The distribution of Cteniloricaria (Siluriformes: Loricariidae): known and new records in Brazil suggest headwater captures as drivers of disjoint distribution

Alejandro Londoño-Burbano1, 2 , Marina Barreira Mendonça3  and Roberto E. Reis2 

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Abstract​


EN

Cteniloricaria is a genus of Neotropical armored catfishes belonging to the Loricariinae, currently including two valid species: C. platystoma and C. napova. Cteniloricaria platystoma is presently recorded across the main coastal drainages of the Guiana Shield, from the Sinnamary River, French Guiana, to the Essequibo River basin, Guyana, and is considered to be restricted to the region. Cteniloricaria napova is only known from its type locality at the headwaters of the Paru de Oeste River, Amazon basin, Sipaliwini Savannah, Trio Amerindian territory in Suriname, close to the Brazilian border. Based on a specimen of C. napova, captured in the Cuminapanema River, a tributary to the Curuá River, within Brazilian territory, the geographic distribution of the species and the genus is extended, representing the first record of Cteniloricaria in Brazil. The genusshows a disjoint distribution, and divergence between populations in the north-flowing coastal rivers of the Guianas and the south-flowing Amazon tributaries, and more recent headwater capture between south-flowing Amazon tributaries, may have played a key role in shaping its current distribution. Illustrations, diagnostic characters, morphometrics, description of the habitat where the new specimen was captured, extinction risk assessment, and a discussion of the distribution of the genus are provided.

Keywords: Amazon basin, Armored catfish, Cuminapanema, Loricariinae, Range extension.

PT

Cteniloricaria é um gênero de cascudos neotropicais pertencente à Loricariinae, atualmente incluindo duas espécies válidas: C. platystoma e C. napova. Atualmente, C. platystoma é registrada nas principais drenagens costeiras do Escudo das Guianas, desde o rio Sinnamary, na Guiana Francesa, até a bacia do rio Essequibo, Guyana, sendo considerada restrita à região. Cteniloricaria napova é conhecida unicamente por sua localidade-tipo nas cabeceiras do rio Paru de Oeste, bacia Amazônica, Savana Sipaliwini, território indígena de Trio, no Suriname, próximo à fronteira com o Brasil. Com base em um espécime de C. napova, capturado no rio Cuminapanema, afluente do rio Curuá, em território brasileiro, a distribuição geográfica da espécie e do gênero se estende até a bacia do rio Curuá, representando o primeiro registro de Cteniloricaria no Brasil. O gênero apresenta uma distribuição disjunta e, eventos como divergência entre as populações dos rios costeiros das Guianas e nos afluentes do Amazonas, e mais recente captura de cabeceiras entre os afluentes do Amazonas, podem ter desempenhado um papel fundamental em sua distribuição atual. São fornecidos ilustrações, caracteres diagnósticos, morfometria, descrição do habitat onde o novo espécime foi capturado, avaliação do risco de extinção e uma discussão sobre a distribuição do gênero.

Palavras-chave: Bacia Amazônica, Cascudo, Cuminapanema, Extensão de distribuição, Loricariinae.

Introduction​


One of the main components of the order Siluriformes is the family Loricariidae, which currently includes more than 1,000 species and comprises six subfamilies: Delturinae, Hypoptopomatinae, Hypostominae, Lithogeninae, Loricariinae, and Rhinelepinae (Van der Laan et al., 2021). Species belonging to the family are recognized by having the body covered in ossified dermal plates, integumentary teeth known as odontodes (Garg et al., 2010), and a ventral oral disk that facilitates surface attachment and feeding (Geerinckx et al., 2011). Fishes belonging to Loricariidae are commonly known as cascudos or acaris (Brazil), corronchos or cuchas (Colombia, Venezuela), carachamas (Peru), or viejas (Argentina, Paraguay, and Uruguay).

Loricariinae currently includes 255 valid species, classified in 31 genera (Van der Laan et al., 2021), distributed from the La Plata River basin in Argentina to southern Central America (Ferraris, 2003). Species in this subfamily are characterized by a long and depressed caudal peduncle and absence of an adipose fin. They usually live on the substrate and present marked variations in body shape due to the different habitats, from lotic to lentic systems, over organic or inorganic substrates such as rocks, fallen tree trunks, or soft substrate (Covain et al., 2008).

