Characiformes: Crenuchidae) from the Central Amazon, Brazil

Canadian Journal of Zoology

A new species of Microcharacidium (Characiformes: Crenuchidae) from the Central Amazon, Brazil

Journal: Canadian Journal of Zoology

Manuscript ID cjz-2020-0138.R1

Manuscript Type: Article

Date Submitted by the 07-Aug-2020 Author:

Complete List of Authors: Vieira, Lorena; UFRGS Instituto de Biociencias, Zoologia Netto-Ferreira, Andre; UFRGS Instituto de Biociencias, Zoologia

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Microcharacidium, Miniaturization, Neotropical Fishes, South American Keyword: darters, Taxonomy

A new species of Microcharacidium (Characiformes: Crenuchidae) from the

Central Amazon, Brazil

L.S. Vieira1, A.L. Netto-Ferreira2

¹Laboratório de Ictiologia, Departamento de Zoologia, Instituto de Biociências,

Universidade Federal do Rio Grande do Sul, Avenida Bento Gonçalves, 9500, 91501-

970, Porto Alegre, Rio Grande do Sul, Brazil, [email protected]

²Laboratório de Ictiologia, Departamento de Zoologia, Instituto de Biociências,

Universidade Federal do Rio Grande do Sul, Avenida Bento Gonçalves, 9500, 91501-

970, Porto Alegre, Rio Grande do Sul, Brazil, [email protected]

Corresponding author. Lorena Sanches Vieira; Address: Laboratório de Ictiologia,

Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio

Grande do Sul, Avenida Bento Gonçalves,Draft 9500, 91501-970, Porto Alegre, Rio Grande

do Sul, Brazil; Tel.: +55 51 99566 0173; Email: [email protected]

A new species of Microcharacidium (Characiformes: Crenuchidae) from the

Middle Rio Amazonas, Brazil

L.S. Vieira1, A.L. Netto-Ferreira2

Abstract

A new species of Microcharacidium Buckup 1993 is described from the Rio Negro, Rio

Trombetas, Rio Tapajós, tributaries of the Rio Madeira, and the middle Rio Amazonas.

The new species is promptly distinguished from all congeners, Microcharacidium eleotrioides Géry 1960, M. gnomus Buckup 1993b and M. weitzmani Buckup 1993b, by the presence of 12 circumpeduncular scales, 19 precaudal vertebrae, and seven dark bars on the flanks connected to their contralateral parts both dorsally and ventrally; two short, dark suborbital stripes; all teethDraft on both jaws conical; 10–11 total dorsal-fin rays; and 3–4 perforated lateral line scales. An updated identification key for the genus is provided, and its affinities with other Microcharacidium are discussed.

Key words: Microcharacidium, Miniaturization, Neotropical Fishes, South American darters, Taxonomy.

Introduction

The genus Microcharacidium Buckup 1993 currently includes three valid species of

characidiins: Microcharacidium eleotrioides Géry 1960, M. gnomus Buckup1993b and

M. weitzmani 1993b Buckup, all considered miniatures (sensu Weitzman and Vari

1988) with the maximum size of less than 26 mm standard length (Toledo-Piza et al.

2014). The genus is widely distributed throughout cis-Andean northern South America,

with representatives occurring in the upper Orinoco, most of the Rio Amazonas basin,

and adjacent coastal basins draining from the Guiana and Brazilian Shields (Buckup

1993a; Buckup 2003; Ohara et al. 2013; Buckup and Van der Sleen 2017). The

diagnostic features originally proposed for the genus recognition are (1) the presence of

17 principal caudal-fin rays; (2) constrictionDraft of the space between the pelvic bones; (3)

fusion of postcleithra 1 and 2; and (4) the presence of a longitudinal stripe, which is

broad and with well-defined edges, when compared representatives of other characidiin

genera, and especially Characidium (Buckup 1993b).

Zarske (1997) described a fourth species for the genus, 'Microcharacidium' geryi, which

was allocated in Microcharacidium based mainly on the absence of maxillary teeth, and

the reduced number of rays on the caudal and pectoral fins (17 caudal-fin rays and 8-9

pectoral-fin rays). However, the inclusion of that species in the genus was questioned by

Buckup (2003), who considered M. geryi as incertae sedis in Crenuchidae. Later, Melo

et al. (2016) suggested relocating the species in Characidium, classification assumed

since then.

