SciELO - Scientific Electronic Library Online

 
vol.49 issue3New record of the fringed leaf frog, Cruziohyla craspedopus (Anura: Phyllomedusidae) extends its eastern range limitEffects of the introduction of an omnivorous fish on the biodiversity and functioning of an upland Amazonian lake author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand

Journal

Article

Indicators

Related links

Share


Acta Amazonica

Print version ISSN 0044-5967On-line version ISSN 1809-4392

Acta Amaz. vol.49 no.3 Manaus July/Sept. 2019  Epub Aug 12, 2019

http://dx.doi.org/10.1590/1809-4392201804392 

Biodiversity and Conservation

Sexual dimorphism in the electric knifefish, Gymnorhamphichthys rondoni (Rhamphichthyidae: Gymnotiformes)

Dimorfismo sexual no peixe elétrico, Gymnorhamphichthys rondoni (Rhamphichthyidae: Gymnotiformes)

Elisa Queiroz GARCIA1  * 
http://orcid.org/0000-0003-2393-8870

Jansen ZUANON2 

1Instituto Nacional de Pesquisas da Amazônia - INPA, Programa de Pós-Graduação em Ecologia, 69080-971, Manaus, AM, Brazil

2Instituto Nacional de Pesquisas da Amazônia - INPA, Coordenação de Biodiversidade - COBIO, 69067-375, Manaus, AM, Brazil

ABSTRACT

Sexual dimorfism refers to morphological differences between males and females of a species. It may be a result of different selection pressures acting on either or both sexes and may occur in any sexually-reproducing dioecious species, including fishes. We analyzed 63 females and 63 adult males of Gymnorhamphichthys rondoni (Gymnotiformes) collected by us or deposited in museum collections. Sex was identified through abdominal dissection. We measured length from snout to posterior end of anal-fin, anal-fin length, distance from anus to anal-fin origin, distance from genital papilla to anal-fin origin, body width at beginning of anal-fin, and head length. Morphometric data submitted to a Principal Component Analysis (PCA) grouped males and females according to variables related to body size (along the first component) and to head length and body height along the second and third components. Females were larger than males, whereas males had proportionally larger heads and higher bodies than females. The urogenital papilla of males and females showed differences in shape, size and relative position on the body. The female papilla was elongated horizontally, larger than that of males, and was located on a vertical line below the eye, while the papilla of the males was vertically elongated and located on a vertical line below the operculum. To our knowledge, this is the first recorded case of sexual dimorphism in a species of Rhamphichthyidae, a condition that is now known in all the currently recognized families of Gymnotiformes.

Keywords: electric fish; head morphology; morphological variation; sexual differences; urogenital papilla

RESUMO

Dimorfismo sexual é caracterizado por diferenças entre machos e fêmeas de uma espécie. Pode estar presente em qualquer ser vivo dioico que se reproduza sexualmente, inclusive peixes. Analisamos 63 fêmeas e 63 machos adultos de Gymnorhamphichthys rondoni (Gymnotiformes) coletados por nós ou obtidos em coleções. O sexo foi determinado por dissecção abdominal. Medimos o comprimento do focinho até o final da origem da nadadeira anal, comprimento da nadadeira anal, distância da papila genital até a origem da nadadeira anal, distância do ânus até a origem da nadadeira anal, altura do corpo e comprimento da cabeça. Dados morfométricos submetidos a uma Análise de Componentes Principais (PCA) agruparam machos e fêmeas de G. rondoni em função de variáveis relacionadas ao tamanho do corpo ao longo do primeiro componente, ao comprimento da cabeça e à altura do corpo ao longo do segundo e terceiro componentes. Fêmeas foram maiores que os machos, enquanto machos tiveram a cabeça proporcionalmente maior e o corpo mais alto que as fêmeas. A papila urogenital de machos e fêmeas diferiu no formato, tamanho e posição relativa no corpo. A papila das fêmeas foi alongada horizontalmente, maior que a dos machos e localizada na linha vertical abaixo do olho, enquanto que a papila dos machos foi alongada verticalmente e localizada na linha vertical abaixo do opérculo. Até onde sabemos, esse é o primeiro caso registrado de dimorfismo sexual em uma espécie de Rhamphichthyidae, uma condição que é agora conhecida para todas as famílias atualmente reconhecidas de Gymnotiformes.

Palavras-chave: peixe elétrico; morfologia da cabeça; variação morfológica; diferenças sexuais; papila urogenital

INTRODUCTION

Sexual dimorphism refers to differences between males and females of a species in secondary sex-related features, like body size, color pattern, morphological details of specific body parts, and behavior. Sexual dimorphism may be present in any sexually-reproducing dioecious organism, including plants (e.g. Lloyd and Webb 1977; Barret 2002; Tsuji and Fukami 2018) and animals (e.g. Garcia et al. 2006; Loker and Brant 2006; Ceballos et al. 2013). Darwin (1871) described several examples of sexual dimorphism when proposing his theory of sexual selection, and Andersson (1994) postulated that sexual dimorphism would result from different sexual selection pressures acting on the two sexes.

For fish, secondary sexual dimorphism has been recorded in body size (e.g. Parker 1992; Erlandsson and Ribbink 1997; Neat et al. 1998; McMillan 1999; Morbey 2018), fin size and shape (e.g. Skjæraasen et al. 2006; Pires et al. 2016), color pattern (e.g. Robertson and Warner 1978; Karino and Someya 2007), and head morphology (e.g. Hastings 1991; Gramitto and Coen 1997; Cox Fernandes 1998; Cox Fernandes et al. 2002, 2009; de Santana and Vari 2010). In some species, jaws, mouth and snout are larger in males than in females (Goto 1984; Crabtree 1985). Dentition may also be sexually dimorphic, with differences between males and females in number, shape and arrangement of teeth (Gomes and Tomas 1991; Kajiura and Tricas 1996; Böhlke 1997; Rapp Py-Daniel and Cox Fernandes 2005; de Santana and Vari 2010). The shape of the urogenital papilla may also differ between males and females (Esmaeili et al. 2017).

Secondary sexual dimorphism may also be expressed in communication systems, such as in sound-producing mechanisms (Ali et al. 2016; Parmentier et al. 2018) or as differences in electrical signal repertoires of male and female electric fishes (Fugere and Krake 2009; Ho et al. 2010, 2013). Among Neotropical electric fishes of the order Gymnotiformes, the most common forms of sexual dimorphism occur in body size (Hilton and Cox Fernandes 2006; de Santana and Cox Fernandes 2012), snout shape (de Santana 2003; Albert and Crampton 2009; Evans et al. 2018), and caudal filament size and shape (Hopkins et al. 1990; Giora et al. 2008). Differences in mouth shape, position and shape of teeth (de Santana and Vari 2010; Cox Fernandes et al. 2010), and electric organ discharge (Nogueira 2006; de Santana and Crampton 2007; Smith and Combs 2008; Fugere and Krake 2009; Ho et al. 2010, 2013) have also been reported.