Isbrücker, Nijssen (in Isbrücker, 1979) described Cteniloricaria, designating Loricaria platystoma Günther, 1868 as the type species, along with Oxyloricaria fowleri Pellegrin, 1908 (=Harttia fowleri), and Parasturisoma maculata Boeseman, 1971 (=Cteniloricaria platystoma). The authors compared the new genus to Harttia Steindachner, 1877 and diagnosed the former by having the abdomen completely covered by plates (vs. variable covering of abdominal plates), and a more slender body (vs. robust body; see Identification for a diagnosis of Cteniloricaria from Harttia).

Cteniloricaria historically has been treated either as a synonym of Harttia (Oyakawa, 1993; Rapp Py-Daniel, 1997; Rapp Py-Daniel, Oliveira, 2001; Provenzano et al., 2005; Covain et al., 2006; Covain, Fisch-Muller, 2007; Provenzano, 2011) or as a valid genus (Isbrücker, 1980, 1981, 2001; Ferraris, 2003, 2007; Covain et al., 2012, 2016; Oyakawa et al., 2013; Londoño-Burbano, Reis, 2019, 2021). Covain, Fisch-Muller (in Covain et al., 2012) described the second species included in Cteniloricaria, C. napova, diagnosing the new species from C. platystoma by its distinctly spotted color pattern, more numerous premaxillary teeth, and body and head proportional measurements (Covain et al., 2012:136).

Cteniloricaria napova is currently known by the type series, 12 specimens from the type locality at the headwaters of the Paru de Oeste River, Sipaliwini Savannah, Trio Amerindian territory, Four Brothers Mountains, Suriname. This species has recently been recorded from the Brazilian territory in Pará State from a different, despite contiguous, river basin than the type locality. Dutra et al. (2020), in a rapid assessment of the ichthyofauna of the southern Guiana Shield tributaries of the Amazon River in Pará, listed C. napova along seven other species recorded as the first record for the Brazilian territory, but did not include the species as a novelty for the region. Here we describe the specimen of C. napova comprising that first record of the genus and the species to Brazil, from the Cuminapanema River, Curuá River basin, northern Brazil. The type species, C. platystoma, is more widely distributed in coastal rivers of the Guianas from the Essequibo in Guyana to the Sinnamary in French Guiana and is here compared to C. napova.

Material and methods


Study area. The broadest amount of protected areas in the world is located at the left bank of the Amazon River, the so-called Northern Pará Drainage System – NPDS (Dutra et al., 2020), with approximately 22 million ha (SEMA, 2010). In 2011 the State Environmental Agency of Pará (SEMA) established a partnership with Conservation International (CI) and Institute of Man and Environment of the Amazon (IMAZON) to develop management plans for the protected areas of the NPDS based, in part, on the field expeditions for ichthyofaunal studies accomplished by the Museu Paraense Emilio Goeldi (MPEG) in 2008 and 2009 (SEMA, 2011). The Trombetas State Forest (FLOTA Trombetas), one of the seven protected areas, represents 14% (almost 3.2 million ha) of the NPDS and is mainly drained by the Trombetas, Cuminá, and Cuminapanema rivers (Fig. 1) (SEMA, 2011).

Fieldwork. In April 2008, the Cuminapanema River and 13 tributary streams were sampled inside the FLOTA Trombetas. During this expedition, one specimen of Cteniloricaria napova (MPEG 34190) was collected from the Cuminapanema River basin, Óbidos, Pará State, Brazil (Tab. 1; Fig. 2). As stated by Dutra et al. (2020), that research was authorized by the Brazilian System of Biodiversity Information and Authorization (SISBIO), license number 4681–1. It was also approved by the Ethics Committee on the Use of Animals in Research of the Federal University of Pará, process CEUA 8293020418.

FIGURE 1 | Distribution of Cteniloricaria in the Guiana Shield. Circles = C. platystoma according to Covain et al. (2012); black dots = C. platystoma, examined specimens. White star, type locality of C. napova; red star, new locality of C. napova. Each symbol can cover more than one lot or locality. 

