Research Article |
Corresponding author: Jairo Arroyave ( jarroyave@ib.unam.mx ) Academic editor: Maria Elina Bichuette
© 2024 Jairo Arroyave, Arturo Angulo, Sonia Gabriela Hernández-Ávila, Martín Alonso Buenavad-González, Pablo Rojas-Rodríguez, Stanimira Deleva, Andrés Ulloa, Sophie Picq, Caleb D. McMahan.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Arroyave J, Angulo A, Hernández-Ávila SG, Buenavad-González MA, Rojas-Rodríguez P, Deleva S, Ulloa A, Picq S, McMahan CD (2024) New vouchered and taxonomically verified records of cave-dwelling populations of catfishes of the genus Rhamdia (Siluriformes, Heptapteridae) from Costa Rica. Subterranean Biology 50: 29-52. https://doi.org/10.3897/subtbiol.50.134387
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Dedicated ichthyological surveys in two karstic caves in Costa Rica resulted in the discovery of hypogean populations from three epigean species of catfishes of the genus Rhamdia. The taxonomic identity of these populations was initially determined based on morphological traits and subsequently corroborated with comparative DNA sequence data in a phylogenetic framework. Individuals from all hypogean populations documented herein exhibit only partial troglomorphism, characterized by only moderate (vs. complete) integumentary depigmentation without extreme eye reduction/loss. A similar pattern of incomplete troglomorphism at the individual level has been observed in other cave-dwelling species/populations of Middle American Rhamdia, and tentatively attributed to gene flow with and/or incipient speciation from epigean lineages. Since most hypogean forms of Rhamdia derive from/are part of a larger clade of primarily R. laticauda, our discovery of cave-dwelling populations assignable to R. nicaraguensis and R. guatemalensis is noteworthy, particularly in the case of the former, which represents the first taxonomically verified record of a cave-dwelling population of this epigean species. Among our findings is the remarkable discovery of hypogean populations from two different species of Rhamdia (R. laticauda and R. nicaraguensis) inhabiting the same cave (Gabinarraca). This finding is particularly significant because it represents the first time that cave-dwelling populations from different species of Rhamdia are reported to be living in syntopy. Continued discovery of cave-dwelling populations during targeted ichthyological surveys reinforces the notion that our understanding of the diversity of hypogean Rhamdia is incomplete and that sustained exploration and taxonomically sound documentation work are paramount to advancing knowledge about the diversity and evolution of these group of Neotropical catfishes.
Cavefishes, hypogean, stygobionts, stygofauna, troglomorphism
With 27 currently valid species distributed throughout most of the tropical Americas, catfishes of the genus Rhamdia Bleeker 1858 are a group of moderately diverse Neotropical freshwater fishes noteworthy, among other things, because of their tendency to colonize subterranean waters and maintain resident hypogean populations (
Despite its widespread distribution, the bulk of the subterranean diversity of the genus Rhamdia has been primarily described from karstic regions in Mexico. Mexican cave Rhamdia includes four of the six currently valid troglobitic species in the genus plus at least 10 cave-dwelling populations taxonomically assigned, for the most part, to the epigean species R. laticauda (Kner 1858) (
Whereas recent studies have uncovered and documented the existence of previously unknown cave-dwelling populations of Rhamdia in Mexico (
Historical accounts of hypogean Rhamdia from Costa Rica include reported sightings of cave-dwelling forms of R. guatemalensis (five sites), R. nicaraguensis (one site), and Rhamdia sp. (four sites) (
In a first effort towards properly and accurately documenting the taxonomic diversity of cave Rhamdia in Costa Rica, we conducted dedicated ichthyological surveys in two karstic caves with anecdotal reports on the presence of these catfishes: Corredores and Gabinarraca (or Cavernas de Venado) (Fig.
Location of the surveyed caves A map of Costa Rica displaying the location of Gabinarraca and Corredores caves (green dots) at the country-level scale (borders with Nicaragua to the north and Panama to the south highlighted in light purple). Maps displaying the location of the surveyed caves at the local scale, including geomorphological and hydrological features: B Gabinarraca and C Corredores.
Gabinarraca and Corredores caves are located in the Costa Rican provinces of Alajuela and Puntarenas, respectively (Fig.
Photographs displaying physical features of the surveyed caves and associated rivers/streams A Gabinarraca cave entrance, showing the outflow of water into Quebrada El Túnel B inside Gabinarraca cave while electrofishing C Quebrada El Túnel close to the entrance of Gabinarraca cave D Corredores cave entrance E Río Corredor as seen from the cave entrance higher up F Río Corredor riverbed at a small canyon on the way to the cave access point.
