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C I F I T N E I C S HOW TAXONOMIC MISIDENTIFICATIONS MAY AFFECT PHYLOGENETIC : AN ANALYSIS ON VOUCHER SPECIMENS USED IN GARCÍA­MELO ET AL. (2019)

CÉSAR ROMÁN­VALENCIA Universidad del Quindío, Laboratorio de Ictiología, P.O. Box. 2639, Armenia, Quindío, Colombia, [email protected]

Abstract: I evaluated the taxonomic identifications used in García­Melo et al. (2019; GMEA hereaf­ ter) to infer the phylogenetic relationships among 372 fish within the Stevardiinae (Characi­ dae). The taxonomic assessment presented in this paper was based on taxa within my area of expertise, representing 13% of the species sampled in GMEA (59 of 372) and comprising species his­ torically classified under Bryconamericus (21 species in GMEA), Carlastyanax (one species), Eretmo­ brycon (nine species), Hemibrycon (eight species), and Knodus (20 species). I detected potential taxonomic misidentifications in 17% of the taxa that were here evaluated (10 of 59 species). Finally, I provide additional details on (i) why taxa were misidentified in GMEA and (ii) how phylogenetic con­ clusions were potentially compromised by taxonomic errors.

Keywords: , fishes, neotropical, South America, systematics. 17 COMO LAS IDENTIFICACIONES TAXONOMICAS ERONEAS PODRIAN AFECTAR LAS FILOGENIAS: UN ANALISIS SOBRE LOS EJEMPLARES TESTIGO EN GARCÍA­MELO ET AL. (2019)

Resumen: Evalúo la validez de las identificaciones taxonómicas usadas en García­Melo et al. (2019; GMEA en adelante) para inferir las relaciones filogenéticas entre 372 especies de peces dentro de Stevardiinae (Characidae). La valoración taxonómica presentada en éste artículo se basa en taxones dentro de mi área de experticia, representan el 13% de las especies en GMEA (59 de 372) y com­ prenden especies históricamente clasificadas en Bryconamericus (21 especies muestreadas en GMEA), Carlastyanax (una especie), Eretmobrycon (nueve especies), Hemibrycon (ocho especies) y Knodus (20 especies). Detecto errores de identificación en 17% de los taxones evaluados en este ar­ tículo (10 de 59 especies). Finalmente, proporciono detalles adicionales sobre (i) por qué los taxones se identificaron erróneamente en GMEA y (ii) cómo potencialmente se comprometieron las conclusio­ nes filogenéticas.

Palabras clave: Characidae, peces, neotropical, Sur América, sistemática.

matic identification may have compromised the A recent paper by García­Melo et al. validity of several of their conclusions. Taxono­ (2019) (GMEA) evaluated the systematics within mic issues were even detected by the authors of the subfamily Stevardiinae, the largest clade of the same study: “… some morphospecies are neotropical characids. García­Melo et al. (2019) not congruent with the exploratory delimitation suggested species limits within Bryconamericus, (highlighted in red letters, Fig. 2) suggesting the Hemibrycon, Knodus, and Eretmobrycon based existence of problems and errors in the identifi­ on an extensive species­and molecular­level cation of species of the genera studied.” Here I sampling. Despite the remarkable efforts made evaluated taxonomic identification errors that by the authors towards establishing a novel may have affected the phylogenetic conclusions, phylogenetic hypothesis for the clade, proble­ and may also have important effects on the