Rapp Py-Daniel and Cox Fernandes (2005) discuss the evolution of sexual dimorphism in Gymnotiformes by mapping sex-related features on phylogenetic hypotheses and presenting evidences that secondary sexual differences arose independently both among the gymnotiform families and inside Apteronotidae, where most cases of sexual dimorphism in electric knifefishes were reported (de Santana 2003; Hilton and Cox Fernandes 2006; Albert and Crampton 2009; Cox Fernandes et al. 2010; de Santana and Vari 2010; Ho et al. 2013). Sexual dimorphism in Hypopomidae (Hopkins et al. 1990; Hopkins 1999; Giora et al. 2008; Gavassa et al. 2013), Gymnotidae (Mendes-Júnior 2015) and in Sternopygidae (Zakon et al. 1991; Giora and Fialho 2009; Vari et al. 2012) has also been reported. However, for Rhamphichthyidae (Ramphichthys + Gymnorhamphicthys + Iracema + Hypopygus + Steatogenys; Carvalho 2013; Tagliacollo et al. 2015) we have found no recorded instances of sexual dimorphism in the literature.

Recently, we had the opportunity to study the reproductive biology and spatial distribution of individuals of Gymnorhamphichthys rondoni (Miranda Ribeiro, 1920), a strictly psammophilous electric knifefish widely distributed in the Amazon Basin and a common inhabitant of upland forest streams of the Brazilian Amazon (Zuanon et al. 2006; Carvalho 2013). During the study, we noted differences in the proportional size of the head, as well as in the conspicuouness of the urogenital papilla between male and female specimens, which suggested a possible case of sexual dimorphism. Therefore, our objective was to evaluate the occurrence of secondary sexual dimorphism in a population of G. rondoni in a Central Amazon forest stream by analyzing external morphometric parameters.

MATERIAL AND METHODS

We collected 45 adult individuals (36 females and nine males) of Gymnorhamphichthys rondoni using an electric fish detector (Crampton et al. 2007) and hand nets in a terra firme forest stream at Fazenda Dimona of the Biological Dynamics of Forest Fragments Project (BDFFP - http://pdbff.inpa.gov.br/), located about 80 km north of Manaus, Amazonas state, Brazil. The studied forest stream is a tributary of the Cuieiras River in the Negro River basin, in the central Brazilian Amazon. The studied stream section (2º21’1.41”S, 60º5’44.31”W) has a width of 3 - 5 m, maximum depth of 1.5 m, a predominantly sandy substrate with coarse litter deposits, and the channel almost completely shaded by riparian forest canopy. The water was clear, acidic (pH ~5.0), with low electric conductivity (~10 µS*cm-1), and temperature of 23-24 ºC. In addition to the collected fish, we also used preserved specimens from the Fish Collection of the Instituto Nacional de Pesquisas da Amazônia (INPA-ICT). All specimens had the abdominal cavity opened for identification of sex via gonadal examination. We retained for subsequent analyzes only the adult specimens (i.e. those with gonads classified as in late maturation, spawning or regenerating, according to definitions by Brown-Peterson et al. 2011). Combining the 45 specimens collected by us with 81 adult specimens from INPA’s Fish Collection we had a final sample of 63 females and 63 males (Supplementary Material, Table S1).

To quantify morphological characteristics, we used digital calipers and measured (in mm) the length of snout to posterior end of anal-fin (LEA), length of anal-fin length (LAF), distance from anus to anal-fin origin (DAAF), distance from the genital papilla to anal-fin origin (DPAF), body height (BH), and head length (HL) (Figure 1). Morphometric differences between males and females were tested with a Kruskal-Wallis test, as the data distribution lacked normality. The morphometric variables were also analyzed using Principal Component Analysis (PCA) via R statistical software (R Core Team 2016). Since the first component usually is strongly influenced by the size of the specimens, we plotted the data considering the first principal component (PC1 x PC2) and the next two components (PC2 x PC3) to depict the ordination without the effect of body size.

Figure 1 Schematic drawing of Gymnorhamphichthys rondoni in lateral view showing the morphological measurements used in this study: DAAF = distance from anus to anal-fin origin; DPAF = distance from urogenital papilla to anal-fin origin; HL = head length; LAF = length of anal-fin; LEA = length from snout to posterior end of anal-fin. 

To check for occurrence of sexual dimorphism in the urogenital papilla, we used an extended focus stereomicroscope to produce lateral and ventral images of the papillae of adult male and female G. rondoni. All the procedures in this study involving animals were in accordance with and duly approved by the Ethics Committee on Animal Use (CEUA/INPA, protocol #022/2016).

RESULTS

The morphometric analysis showed that female G. rondoni had a longer anal-fin (LAF), a larger distance between the urogenital papilla and the anal-fin origin (DPAF) and a larger distance from the anus to the anal-fin origin (DAAF), whereas males presented a longer head (HL) (Figure 2, Table 1).

Figure 2 Images of a female and male Gymnorhamphichtys rondoni collected in a forest stream tributary of the Cuieiras River in the Negro River basin, central Brazilian Amazon. LEA female = 123.74 mm; LEA male = 117.3 mm. Scale bars = 10 mm 

Table 1 Summary of morphometric measurements (median (minimum - maximum)) in mm, and statistics of the Kruskal-Wallis rank sum test for females (n=63) and males (n=63) of Gymnorhamphichthys rondoni. For all tests, df = 1. Values followed by * indicate significant differences between genders.  

Measurements Females Males H p-value
Length from snout to posterior end of anal-fin (LEA) 129.99 (77.19 - 185.15) 126.3 (102.1 - 153.3) 0.9006 0.3426
Length of anal-fin (LAF) 103.54 (60.32 - 143.50) 94.56 (65.38 - 120.87) 54.736 0.01931*
Distance from the urogenital papilla to the anal-fin origin (DPAF) 13.65 (2.24 - 22.14) 4.32 (2.42 - 5.88) 82.678 2.20E-16*
Distance from the anus to the anal-fin origin (DAAF) 11.070 (0.94 - 19.310) 4.82 (2.67 - 6.64) 67.635 2.20E-16*
Body height (BH) 4.05 (2.05 - 6.65) 4.03 (3.07 - 5.09) 0.45012 0.5023
Head length (HL) 28.18 (12.13 - 40.53) 32.01 (26.17 - 38.79) 14.042 0.0001788*

The first three morphometric-based PCA components explained 64.5%, 21% and 8.4% of observed variance, respectively (Figure 3). The first principal component (PC1) was strongly influenced by negative values of variables related to body size of the specimens, such as length from snout to posterior end of anal-fin (LEA) and LAF. The second component (PC2) was positively influenced by head length (HL) and negatively by DPAF and DAAF. The third component was negatively influenced by HL and positively by LAF (Table 2). PCA ordination separated males and females of G. rondoni mainly along the second principal component (Figures 3a and 3b). Females were larger than males, had a shorter head and body heigth, and a wider distance between the urogenital papilla and the anal fin origin, whereas males were smaller, had a longer head and a higher body height, and a smaller space between the urogenital papilla and the anal fin origin.