The number of circumpeduncular scales is an important diagnostic character allowing

the prompt recognition between M. gnomus (14 scales) from M. eleotrioides and M.

weitzmani (both with 10 scales), with the distinction between the latter two based

mostly on the number of tooth cusps, and the number of scales of the lateral line series, among other characters (Buckup 1993b). During a revisionary study of the genus, an additional species with a color pattern resembling that of M. eleotrioides with 12 circumpeduncular scales and conical teeth was identified from the middle Rio

Amazonas and its major tributaries in the central Amazon, and is described herein. In addition, an updated identification key for the genus is provided, and its affinities with other Microcharacidium are discussed.

Material and Methods

Counts and measurements followed Buckup (1993b). Measurements were made under a stereoscopic microscope (BinocularDraft Model, Zoom 0.8X ~ 5X, Magnification 8X ~ 50X and 2W Transmitted and Reflected LED illumination) with a scaled reticle. All measurements are presented as proportions of standard length (SL), except for subunits of the head, which are presented as proportions of the head length (HL). In the description, the values for each meristic data are followed by their frequency in parentheses with an asterisk indicating the values for the holotype. Counts of vertebrae, supraneurals, procurrent caudal-fin rays, branchiostegal rays, and teeth were taken from cleared and stained paratypes (C and S), prepared according to Taylor and Van Dyke

(1985). The total number of vertebrae includes those of the Weberian Apparatus

(counted as four elements) and the fused PU1+ U1 of the caudal region as a single element. In the present contribution bars are preferred over vertical bands (sensu

Buckup 1993b) as a more widely employed term for vertically arranged color pattern elements in the Characiformes literature.

Institutional abbreviations are Academy of Natural Sciences of the Drexel University

(ANSP), Instituto Nacional de Pesquisas da Amazônia (INPA), Museo de Biología de la

Universidad Central de Venezuela (MBUCV), Natural History Museum of Geneva

(MHNG), Museu Paraense Emílio Goeldi (MPEG), Museu de Zoologia da

Universidade de São Paulo (MZUSP), Universidade Federal do Rio Grande do Sul

(UFRGS) and National Museum of Natural History/Smithsonian Institution (USNM).

Results

Microcharacidium bombioides, new species

urn: lsid: zoobank.org: ato: F2C9E68A-953C-48FC-B25E-4C75CD079AE9

DraftFig. 1; Tab. 1

Microcharacidium eleotrioides non-Géry 1970. – Dias et al. 2010 (environmental

impact study, inferred according to the distribution). – Rodrigues-Filho et al. 2018

(ecological study, inferred according to the distribution).

Holotype. UFRGS 28560, 15.7 mm SL, Brazil, Amazonas, Novo Airão, Rio Negro

basin, 02°37'17"S 60°56'39"W, 07 Sep 2007, H. M. V. Espírito Santo.

Paratypes. All from Brazil, Rio Amazonas basin: INPA 29389 (45, 11.0-15.5 mm SL),

Amazonas, Novo Airão, 02°37'17"S 60°56'39"W, 07 Sep 2007, H. M. V. Espírito

Santo; INPA 29912 (29, 10.0-13.5 mm SL), Amazonas, Manaus, 03°06'07"S

60°1'30"W, 11 Jul 2005, L. N. Carvalho; INPA 31722 (33, 10.0-15.5 mm SL),

Amazonas, Itacoatiara, 03°08'35"S 58°26'39"W, 26 Jul 2007, M. S. Dias; INPA 32754

(7, 12.7-14.7 mm SL), Amazonas, Novo Airão, 02°37'17"S 60°56'39"W, 05 Apr 2008,

M. S. Dias, R. G. Frederico; INPA 37394 (9, 13.5-15.1 mm SL), Amazonas, São

Sebastião do Uatumã, 02°34'17"S 57°52'13"W, 23 Sep 2011, L. Rapp Py-Daniel et al.;