Rev. Biol. Neotrop. / J. Neotrop. Biol., Goiânia, v. 18, n. 1, p. 17­25, jan.­jun. 2021 conservation status of different species, based Ruiz­C, Taphorn & García­Alzate, 2014 on taxa within my area of expertise. Additio­ nally, I propose a potential solution to this pro­ Examined material (GMEA): MPUJ 11134; blem that can be easily incorporated in future Colombia, Magdalena­Cauca, La Libertad Creek, studies. vereda La Libertad en el puente, corregimiento de Arauca, Municipio de Palestina, Caldas. TAXA IN CONTROVERSY Comments: Bryconamericus caldasi is only known to live on the middle Cauca River Basin I evaluated species­level identifications in in La Libertad Creek, San José county, Caldas, GMEA by comparing known geographical ranges Colombia (Román­Valencia et al., 2014a; and topotypical localities to collection localities Román­Valencia et al., 2017a). Collection site in in GMEA. Very often, studies defining new spe­ GMEA does not correspond to B. caldasi. In an earlier work, Román­Valencia et al. (2014a) cies include geographical information as a rele­ concluded that the Bryconamericus from La vant species descriptor. Here, I use geographical Libertad Creek, La Libertad village in the Arauca overlap to assess whether sampled species in bridge (municipality of Palestine), correspond to GMEA were potentially misidentified. I ackno­ B. caucanus. Here I suggest that GMEA wledge that my indirect assessment based on examined samples of B. caucanus instead of B. geographical data may not be completely accu­ caldasi. Román­Valencia et al. (2014a; 2017a) rate. However, given than 84% of all Brycona­ meaning that samples in GMEA for B. caldasi mericus (n=61 especies), 92% Hemibrycon and H. boquiae are both actually B. caucanus. (n=51 especies), and 93% Knodus (n=28 espe­ cies) occur in allopathy (Data available in the 3. Bryconamericus galvisi Román­Valencia, figshare repository, see in box at the end) with 2000 species in the same , geographical infor­ mation generally reflects taxonomic boundaries. Examined material (GMEA): MPUJ 11046; Relevant to this discussion is also the fact that Colombia, Amazonas, Putumayo, Colón, Vereda Carlastyanax, a monotypic genus, is restricted Las Palmas, Zanjón, afluente del Putumayo Ri­ to the Alto Cauca River in Colombia (Román­Va­ ver. lencia et al., 2018). Analyzing these distributi­ ons does in fact lend taxonomic and Comments: Bryconamericus galvisi is only identified to be from the Sibundoy Valley, phylogenetic studies a cutting edge, and thus 18 the biogeographical compo nent often takes Putumayo in Colombia (Román­Valencia, 2000; Román­Valencia & Muñoz, 2001; Román­ precedence (Procheş, 2020). Here the Valencia et al., 2017a). GMEA did not examine geographical distribution is considered based on samples of B. galvisi. Román­Valencia (2000) current data for each taxon. Below, I summarize and Román­Valencia & Muñoz (2001) suggested information on 10 species of Bryconamericus, that B. galvisi in GMEA corresponds to another Hemibrycon, Knodus, and Eretmobrycon that species of Bryconamericus or Knodus. were sampled in GMEA. I did not detect problems in the remaining 40 species sampled 4. Bryconamericus huilae Román­Valencia, in the same genera. 2003a

1. Bryconamericus andresoi Román­Valencia, Examined material (GMEA): MPUJ 11033; 2003a Colombia, Magdalena River, Garzón Creek, casco urbano de Garzón, Huila. Examined material (GMEA): MPUJ 11047; Colombia, Cauca, Patia, Timbío, 800 m arriba Comments: B. huilae was described from the del casco urbano. Alto Magdalena River, Suaza, Guachico and Timaná River system (Román­Valencia, 2003a; Comments: Bryconamericus andresoi is Román­Valencia et al., 2017a). Sampling for B. identified in the upper Patia River in small huilae in GMEA does not correspond with B. creeks of the Junaba and Molinoyaco rivers, huilae. However, sampling sites for B. huilae in Colombia (Román­Valencia, 2003a). GMEA did GMEA overlap with the distribution of B. not examine samples of B. andresoi. Although tolimae. Previous research by Román­Valencia (2003a; 2004) and Román­Valencia et al. taxonomic identity of the material examined in (2017a) suggested that B. huilae, in GMEA, GMEA is still ambiguous, their samples clearly must correspond with B. tolimae. do not correspond to B. andresoi. Furthermore, previous research by Román­Valencia (2003a) 5. Bryconamericus macarenae Román­ has suggested that B. andresoi in GMEA should Valencia, García­Alzate, Ruiz­C. and Taphorn, be B. guaytarae. What GMEA classifies as H. 2010 guaytarae might correspond to an Eretmobry­ con or Bryconamericus. Examined material (GMEA): MPUJ 76479, 2. Bryconamericus caldasi Román­Valencia, 76478, 76481 and 76482; Colombia, Orinoco,