Figure 3 Principal Component Analysis of morphometric data of male and female specimens of Gymnorhamphichthys rondoni showing (a) the first and second components (PC1 x PC2), and (b) the second and third components (PC2 x PC3). Blue dots = males, red dots = females. HL = head length; BH = body height; LEA = length from snout to posterior end of anal-fin; LAF = length of anal-fin; DAAF = distance from anus to anal-fin origin; DPAF = distance from urogenital papilla to anal-fin origin. This figure is in color in the electronic version. 

Table 2 Variable loadings on the first two principal components (PCs) for Gymnorhamphichthys rondoni (n= 126) 

Measurements PC1 PC2 PC3
Length from snout to posterior end of anal-fin (LEA) -1.995 0.4436 0.5030
Length of anal-fin (LAF) -1.944 0.1023 0.8152
Distance from the urogenital papilla to the anal-fin origin (DPAF) -1.559 -1.3665 -0.4481
Distance from the anus to the anal-fin origin (DAAF) -1.790 -1.0331 -0.4671
Body height (BH) -1.718 0.7164 0.0462
Head length (HL) -1.147 1.4522 -0.9878
Explained variance 64.5 21.0 8.4
Cumulative variance (%) 64.5 85.5 93.9

We found differences in the shape and position of the urogenital papilla between males and females (Figure 4). Female papillae were more horizontally elongated and approximately 10 times larger than those of males, and were located on a vertical line below the eye, while male papillae were located on a vertical line below the operculum. In females, papillae may expand remarkably during oocyte passage (Figures 4g and 4h).

Figure 4 Urogenital papilla of female and male Gymnorhamphichthys rondoni. In all images, the anterior portion of the body is towards the left. (a) Side view of head of a female showing urogenital papilla (blue arrow). (b) Side view of head of a male showing urogenital papilla (blue arrow). (c) Ventral view of head of a female showing urogenital papilla (blue arrow) and anus (green arrow). (d) Ventral view of head of a male showing urogenital papilla (blue arrow) and anus (green arrow). (e) Side view of female urogenital papilla. (f) Side view of male urogenital papilla. (g) Side view of urogenital papilla of a female with an oocyte (red arrow) inside. (h) Ventral view of head of a female with oocyte at the end of urogenital papilla. Blue arrow = urogenital papilla, green arrow = anus, red arrow = oocyte position. LEA female = 145.83 mm; LEA male = 144.83 mm. This figure is in color in the electronic version. 

DISCUSSION

The observed sexual dimorphism in G. rondoni was related to body size, anal fin length, head length and to urogenital papilla shape and relative position on the body. Males had a proportionally larger head than females, whereas females had a longer anal fin, a larger distance between the urogenital papilla and the anal-fin origin, and a larger distance from the anus to the anal-fin origin. In females the papilla was elongated horizontally, longer than that of males and located on the vertical line below the eye. In males the papila was vertically elongated, smaller than that of females and located on a vertical line below the opercular opening. As far as we searched the scientific litterature, this is the first recorded case of sexual dimorphism in a species of Rhamphichthyidae.

In Gymnotiformes, it is relatively common to find sexual dimorphism in head shape and snout size (de Santana 2003; Albert and Crampton 2009). Tooth shape, size and position also differ between genders of several species of the apteronotid genus Sternarchorhynchus (de Santana and Vari 2010), and in “super-males” of Sternarchogiton nattereri (Cox Fernandes et al. 2010), in which males have hypertrophied and partially exteriorized teeth that seems to be related to male-male conflicts, or to their use when courting females (Cox Fernandes et al. 2010). However, the ecological or behavioral meaning of the larger head in male G. rondoni is not clear. Contrary to the obvious potential use of a hyperthophied mouth and teeth during aggressive encounters or agonistic displays by male apteronotid knifefishes, the small mouth and delicate tubular snout of male G. rondoni seems of little value during a male-male conflict. A possible alternative explanation for such a sexually dimorphic characteristic may be related to differences in foraging tactics or microhabitat use between genders, which remains to be verified.

Sexual dimorphism of the Gymnotiform urogenital papilla position was reported for 15 species of Sternarchorhynchus (Santana and Vari 2010). However, unlike G. rondoni, in Sternarchorhynchus species the urogenital papilla of males is located in a more anterior position on the body compared to females (de Santana and Vari 2010). In addition to this form of dimorphism, Cox Fernandes et al. (2014) also found a difference in the size of the urogenital papillae in Procerusternarchus pixuna (Hypopomidae), with male papillae smaller than those of females, as recorded here for G. rondoni.

When describing Gymnorhamphichthys rosamariae, Schwassmann (1989) reported mature males and females with elongated urogenital papillae and located at the vertical line passing through the eye, and that papilla growth and position are related to gonad development. In this way, papillae larger and closer to the eye line would indicate reproductively mature individuals, regardless of sex. There are records in Gymnotiformes species of the anus and urogenital papilla changing position on the body during ontogeny, moving gradually from the posterior region of the abdominal cavity to the cephalic region (e.g. Apteronotus caudimaculosus: de Santana 2003; Archolaemus blax: Vari et al. 2012; Distocyclus conirostris:Dutra et al. 2014; Eigenmannia besouro: Peixoto and Wosiacki 2016; E. meeki: Dutra et al. 2017; and E. sayona:Peixoto and Waltz 2017). This change in the relative position of the anus and urogenital papila was not detected in other examined apteronotids (Apteronotus eschmeyeri: de Santana et al. 2004; Sternarchogiton labiatus: de Santana and Crampton 2007; S. nattereri: de Santana and Crampton 2007, and Crampton 2007; Apteronotus anu: de Santana and Vari 2013; A. baniwa: de Santana and Vari 2013). We did not find evidence of an ontogenetic change in the position of the urogenital papilla of G. rondoni, as our study was limited to the analysis of adult specimens, which prevented the detection of ontogenetic variations.

The presence of larger urogenital papillae in females than in males may be related to the size of the gametes to be released, so that this characteristic should be more apparent in those species whith proportionately larger oocytes, such as G. rondoni (Garcia and Zuanon, unpublished data). On the other hand, the elongated urogenital papilla of Gymnotiform females may be related to some tactic of oocyte deposition. Gymnorhamphichthys rondoni lives only in places where the substrate is composed largely of sand, in which individuals remain buried during the day, emerging only at night to forage and perform reproductive activities (Zuanon et al. 2006). It is therefore possible that the horizontally elongated papilla aid in selection of oviposition sites, which remains to be studied. At the moment, we lack a functional explanation for the difference in the position of the urogenital papilla and anus observed in male and female G. rondoni. An anatomical study involving a complete ontogenetic series from the larval phase to sexually mature adults, would likely help to better understand the process and the biological significance of the differences reported here.

