A new sexually dichromatic miniature Hyphessobrycon (Teleostei: Characiformes: Characidae) from the Rio Formiga, upper Rio Juruena basin, Mato Grosso, Brazil, with a review of sexual dichromatism in Characiformes

Introduction

Hyphessobrycon Durbin 1908 is currently one of the most species-rich genera of Characidae, comprising 144 valid species (Eschmeyer et al., 2017), with at least one quarter of its diversity described in the last decade (Dagosta et al., 2016). The genus is distributed from Atlantic slope rivers in southern Mexico to the Río de La Plata basin in Argentina (Eschmeyer et al., 2017) and its greatest species diversity occurs in the Amazon basin (Lima et al., 2003).

Monophyly of Hyphessobrycon has been questioned by several authors (Géry, 1977; Weitzman & Fink, 1983; Weitzman & Palmer, 1997), but only recently has the paraphyletic nature of the genus been demonstrated (Mirande, 2009, 2010; Javonillo et al., 2010; Oliveira et al., 2011; Malabarba et al., 2012; Ohara et al., 2017). Despite several studies of Characidae phylogenetics, the genus still lacks a cladistic definition. The new species described herein is therefore assigned to Hyphessobrycon following the traditional classification system proposed by Durbin in Eigenmann (1918).

The new Hyphessobrycon species was found during an examination of the ichthyological collection of the Laboratório de Ictiologia de Ribeirão Preto (LIRP) and Museu de Zoologia da Universidade de São Paulo (MZUSP). It is a miniature species (sensu Weitzman & Vari, 1988) with a conspicuous sexual dichromatism, in which adult males present an overall red colour and females and immatures are pale yellow. This remarkable dichromatism is a rather common secondary sexual characteristic in Characidae that has been little discussed in characiforms. This paper describes the new species and comments on the sexual dichromatism present in Characiformes.

Materials and methods

Morphometric and meristic data follow Fink & Weitzman (1974) and Menezes & Weitzman (1990), with the exception of counts of horizontal scale rows below the lateral line, which were counted to the pelvic-fin insertion; and the addition of: head depth, measured at vertical through the tip of supraoccipital spine, and the distance between pelvic-fin insertion and anal-fin origin. Counts of horizontal scale rows between the dorsal-fin origin and the lateral line do not include the median predorsal series of scales situated right anteriorly to the first unbranched dorsal-fin ray. Standard length (L_S) is given in millimetres (mm). Morphometric data are expressed as percentages of L_S, except for subunits of the head, which are expressed as per cent of head length (L_H). Frequency of each count is provided in parentheses and an asterisk indicates counts of the holotype. Counts of maxillary tooth cusps, number and cusps of small dentary teeth, supraneurals, branchiostegal rays, gill rakers, vertebrae and procurrent caudal-fin rays were taken from two specimens (LIRP 11918, 18·6 and 20·2 mm L_S) that were cleared and stained (c&s) for cartilage and bone using the method of Taylor & Van Dyke (1985). Vertebrae of the Weberian apparatus were counted as four elements and the fused PU1 + U1 as a single element. Sex was determined by dichromatic colouration of the dorsal fin and confirmed by macroscopic analyses of gonads in 20 specimens (10 males and 10 females) according the methodology of Vazzoler (1996). All 20 sexed specimens were adults and were used to describe sexual dimorphism. Live colour descriptions are based on photographs and direct observations in the field.

A list of sexually dichromatic Characiformes is given in Table S1 (Supporting information) and is organized in four columns: name of taxon; type of the dichromatic pigment; temporal expression of the dichromatism; source of information of sexual dichromatism. In the list provided, most taxa are represented by species, but some encompass broader taxonomic categories (i.e. group of species, genera). In such cases, taxa were added to the list only when sexual dichromatism could be confirmed for all species of a given genera or species group.

Institutional abbreviations follow Fricke & Eschmeyer (2017): INPA, Instituto Nacional de Pesquisas da Amazônia, Manaus; MCP, Museu de Ciências e Tecnologia, Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre.

Results

Hyphessobrycon myrmex, nov. sp

urn:lsid:zoobank.org:act:EDAD2F11-632E-436F-B218-55CEEE39F247.

Holotype

MZUSP 118671 (21·0 mm L_S, male), Brazil, Mato Grosso, Campos de Júlio, Rio Formiga at PCH Divisa, upper Rio Juruena, Rio Tapajós basin; 13° 22′ 29·3″ S; 59° 08′ 35·2″ W; F. C. P. Dagosta, M. M. F. Marinho, V. Giovanetti and P. Camelier, 13 August 2015.