TABLE 1 | Descriptive morphometrics and meristic data of Cteniloricaria napova from the Cuminapanema River. Asterisk = broken spine.

 

 

MPEG 34190 (n=1)

Standard length (SL)

117.4

Percentages of standard length

Head length (HL)

21.1

Predorsal length

31.4

Postdorsal length

57.9

Caudal-peduncle length

48.5

Cleithral width

18.1

Abdominal length

16.7

Thoracic length

15.0

Pectoral-fin unbranched ray length

22.5

Pelvic-fin unbranched ray length

19.4

Dorsal-fin unbranched ray length

*

Anal-fin unbranched ray length

16.5

Anus to pelvic-fin origin length

10.3

Anus to pectoral-fin origin length

24.6

Anus to anal-fin origin length

8.4

Anus to tip of snout length

39.0

Body width at dorsal-fin origin

15.3

Body width at anal-fin origin

13.1

Body width at eighth postdorsal plate

13.0

Body width at fourteenth postdorsal plate

8.6

Body depth at dorsal-fin origin

10.6

Minimum caudal peduncle depth

1.7

Percentages of head length

Snout length

51.4

Nostril to tip of snout length

36.0

Distal end of operculum to tip of snout length

75.6

Maximum orbital diameter

17.7

Interorbital width

24.2

Head depth

49.4

Head depth at internostril

22.3

Meristic data

Number of premaxillary teeth

45

Number of dentary teeth

31

Number of plates before coalescence

20

Number of plates after coalescence

9

Number of plates in the lateral series

29

Number of plates of lateral abdominal plates

6

Pectoral-fin rays

i.6

Dorsal-fin rays

i.7

Pelvic-fin rays

i.5

Anal-fin rays

i.5

Caudal-fin rays

i.11.i

 

Laboratory work. The specimen was identified following Covain et al. (2012) and deposited in the fish collection of the MPEG, Belém, Pará (MPEG 34190). Institutional acronyms follow Sabaj (2020).

Results​


Identification. Cteniloricaria can be diagnosed (besides characters mentioned above) from Harttia by having a dark transverse, half-moon shaped band on the caudal-fin base, occupying the base of all rays on upper and lower lobes (vs. dark blotch at caudal-fin base); tip of snout covered with plates (vs. tip of snout naked, devoid of plates); and abdominal plates shaped as medium-sized polygonal plates completely covering the abdomen (vs. abdominal plates absent or present as small platelets, partially or entirely covering the abdomen) (Londoño-Burbano, Reis, 2021). Cteniloricaria napova was initially diagnosed by Covain, Fisch-Muller (in Covain et al., 2012) from its only congener, C. platystoma, by having a distinctly spotted color pattern (our specimen, Fig. 2; vs.indistinctly marbled without spots, Fig. 3) and from its molecular barcode. Besides, the authors listed five proportional measurements and one count that supposedly distinguish the two species, but these were presented as mean, standard deviation, and P values. When looking at the range for each of those variables and the entire table of comparative measurements, all ranges extensively overlap, not being actually diagnostic. The Brazilian specimen was identified as Cteniloricaria napova based on the color pattern, its locality, morphometric measurements, and meristic counts obtained as additional information (Tab. 1).

FIGURE 2 | Cteniloricaria napova, MPEG 34190, 117.4 mm SL, Brazil, Pará State, Óbidos municipality, unnamed creek tributary to Cuminapanema River, Curuá River basin (approx. 0°57’S 55°30’W).

Conservation status. Cteniloricaria napova is known from the headwaters of the Paru de Oeste River in southern Suriname and the middle Cuminapanema River in Brazil, both draining to the Amazon basin in the southern border of the Guiana Shield (Fig. 1). Both river basins are mostly unexplored, and the species is likely to occur in other localities within these basins. The two known collecting sites are located inside conservation areas, the Trio Amerindian territory in Sipaliwini District, Suriname, and the Trombetas State Forest in Brazil. Despite gold mining and moderate deforestation in the region, rivers and forests are mostly well preserved, and no specific threats to the species were identified. For these reasons, C. napova is preliminarily assessed as Least Concern (LC) according to the IUCN criteria and categories (IUCN Standards and Petitions Committee, 2019).

