Redescription of Moenkhausia melogramma (Characiformes: Characidae), a poorly known tetra from the western Amazon basin

Moenkhausia melogramma is herein redescribed, based on the examination of the holotype plus additional specimens from the western Amazon basin in Brazil, Colombia, Peru, and Ecuador. Moenkhausia melogramma shares with M. collettii, M. conspicua, M. copei, M. venerei, and M. flava a broad dark longitudinal stripe across the eye, and a well-defined dark stripe on the anal-fin base. It can be promptly distinguished from these species by having two humeral blotches. Additionally, we provide comments on the putative relationships of Moenkhausia melogramma with the aforementioned congeners and the Hemigrammus lunatus species-group.

Moenkhausia melogrammus was described by Eigenmann (1908) based on a single specimen from upper Amazon basin in Tabatinga, Amazonas State, Brazil (MCZ 20825), which was collected during the Thayer Expedition and was only described 43 years later (Fig. 1). The name of the species was later amended to M. melogramma by Eigenmann (1910). The original description only mentioned the number of fin rays, the misalignment of the third premaxillary tooth of the outer row in relation to the other teeth, and general color pattern, characterized by the absence of blotches, presence of a faint stripe along mid-body, and presence of a dark stripe along the anal-fin base. Later, Eigenmann (1917: 78-79) provided a more detailed description of the species, including a retouched picture of the holotype (pl. 6, fig. 1) but, once again, solely based on the holotype. Géry (1977) proposed an artificial key to Moenkhausia and divided the genus into three groups of species -M. lepidura, M. grandisquamis, and M. chrysargyrea -according to the shape of body, number of scales above and below lateral line).
3/17 ni.bio.br | scielo.br/ni Géry (1977) placed M. melogramma within the M. grandisquamis group, composed by deep-bodied species, with five scale rows above and three or four rows below lateral line, whereas M. collettii (Steindachner, 1882) andM. copei (Steindachner, 1882) were allocated in the M. lepidura group, composed by small species with body depth usually more than 2.75 in the standard length. Since then, other than citations in checklists and catalogs (which did not add any additional information on the species) there was little mention for the species in the literature.
Moenkhausia melogramma was commonly misidentified as M. collettii or even as Hemigrammus lunatus Durbin, 1918 in fish collections, since these species are very similar in color and shape. In this context, our main goal is to redescribe M. melogramma, based on the examination of the holotype and additional material, including topotypes, identified during examination of extensive material by the first author. Additionally, we updated the geographic distribution of M. melogramma, and discussed the putative relationships between species sharing a broad dark longitudinal stripe across the eye and a dark longitudinal stripe on the anal-fin base.