In a review of the Rhamphichthyoidea, Carvalho (2013) did not mention the occurrence of sexual dimorphism in species of Rhamphichthys, Gymnorhamphichthys or in Iracema caiana (Rhamphichthyinae sensu Carvalho 2013). However, our study found sexual dimorphism in relation to head length and the shape, size and position of urogenital papila for G. rondoni. Accordingly, it is possible that this species might also show sexual dimorphism in other characteristics, such as electric organ discharge patterns or in behavioral aspects, which deserve to be investigated.

CONCLUSIONS

The description and quantification of secondary sexual differences in a rhamphichthyid species may help providing important new information for the understanding of the evolution of sexual dimorphism among Gymnotiformes. Moreover, the known occurrence of external morphological differences could allow sex identification of living individuals in ecological or behavioral studies, avoiding the unnecessary sacrifice of fish and reducing impacts in natural populations, which may be specially important in protected areas.

ACKNOWLEDGMENTS

We thank L. Rapp Py-Daniel for providing access to the ichthyological collection of Instituto Nacional de Pesquisas da Amazônia (INPA), and M. Oliveira, curator of INPA’s invertebrate colletion, for the loan of the extended focus stereomicroscope. We also thank J. Lopes, D. Bastos, E. Borghezan and C. Gualberto for assistance in the field and R. Reis for the drawing of G. rondoni. Supplementary logistics and financial support were provided by the Biological Dynamics of Forest Fragment Project’s (BDFFP) Thomas Lovejoy Research Fellowship Program, and by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (process #477251/2012-9). EQG received a research grant from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and JZ received a productivity grant from CNPq (#313183/2014-7). Adrian Barnett kindly provided the English language revision of the manuscript. This is contribution #59 of the Igarapés Project Technical Series and #757 of the BDFFP Technical Series.

REFERENCES

Albert, J.A.; Crampton, W.G.R. 2009. A new species of electric knifefish, genus Compsaraia (Gymnotiformes: Apteronotidae) from the Amazon River, with extreme sexual dimorphism in snout and jaw length. Systematics and Biodiversity, 7: 81-92. [ Links ]

Ali, H.A.; Mok, H.K.; Fine, M.L. 2016. Development and sexual dimorphism of the sonic system in deep sea neobythitine fishes: The upper continental slope. Deep-Sea Research I, 115: 293-308 [ Links ]

Andersson, M. 1994. Sexual selection. Princeton University Press, Princeton. 599p. [ Links ]

Barrett, S.C.H. 2002. The evolution of plant sexual divert. Nature Reviews Genetics 3: 274-284. [ Links ]

Böhlke, E.E. 1997. Gymnothorax robinsi (Anguilliformes, Muraenidae), a new dwarf moray with sexually dimorphic dentition from the Indo-Pacific. Bulletin of Marine Science, 60: 648-655. [ Links ]

Brown-Peterson, N.J.; Wyanski, D.M.; Saborido-Rey, F.; Macewicz, B.J.; Lowerre-Barbieri, S.K. 2011 A standardized terminology of describing reproductive development in fishes. Marine and Coastal Fisheries, Dynamics, Management and Ecosystem Science, 3: 52-70. [ Links ]

Carvalho, T.P. 2013. Systematics and Evolution of the toothless knifefishes Rhamphichthyoidea Mago-Leccia (Actinopterygii: Gymnotiformes): Diversification in South American Freshwaters. Doctoral thesis, University of Louisiana at Lafayette. 487p. [ Links ]

Ceballos, C.P.; Adams, D.C.; Iverson, J.B.; Valenzuela, N. 2013. Phylogenetic patterns of sexual size dimorphism in turtles and their implications for Rensch’s Rule. Evolutionary Biology 40: 194-208. [ Links ]

Cox Fernandes, C. 1998. Sex-related morphological variation in two species of Apteronotid fishes (Gymnotiformes) from the Amazon River Basin. American Society of Ichthyologists and Herpetologists, 3: 730-735. [ Links ]

Cox Fernandes, C.; Lundberg, J.G.; Riginos, C. 2002. Largest of all electric-fish snouts: hypermorphic facial growth in male Apteronotus hasemani and the identity of Apteronotus anas (Gymnotiformes: Apteronotidae). Copeia, 2002: 52-61. [ Links ]

Cox Fernandes, C.; Lundberg, J.G.; Sullivan, J.P. 2009. Oedemognathus exodon and Sternarchogiton nattereri (Apteronotidae, Gymnotiformes): the case for sexual dimorphism and conspecificity. Proceedings of the Academy of Natural Sciences of Philadelphia, 158: 193-207. [ Links ]

Cox Fernandes, C.; Smith, G.T.; Podos, J.; Nogueira, A.; Inoue, L.; Akama, A.; Ho, W.W.; Alves-Gomes, J. 2010. Hormonal and behavioral correlates of morphological variation in an Amazonian electric fish (Sternarchogiton nattereri: Apteronotidae). Hormones and Behavior, 58: 660-668. [ Links ]

Cox Fernandes, C.; Nogueira, A.; Alves-Gomes, J.A. 2014. Procerusternarchus pixuna, a new genus and species of electric knifefish (Gymnotiformes: Hypopomidae, Microsternarchini) from the Negro River, South America. Proceedings of the Academy of Natural Sciences of Philadelphia, 163: 95-118. [ Links ]

Crabtree, C.B. 1985. Sexual dimorphism of the upper jaw in Gillichthys mirabilis. Bulletin Southern California Academy Science, 84: 96-103. [ Links ]

Crampton, W.G.R.; Wells, J.K.; Smyth, C.; Walz, S.A. 2007. Design and construction of an Electric Fish Finder. Neotropical Ichthyology, 5: 425-428. [ Links ]

Crampton, W.G.R.; de Santana, C.D.; Waddell, JC.; Lovejoy, N.R. 2016. A taxonomic revision of the Neotropical electric fish genus Brachyhypopomus (Ostariophysi: Gymnotiformes: Hypopomidae), with descriptions of 15 new species. Neotropical Ichthyology,14: e150146. [ Links ]

Darwin, C.R. 1871. The descent of man, and selection in relation to sex. John Murray, London. 864p. [ Links ]

de Santana, C.D. 2003 Apteronotus caudimaculosus n. sp. (Gymnotiformes: Apteronotidae), a sexually dimorphic black ghost knifefish from the Pantanal, Western Brazil, with a note on the monophyly of the A. albifrons species complex. Zootaxa, 252: 1-11. [ Links ]

de Santana C.D.; Cox Fernandes, C. 2012. A new species of sexually dimorphic electric knifefish from the Amazon Basin, Brazil (Gymnotiformes: Apteronotidae) Copeia, 2012: 283-292. [ Links ]

de Santana, C.D.; Crampton, W.G.R. 2007. Revision of the deep-channel electric fish genus Sternarchogiton (Gymnotiformes: Apteronotidae). Copeia, 2007: 387-402. [ Links ]

de Santana, C.D.; Maldonado-Ocampo, J.A. Severi, W.; Mendes, G.N. 2004. Apteronotus eschmeyeri, a new species of ghost knifefish from the Magdalena Basin, Colombia (Gymnotiformes: Apteronotidae) Zootaxa, 410: 1-11. [ Links ]

de Santana, C.D.; Vari, R.P. 2010. Electric fishes of the genus Sternarchorhynchus (Teleostei, Ostariophysi, Gymnotiformes); phylogenetic and revisionary studies. Zoological Journal of the Linnean Society, 159: 223-371. [ Links ]

de Santana, C.D.; Vari, R.P. 2013. Brown ghost electric fishes of the Apteronotus leptorhynchus species-group (Ostariophysi, Gymnotiformes); monophyly, major clades, and revision. Zoological Journal of the Linnean Society, 168: 564-596. [ Links ]