FIGURE 3 | Loricaria platystoma, BMNH 1866.8.14.124, lectotype, 171.5 mm SL, Suriname. Photo by Mark Allen (WAM; ACSI Images Database). 

Discussion​


The Guianas Region is a significant Neotropical area of endemism across most taxonomic groups (Cardoso, Montoya-Burgos, 2009). Rivers in the Guianas Region drain towards the Atlantic Ocean and are separated from the Amazon basin by a series of old mountains in the northern border of Brazil, markedly isolating the hydrological systems of the Guianas Region (Cardoso, Montoya-Burgos, 2009). The relative isolation of the Guianese hydrological systems, along with the possibility that this region was a Pleistocene humid refuge, may explain its high level of endemic freshwater fishes and other organisms (Cardoso, Montoya-Burgos, 2009). However, the authors stated that this hypothesis has been difficult to conciliate with freshwater fish diversification at the temporal scale because most of the diversity predates the Pleistocene; contrary to what Miller et al. (2005) suggested, in that significant and periodic sea-level fluctuations have persisted throughout the last six million years, with an accelerated rhythm during the Pleistocene. On the other hand, Rocha, Kaefer (2019) discussed that the Amazonian diversity appears to be the result of multiple factors with contribution of both allopatric and parapatric diversification mechanisms across different taxa, in addition to vicariant processes (see also Noonan, Gaucher, 2005; Whinnett et al., 2005; Antonelli et al., 2010). Even though the Pleistocene humid refuge remains to be accepted as one of the primary process in diversification of freshwater fishes in the region (Weitzman, Weitzman, 1982), low sea-level periods might have allowed river interconnections at their lower section, enhancing freshwater taxa dispersal from one basin to another. In contrast, high sea level periods would have fragmented populations into newly isolated river basins thus promoting allopatric differentiation (Cardoso, Montoya-Burgos, 2009).

Cteniloricaria napova was considered an endemic species of the Sipaliwini region in southern Suriname, southern Guiana Shield with altitudes varying from 100 to 500 m above sea level, including areas of both Amazon rainforest and savanna vegetation (Vari et al., 2009). Nevertheless, the fish fauna of the Guianas is among the best known in South America due to a series of intensive investigations and inventories, particularly in French Guiana, and new species are being found by every expedition conducted in that region (see Lemopoulos, Covain, 2018). Several fishes appear to have dispersed north-south across this watershed divide, rising evidence for the southern Guiana Shield slope being a north-south dispersal region (Lujan et al., 2020).

River capture is potentially a key geomorphological driver of range expansion and cladogenesis in freshwater limited taxa (Cardoso, Montoya-Burgos, 2009; Albert, Reis, 2011). River capture is characterized by the transference of a river (or a segment of a river) between basins caused by erosion and/or tectonic processes and, as a result, the biodiversity associated with the diverted river (i.e., species and genetic diversity) will then be present in the receiver basin (Albert, Reis, 2011; Souza et al., 2020). Considering the current distribution of the two species of Cteniloricaria, two main stream capture events may have played a key role in shaping their current distributions.

The first event might have caused the divergence between Cteniloricaria platystoma, distributed in the north-flowing coastal rivers of the Guianas from the Essequibo in Guyana to the Sinnamary in French Guiana, and C. napova, occurring in the south-flowing Amazon tributaries Paru de Oeste and Curuá (Fig. 1). Headwaters of the Corantijn River are separated from the headwaters of above Amazon tributaries by two mountain chains: the Grens and the Acarai mountains, although these highlands are supposedly semi-permeable to fish dispersal because of headwater interdigitations (Lujan, Armbruster, 2011). A possible connection already hypothesized by Nijssen (1970) is located in the Sipaliwini Savannah, connecting the Paru de Oeste River (a tributary to the Trombetas River and type locality of C. napova) to the Sipaliwini River (a tributary to the Corantijn River). Nijssen (1970) described several potential headwater corridors that might have provided dispersal routes for fishes between the north-flowing Corantijn and south-flowing Paru de Oeste rivers across the Grens and Acarai Mountains, which form the drainage divide. However, a parsimony analysis of endemism in fish communities across the eastern Guiana Shield by Lemopoulos, Covain (2018) raised doubts for Nijssen’s (1970) corridor hypothesis, given the distinctiveness of the fish samples between headwaters of Paru de Oeste and Corantijn rivers; thus the authors hypothesized vicariant assemblages for such region.