Paratypes

All from Brazil, Mato Grosso, Campos de Júlio, Rio Formiga at PCH Divisa, upper Rio Juruena, Rio Tapajós basin; 13° 22′ 29·3″ S; 59° 08′ 35·2″: MZUSP 118672 (106 specimens, 10·6–24·3 mm L_S); INPA 50871 (20 specimens, 12·9–23·6 mm L_S); MCP 49381 (20 specimens, 14·3–22·4 mm L_S); collected with holotype. All collected by R Ilário: LIRP 11918 (24 specimens, 2 c&s, 14·1–20·7 mm L_S, 2 c&s_, 18·6–20·2 mm L_S); May 2015; LIRP 12229 (3 specimens, 15·1–20·6 mm L_S); August 2011; LIRP 12230 (75 specimens, 11·2–21·9 mm L_S); April 2014; LIRP 12231 (51 specimens, 17·2–23·9 mm L_S); December 2011; LIRP 12249 (57 specimens, 15·6–25·6 mm L_S); October 2014; LIRP 12232 (25 specimens, 13·9–21·9 mm L_S); August 2012; LIRP 12250 (19 specimens, 18·5–24·2 mm L_S); April 2013; LIRP 12251 (8 specimens, 16·5–24·6 mm L_S); August 2013.

Diagnosis

Hyphessobrycon myrmex differs from all congeners, except Hyphessobrycon agulha Fowler 1913, Hyphessobrycon clavatus Zarske 2015, Hyphessobrycon herbertaxelrodi Géry 1961, Hyphessobrycon klausanni García-Alzate, Urbano-Bonilla & Taphorn 2017, Hyphessobrycon loretoensis Ladiges 1938, Hyphessobrycon lucenorum Ohara & Lima 2015, Hyphessobrycon margitae Zarske 2016, Hyphessobrycon metae Eigenmann & Henn 1914, Hyphessobrycon mutabilis Costa & Géry 1994, Hyphessobrycon peruvianus Ladiges 1938 and Hyphessobrycon wadai Marinho, Dagosta, Camelier & Oyakawa 2016, by having the lower half of body deeply pigmented with dark chromatophores, mainly above the anal fin, forming a broad, diffuse, dark midlateral stripe (v. absence of a longitudinal stripe, narrow stripe starting approximately at vertical through the dorsal-fin origin, or relatively narrow, well-defined, dark midlateral stripe on body extending from the posterior margin of the eye to the middle caudal-fin rays). The new species can be distinguished from the aforementioned species by the presence of a high concentration of dark chromatophores along unbranched dorsal-fin rays and distal portions of the two or three subsequent branched rays (v. dark chromatophores absent or, when present, only scattered on fin).

Description

See Fig. 1 for general body shape. Morphometric data for holotype and 29 paratypes (12 females, 17·3–23·8 mm L_S; 17 males, 18·6–23·4 mm L_S) are presented in Table I. Miniature species, largest specimen female, 25·6 mm L_S (LIRP 12249); males and females about 17·5 mm L_S already exhibiting sexual dichromatism. Body compressed, moderately short and deep. Greatest body depth slightly anterior to dorsal-fin origin. Dorsal profile of head convex from tip of snout to vertical through anterior nostril; straight from that point to anterior edge of frontal fontanel; slightly concave from this point to tip of supraoccipital spine. Dorsal profile of body convex from tip of supraoccipital spine to dorsal-fin origin; dorsal-fin base straight and posteroventrally inclined from posterior terminus of dorsal fin to adipose-fin insertion; slightly concave from adipose-fin insertion to origin of anteriormost dorsal procurrent caudal-fin ray. Ventral profile convex from tip of dentary to anal-fin origin; anal-fin base slightly convex; ventral profile of caudal peduncle slightly concave from distal tip of last anal-fin ray to origin of anteriormost ventral procurrent caudal-fin ray.