Rev. Biol. Neotrop. / J. Neotrop. Biol., Goiânia, v. 18, n. 1, p. 17­25, jan.­jun. 2021 Guaviare. the upper Ucayali River drainage, Ucayali, Peru (Fricke et al., 2020; Bertaco & Malabarba, Comments: B. macarenae has only been 2010). Collection locality reported in GMEA for identified in the Güejar River basin in the Meta these samples of this species do not correspond department, Macarena Mountain range, Orinoco to H. mikrostiktos. More importantly, H. system in Colombia (Román­Valencia et al., mikrostiktos is not known from Colombia (Do 2010; Román­Valencia et al., 2017a). Samples Nascimiento et al., 2017). Therefore, H. examined by GMEA do not correspond to B. mikrostiktos in GMEA must correspond to macarenae. However, samples in GMEA were another species of Hemibrycon. collected of B. alpha (Román­Valencia, 2003b; Román­Valencia et al., 2008a; Fricke et al., 9. Hemibrycon raqueliae Román­Valencia and 2020). I also note that previous research by Arcila­Mesa, 2010 Román­Valencia (2003b), Román­Valencia et al. (2008a), Fricke et al., (2020), and Román­ Examined material (GMEA): CZUT 11920; Valencia et al. (2010; 2017a) has shown that B. Colombia, Magdalena River, Bocaya Creek; macarenae in GMEA may correspond to another CZUT 15751, Colombia, Magdalena River, species of Bryconamericus or Knodus. Samaná, vereda Modín, Tasajos River.

6. Bryconamericus orinocoense Román­ Comments: H. raqueliae is identified in the La Valencia, 2003c Miel River, middle basin of the Magdalena River (Román­Valencia & Arcila­Mesa, 2010; Román­ Examined material (GMEA): LBP 16928; Valencia et al., 2017a). Therefore, Hemibrycon Brasil, Tocantins, Araguaia. aff. raqueliae in GMEA must correspond to another species of Hemibrycon. GMEA do not Comments: B. orinocoense is identified in examine topotypic material, and samples were Amazonas State, Venezuela, from the Rio collected from localities outside of the geographic range for this species. Mavaca in the south to the Rio Cataniapo in the north (Román­Valencia, 2003c). The material 10. Knodus meridae Eigenmann, 1911 examined in GMEA correspond to B. breviceps (Román­Valencia, 2005; Fricke et al., 2020). Examined material (GMEA): LBP 15818; The samples probably was collected from Venezuela, Orinoco localities outside the distribution of B. orinoco­ ense. 19 Comments: K. meridae is identified in the Lake Maracaibo basin, Venezuela and Colombia 7. Hemibrycon boquiae Eigenmann, 1913 (Román­Valencia, 2005; Fricke et al., 2020). Furthermore, Román­Valencia (2005) and Fricke Examined material (GMEA): MPUJ 11050; et al., (2020) suggest that K. meridae in GMEA Colombia, Alto Cauca, Quindío River. must correspond to another species of Bryconamericus or Knodus. GMEA did not Comments: H. boquiae was described from examine topotypic material and sampling sites Boquia Creek, tributary of the Quindío River in for their samples do not overlap with the Boquia, Salento, Quindío, Colombia (Eigen­ geographical range for this species. Because mann, 1913; Román­Valencia, 2001; Román­ distribution data recorded in GMEA are more Valencia et al., 2008b; 2009a). Román­Valencia congruent with species from the Orinoco basin. et al.(2009a;b; 2018) also identified in other drainages of Quindío River (e.g. Hojas anchas, In short, 17% of the species examined in La Sonadora, La Vibora, Doña Juana, Villa Pao­ this study have problematic taxonomic identifi­ la, Canceles, La Florida, La Venada, El Macho cations (10 of 59 species) (Fig.1 in this study). and El Broche creeks; 1500­1800 meters above As a consequence of uncoupling between the sea level). However, given that the collection identity for these 10 species and the collection locality in GMEA for H. aff. boquiae is extremely localities in GMEA, conclusions reached by the inaccurate, samples are probably from a more authors on the phylogenetic relationships within widespread species in the area (B. caucanus). the Stevardiinae are potentially problematic. Below, I discuss how taxonomic misidentificati­ 8. Hemibrycon mikrostiktos Bertaco and Ma­ ons may have influenced the inferred phyloge­ labarba, 2010 netic patterns within clades 2, 4, and outside of the four major clades proposed by GMEA (Fig.1 Examined material: CZUT 12038; Colombia, and 2). Amazonas, Caquetá, on the road from Florencia First, problematic identifications that we­ to Neiva, Quebrada La Sardina; CZUT 12048, re previously corrected elsewhere were not ac­ Colombia, Amazonas, Caquetá, Belén de los counted for in GMEA (Román­Valencia, 2002; Andaquíes, La Arenosa Creek; CZUT 12052, Román­Valencia, 2003a; b; c; 2004; Román­ Caquetá, Morelia, quebrada Aguascalientes. Valencia & Vanegas­Ríos, 2009; Román­ Comments: H. mikrostiktos is identified from Valencia et al., 2008; 2009a;b; 2014a;