MPEG 14585 (14.0 mm SL), Pará, Oriximiná, Rio Patauá, 01°45'31"S 56°21'40"W, 11

Jun 2007, L. F. A. Montag; MPEG 24056 (14, 10.0-12.8 mm SL), Pará, Santarém, Rio

Maró, afluente do rio Arapiuns, 03°10'32"S 56°20'38"W, 17 Jun 2011, N. Benone;

MPEG 24080 (13, 10.5-13.5 mm SL; 2 C and S), Pará, Santarém, Rio Maró, afluente do rio Arapiuns, 03°10'56"S 55°50'57"W, 17 Jun 2011, N. Benone; MPEG 26000 (4, 12.1-

13.1 mm SL), Pará, Juruti, Igarapé da Ponte, 02°10'48"S 56°04'40"W, 29 Nov 2012, M.

Mendonça; MPEG 30301 (5, 13.0-16.4 mm SL), Pará, Juruti, Igarapé Rio Branco,

02°20'58"S 56°01'26"W, 12 Dec 2013, M. Mendonça; MPEG 30303 (6, 10.6-12.6 mm

SL), Pará, Juruti, Igarapé Café Torrado, 02°18'02"S 56°04'21"W, 12 Dec 2013, M.

Mendonça; MPEG 32637 (11, 13.6-15.0 mm SL), Pará, Juruti, Igarapé Socó,

02°27'31"S 56°00'54"W, 22 Mar 2015,Draft M. Mendonça; MPEG 32638 (7, 11.3-12.7 mm

SL), Pará, Juruti, Igarapé São Francisco, 02°34'52"S 55°54'11"W, 26 Mar 2015, M.

Mendonça; MPEG 32639 (32, 13.1-14.0 mm SL), Pará, Juruti, Igarapé Mutum,

02°36'46"S 56°11'37"W, 20 Mar 2015, M. Mendonça; UFRGS 28565 (7, 12.0-16.2 mm

SL), Amazonas, Novo Airão, 02°37'17"S 60°56'39"W, 07 Sep 2007, H. M. V. Espírito

Santo.

Diagnosis. Microcharacidium bombioides, new species, differs from all congeners by the presence of 12 circumpeduncular scales (vs. 10 in M. eleotrioides and M. weitzmani, and 14 in M. gnomus), the presence of 19 precaudal vertebrae (vs. 16-17), and the presence of seven dark bars on the body connected to their contralateral parts both dorsally and ventrally (vs. 8–9 not contacting their contralateral parts ventrally). The new species further differs from M. weitzmani and M. gnomus by the presence of two, short dark suborbital stripes (vs. a single suborbital stripe). Microcharacidium bombioides differs from M. eleotrioides by the having conical teeth on both jaws (vs.

tricuspid teeth); and from M. gnomus by the presence of less total dorsal-fin rays (10–11

vs. 12), and the presence of less perforated scales in the lateral line series (3–5 vs. 7–

11).

Description. Morphometric data for the holotype and 66 paratypes summarized in Tab.

1. Body fusiform, relatively compressed. Head comparatively short (4.0% of SL).

Greatest body depth anterior to dorsal-fin origin, between pectoral and pelvic fins.

Dorsal profile slightly convex between snout and vertical through half of orbit, inclined

to supraoccipital region; uniformly convex from that point to dorsal-fin terminus,

almost straight to that point to anteriormost dorsal caudal-fin procurrent ray. Ventral

profile slightly convex from snout tip to vertical through of pectoral-fin insertion,

becoming distinctly convex from thatDraft point to anal-fin origin, and slightly concave from

that point to anteriormost ventral caudal-fin procurrent ray.

Snout smoothly rounded in dorsal view. Mouth small and subterminal. Premaxillary

with single row of 12(1) or 13(1) conical teeth decreasing in size laterally. Maxillary

edentulous; posterior margin reaching vertical line over anterior margin of orbit.

Dentary with two series of teeth. Outer series with 11(1) or 12(1), conical teeth; inner

series with 14(1) or 15(1) conical teeth; relatively smaller than those of outer series.

Ectopterygoid with small, conical teeth. Endopterygoid edentulous. Branchiostegal rays

4(2); three (2) attached to anterior ceratohyal, one (2) attached to posterior ceratohyal.

