. paludinosus from Satansplatz in South Africa (nowadays Namibia, Orange River drainage, Atlantic basin) ( Greenwood 1962: 162). Neither E. apleurogramma nor E. amboseli has been reported from Ethiopian drainage systems. Enteromius yardiensis sp. nov. is readily distinguished from both species by a complete lateral line (vs. incomplete) and a higher number of lateral-series scales (32-35 vs. 20-25).

Figures

Figure 1. Map of Ethiopia, presenting sampling sites and examined material. Sampling sites: 1 - 13 Main Ethiopian Rift (1 - 5 Lower Awash R., distribution of Enteromius yardiensis sp. nov.; 6 - 12 lakes and rivers in Central Main Ethiopian Rift; 13 Akaki R., type locality of E. akakianus); 14 - 15 Blue Nile drainage, type locality of E. pleurogramma. In blue, known populations of small-sized E. paludinosus - like smiliogastrin barbs in Ethiopia. Locations in southern Africa included in CO 1 and cytb analyses in red, green, and purple. Distribution data for Ethiopian populations from Golubtsov and Berendzen (2005).

Figure 3. Maximum Likelihood (ML) analysis, 520 bp of partial cytb. Posterior probabilities from BI analysis and bootstrap (bs) values for ML (1000 bootstrap replications) above and below slash. Values below 0.70 / 50 considered as collapsed. Colours corresponding to those in Fig. 1.

Figure 6. General appearance of Enteromius yardiensis sp. nov. A holotype, BMNH 2019.10.10.1, side channel of Awash R. at Kada Bada (site 2), 40.2 mm SL, The Trustees of the Natural History Museum, London B longest paratype, NMW 99642, Lake Gamari (site 5), 52.8 mm SL.

Figure 7. Enteromius yardiensis sp. nov. alive, paratype, NMW 99640, Awash R. at Aditu (site 3), 35.4 mm SL. Photograph by W. Graf.

Figure 8. Dorsal fin in Enteromius yardiensis sp. nov., paratype, NMW 99259, side channel of Awash R. at Kada Bada (site 2), 37.6 mm SL, with four unbranched rays. Arrow 1 showing first unbranched dorsal-fin ray, arrow 2 showing relative positions of tip of penultimate (3 rd) unbranched dorsal-fin ray and lowermost limit of serrated part of last (4 th) unbranched dorsal-fin ray.

Figure 9. Alizarin-stained specimens showing cephalic sensory canals and infraorbitals in A Enteromius yardiensis sp. nov. (same specimen as in Fig. 8) B Enteromius sp. CMER, NMW 99237, Lake Ziway (site 8), 34.8 mm SL. Arrows showing part of frontal with no canal in A and medial branch of supraorbital canal (CSO) in B.

Figure 10. Axial skeletons of Enteromius. A E. yardiensis sp. nov. (same specimen as in Fig. 6 B), 11 showing last predorsal abdominal vertebra and 18 last abdominal vertebra, total vertebrae 33: 18 + 15 B E. akakianus, holotype, BMNH 1908.1.20.85, Akaki R. (site 13), 66.0 mm SL, 10 showing last predorsal abdominal vertebra and 21 last abdominal vertebra, total vertebrae 37: 21 + 16, The Trustees of the Natural History Museum, London C E. paludinosus, paralectotype, BMNH 1861.3.10.6 - 7, Quellimane Mozambique, 50.0 mm SL, 10 showing last predorsal abdominal vertebra and 19 last abdominal vertebra, total vertebrae 34: 19 + 15, The Trustees of the Natural History Museum, London. Arrows showing relative positions of tip of penultimate unbranched dorsal-fin ray and lowermost limit of serrated part of last unbranched dorsal-fin ray.

Figure 11. Habitat of Enteromius yardiensis sp. nov. A Side channel of Awash R. at Kada Bada (site 2; 10 ° 13 ' 53 " N, 40 ° 34 ' 43 " E; 562 m a. s. l.), type locality of E. yardiensis sp. nov. B Lake Yardi (site 1; 10 ° 15 ' 10 " N, 40 ° 32 ' 9 " E; 562 m a. s. l.).

Figure 12. General appearance of A Enteromius akakianus (same specimen as in Fig. 10 B) The Trustees of the Natural History Museum, London B Enteromius sp. CMER, NMW 99239, Labo R., Meki R. drainage (site 6), 70.4 mm SL C Enteromius sp. CMER, NMW 99238, Lake Ziway (site 7), 45.4 mm SL.

Figure 13. General appearance of Enteromius paludinosus (same specimen as Fig. 10 C) The Trustees of the Natural History Museum, London.