Rev. Biol. Neotrop. / J. Neotrop. Biol., Goiânia, v. 18, n. 1, p. 17­25, jan.­jun. 2021 2017a;b; Román­Valencia & Arcila­Meza, 2010). GMEA did not account for taxonomic errors A species­by­species outline of the taxonomic corrected elsewhere raises doubts on the omission made in GMEA is presented in this accuracy of the conclusions on the systematics manuscript under results. In short, the fact that of the group.

20

Fig. 1. Bayesian phylogenetic tree of Eretmobrycon, Bryconamericus, and Hemibrycon obtained with COI data. Modified of Garcia­Melo et al. (2019).

Rev. Biol. Neotrop. / J. Neotrop. Biol., Goiânia, v. 18, n. 1, p. 17­25, jan.­jun. 2021 21

Fig. 2. Bayesian phylogenetic tree of Bryconamericus, and Knodus obtained with COI data. Modified of Garcia­Melo et al. (2019).

Rev. Biol. Neotrop. / J. Neotrop. Biol., Goiânia, v. 18, n. 1, p. 17­25, jan.­jun. 2021 Secondly, GMEA synonymized one Bryco­ Bryconamericus, Hemibrycon, and Knodus (B. namericus species (B. turiuba to B. exodon) orinocoense is B. breviceps or potentially Kno­ and transferred 12 Bryconamericus species to dus). Specifically, GMEA identifies several sam­ other genera (Eretmobrycon, Hemibrycon and ples collected from lowland localities (<1000 m. Knodus; Table 2 therein): B. andresoi (to H. an­ asl) in the Orinoco basin as Hemibrycon sp. dresoi), B. arilepis (to H. arilepis), B. cismonta­ (fig. 2, S1 table 1 therein). However, these nus (to K. cismontanus), B. diaphanus (to K. samples must correspond to Knodus and not diaphanus), B. foncensis (to H. foncensis), B. Hemibrycon given that most Hemibrycon are ichoensis (to E. ichoensis), B. macarenae (to K. distributed in highland creeks (>1500 m; the macarenae), B. multiradiatus (to H. multiradia­ only exception being H. dariensis, Román­ tus), B. tolimae (to H. tolimae), B. dahli (to E. Valencia & Arcila­Meza, 2009; Román­Valencia guaytarae), B. caldasi (to H. caucanus), and B. et al., 2009a; b; 2014a; b). huilae (to H. tolimae). Among these taxonomic Taxonomic errors as the ones summari­ changes, 42% may be invalid due to taxonomic zed in this paper also imply significant changes misidentifications (i.e. B. andresoi, B. macare­ to the conclusions in previous studies from the nae, B. tolimae, B. huilae, and B. caldasi). Ta­ same authors (e.g. García­Melo et al., 2018, xonomic changes in GMEA (table 2, fig. 2 García­Melo, 2017). For instance, samples in therein) are poorly supported according to the García­Melo et al. (2017; 2018) assigned to H. rules of the International Commission on Zoolo­ cardalensis and H. jabonero do not correspond gical Nomenclature (1999: chapter 6 article 23, to the same species (see Román­Valencia et al., recommendation 24A). Thus, I suggest that ta­ 2013; see Román­Valencia et al., 2018). Ne­ xonomic changes proposed in GMEA for these vertheless, none of these species were sampled five species are invalid. in GMEA. Third, unsupported taxonomic changes in I also note that taxonomic misidentificati­ GMEA may have compromised their phylogene­ ons not only affect phylogenetic conclusions in tic conclusions. Below I summarize the implica­ GMEA but also may have important effects on tions that incorrect taxonomic identifications the conservation status of different species. For may have placed on the composition of clades instance, treating B. caldasi under a single wi­ proposed by GMEA (Fig. 1 and 2): despread species such as B. caucanus would li­ Clade 1: No taxonomic misidentifications were kely change the conservation status of B. observed. caldasi to a less threatened category. Taxono­ Clade 2: First, samples assigned to H. nikros­ mic changes like this will have major implicati­ 22 tiktus in GMEA were probably