Supraorbital absent. Parietal branch of the supraorbital sensory canal absent.

Supraorbital laterosensory canal not connected to pterotic canal. Large parietal fontanel

bordered anteriorly by frontal bones, laterally by parietals and posteriorly by

supraoccipital. Frontal foramina above the supraorbital canal absent.

Anterior and posterior nostrils distinctly separated by fleshy bridge, anterior diameter nostril smaller than posterior nostril, approximately circular, dermal flap present.

Posterior nostril with small dermal flap on margin; closer to orbit than to anterior nostril. Orbit circular, margins free, approximately on median portion of head. Cheek narrower than orbit, depth about half to two thirds orbital diameter.

Scales cycloid. Lateral line longitudinal series with 19(1), 20(1), 21(3), 22(10), 23(12),

24(13), 25(10), 26*(11) or 27(1) scales, of which 3(16), 4*(44) or 5(5) are perforated.

Series of scales above lateral line 2(1), 3*(62) or 4(2); series below lateral line 2(2),

3*(56) or 4(6). Axillary scale present. Predorsal scales 7(8), 8(25), 9*(24), 10(6) or

11(3). Isthmus completely scaled. Circumpeduncular scales 12*(67). Pseudotympanum formed by well-developed muscular hiatus, relatively large and rounded, exposing the rib of the fifth vertebra (see details inDraft the Discussion).

Pectoral-fin rays iv,1(1), iv,2(6), iii,3(3), iv,3*(35), ii,4(2), iii,4(8), iv,4(1), or ii,5(1); second, third and fourth rays longest, reaching pelvic-fin origin. Pelvic-fin rays ii,4(27), i,5*(33) or ii,5(5); first ray at vertical through dorsal-fin origin; third longest, not reaching anal-fin origin. Supraneurals 4(2), anterior to neural spines of vertebral centra

6-9(2). First dorsal-fin pterygiophore inserted anteriorly to neural spine of centrum

10(2). Dorsal-fin origin slightly ahead of pelvic-fin insertion, distinctly closer to snout tip than to caudal-fin base; dorsal-fin rays iv,4(1), iv,5(3), v,5(1), iii,6(13), iv,6*(11), v,6(1), ii,7(3), iii,7(8), iv,7(15), ii,8(1) or iii,8(8); second and third rays longest, usually reaching adipose-fin origin), last ray adnate. Adipose fin present. Anal-fin rays i,4(1), ii,4*(59), i,5(4) or ii,5(1); origin posterior to dorsal-fin terminus; third, fourth and fifth ray longest. First anal-fin pterygiophore inserted anteriorly to haemal spine of 22nd(2) centrum. Principal caudal-fin rays 14(1), 15(7), 16*(56) or 17(1); procurrent caudal-fin rays, dorsal 2(1) or 5(1), ventral 2(1) or 5(1). Epurals 2(2). Uroneurals absent. Precaudal

vertebrae 19(2), caudal 12(1) or 13(1); total vertebrae 31(1) or 32(1). Posterior chamber

of swimbladder elongate, approximately three times larger than anterior chamber;

posterior margin of posterior chamber reaching rib of vertebra 16 or 17.

Color in Alcohol. Background color of body light yellow. Back of head with brown

chromatophores scattered between the upper lip and anterior region of frontal bones.

Head with dark brown longitudinal stripe, originating at snout tip, across eye and ending

near anterodorsal portion of opercle. Two small dark suborbital bars, in an inverted V-

shape from ventral margin of eye towards articulation of angulo-articular with quadrate;

two dark bars on head, below longitudinal stripe towards ventral portion of head:

between preopercle and opercle; and through posterior margin of opercle, ahead

pectoral-fin origin; large, dark chromatophores scattered onto opercle. Well-defined

dark supra-orbital spot, between theDraft dorsal margin of the orbit and the sides of the

frontal bones. Predorsal area with brown round blotch. Skin folds of anterior nostrils

intensely pigmented; skin folds of posterior nostrils with scarce pigmentation. Body

scales with chromatophores close to distal margins. Humeral blotch present, usually

diffuse. Longitudinal stripe present, posterior to humeral blotch, passing throughout

flanks, becoming broader near caudal peduncle, and extending to caudal-fin rays base.