Table I. Morphometric data from the holotype (H) and 29 paratypes of Hyphessobrycon myrmex from Mato Grosso, upper Rio Formiga, Rio Tapajós drainage

	H	Paratypes
		Range	Mean	S.D.
Standard length (LS, mm)	21·0	17·3–23·8	20·2	—
% LS
Depth at dorsal-fin origin	37·6	30·8–37·7	34·6	1·3
Snout to dorsal-fin origin	54·1	50·6–55·7	53·9	1·3
Snout to pectoral-fin origin	28·6	26·6–32·2	28·9	1·9
Snout to pelvic-fin origin	50·9	45·9–53·7	50·5	1·8
Snout to anal-fin origin	66·2	61·3–70·4	65·2	0·6
Caudal peduncle depth	13·6	11·3–14·0	12·7	1·2
Caudal peduncle length	13·9	11·4–15·8	13·4	1·2
Pectoral-fin length	17·4	13·8–18·7	16·7	1·1
Pelvic-fin length	14·2	10·6–15·6	13·6	1·0
Pelvic-fin insertion to anal-fin origin	16·0	13·9–18·1	15·5	1·7
Dorsal-fin origin to anal-fin origin	36·7	30·6–38·2	34·5	1·8
Dorsal-fin origin to pelvic-fin insertion	34·6	30·3–36·8	33·6	1·6
Dorsal-fin origin to pectoral-fin insertion	38·5	36·5–43·0	38·8	1·7
Dorsal-fin length	28·1	21·2–30·2	25·7	0·9
Dorsal-fin base length	14·1	11·1–15·5	13·9	1·1
Anal-fin length	15·3	12·4–16·7	15·0	1·4
Anal-fin base length	24·2	23·5–29·1	25·9	1·3
Eye to dorsal-fin origin	40·1	35·3–42·3	39·8	1·4
Dorsal-fin origin to caudal-fin base	50·5	46·1–52·8	49·6	1·3
Head length (LH)	27·2	23·9–28·7	26·8	4·2
% LH
Head depth	103·2	103·2–117·5	109·2	2·4
Horizontal eye diameter	43·2	38·7–46·8	42·7	1·5
Snout length	24·0	22·7–28·7	25·8	2·7
Interorbital width	35·8	32·5–42·4	37·0	3·1
Upper jaw length	41·1	37·7–48·9	42·6	3·1

Upper and lower jaws aligned, mouth terminal. Premaxillary teeth in two rows: outer row with two (1), three* (28) or four (1) tricuspid teeth, median cusp more developed than others; inner row with four (6) or five* (24) pentacuspid teeth, gradually decreasing in size laterally. Maxilla with two (24), three* (5) or four (1) tricuspid teeth; posterior tip of maxilla approximately at vertical through anterior border of pupil. Dentary with four* (30) pentacuspid teeth followed by a series of five (2) small conical to tricuspid teeth. Tricuspid and pentacuspid dentary teeth with median cusp more developed than others.

Frontal fontanel wide. Sensorial canal of extrascapular not completely enclosed in extrascapular lamella. Parietal branch of supraorbital canal absent. Antorbital and infraorbitals one to three present; antorbital and first infraorbital non-ossified; fourth infraorbital, when present, restricted to a poorly ossified tube with a much reduced lamellar portion; fifth and sixth infraorbitals absent (Fig. 2). First gill arch with 15 (2) gill rakers: four (2) on epibranchial, one (2) on cartilage between epibranchial and ceratobranchial, nine (2) on ceratobranchial and one (2) on hypobranchial. Branchiostegal rays four (2), three attaching to anterior ceratohyal and one to posterior ceratohyal.

Scales cycloid, with circuli weakly marked on posterior portion of scales; usually up to four radii diverging from focus to posterior portion of scale. Lateral line incompletely pored, slightly curved ventrally, with six* (10), seven (19) or eight (1) perforated scales. Horizontal series with 30* (14), 31 (11) or 32 (5) scales. Horizontal scale rows between dorsal-fin origin and lateral line series five* (30); scale rows between lateral line and pelvic-fin origin four* (30). Single row of 10* (18) or 11 (12) predorsal scales. Circumpeduncular scale rows 12* (30). Caudal-fin scales restricted to basal portion of fin.