misidentified. ons in future conservation actions that take Consequently, the closest relative to H. metae place within the geographical ranges of different and H. taeniurus is not H. nikrostiktus but pro­ taxa (Lamprea, 2019). bably another Hemibrycon species. Second, the In sum, I show that the inclusion of type closest relative of B. multiradiatus and B. an­ material is critical for supporting the validity of dresoi is potentially a Hemibrycon or Brycona­ potential taxonomic changes that are based on mericus species but probably not H. aff. phylogenetic analysis. Nevertheless, I did not raqueliae and not H. galvisi respectively as sta­ discuss whether the inferred phylogenetic rela­ ted in GMEA. Third, Bryconamericus caucanus is tionships based on COI (Cytochrome c Oxidase actually monophyletic if the correct taxonomy is I) are correct or not. This aspect should be ad­ used for H. aff. boquiae and B. caldasi (i.e. both species are B. caucanus). Fourth, under the dressed in future studies. The taxonomic sam­ corrected taxonomy, B. tolimae comprise sam­ pling in Garcia­Melo et al. (2019) is inadequate ples that GMEA assigned to B. huilae. Therefo­ for the proposed nomenclature changes (see al­ re, these two species are not sister lineages. so Reis et al. 2019). Several of the species po­ Fifth, B. tolimae is monophyletic if the correct tentially misidentified in Garcia­Melo et al. taxonomy is used. (2019), B. andresoi, B. caldasi, B. galvisi, B. Clade 3: No taxonomic misidentifications were huilae, B. macarenae, B. orinocoense, H. observed. However, Menezes et al. (2020), cardalensis and H. raqueliae, have type series analyze that the close relationship of B pacha­ deposited at the Laboratorio de Ictiología de la cuti with B. exodon in GMEA may be an analyti­ Universidad del Quindío, Armenia, Colombia cal artifact. (IUQ) (Román­Valencia et al., 2017a). These Clade 4: First, Knodus meridae is actually a samples, along with others that may be of inte­ Bryconamericus or another Knodus species. Se­ rest to researchers in the field, are available for cond, B. macarenae is actually another Bycona­ future studies. Phylogenetic studies in the field mericus species. Third, Menezes & Netto­ should rely on the inclusion of type material Ferreira (2019) propose that Knodus sp. nov2, from as many species as possible to avoid issu­ K. heteresthes, K. chapadae, and Knodus sp.5, es like those summarized in this document. Si­ in GMEA, are likely to be within the Rhinopeti­ milarly, collaboration and cooperation among tia. researchers may also help to alleviate the diffe­ Species outside of Clades 1­4: Taxa outside rent problems like the ones highlighted in this of the four clades in GMEA include species in article.

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Rev. Biol. Neotrop. / J. Neotrop. Biol., Goiânia, v. 18, n. 1, p. 17­25, jan.­jun. 2021 Román­Valencia, C., D. C. Taphorn, C. A. García­Alzate, P. S. Vásquez & R. Ruiz­ C. 2017a. Lista anotada de los tipos de pe­ ces en la colección del laboratorio de ictio­ logía, Universidad del Quindío, Armenia, Colombia (IUQ). Biota Colomb. 18: 216­ 241. DOI: https://doi.org/10.21068/ c2017.v18n01a14

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Editor Cientifico / Scientific Editor: David Veliz, UChile, Chile Recebido / Recibido / Received: 09.08.2020 Revisado / Revised: 17.12.2020 Aceito / Aceptado /Accepted: 18.12.2020 Publicado / Published: 04.01.2021

Dados disponíveis / Datos disponibles / Available data: https://figshare.com/articles/dataset/Table_1_Geographical_distri­ bution_of_Bryconamericus_Hemibrycon_and_Knodus_species_xlsx/13503390

Rev. Biol. Neotrop. / J. Neotrop. Biol., Goiânia, v. 18, n. 1, p. 17­25, jan.­jun. 2021