The second event that may have played an essential role in shaping the distribution of Cteniloricaria napova is a possible, more recent headwater capture between south-flowing Amazon tributaries, namely the Paru de Oeste and the Cuminapanema rivers, leading to the presence of the species in both parallel basins (Fig. 1). The alternative scenario of C. napova passing between these two basins through the Amazon River is less probable considering the alluvial environment of the Amazon main channel.

There are other examples within the Loricarioidea about disjoint distribution of taxa, such as the reported here for Cteniloricaria. One of them is related to the poorly known but unique genus Lithogenes Eigenmann, 1909. Lithogenes villosus Eigenmann, 1909 (Potaro-Essequibo) and L. wahari Schaefer & Provenzano, 2008 (Cuao-Orinoco) are found in the Guiana Shield, and a third species, L. valencia Provenzano, Schaefer, Baskin & Royero, 2003, is thought to be from the Lago Valencia drainage in the coastal mountains of northern Venezuela (Lujan, Armbruster, 2011). Dispersal via headwater capture seems a likely avenue for Lithogenes, as well as for Cteniloricaria, which live in clear, swift-flowing streams (Schaefer, Provenzano, 2008). The type of habitat described for Lithogenes is the same as for Cteniloricaria regarding water conditions and type of current, although the latter is also found on sandy bottom (see Londoño-Burbano et al., 2014, 2020; Lujan et al., 2018, 2020 for additional examples of disjoint distribution within Loricariidae and Loricariinae).

Most distributions within the Guiana Shield can be explained by current watershed boundaries, stream capture events in the uplands of larger systems, and/or ancient river systems such as the proto-Berbice (Lujan, Armbruster, 2011); stream capture events seems to be more suitable regarding Cteniloricaria. River captures can contribute both to a range expansion, allowing species to reach new basins, and to a secondary contact between populations of species previously present in neighboring basins (Souza et al., 2020); ideally, both geological and biological evidence converge when inferring drainage rearrangement events (Waters et al., 2001, 2006). However, geological evidence is not always available or is generally based on controversial morphological features (e.g., ‘capture elbows’; Souza et al., 2020). Therefore, in many cases, it is necessary to rely on biological data, particularly species distribution and genetics, for supporting cases of drainage rearrangements (Souza et al., 2020).

As stated above, even though several scenarios for the disjoint distribution of C. napova are possible, river capture seems to be the more appropriate for the distribution area and adaptations shown by the species (i.e., types of substrate, fast currents, water quality). Nevertheless, further studies within and between populations of Cteniloricaria using molecular evidence to test genetic distances, haplotype diversity, niche partitions, and phylogeographic analyses, encompassing the entire distribution of the genus, are necessary to offer a more robust hypothesis for the origin of the distribution of this group across the Guiana and Brazilian shields.

Material examined: Cteniloricaria napova: MHNG 2704.030, 6, 71.0–128.7 mm SL, paratypes, Suriname, Sipaliwini District, Savannah in Trio Amerindian territory at the Suriname-Brazil border, Four Brothers Mountains in an unnamed tributary creek of the Paru de Oeste River, collected and donated by the Trio tribe in Sipaliwini. MPEG 34190, 1, 117.4 mm SL, Brazil, Pará State, Óbidos municipality, unnamed creek tributary to Cuminapanema River, Curuá River basin, approx. 0°57’S 55°30’W. Cteniloricaria platystoma:AUM 37942, 1, 67.2 mm SL, Guyana, Essequibo River basin, Region 10 Upper Demerara-Berbice, Essequibo River at Kurukupari, east bank. AUM 38822, 4, 47.8–157.3 mm SL, Guyana, Essequibo River basin, Region 9 Upper Takutu and Essequibo, Kuyuwini River at Kuyuwini Landing. AUM 39038, 4, 47.8–102.4 mm SL, Guyana, Essequibo River basin, Region 9 Upper Takutu and Essequibo, Essequibo River at Yukanopito Falls, 44.5 km southwest mouth of Kuyuwini River. AUM 39055, 11, Guyana, Essequibo River basin, Region 9 Upper Takutu and Essequibo, Essequibo River at Kassi-Attae rapids, 5.5 km SE mouth of Kuyuwini River.AUM 44325, 1, 56.2 mm SL, Guyana, Essequibo River basin, Region 8 Essequibo River at Kurukapari Falls, upstream from Iwokrama. AUM 45341, 12, 53.9–74.4 mm SL, Guyana, Essequibo River basin, Region 8 Potaro-Siparuni, Essequibo River, in rapids. AUM 45352, 11, 51.0–85.3 mm SL, Guyana, Essequibo River basin, Region 8 Potaro-Siparuni, Essequibo River, side channel in rapids. AUM 48174, 8, 1 c&s, 86.7–140.3 mm SL, Guyana, Rupununi-Essequibo River drainage, Region 8 Potaro-Siparuni, Burro Burro River at Suraima.