Supraneurals four (2); poorly ossified. Dorsal-fin rays ii, eight (3) or ii, nine* (27); dorsal-fin proximal-middle radials poorly ossified, dorsal tips of proximal-middle radials progressively less ossified and thus more cartilaginous posteriorly. Distal radials and dorsal-fin end piece predominantly cartilaginous. Dorsal-fin origin approximately at middle-body; slightly posterior to vertical through pelvic-fin origin; base of last branched dorsal-fin ray slightly posterior to vertical through anal-fin origin. First unbranched dorsal-fin ray about one-half length of second unbranched ray. Anteriormost dorsal-fin pterygiophore inserted behind neural spine of ninth centrum (2). Adipose fin present. Pectoral-fin rays i, 10* (30); tip of pectoral fin not reaching pelvic-fin insertion. Pelvic-fin rays i, seven* (30); tip of pelvic fin not reaching anal-fin origin. Anal-fin rays iii, 16* (10), iii, 17 (16) or iii, 18 (4); ventral tips of proximal-middle radials progressively more cartilaginous posteriorly. Distal radials and anal-fin end piece predominantly cartilaginous. Three anteriormost branched rays longest, subsequent rays gradually decreasing in size. Distal margin of anal fin slightly concave. Principal caudal-fin rays i, 9/8, i* (30). Caudal fin forked; lobes of similar size. Dorsal caudal-fin procurrent rays 11 (2); ventral caudal-fin procurrent rays seven (1) to nine (1). Vertebrae 32 (2). Precaudal vertebrae 14 (1) or 15 (1), caudal vertebrae 18 (1) or 17 (1).

Colour in alcohol

Overall background colouration pale yellow (Fig. 1). Dorsal portion of head and body dark. High concentration of dark chromatophores on dorsal midline of body, from tip of supraoccipital spine to adipose-fin origin. Snout and anterior portion of dentary and premaxilla with a high concentration of dark chromatophores. Ventral portion of head with few scattered chromatophores. Antorbital and first infraorbital lacking pigmentation; remaining infraorbitals and opercular region with scattered dark chromatophores. Humeral blotch present, with diffuse borders. Blotch vertically elongated; merging with midlateral stripe dorsally and encompassing approximately three scales horizontally and two vertically; middle region of humeral spot darker. A thin longitudinal line formed by embedded dark pigmentation along horizontal septum between hypaxial and epaxial muscles extending approximately from humeral region to end of caudal peduncle. Dark, broad midlateral stripe on body, extending from upper half of posterior margin of opercle to tip of middle caudal-fin rays; stripe varying in intensity among analysed specimens, wider at caudal peduncle and not forming a distinct caudal-peduncle blotch. Dark midlateral stripe less conspicuous in adult males, especially on its anterior portion. Lower half of body deeply pigmented with dark chromatophores, mainly above anal-fin base; pigments more intense in adult males. Adult males with an irregular dark blotch on anterodistal tip of dorsal fin, formed by a high concentration of dark chromatophores along unbranched dorsal-fin rays and distal portions of the two or three subsequent branched rays. Adult females and juveniles with dark chromatophores concentrated along distal portion of unbranched and first branched dorsal-fin rays. Remaining rays and interradial membranes with scattered dark chromatophores, more concentrated on distal portion of branched fin rays. Concentration of chromatophores in remaining fins not sexually dimorphic. Anal fin with sparse dark chromatophores on distal portion of unbranched and branched fin rays. Pectoral and pelvic fins with chromatophores along distal edge of unbranched and anteriormost branched rays. Adipose fin hyaline, except by distal portion with dark pigmentation. Caudal-peduncle blotch absent. Dorsal and ventralmost caudal-fin rays with dark chromatophores on its distal portion, interradial membranes of remaining branched rays with scattered dark pigmentation posteriorly. Middle caudal-fin rays darkly pigmented, continuous to dark midlateral stripe.

Colour in life

Dark colouration as in preserved specimens. Colour in life sexually dimorphic. Adult male [Fig. 3(a)] overall ground colouration red to orange, less intense between distal tip of supraoccipital process to dorsal-fin terminus. Head predominantly red with silver pigmentation in opercular region. Jaws and gular area intensely orange. Dorsal portion of pupil intensely orange, anterior margin light orange and posterior margin silver. All fins intensely orange to red, except dorsal fin, which is hyaline, with few orange chromatophores at base of last three to four branched dorsal-fin rays. Field observations revealed differences in pigmentation intensity among males, in which the largest specimens were usually the most brightly coloured.

Female [Fig. 3(b)] and juvenile overall ground colouration pale yellow. Dorsal and dorsolateral portion of the head pale yellow; jaws and gular area light yellow. Infraorbital and opercular regions silvery. Eye pigmentation yellow to orange. Dorsal and adipose fins light yellow, remaining fins light orange.

Sexual dimorphism

Sexually dichromatic species. Adult male specimens usually darker and more brightly coloured than females (see colour in alcohol and colour in life sections for further details). Additionally, adult males with distal margin of anal fin straight to slightly concave (v. always concave in females).