Dutra, G.M.; de Santana, C.D.; Vari, R.P.; Wosiacki, W.B. 2014. The south american electric glass knifefish genus Distocyclus (Gymnotiformes: Sternopygidae): Redefinition and revision. Copeia, 2: 345-354. [ Links ]

Dutra, G.M.; de Santana, C.D.; Vari, R.P.; Wosiacki, W.B. 2017. A new species of the glass electric knifefish genus Eigenmannia Jordan and Evermann (Teleostei: Gymnotiformes: Sternopygidae) from Río Tuíra Basin, Panama. Copeia, 2017: 85-91. [ Links ]

Erlandsson, A.; Ribbink, A.J. 1997. Patterns of sexual size dimorphim in african cichlid fishes. South African Journal of Science, 93: 498-508. [ Links ]

Esmaeili, H.R.; Sayyadzadeh, G.; Amini Chermahini, M. 2017. Sexual dimorphism in two catfish species, Mystus pelusius (Solander, 1794) and Glyptothorax silviae Coad, 1981 (Teleostei: Siluriformes). Turkish Journal of Zoology, 41: 144-149. [ Links ]

Evans, K.M.; Bernt, MJ.; Kolmann, M.A.; Ford, K.L.; Albert, J.S. 2018. Why the long face? Static allometry in the sexually dimorphic phenotypes of Neotropical electric fishes. Zoological Journal of the Linnean Society, XX: 1-17. [ Links ]

Fugere, V.; Krake, R. 2009. Electric signals and species recognition in the wave-type gymnotiform fish Apteronotus leptorhynchus. The Journal of Experimental Biology, 213: 225-236. [ Links ]

Garcia, E.Q.; Cambra, R.; Melo, G.A.R. 2006. Sexual associations for two species of mutillid wasps (Hymenoptera, Mutillidae), with the description of a new species of Anomophotopsis. Revista Brasileira de Entomologia, 50: 379-384. [ Links ]

Gavassa, S.; Roach, J.P.; Stoddard, P.K. 2013. Social regulation of electric signal plasticity in male Brachyhypopomus gauderio. Journal of Comparative Physiology A, 199: 375-384. [ Links ]

Giora, J.; Fialho, C.B. 2009. Reproductive biology of weakly electric fish Eigenmannia trilineata López and Castello, 1966 (Teleostei, Sternopygidae). Brazilian Archives of Biology and Technology, 52: 617-628. [ Links ]

Giora, J.; Malabarba, L.R.; Crampton, W. 2008. Brachyhypopomus draco, a new sexually dimorphic species of Neotropical electric fish from southern South America (Gymnotiformes: Hypopomidae) Neotropical Ichthyology, 6: 159-168. [ Links ]

Gomes, U.L.; Tomas, A.R.G. 1991. Secondary sexual dimorphsim in the shark Scyliorhinus haeckelli Ribeiro, 1907 (Elasmobranchii, Scyliorhinidae). Anais da Academia Brasileira de Ciências, 63: 192-200. [ Links ]

Goto, A. 1984. Sexual dimorphism in a river sculpin Cottus hangiongensis. Japanese Journal of Ichthyology, 31: 161-166. [ Links ]

Gramitto, M.E.; Coen, B. 1997. New records of Bellottia apoda (Bythitidae) in the Adriatic Sea with notes on morphology and biology. Cybium, 21: 163-172. [ Links ]

Hagedorn, M.; Carr, C. 1985. Single electrocytes produce a sexually dimorphic signal in South America electric fish, Hypopomus occidentalis (Gymnotiformes, Hypopomidae). Journal of Comparative Physiology, 156: 511-523. [ Links ]

Hastings, P.A. 1991. Ontogeny of sexual dimorphism in the angel blenny, Coralliozetus angelica (Blennioidei: Chaenopsidae). Copeia, 1991: 969-978. [ Links ]

Hilton, E.; Cox Fernandes, C. 2006. Sexual dimorphism in Apteronotus bonapartii (Gymnotiformes: Apteronotidae). Copeia, 2006: 826-833. [ Links ]

Ho, W.W.; Cox Fernandes, C.; Alves-Gomes, J.A.; Smith, G.T. 2010. Sex diferences in the electrocommunication signals of the electric fish Apteronotus bonapartii. Ethology, 116: 1050-1064. [ Links ]

Ho, W.W.; Rack, J.M.; Smith, G.T. 2013. Divergence in androgen sensitivity contributes to population differences in sexual dimorphism of electrocommunication behavior. Hormones and Behavior, 63: 49-53. [ Links ]

Hopkins, C.D. 1999. Design features for electric communication. The Journal of Experimental Biology, 202: 1217-1228. [ Links ]

Hopkins, C.D.; Confort, N.C.; Bastian, J.; Bass, A.H. 1990. Functional analysis of sexual dimorfism in an electric fish, Hypopomus pinnicaudatus, Order Gymnotiformes. Brain, Behavior and Evolution, 35: 350-367. [ Links ]

Kajiura, S.M.; Tricas, T.C. 1996. Seasonal dynamics of dental sexual dimorphism in the Atlantic stingray Dasyatis sabina. Journal of Experimental Biology, 10: 2297-2306. [ Links ]

Karino, K.; Someya, C. 2007. The influence of sex, line, and fight experience on aggressiveness of the Siamese fighting fish in intrasexual competition. Behavioural Processes, 75: 283-289. [ Links ]

Lloyd, D.G.; Webb, C.J. 1977. Secundary sex characters in plants. The Botanical Review 43: 177-216. [ Links ]

Loker, E.S.; Brant, S. 2006. Diversification, dioecy and dimorphism in schistosomes. Trends in Parasitology, 22: 521-528. [ Links ]

McMillan, P.J. 1999. New grenadier fishes of the genus Coryphaenoides (Pisces; Macrouridae), one from of New Zealand and one widespread in the southern Indo West pacific and Atlantic Oceans. New Zealand Journal of Marine and Freshwater Research, 33: 481-489. [ Links ]

Mendes-Júnior, R.N.G.; Sá-Oliveira, J.C.; Ferrari, S.F. 2015. Biology of the electric eel, Electrophorus electricus, Linnaeus, 1766 (Gymnotiformes: Gymnotidae) on the floodplain of the Curiau´ River, eastern Amazonia. Reviews in Fish Biology and Fisheries 26: 83-91. [ Links ]

Morbey, Y.E. 2018. Female-biased dimorphism in size and age at maturity is reduced at higher latitudes in lake whitefish Coregonus clupeaformis. Journal of Fish Biology, 93: 40-46. [ Links ]