Acknowledgments​


For lending material under their care and hospitality and technical assistance to the first author during visits to their museums and collections, we are very grateful to David C. Werneke and Jonathan W. Armbruster (AUM), and Raphaël Covain and Sonia Fisch-Muller (MHNG). Thanks to Mark Allen (WAM) for allowing the use of the photo of Loricaria platystoma in Fig. 3. Comments from three anonymous reviewers improved the quality of the manuscript. AL-B was supported by a PhD scholarship by CNPq process 140600/2014–0, financial support from Colciencias (#2011/529), and a Postdoctoral Fellowship from FAPERJ Pós-Doutorado Nota 10 (05/2019 – E-26/202.356/2019). MBM was financially supported by MCTIC/CNPq (processes 444338/2018–7 and 301339/2020–1). RER is partially funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq processes 306455/2014–5 and 400166/2016–0).

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Authors


Alejandro Londoño-Burbano1, 2 , Marina Barreira Mendonça3  and Roberto E. Reis2 

[1]    Museu Nacional, Universidade Federal do Rio de Janeiro, Departamento de Vertebrados – Setor de Ictiologia, Quinta da Boa Vista, São Cristóvão, 20940-040 Rio de Janeiro, RJ, Brazil. (ALB) alondonoburbano@gmail.com (corresponding author).

[2]    Pontifícia Universidade Católica do Rio Grande do Sul, Av. Ipiranga, 6681, 90619-900 Porto Alegre, RS, Brazil.
(RER) reis@pucrs.br.

[3]    Museu Paraense Emilio Goeldi, Coordenação Zoologia, Programa de Capacitação Institucional (PCI), Setor Ictiologia, Campus Pesquisa, Avenida Perimetral, 1901, 66077-530 Belém, PA, Brazil. (MBM) barreira.mm@gmail.com.

Authors Contribution


Alejandro Londoño-Burbano: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Software, Supervision, Visualization, Writing-original draft, Writing-review and editing.

Marina Barreira Mendonça: Data curation, Formal analysis, Investigation, Methodology, Project administration, Supervision, Visualization, Writing-original draft, Writing-review and editing.

Roberto E. Reis: Conceptualization, Data curation, Formal analysis, Funding acquisition, Methodology, Project administration, Visualization, Writing-original draft, Writing-review and editing.

Ethical Statement​


The research was authorized by the Brazilian System of Biodiversity Information and Authorization (SISBIO), license number 4681–1. It was also approved by the Ethics Committee on the Use of Animals in Research of the Federal University of Pará, process CEUA 8293020418.

Competing Interests


The authors declare no competing interests.

How to cite this article


Londoño-Burbano A, Mendonça MB, Reis RE. The distribution of Cteniloricaria (Siluriformes: Loricariidae): known and new records in Brazil suggest headwater captures as drivers of disjoint distribution. Neotrop Ichthyol. 2021; 19(2):e210018. https://doi.org/10.1590/1982-0224-2021-0018

Copyright​


This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Distributed under

Creative Commons CC-BY 4.0

© 2021 The Authors.

Diversity and Distributions Published by SBI

Submitted January 14, 2021

Accepted April 13, 2021 by Marcelo Britto

Epub Jun 21, 2021