Geographical distribution

The new species is known from the type locality, Rio Formiga, a tributary of Rio Juruena, upper Rio Tapajós basin, Mato Grosso State, Brazil (Fig. 4).

Etymology

The specific epithet myrmex is derived from the Greek word for ant, in allusion to the small size of adult specimens of the species and also refers to the type locality, the Rio Formiga, which means ‘Ant River’ in Portuguese.

Habitat and ecological notes

The Rio Formiga is a right-bank tributary of the Rio Juína, in the headwaters of the Rio Juruena, Rio Tapajós basin. Its water is transparent and the river bottom is composed of stones, sand and a moderate amount of vegetal debris. The type locality is a hydroelectric reservoir (PCH Divisa) built in 2010 in the Rio Formiga, occupying an area of 6·8 km², where the new species can be extensively collected. Prior to the dam construction, the type locality would have resembled the adjacent up and downstream areas of the river, i.e. a relative narrow (10–15 m wide) and shallow (maximum depth approximately 1·8 m in some sites) river stretch, characterized by rapid waters and rifles.

Stomach-contents analysis based on total consumed items was based on 20 paratypes (LIRP 12232). The analysis revealed a diet based on filamentous algae (c. 10%), vascular plant tissue (c. 6%), microcrustaceans (c. 10%), Chironomidae larvae (c. 10%) and Ephemeroptera nymphs (c. 64%). The main food resources exploited by Hyphessobrycon myrmex are aquatic invertebrates, but it may be considered an omnivorous species with a tendency toward invertivory. Approximately 50% of the analysed specimens of the new species had parasitic isopods (Cymothoidae) associated with the tongue. Specimens presenting parasites exhibited a bag-shaped lower jaw, tongue atrophy and softening of the cartilaginous tissues.

Discussion

Weitzman & Vari (1988) published the first comprehensive overview on miniature fishes of South America. The authors provided a list of 85 taxa from several fish lineages classified as miniature either by reaching sexual maturity under 20 mm L_S, or by not exceeding a maximum size of 26 mm L_S. Although arbitrary, the cut-off size adopted by the authors was not the primary criterion for distinguishing miniature fishes. Rather, it also involved the presence of several apparently paedomorphic morphological features in the miniature species. This list was recently reviewed and updated by Toledo-Piza et al. (2014) increasing the number of miniatures from 85 to 213.

Hyphessobrycon myrmex can be considered a miniature species (sensu Weitzman & Vari, 1988) since the largest examined specimen was 25·6 mm L_S (n = 411) and sexual dichromatism (indicating sexual maturity) is already expressed in specimens about 17·5 mm L_S of both sexes. Furthermore, the new species exhibits some reductive osteological traits common in miniature species, such as: wide frontal fontanel; absence of the parietal branch of supraorbital canal; absence of fifth and sixth infraorbitals; reduction of the lamellar portion of the first and fourth infraorbitals (represented only by the non-ossified infraorbital canal without associated lamellar portion); extrascapular canal not completely enclosed in an extrascapular lamella; supraneurals poorly ossified; dorsal and anal-fin distal radials predominantly cartilaginous. According to Toledo-Piza et al. (2014), both the family and the genus of the taxon described herein account for most species of miniatures among Neotropical fishes and the description of another species further increases these numbers.

Rüber et al. (2007) and Britz & Conway (2009) distinguish two different types of miniature species: proportioned dwarfs, which are miniaturized copies of their relative taxa and developmentally truncated miniatures, which resemble the early developmental stages of larger relatives. Among Characiformes, very few miniature taxa exhibit osteological descriptions in sufficient detail to allow osteological comparisons and studies of miniaturization [e.g. Amazonspinther dalmata Bührnheim, Carvalho, Malabarba & Weitzman 2008, Cyanogaster noctivaga Mattox, Britz, Toledo-Piza & Marinho 2013, Iotabrycon praecox Roberts 1973; Lepidarchus adonis Roberts 1966; Paracheirodon innesi (Myers 1936); Paracheirodon simulans (Géry 1963); Priocharax spp. Weitzman & Vari 1987]. From the abovementioned taxa, most are categorized as proportioned dwarves due to their mostly complete skeletons (Mattox et al., 2016). An exception among the Characiformes is the genus Priocharax, which presents several bone losses and reductions and holds the title of the only developmentally truncated Characiformes taxon so far known (Mattox et al., 2016). Although presenting some reductive osteological characters, H. myrmex shows few anatomical losses when compared to the abovementioned species, especially when compared with Priocharax spp. In view of that, H. myrmex is herein assigned as a proportioned dwarf characid.