MATERIAL AND METHODS
Counts and measurements were taken on the left side of specimens whenever possible, using a digital caliper with precision of 0.1 mm, and the methodology follow Fink, Weitzman (1974) and Menezes, Weitzman (1990), with addition of head depth, which was measured at the vertical through the tip of the supraoccipital spine. Measurements are given as percentage of standard length (SL), except subunits of head that are given as percentage of head length (HL). Counts of vertebrae, supraneurals, procurrent caudal-fin rays, and unbranched rays of the anal fin were taken from cleared and double-stained specimens (c&s) prepared according to Taylor, Van Dyke (1985). Total vertebral counts include the Weberian apparatus, counted as four elements, and the fused PU1+U1 counted as a single vertebral element. The gill raker at the junction of the ceratobranchial and the epibranchial is included in the count of gill rakers of the lower limb.
Counts and measurements of holotype were taken by the last author (RCB), while vertebral, supraneurals, and procurrent caudal-fin rays counts were taken from radiograph of the holotype, available on the website of the Museum of Comparative Zoology (MCZ). Counts are followed by the total number of examined specimens, which is given first, followed by the number of cleared and stained individuals (if any); asterisks indicate values for the holotype. The map was prepared using QGis 3.4.6 Madeira (QGIS Geographic Information System, 2020). Institutional abbreviations are listed as in Sabaj (2019).  Ibarra, Stewart, 1989:369, 377 [in part;Ecuador, río Napo basin; abundance]. Hemigrammus cf. lunatus (not Durbin). -Galacatos et al., 1996:881, 889 [in part; Ecuador, río Napo basin; abundance]. - Galacatos et al., 2004:40-41, 44, 48   Description. Morphometric data summarized in Tab. 1. Body compressed, moderately deep; greatest body depth anterior to dorsal-fin origin. Dorsal profile of head convex from tip of snout to anterior nostrils, straight to slightly concave from anterior nostrils to tip of supraoccipital spine. Dorsal profile of body moderately convex from tip of supraoccipital spine to dorsal-fin origin, posteroventrally slanted and straight from latter point to adipose fin, and slightly concave to straight along caudal peduncle. Ventral profile of body convex from anterior tip of lower jaw to pelvic fin; straight to slightly convex from pelvic-fin origin to anal-fin origin; posterodorsally slanted and straight along anal-fin base, and slightly to moderately concave along caudal peduncle.
Supraneurals four* (6), "I" or "Y" shaped with laminar bone almost along entire length. Precaudal vertebrae 15* (6); caudal vertebrae 18* (3) or 19 (3) Fig. 3) and in the photo of one specimen provided by Galvis et al. (2006: 468, pl. 43 b). Overall color pattern clear, dorsum light grey, with an olive hue; top of head with metallic green-coppery color; midline with metallic green color, especially intense in area immediately before first humeral blotch. Lower portion of head and abdominal region clear, with silvery hue. Area immediately above anal fin slightly translucent. Fins mostly hyaline, yellowish pigmentation on anterior portion of dorsal, anal, and pelvic fins; tip of dorsal and anal fins whitish in some specimens. Black markings as in preserved specimens.
Sexual dimorphism. Mature males possess bony hooks on pelvic-and anal-fin rays or only on anal-fin rays. Pelvic fin with one small and slender bony hook per lepidotrichium segment, arranged along the middle portion of the unbranched ray and anteriormost first to second branched fin rays. Anal fin with one or two (rarely three) pairs or unpaired bony Geographic distribution. Moenkhausia melogramma is distributed across the western portion of the Amazon basin in Brazil, Colombia, Peru, and Ecuador, with its easternmost records for the rio Curuá and rio Tapajós basins on the lower Amazon basin (Fig. 4). Although we have examined only two lots of M. melogramma from Ecuador in the present study, a cursory examination of the material identified as Hemigrammus lunatus from both the Napo and Putumayo basins in Ecuador, deposited at FMNH and MEPN, by one of the authors (FCTL), showed it to belong mostly to M. melogramma (see also comments in Ota et al., 2019: 343). Records in the literature for the species, outside the range discussed above (Lasso et al., 2004) are discussed in the "Remarks" below.
Ecological notes. Moenkhausia melogramma was collected in moderate to relatively large clearwater terra firme streams, in the area of Tabatinga and Benjamin Constant, FIGURE 4 | Distribution of Moenkhausia melogramma in the western Amazon basin. Red star represents the type locality; black circles represent remaining known localities (one symbol may represent more than one lot).
10/17 ni.bio.br | scielo.br/ni Amazon State, western Amazon basin of Brazil, and both black and slightly muddy water terra firme streams in the rio Juruá basin, Acre State (Flávio C. T. . The species was collected in the same type of habitat in the region of Leticia, Colombia (Galvis et al., 2006: 221). Moenkhausia melogramma was considered to be ubiquitous in both piedmont (235-295 m asl) and lowland (below 220 m asl) areas in the río Napo basin (Galacatos et al., 1996;as Hemigrammus cf. lunatus, in part). Moenkhausia melogramma was collected in syntopy with M. collettii at the lago Amanã, rio Solimões basin (INPA 32161) and in a tributary of the middle rio Madeira (ZUEC 6736). The species was found to be an omnivore, ingesting terrestrial invertebrates and aquatic vegetation (Galvis et al., 2006: 221).

Conservation status.
Moenkhausia melogramma is broadly distributed across the western Amazon basin, in relatively little disturbed areas, and it is considerably abundant at several sites. The species is known to occur in at least three Conservation Units: Canutama State Forest and Canutama Extractive Forest (rio Purus), both in Brazil, and at the Yasuní National Park in Ecuador. Due to broad geographical distribution, relatively high abundance, and relatively little impact from anthropogenic activities in the areas inhabited by the species, M. melogramma is herein categorized as Least Concern (LC), according to the International Union for Conservation of Nature (IUCN) categories and criteria (IUCN Standards and Petitions Subcommittee, 2017).