Neat, F.C.; Huntingford, F.A.; Beveridge, M.M. 1998. Fighting and assessment in male cichlid fish: the effects of asymmetries in gonadal state and body size. Animal Behaviour, 55: 883-891. [ Links ]

Nogueira, A.P.R. 2006. Diversidade do repertório eletrocomunicativo de Microsternachus cf. bilineatus Fernández-Yépez, 1968 (Pisces: Gymnotiformes) durante a maturação sexual em cativeiro. Master’s dissertation, Instituto Nacional de Pesquisas da Amazônia, Brazil. 82p. (https://bdtd.inpa.gov.br/bitstream/tede/2285/5/Dissertac%CC%A7a%CC%83o%20-%20Dalton%20Nunes%20versa%CC%83o%20final.pdf) [ Links ]

Parker, G.A. 1992. The evolution of sexual size dimorphism in fish. Journal of Fish Biology, 41: 1-20. [ Links ]

Parmentier, E.; Boistel, R.; Bahri, M.A.; Plenevaux, A.; Schwarzhans, A. 2018. Sexual dimorphism in the sonic system and otolith morphology of Neobythites gilli (Ophidiiformes). Journal of Zoology, 305: 274-280. [ Links ]

Peixoto, L.A.W.; Waltz, B.T. 2017. A new species of the Eigenmannia trilineata (Gymnotiformes: Sternopygidae) species group from the río Orinoco basin, Venezuela. Neotropical Ichthyology, 15: e150199. [ Links ]

Peixoto, L.A.W.; Wosiacki, W.B. 2016. Eigenmannia besouro, a new species of the Eigenmannia trilineata species-group (Gymnotiformes: Sternopygidae) from the rio São Francisco basin, northeastern Brazil. Zootaxa, 4126: 262-270. [ Links ]

Pires, T.H.S.; Farago, T.B.; Campos, D.F.; Cardoso, G.M.; Zuanon, J. 2016. Traits of a lineage with extraordinary geographical range: ecology, behavior and life-history of the sailfin tetra Crenuchus spilurus. Environmental Biology of Fishes, 99: 925-937. [ Links ]

Rapp Py-Daniel, L.; Cox Fernandes, C. 2005. Dimorfismo sexual em Siluriformes e Gymnotiformes. Acta Amazonica, 35: 97-110. [ Links ]

Robertson, D.R.; Warner, R.R. 1978. Sexual patterns in the labroid fishes of the western Caribbean, II: The Parrotfishes (Scaridae). Smithsonian Contribuitions to Zoology, Nr. 255. 36p. [ Links ]

RStudio Team. 2016. RStudio: Integrated Development for R. RStudio, Inc., Boston. (http://www.rstudio.com/). [ Links ]

Schwassmann, H.O. 1989. Gymnorhamphichthys rosamariae, a new species of knifefish (Ramphichthyidae, Gymnotiformes) from the upper Rio Negro, Brazil. Studies on Neotropical Fauna and Environment, 24: 157-167. [ Links ]

Skjæraasen, J.E.; Rowe, S.; Hutchings, J.A. 2006. Sexual dimorphism in pelvic fin length of Atlantic cod. Canadian Journal of Zoology , 84: 865-870. [ Links ]

Smith, G.T.; Combs, N. 2008. Serotonergic activation of 5HT1A and 5HT2 receptors modulates sexually dimorphic communication signals in the weakly electric fish Apteronotus leptorhynchus. Hormones and Behavior, 54: 69-82. [ Links ]

Stoddard, P. 1999. Predation enhances complexity in the evolution of electric fish signals. Nature, 400: 254-256. [ Links ]

Tagliacollo, V.A.; Bernt, M,J.; Craig, J.M.; Oliveira, C.; Albert, J.S. 2015. Model-based total evidence phylogeny of Neotropical eletric knifefishes (Teleostei, Gymnotiformes). Molecular Phylogenetics and Evolution, 95: 20-33. [ Links ]

Tsuji, K.; Fukami, T. 2018. Community-wide consequences of sexual dimorphism: néctar microbes in dioecious plants. Ecology 99: 2476-2484. [ Links ]

Vari, R.P.; de Santana, C.D.; Wosiacki, W.B. 2012. South American electric knifefishes of the genus Archolaemus (Ostariophysi, Gymnotiformes): undetected diversity in a clade of rheophiles. Zoological Journal of the Linnean Society, 165: 670-699. [ Links ]

Zakon, H.H.; Thomas, P.; Yan, H.Y. 1991. Electric organ discharge frequency and plasma sex steroid levels during gonadal recrudescence in a natural populaion of the weakly electric fish Sternopygus macrurus. Journal of Comparative Physiology A, 169: 493-499. [ Links ]

Zuanon, J.A.S.; Bockmann, F.A.; Sazima, I. 2006. A remarkable sand-dwelling fish assemblage from central Amazonia, with comments on the evolution of psammophily in South American freshwater fishes. Neotropical Ichthyology, 4: 107-118. [ Links ]

CITE AS: Garcia, E.Q.; Zuanon, J. 2019. Sexual dimorphism in the electric knifefish, Gymnorhamphichthys rondoni (Rhamphichthyidae: Gymnotiformes). Acta Amazonica 49: 213-220

SUPPLEMENTARY MATERIAL

(only available in the electronic version)

GARCIA & ZUANON. Sexual dimorphism in the electric knifefish, Gymnorhamphichthys rondoni (Rhamphichthyidae: Gymnotiformes)

Table S1 Measurements (mm) used in the study of sexual dimorphism of females (F) and males (M) of Gymnorhamphichthys rondoni. LEA - length from snout to posterior end of anal fin, LAF - length of anal fin, DPAF - distance from urogenital papilla to anal fin, DAAF - distance from anus to anal fin, BH - body height, HL - length of head. DIMONA = study area at the BDFF Project; INPA-ICT = specimens from INPA’s ichthyological collection. * = Uncatalogued specimen. 