Another distinctive feature of H. myrmex is its sexual dichromatism [(Fig. 3(a), (b)]. Secondary sexual dimorphism is frequently reported and discussed among characiforms, mainly regarding the presence of bony hooks on fins (Wiley & Collette, 1970; Fink & Weitzman, 1974; Weitzman & Fink, 1985; Weitzman et al., 1994; Malabarba & Weitzman, 1999, 2000, 2003; Lima & Sousa, 2009; Camelier & Zanata, 2014; Vieira et al., 2016) or shape of the dorsal and anal fins (Costa & Géry, 1994; Weitzman & Palmer, 1997; Moreira et al., 2002a,b; Teixeira et al., 2013; Ingenito et al., 2013; Dagosta et al., 2014; Marinho et al., 2014; Pastana & Ohara, 2016). Although sexual dichromatism in Characidae has been known for over a century (Eigenmann, 1912, 1917), descriptions of such dimorphism are still scarce in taxonomic literature.

Sexual dichromatism is a type of dimorphism in which males and females differ in colouration (Bell & Zamudio, 2012) and can be expressed by one (e.g. melanophore) or more sets of pigments (e.g. melanophore and carotenoid-based pigments). Among Neotropical fishes, sexual dichromatism is commonly reported in representatives of the families Cichlidae (Lucena & Kullander, 1992; Kullander & Lucena, 2006; Kullander et al., 2009; Varella & Sabaj Pérez, 2014; Malabarba et al., 2015; Varella, 2016) and Cynolebiidae (Costa, 1998, 2006, 2007; Costa et al., 2012). Sexually dichromatic males of these taxa develop a very bright colour pattern, often making them very popular in the aquarium trade. Despite being known and frequently observed among Characiformes, sexual dichromatism is rarely mentioned or depicted in taxonomic descriptions. In view of that, a compilation of representatives of characiforms exhibiting sexual dichromatism is presented (Table S1, Supporting information). Although far from being complete, the list provides a starting point for future studies concerning sexually dichromatic traits in Characiformes.

In characiforms, reports of sexual dichromatism could be found for 108 different taxa, distributed in six different families (Alestidae, Characidae, Crenuchidae, Curimatidae, Lebiasinidae and Serrasalmidae) [Fig. 2 (c)–(n); Table S1, Supporting information]. The largest diversity of dichromatic Characiformes is represented by the family Characidae (57, comprising 52·7% of total), followed by Lebiasinidae and Serrasalmidae (13·8% and 12·9% of total, respectively). Within the Characidae, sexual dichromatism is known for 23 different genera (Table S1, Supporting information), with Hyphessobrycon accounting for the bulk of dichromatic species of the family (at least 19 species).

Within the Crenuchidae, most references to sexual dichromatism are available for the genus Characidium Reinhardt 1867, which is by far the most species-rich genus of the family (Eschmeyer et al., 2017). Among Characidium species, sexual dichromatism has been used as a diagnostic character (e.g. Characidium satoi Melo & Oyakawa 2015) and as a phylogenetic trait, supporting the putative monophyly of a species-group encompassing Characidium occidentale Buckup & Reis 1997, Characidium orientale Buckup & Reis 1997, Characidium rachovii Regan 1913, Characidium stigmosum Melo & Buckup 2002 and Characidium vestigipinne Buckup & Hahn 2000 (Buckup & Reis, 1997;Buckup & Hahn, 2000 ; Melo & Buckup, 2002 ; Netto-Ferreira et al., 2013 ; Mendonça & Netto-Ferreira, 2015). Adult males of these species share black bands along the distal margin of anal and pelvic fins and bright orange to red colouration on all fins (Buckup & Hahn, 2000; Melo & Buckup, 2002; Netto-Ferreira et al., 2013; Mendonça & Netto-Ferreira, 2015).