Dark bars on body 7*(67): First bar immediately past pectoral-fin base; second ahead of

the dorsal-fin origin; third near vertical through middle of dorsal-fin base; fourth

posterior to dorsal-fin terminus; fifth ahead of anal-fin, the sixth at anal-fin base, and

seventh on caudal-peduncle tip; all bars (except the first in some specimens) extending

from dorsal portion, and reaching ventral region of body, usually two or three scales

wide; space between bars usually equivalent to the width of one or two scales. Base of

first dorsal-fin ray with an irregular dark pigmentation; each dorsal-fin ray with three to

six small brown blotches, forming two to three stripes. Pectoral and pelvic fins usually

hyaline, some specimens with two or three irregular brown blotches onto rays. Anal fin with two brown blotches near its base, and three dark blotches on the median portion of rays, forming a small transverse band. Two small, semicircular brown blotches at base of caudal-fin rays. Adipose fin brown near its base and hyaline on distal half.

Sexual dimorphism. No secondary sexually dimorphic character was observed among specimens of Microcharacidium bombioides, although ripe female specimens may present a discretely deeper body.

Distribution. The new species is widely distributed in the middle Rio Amazonas and its tributaries Rio Negro, Rio Trombetas and Rio Tapajós. Fig. 2. Draft

Etymology. The specific epithet bombioides is given in allusion to the colour pattern of the new species consisting in thick, dark bars, alternated by clear, light areas, resembling that of the common Bumblebees of the genus Bombus (Hymenoptera,

Apidae) plus the suffix -oides (= similar to). A noun.

Remarks

The inclusion of Microcharacidium bombioides in Microcharacidium is justified herein as the new species presents all four synapomorphies proposed by Buckup (1993b) for

Microcharacidium: (1) the presence of 17 or less principal caudal-fin rays; (2) the constriction of the space between the pelvic bones; (3) the fusion of postcleithra 1 and

2; and (4) the presence of a longitudinal stripe, which is broad and with well-defined edges, when compared to that of representatives of other characidiin genera, especially

Characidium.

Besides the differences in the number of circumpeduncular scales, predorsal vertebrae

and bars detailed in the Diagnosis section allowing the recognition of

Microcharacidium bombioides, it shares several morphological characters with M.

eleotrioides and M. weitzmani. Most of the meristic data for the three species overlap

and the characters referring to the color present subtle differences in each species of the

genus. Buckup (1993c) recognizes in his phylogenetic study a close relationship

between M. eleotrioides and M. weitzmani, that group sister to M. gnomus. Thus, the

sharing of numerous morphological features among M. bombioides, M. eleotrioides and

M. weitzmani could be indicative that new species would be more closely related to the

first two than to M. gnomus. However, these assumptions will remain open until a

detailed phylogeny addressing all species of Microcharacidium is provided. Draft

Comparative Material. Microcharacidium eleotrioides – Holotype image, MHNG

2201.13 (20.5 mm SL); MZUSP 108858 (16.7 mm SL); MZUSP 108906 (17.2 mm SL);

MZUSP 108971 (13.2 mm SL); MZUSP 109008 (17.0 mm SL); USNM 225750 (13.7

mm SL); USNM 409823 (6, 16.3-18.5 mm SL; 2 C and S). Microcharacidium gnomus

– MBUCV 21790 (20.2 mm SL); USNM 270150 (16.2 mm SL); USNM 270154 (2,

13.8-16.3 mm SL); USNM 270158 (3, 14.9-15.2 mm SL); USNM 285676 (19.7 mm

SL); USNM 296519 (5, 15.1-17.2 mm SL; 2 C and S); USNM 322083 (3, 15.3-17.6

mm SL). Microcharacidium weitzmani – ANSP 159783 (10.7 mm SL); Paratypes,

ANSP 169031 (6, 9.0-9.6 mm SL); ANSP 177511 (10.2 mm SL; 1 C and S).