Code LEA LAF DPAF DAAF BH HL Sex Source Catalog Number Drainage
F1 149.94 115.8 17.67 15.61 5.8 33.37 F DIMONA * Negro River
F2 155.06 124.27 15.52 14.92 4.92 32.44 F DIMONA * Negro River
F3 152.18 118.87 17.39 15.52 4.32 34.48 F DIMONA * Negro River
F4 140.84 112.48 13.61 9.92 4.05 28.61 F DIMONA * Negro River
F5 128.77 102.64 13.04 9.26 3.86 26.53 F DIMONA * Negro River
F6 117.98 94.4 11.11 9.79 3.94 12.26 F DIMONA * Negro River
F7 159.11 124.93 19.65 17.72 4.95 36.5 F DIMONA * Negro River
F8 151.48 121.22 17.65 14.92 5.05 32.19 F DIMONA * Negro River
F9 148.26 116.12 16.38 14.73 4.47 32.76 F DIMONA * Negro River
F10 145.52 118.54 12.8 11.07 4.48 28.06 F DIMONA * Negro River
F11 167.47 131.73 20.68 18.08 6.06 34.53 F DIMONA * Negro River
F12 171.96 134.28 21.61 19.31 4.85 37.02 F DIMONA * Negro River
F13 171.88 135.5 20.13 17.22 4.91 37.2 F DIMONA * Negro River
F14 159.1 124.65 19.26 16.69 5.56 34.05 F DIMONA * Negro River
F15 161.94 125.71 19.62 17.37 5.73 35.59 F DIMONA * Negro River
F16 157.52 125.81 17.78 14.81 5.12 31.13 F DIMONA * Negro River
F17 160.86 125.74 19.4 16.43 6.65 35.96 F DIMONA * Negro River
F18 159.12 127.17 19.33 17.05 4.84 33.47 F DIMONA * Negro River
F19 131.72 103.54 14.9 12.43 4.29 26.19 F DIMONA * Negro River
F20 119.28 93.47 10.33 9.78 4.12 25.07 F DIMONA * Negro River
F21 77.19 60.32 3.29 2.55 2.44 17.11 F DIMONA * Negro River
F22 185.15 143.5 22.14 18.9 5.63 40.53 F DIMONA * Negro River
F23 158.9 121.08 17.68 15.23 5.01 36.89 F DIMONA * Negro River
F24 154.37 123.02 17.18 14.95 5.14 31.42 F DIMONA * Negro River
F25 162.68 128.36 16.06 13.62 4.62 33.33 F DIMONA * Negro River
F26 164.05 132.24 16.24 13.84 5.18 32.86 F DIMONA * Negro River
F27 164.85 130.47 16.01 13.51 4.61 34.5 F DIMONA * Negro River
F28 167.98 134.25 16.3 12.73 5 33.73 F DIMONA * Negro River
F29 140.56 112.06 14.98 13.82 4.45 28.69 F DIMONA * Negro River
F30 137.41 107.57 13.88 12.24 4.32 30.41 F DIMONA * Negro River
F31 152.8 119.8 17.8 15.89 4.84 33.1 F DIMONA * Negro River
F32 95.14 75.54 2.24 0.94 2.67 20.11 F DIMONA * Negro River
F33 152.23 123.83 16.8 16.01 4.25 32.01 F DIMONA * Negro River
F34 151.27 120.43 11.79 11.33 4.53 31.09 F DIMONA * Negro River
F35 133.93 107.32 11.69 10.82 4.09 29.07 F DIMONA * Negro River
F36 141.96 111.79 16.52 15.5 4.6 31.86 F DIMONA * Negro River
F37 123.74 111.61 9.42 6.16 2.68 12.13 F INPA-ICT INPA-ICT 014995 Negro River
F38 126.35 92.65 13.54 6.15 2.59 33.7 F INPA-ICT INPA-ICT 015876 Negro River
F39 104.07 77.29 9.89 6.28 2.24 26.78 F INPA-ICT INPA-ICT 020101 Negro River
F40 108.33 74.29 9.91 5.4 2.41 34.04 F INPA-ICT INPA-ICT 020101 Negro River
F41 114.19 87.54 10.81 6.79 2.65 26.65 F INPA-ICT INPA-ICT 022461 Negro River
F42 120.52 94.68 11.74 6.65 3.08 25.84 F INPA-ICT INPA-ICT 023164 Negro River
F43 111.52 84.55 11.37 6.92 2.99 26.97 F INPA-ICT INPA-ICT 023223 Negro River
F44 111.03 84.61 11.1 6.72 2.78 26.42 F INPA-ICT INPA-ICT 024657 Negro River
F45 121.85 97.41 14.64 6.99 2.88 24.44 F INPA-ICT INPA-ICT 024657 Negro River
F46 115.9 90.41 10.25 7.41 3 25.49 F INPA-ICT INPA-ICT 024657 Negro River
F47 95.03 76.86 8.65 6.34 2.3 18.17 F INPA-ICT INPA-ICT 024657 Negro River
F48 107.67 81.15 10.93 7.39 3.74 26.52 F INPA-ICT INPA-ICT 024657 Negro River
F49 107.24 86.56 11.9 6.47 2.58 20.68 F INPA-ICT INPA-ICT 029952 Negro River
F50 113.27 87 11.52 6.1 2.73 26.27 F INPA-ICT INPA-ICT 029952 Negro River
F51 88.12 66.64 9.22 6.19 2.33 21.48 F INPA-ICT INPA-ICT 029963 Negro River
F52 104.86 82.52 9.28 7.44 3.05 22.34 F INPA-ICT INPA-ICT 029963 Negro River
F53 97.65 74.7 8.3 5.52 2.19 22.95 F INPA-ICT INPA-ICT 029963 Negro River
F54 101.08 81.35 10.79 7.93 2.67 19.73 F INPA-ICT INPA-ICT 029963 Negro River
F55 129.29 101.21 10.25 8.33 3.41 28.08 F INPA-ICT INPA-ICT 030026 Preto da Eva River
F56 99.58 75.77 10 8.48 2.8 23.81 F INPA-ICT INPA-ICT 030026 Preto da Eva River
F57 114.63 88.32 14.54 12.87 3.18 26.31 F INPA-ICT INPA-ICT 030026 Preto da Eva River
F58 101.95 77.68 12.87 10.33 3.6 24.27 F INPA-ICT INPA-ICT 030026 Preto da Eva River
F59 118.64 92.57 13.33 11.93 3.05 26.07 F INPA-ICT INPA-ICT 030360 Negro River
F60 111.34 89.81 14.73 11.37 3.15 21.53 F INPA-ICT INPA-ICT 030360 Negro River
F61 96.39 74.21 8.08 6.15 2.05 22.18 F INPA-ICT INPA-ICT 030360 Negro River
F62 96.79 75.4 8.82 7.68 2.42 21.39 F INPA-ICT INPA-ICT 030360 Negro River
F63 89.36 72.6 5.79 4.07 2.33 16.76 F INPA-ICT INPA-ICT 030360 Negro River
M1 145.15 110.6 3.15 3.98 4.57 33.47 M DIMONA * Negro River
M2 127.48 98.95 3.59 3.83 3.85 28.24 M DIMONA * Negro River
M3 145.14 116 2.42 2.67 4.17 28.42 M DIMONA * Negro River
M4 135.59 106.2 3.66 3.84 4.14 30.48 M DIMONA * Negro River