The Lebiasinidae are well known for exhibiting several sexually dimorphic characteristics, related to the standard length (Taphorn & Lilyestrom, 1980), anal-fin morphology (Fernandez & Weitzman, 1987; Netto-Ferreira et al., 2011), colour pattern (Weitzman & Cobb, 1975; Zarske, 2009) and even behaviour (Krekorian & Dunham, 1972; Menezes & Vazzoler, 1992). References to sexual dichromatism in lebiasinids are more abundant than those of remaining Characiformes. Reports of sexually dichromatic traits were found for all lebiasinid genera except Copeina Fowler 1906 (Table S1, Supporting information). Several species of the family are very colourful, which makes them common in the aquarium trade (Géry, 1977). In these species both males and females are densely pigmented with dark and red chromatophores, in such a way that the sexual dichromatism is expressed as differences in pigment intensity rather than in distribution on the body and fins (e.g. Zarske, 2009: Fig. 1).

In the Serrasalmidae sexual dichromatism is reported in six genera: Mylesinus Valenciennes 1850, Myleus Müller & Troschel 1844, Metynnis Cope 1878, Myloplus Gill 1896, Ossubtus Jégu 1992 and Tometes Valenciennes1850. Male specimens of these taxa usually exhibit darkening of unpaired fins and an overall yellow to red colouration on body (Zarske & Géry, 1999). During the reproductive season, mature males of some taxa (e.g. Tometes spp.) may even develop irregularly-shaped red spots over flanks and anal fin (Andrade et al., 2013). Serrasalmus Lacépède 1803 is the most species-rich genus of Serrasalmidae (Eschmeyer et al. 2017), but no references to sexual dichromatism in Serrasalmus spp. could be found. The lack of information of sexual dichromatism may possibly result from a scarcity of description rather than the absence of dimorphism. According to Jégu & dos Santos (2001) large specimens of some Serrasalmus species develop an overall violet colouration on the body and a darkening of unpaired fins. The authors even state that these characteristics could possibly be linked to sexual maturity and spawning season, but more study is needed to confirm these hypotheses.

Among curimatids, the genus Curimatopsis Steindachner 1876 was the only taxon for which sexual dimorphisms have been reported (Vari, 1982). Along with sexual dimorphism associated to caudal-peduncle depth (Myers, 1929; Vari, 1982), males and females of Curimatopsis also differ in the extension of the caudal peduncle spot (which is broader and extends through the middle caudal-fin rays in males) and in the intensity of caudal-fin colouration [intensely orange in males v. pale orange in females; Fig. 4(m)–(n); Sidlauskas & Vari, 2012: Fig. 9(a), (b)]. Descriptions of sexual dichromatism are, in fact, uncommon in the Curimatidae and also rare within Anostomoidea (sensu Vari, 1983). Given this context, sexual dichromatism could possibly be an additional synapomorphy for the Curimatopsis lineage.

The Alestidae are the sole family of African characiforms known to exhibit sexual dichromatism. Differences in the sexual colour pattern in alestids have already been described and explored in a phylogenetic analysis of the family by Zanata & Vari (2005). The authors concluded that sexual dichromatism is rare among alestids, being restricted to the genus Arnoldichthys Myers 1926 and Lepidarchus Roberts 1966 and expressed as differences in the concentration of black pigments (Zanata & Vari, 2005: Char. 192–195). Differing from these conclusions, the present survey revealed that sexual dichromatism in Alestidae is more widespread, occurring in six genera and is expressed as differences in intensity of both dark and carotenoid-based pigmentation (Table S1, Supporting information).

Another remarkable aspect related to sexual dichromatism concerns the type of pigments involved (Table S1, Supporting information). In Characiformes, sexual dichromatism is usually expressed by the presence or intensity of two main sets of pigments: red to orange (carotenoid-based) and black or blue (melanophore-based) pigments (Eigenmann, 1917; Table S1, Supporting information). High concentrations of carotenoid-based pigments are responsible for the presence of a vivid red to orange colouration on the bodies of males, more commonly on fins but also present on the gular area, belly and dorsal and ventral portions of the caudal peduncle. These regions tend to be vivid red on adult males of species with sexual dichromatism. These pigments may be absent or less intense in females, in which fin colour ranges from pale yellow to light orange, respectively. Dichromatism involving dark pigmentation is also displayed on body and fins. Male specimens usually exhibit a broader distribution and higher concentration of melanophores along body and fins, with pigment usually more concentrated along flanks, belly, caudal-peduncle region and on interradial membranes. Blue nuptial colouration, although less frequent in characiforms species, does occur in some characids (Table S1, Supporting information) and is commonly displayed as a blue broad stripe along the midline of the body. One or more sets of pigments can be present in a dichromatic male (Table S1, Supporting information). Hyphessobrycon myrmex is an example of a sexually dichromatic species in which both dark and carotenoid-based pigments are involved in sexual dichromatism.