Key to the species of Microcharacidium

1- Circumpeduncular scales 14; total dorsal-fin rays 12; 7-11 lateral line perforated

scales...... Microcharacidium gnomus

1’- Circumpeduncular scales 12 or 10; total dorsal-fin rays 11 or fewer; usually fewer than 7 perforated lateral line scales...... 2

2- Circumpeduncular scales 12; 7 dark bars...... Microcharacidium bombioides

2’- Circumpeduncular scales 10; 8 or more dark bars; precaudal vertebrae 16-

17...... 3

3- Conical teeth; one suborbital bar; 20-25 scales in lateral line longitudinal series...... Microcharacidium weitzmani

3’- Tricuspid teeth; two suborbital bars; 11-12 ectopterygoid teeth; 27-32 scales in lateral line longitudinal series...... Microcharacidium eleotrioides

Acknowledgments

Thanks are due to Luiz Malabarba (UFRGS)Draft for providing facilities for the conduction of the present study. The authors are also thankful to the collections and their staff for access to their facilities and loans of the specimens used in the present study: Mark

Henry Sabaj Pérez (ANSP), Lúcia Helena Rapp Py-Daniel (INPA), Francisco

Provenzano (MBUCV), Sonia Fisch-Muller and Raphaël Covain (MHNG), Wolmar

Wosiacki (MPEG), Aléssio Datovo and Mário César Cardoso de Pinna (MZUSP) and

Jeff Williams (USNM). The lead author was financially supported by CNPq (Conselho

Nacional de Desenvolvimento Científico e Tecnológico; proc. n° 133586/2017-0).

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Figure 1

Microcharacidium bombioides, holotype. UFRGS 28560, 15.7 mm SL, Brazil, Amazonas, Novo Airão, Rio Negro basin, 02°37'17"S 60°56'39"W, 07 Sep 2007, H. M. V. Espírito Santo.

Figure 2

Map of northern portion of South America, showing the distribution of Microcharacidium bombioides, new species. The dark star represent the type locality. Polygons may represent more than one collection event. Figure was created using QGIS version 2.18.0 and assembled from the data sources (shapefiles) of the IBGE (Instituto Brasileiro de Geografia e Estatística).

Draft

Table 1. Morphometric date of Microcharacidium bombioides and 66 paratypes. SD =

Standard deviation; Ave = Average.

Morphometric variable N Holotype Min Max Ave SD Total length (mm) 67 20.0 15.6 23.2 18.2 1.5 Standard length (mm) 67 15.7 11.9 17.8 14.1 1.2 Head length (mm) 67 4.5 2.6 5.2 3.9 0.4 SL percentages (%) Head length 67 26.6 23.1 34.6 27.9 1.8 Prepectoral distance 67 26.1 24.6 33.3 27.2 1.5 Predorsal distance 67 47.5 44.0 61.6 48.7 2.7 Prepelvic distance 67 50.5 47.9 66.0 52.0 2.9 Preanal distance 67 75.0 71.5 82.1 76.0 1.8 Anal-apex distance 67 92.8 87.3 99.8 96.2 2.2 Body width 67 15.3 12.7 19.2 14.4 1.0 Body depth at: Dorsal-fin origin 67 21.4 18.9 29.6 21.9 1.7 Anal-fin origin 67 17.5 14.4 21.7 17.0 1.2 Caudal peduncle 67 16.0 8.9 16.4 13.4 1.1 HL percentages (%) Draft Snout length 67 16.7 12.2 19.0 15.0 1.4 Snout - maxillary tip 67 28.7 17.9 33.0 26.8 2.9 Anterior naris - eye 67 10.2 6.1 12.4 9.6 1.2 Posterior naris - eye 67 5.6 2.8 7.8 4.8 1.0 Cheek depth 67 12.0 7.0 16.3 10.5 1.5 Orbital diameter 67 30.6 29.2 40.0 32.6 2.0 Interorbital distance 67 12.0 11.1 17.4 13.8 1.5

Microcharacidium bombioides, holotype. UFRGS 28560, 15.7 mm SL, Brazil, Amazonas, Novo Airão, Rio Negro basin, 02°37'17"S 60°56'39"W, 07 Sep 2007, H. M. V. Espírito Santo.

Draft

180x127mm (300 x 300 DPI)