M5 145.49 114.85 3.67 4.02 4.76 28.08 M DIMONA * Negro River
M6 117.3 84.03 3.4 3.78 3.49 32.07 M DIMONA * Negro River
M7 142.09 114.25 5.23 5.6 3.9 28.32 M DIMONA * Negro River
M8 152.86 120.14 3.05 4.11 5.08 32.01 M DIMONA * Negro River
M9 153.28 120.87 3.52 3.93 5.09 32.99 M DIMONA * Negro River
M10 109.9 78.24 3.38 4.24 3.72 31.66 M INPA-ICT INPA-ICT 014209 Negro River
M11 126.21 90.52 4.29 4.7 4.42 35.69 M INPA-ICT INPA-ICT 014209 Negro River
M12 117.9 89.44 4.01 4.64 3.4 28.46 M INPA-ICT INPA-ICT 014209 Negro River
M13 108.09 72.05 4.28 5.19 3.07 36.04 M INPA-ICT INPA-ICT 015881 Negro River
M14 116.25 80.23 3.7 4.2 3.58 36.02 M INPA-ICT INPA-ICT 015881 Negro River
M15 125.52 94.28 4.54 5.48 3.76 31.24 M INPA-ICT INPA-ICT 015904 Negro River
M16 133.18 101.23 4.32 4.65 3.13 31.95 M INPA-ICT INPA-ICT 015985 Negro River
M17 130.09 100.67 3.58 3.81 4.19 29.42 M INPA-ICT INPA-ICT 015763 Negro River
M18 147.24 115.82 4.92 6.16 3.43 31.42 M INPA-ICT INPA-ICT 020101 Negro River
M19 142.94 106.32 4.7 6.19 4.11 36.62 M INPA-ICT INPA-ICT 023223 Negro River
M20 109 82.83 4.23 4.52 3.58 26.17 M INPA-ICT INPA-ICT 023223 Negro River
M21 146 107.5 3.24 3.55 3.2 38.5 M INPA-ICT INPA-ICT 024657 Negro River
M22 133.58 97.75 3.5 4.21 3.61 35.83 M INPA-ICT INPA-ICT 024657 Negro River
M23 144.83 111.45 4.06 4.57 4.63 33.38 M INPA-ICT INPA-ICT 029847 Negro River
M24 126.27 98.7 5.8 6.3 4.8 27.57 M INPA-ICT INPA-ICT 029847 Negro River
M25 142.55 108.1 4.93 5.63 4.42 34.45 M INPA-ICT INPA-ICT 029952 Negro River
M26 133.54 105.66 5.5 6.17 3.47 27.88 M INPA-ICT INPA-ICT 029952 Negro River
M27 119.46 84.41 4.34 4.96 4.4 35.05 M INPA-ICT INPA-ICT 029963 Negro River
M28 102.28 65.38 4.47 4.95 4.03 36.9 M INPA-ICT INPA-ICT 029963 Negro River
M29 106.81 78.74 3.23 3.92 4.75 28.07 M INPA-ICT INPA-ICT 029963 Negro River
M30 116.46 79.72 3.24 3.84 4.3 36.74 M INPA-ICT INPA-ICT 029997 Preto da Eva River
M31 146.56 117.55 3.25 3.68 4.94 29.01 M INPA-ICT INPA-ICT 029997 Preto da Eva River
M32 131.6 100.7 3.62 4.13 3.28 30.9 M INPA-ICT INPA-ICT 029997 Preto da Eva River
M33 141.38 108.83 4.22 4.82 3.95 32.55 M INPA-ICT INPA-ICT 030360 Negro River
M34 121.3 84.13 4.75 5.18 3.15 37.17 M INPA-ICT INPA-ICT 030360 Negro River
M35 123.54 84.75 4.49 4.77 4.12 38.79 M INPA-ICT INPA-ICT 030360 Negro River
M36 102.06 70.13 3.28 3.72 4.56 31.93 M INPA-ICT INPA-ICT 030360 Negro River
M37 102.2 71.47 3.92 4.77 3.72 30.73 M INPA-ICT INPA-ICT 030360 Negro River
M38 102.98 65.54 5.6 6.52 4.59 37.44 M INPA-ICT INPA-ICT 030360 Negro River
M39 102.49 75.29 3.18 3.95 4.32 27.2 M INPA-ICT INPA-ICT 030531 Negro River
M40 108.91 74.33 3.33 3.72 4.07 34.58 M INPA-ICT INPA-ICT 030531 Negro River
M41 119.18 89.47 4.57 5.33 4.56 29.71 M INPA-ICT INPA-ICT 027841 Negro River
M42 127.88 94.14 5.88 6.49 3.34 33.74 M INPA-ICT INPA-ICT 027841 Negro River
M43 123.9 97.03 3.24 4.14 3.98 26.87 M INPA-ICT INPA-ICT 030383 Negro River
M44 136.98 109.86 5.33 6.05 4.04 27.12 M INPA-ICT INPA-ICT 030562 Negro River
M45 122.14 87.53 3.84 4.81 3.63 34.61 M INPA-ICT INPA-ICT 027923 Amazonas River
M46 109.23 78.32 3.81 4.12 3.89 30.91 M INPA-ICT INPA-ICT 027235 Solimões River
M47 142.91 112.17 5.54 6.12 3.95 30.74 M INPA-ICT INPA-ICT 027235 Solimões River
M48 136.27 101.79 5.61 5.87 4.1 34.48 M INPA-ICT INPA-ICT 027279 Solimões River
M49 146.79 112.86 5.71 6.35 4.04 33.93 M INPA-ICT INPA-ICT 027279 Solimões River
M50 123.96 90.93 4.19 5.01 3.73 33.03 M INPA-ICT INPA-ICT 027279 Solimões River
M51 144.99 114.67 4.49 4.98 4 30.32 M INPA-ICT INPA-ICT 027302 Solimões River
M52 143.31 109.09 5.81 6.64 4.31 34.22 M INPA-ICT INPA-ICT 027302 Solimões River
M53 140.61 107.97 5.45 6.17 4.7 32.64 M INPA-ICT INPA-ICT 034182 Tapajós River
M54 112.21 82.81 5.61 6.23 3.4 29.4 M INPA-ICT INPA-ICT 034182 Tapajós River
M55 112.69 81.78 5.72 6.52 3.77 30.91 M INPA-ICT INPA-ICT 034182 Tapajós River
M56 103.75 71.08 4.49 4.82 3.33 32.67 M INPA-ICT INPA-ICT 034182 Tapajós River
M57 127.22 88.71 5.81 6.4 3.24 38.51 M INPA-ICT INPA-ICT 034182 Tapajós River
M58 119.18 87.21 5.45 6.06 3.62 31.97 M INPA-ICT INPA-ICT 034182 Tapajós River
M59 108.91 82.28 5.61 6.06 4.95 26.63 M INPA-ICT INPA-ICT 034182 Tapajós River
M60 148.02 113.4 5.71 6.04 4.51 34.62 M INPA-ICT INPA-ICT 034182 Tapajós River
M61 123.91 94.56 4.49 4.81 4.25 29.35 M INPA-ICT INPA-ICT 034182 Tapajós River
M62 114.06 79.41 5.81 6.33 4.5 34.65 M INPA-ICT INPA-ICT 034182 Tapajós River
M63 143.55 110 5.2 6.06 3.55 33.55 M INPA-ICT INPA-ICT 034182 Tapajós River

Received: November 13, 2018; Accepted: March 26, 2019

* Corresponding author: elisaqga@gmail.com

ASSOCIATE EDITOR:

Helder M. Espírito-Santo

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License