Data on temporal expression of sexual dichromatism in characiforms is very scarce, being available only for a restricted set of species (Table S1, Supporting information). Information on sexual dichromatism, when present, is usually limited to descriptions of differences in colour pattern between males and females, leaving aside aspects of the temporal expression of dimorphism. According to Kodric-Brown (1998), within dichromatic fishes, differences in colouration may be permanent (developed at maturity and retained for life) or temporary (seasonal or ephemeral colour changes). With few exceptions (e.g. cichlids of the African great lakes), freshwater fish species usually show temporary sexual dichromatism, while permanent sexual dichromatism, in turn, is common among marine reef fishes (Kodric-Brown, 1998). Contrary to these expectations, H. myrmex is a permanent sexually dichromatic species, with dimorphic males collected year-round in expeditions taken over a period of 5 years (2011–2015). Based on the literature (Eigenmann, 1912: page 112; Eigenmann, 1917: page 41) and on field observations for this study and of aquarium specimens, permanent sexual dichromatism seems to be the most common pattern among characids.

Theoretically, sexually dichromatic colouration functions both to attract sexual partners and to compete for mates or territory (e.g. Hyphessobrycon negodagua Lima & Gerhard 2001), which means that both intra and intersexual selection are shaping the evolution of colour pattern (Robertson & Hoffman, 1977; Kodric-Brown, 1990, 1998; McKaye, 1991). Studies on reproductive behaviour of characiforms, however, are scarce and this scarcity hampers the understanding of associated evolutionary mechanisms. Such aspects and several others of characiform sexual dichromatism remain largely unknown and await exploration in future studies of phylogeny, taxonomy and ethology. It is hoped that the present paper may stimulate further studies of sexually dichromatic fishes in the neotropics.

Additional specimens examined

All from Brazil. Hyphessobrycon bentosi: MZUSP 29854 (47, 23·8–27·1 mm L_S). Hyphessobrycon compressus: MZUSP 18422 (5, 22·2–26·1 mm L_S). Hyphessobrycon copelandi: MZUSP 76232 (24, 24·6–27·2 mm L_S). Hyphessobrycon eques: MZUSP 90070 (111, 15·8–29·8 mm L_S). Hyphessobrycon erythrostigma: MZUSP 77155 (3, 20·8–23·3 mm L_S). Hyphessobrycon haraldschultzi: MZUSP 105356 (33, 16·3–24·9 mm L_S). Hyphessobrycon hasemani: MZUSP 37652 (21, 12·5–28·6 mm L_S). Hyphessobrycon megalopterus: MZUSP 115639 (24, 12·8–17·0 mm L_S). Hyphessobrycon micropterus: MZUSP 47336 (8, 22·8–26·7 mm L_S). Hyphessobrycon pulchripinnis: MZUSP 92682 (48, 18·3–26·7 mm L_S). Hyphessobrycon rosaceus: MZUSP 16900 (38, 22·2–29·4 mm L_S). Hyphessobrycon socolofi: MZUSP 11700 (50, 22·6–28·9 mm L_S). Hyphessobrycon sweglesi: MZUSP 75459 (36, 23·5–35·1 mm L_S). Hyphessobrycon takasei: MZUSP 29842 (32, 22·8–30·3 mm L_S).

We thank T. Teixeira and R. Ota for the valuable comments and critical review. We are grateful to F. Bockmann for loaning specimens under his care. We thank T. Teixeira for confirming the sexual dimorphism. We thank M. H. Sabaj Pérez for the Fig. 3(m)–(n); and N. K. Lujan for Fig. 3(c)–(d), (i)–(l). This paper benefited from comments of N. Menezes, W. Ohara and T. Teixeira. Part of the type series was collected during an expedition funded by the South American Characiformes Inventory (FAPESP 2011/50282-7, http://www.projeto-saci.com/). Analysis of specimens from the Laboratório de Ictiologia de Ribeirão Preto were funded by Protax (CNPq 440621/2015-1). We thank R. Ilário for collecting most of the type-series and M. Marinho, P. Camelier and V. Giovannetti for help in the field. Authors were funded by FAPESP (2012/22685-2 and 2013/26548-2 MNLP; 2011/23419-1 and 2016/07246-3, FCPD) and CAPES (23038.008118/2010-34, ALHE; MNLP).