Remarks.
Despite recorded in the literature, we were unable to confirm the occurrence of Moenkhausia melogramma from the río Orinoco basin (Lasso et al., 2004: 115). We consider this record as very likely the result of a misidentification of a similarlooking species occurring in that basin, such as Hemigrammus barrigonae Eigenmann, Henn, 1914 or M. collettii. The only previous records for the species in the literature that we were able to confirm were those by Arbeláez et al. (2004) and Galvis et al. (2006), from the region of Leticia in Departamento Amazonas, Colombia, from which the voucher material (not cited in the Material Examined) was cursorily examined by one of the authors (FCTL) during a visit to the ICN-MHN and IAvH-P collections.  106697, 11, 21.2-44.6 mm SL (8, 21.2-44.6 mm SL), Mazuko, río Planchon, 36.3 km N of Puerto Maldonado, 12°16'38"S 69°9'9"W, 28 Jul 2010, J. L. Birindelli, N. Lujan, D. Taphorn & D. Brooks. Río Marañón basin: MUSM 25616, 8, 17.6-33.0 mm SL, Andoas, near río Corrientes, 2°33'53.7"S 76°11'53.1"W, 18 Aug 2005MUSM 38008, 9, 29.6-37.6 mm SL, Andoas, río Plantayacu, 3°8'8.4"S 75°45'43.5"W, 18 Aug 2008, R. Quispe. (1908) mentioned that the color pattern of Moenkhausia melogramma consisted in the presence of a line along the anal-fin base, a faint longitudinal midlateral dark stripe, and absence of blotches. Topotypes and additional material from other localities in western Amazon revealed that M. melogramma also possess other conspicuous pigmentation features, i.e., a broad dark stripe across the eye, and two humeral blotches, the first vertically elongated, and the second faint and inconspicuous. Although Eigenmann (1908Eigenmann ( , 1917 did not refer to the presence of the dark stripe across the eye, the examination of a picture of the holotype revealed that this feature is still discernible. The humeral blotches, however, cannot be in fact discerned in the holotype (Fig. 1). The holotype pigmentation is currently faded and judging from the retouched picture provided by Eigenmann (1917: pl. 6, fig. 1), it already was at the time of its description, so the lack of humeral blotches is considered as a preservation artifact.

Eigenmann
Among congeners, Moenkhausia melogramma shares with M. collettii, M. copei, M. venerei, M. conspicua, and M. flava the presence of a broad longitudinal dark band across the eye, and a well-defined dark stripe on the anal-fin base (see Diagnosis). Among the aforementioned species, M. melogramma is more similar to M. flava due to the absence of a large longitudinal midlateral stripe, presence of six rows of scales between dorsalfin origin and lateral line, and four rows of scales between lateral line and pelvic-fin origin. However, M. melogramma differs from M. flava by the presence of two humeral blotches, the first very conspicuous (vs. only one inconspicuous humeral blotch), and by the general clear body color pattern in live specimens (vs. pale-yellowish -see Britzke et al., 2018: fig. 4).
The presence of a broad stripe across the eye and a dark stripe along the anal-fin base are color features that Moenkhausia melogramma also shares with the Hemigrammus lunatus species-group (sensu Ota et al., 2014;2019), which is composed by H. barrigonae, H. lunatus, H. machadoi Ota, Lima, Pavanelli, 2014, H. ulreyi (Boulenger, 1895 Additionally, the species differs from Hemigrammus machadoi, the most similar noncongener species, by having a higher number of precaudal (15 vs. 13-14) and lower number of caudal vertebrae (18-19 vs. 21), 5-8 (mode 6) gill rakers on upper limb and 9-13 (mode 11) gill rakers on lower limb (vs. 4-5, mode 5 and 9-10, mode 10, respectively) of the first branchial arch. Furthermore, M. melogramma is larger (reaching 50 mm SL), whereas H. machadoi is smaller (never surpassing 35 mm SL). Ota et al. (2014), when discussing the Hemigrammus lunatus species-group, highlighted the similarity between those species with M. collettii and congeners with similar color pattern (i.e., a broad stripe across the eye and a dark line along anal-fin basin), that it might indicate a close relationship between the latter species and this species-group. This putative monophyletic group had been partially supported by molecular hypotheses, that recovered a clade composed by the aforementioned species plus M. hemigrammoides Géry, 1965and Aphyodite grammica Eigenmann, 1912(Mariguela et al., 2013Britzke et al., 2018;Mirande, 2019).
In fact, as argued by Britzke et al. (2018), the putative close relationship between M. collettii, M. copei, and M. flava with H. unilineatus Gill, 1858, the type species of Hemigrammus, highlights the weakness of the degree of lateral line perforation as a diagnostic character to distinguish both genera. As earlier remarked by Weitzman, Fink (1983), this character clearly is highly homoplastic, with non-homologous reductions occurring many times within Characidae. The presence of the discontinuous lateral line is a rare condition in M. melogramma, and it also occurs in some specimens of M. collettii and M. copei, even though the pores and canals extend to caudal fin in all specimens analyzed (Isabel M. Soares, 2020, pers. obs.).
A phylogenetic analysis including the species of Hemigrammus lunatus species-group and the similar-looking species of Moenkhausia (i.e., M. collettii, M. copei, M. conspicua, M. flava, M. melogramma, and M. venerei) is currently being conducted by the first author to test the relationships within this putative monophyletic clade and its relationships with the remaining Characidae.