Both sampled caves are wet (containing active watercourses but not fully flooded or submerged) and mostly horizontal, and therefore did not require specialized vertical caving techniques for surveying and sampling. Specimen sampling was accomplished using a combination of baited minnow traps and electrofishing. Inside the surveyed caves, we collected fishes along the main longitudinal axis of the cave up to the point of maximum penetration, which was approximately a few hundred meters in both caves. In addition to the caves, we collected specimens of Rhamdia from epigean populations from streams and rivers mainly near Gabinarraca cave (Río Frío basin), including the very stream flowing out of the cave (Quebrada El Túnel) (Figs
Collecting sites of epigean populations of Rhamdia sampled in this study 1 Quebrada El Túnel (at Gabinarraca cave entrance) 2 Quebrada El Túnel (further downstream from Gabinarraca cave entrance) 3 Río Pataste 4 Río Arenal 5 Quebrada Palma, and 6 Quebrada Altamira. All sites are within the Alajuela province, Atlantic versant. Black outline in map corresponds to the continental water divide.
Sampling localities with their respective species, catalog/vouchers numbers, and GenBank accession numbers of sequences generated in this study and used in phylogenetic analyses. *at Gabinarraca cave entrance; **further downstream from Gabinarraca cave entrance.
Habitat | Locality | Coordinates | Municipality | Province | Basin | Versant | Species | Catalog (n) | Tissued vouchers | DNA voucher | GenBank Accession | |
---|---|---|---|---|---|---|---|---|---|---|---|---|
COI | CYB | |||||||||||
Hypogean | Gabinarraca cave | 10°33'17"N, 84°46'01"W | Venado | Alajuela | Río Frío | Atlantic | Rhamdia laticauda |
|
JA1913-17 | JA1913 | PQ451515 | PQ458956 |
JA1914 | PQ451516 | PQ458957 | ||||||||||
JA1915 | PQ451517 | PQ458958 | ||||||||||
JA1916 | PQ451492 | PQ458959 | ||||||||||
Rhamdia nicaraguensis |
|
JA1902-12 | JA1902 | PQ451502 | PQ458966 | |||||||
JA1903 | n/a | PQ458967 | ||||||||||
JA1904 | PQ451503 | PQ458968 | ||||||||||
JA1905 | PQ451504 | PQ458969 | ||||||||||
JA1906 | PQ451505 | PQ458970 | ||||||||||
JA1907 | PQ451506 | PQ458971 | ||||||||||
JA1908 | PQ451507 | PQ458972 | ||||||||||
JA1909 | PQ451508 | PQ458973 | ||||||||||
JA1910 | PQ451509 | PQ458974 | ||||||||||
JA1911 | PQ451497 | PQ458975 | ||||||||||
JA1912 | PQ451510 | PQ458976 | ||||||||||
Corredores cave | 08°39'23"N, 82°54'44"W | Ciudad Neily | Puntarenas | Río Coto | Pacific | Rhamdia guatemalensis |
|
JA2068-74 | JA2068 | PQ451499 | PQ458950 | |
JA2070 | n/a | PQ458951 | ||||||||||
JA2071 | PQ451500 | PQ458952 | ||||||||||
JA2072 | PQ451501 | PQ458953 | ||||||||||
JA2073 | n/a | PQ458954 | ||||||||||
JA2074 | n/a | n/a | ||||||||||
Epigean | Quebrada El Túnel* | 10°33'17"N, 84°46'01"W | Venado | Alajuela | Río Frío | Atlantic | Rhamdia laticauda |
|
JA1921-23 | JA1921 | PQ451518 | PQ458960 |
JA1922 | PQ451493 | PQ458961 | ||||||||||
JA1923 | PQ451519 | PQ458962 | ||||||||||
Rhamdia nicaraguensis |
|
JA1918-20 | JA1918 | PQ451511 | PQ458977 | |||||||
JA1919 | PQ451512 | PQ458978 | ||||||||||
JA1920 | PQ451513 | PQ458979 | ||||||||||
Quebrada El Túnel** | 10°33'17"N, 84°45'20"W | Venado | Alajuela | Río Frío | Atlantic | Rhamdia laticauda |
|
JA1924-30 | JA1927 | PQ451520 | n/a | |
JA1928 | PQ451494 | PQ458963 | ||||||||||
Rhamdia nicaraguensis |
|
JA1931-32 | n/a | n/a | n/a | |||||||
Epigean | Río Arenal | 10°30'09"N, 84°35'38"W | Venado | Alajuela | Río San Carlos | Atlantic | Rhamdia laticauda |
|
JA1952-59 | JA1955 | PQ451495 | PQ458964 |
Rhamdia nicaraguensis |
|
JA1960-61 | n/a | n/a | n/a | |||||||
Río Pataste | 10°34'07"N, 84°40'02"W | Venado | Alajuela | Río Frío | Atlantic | Rhamdia laticauda |
|
JA1943-46 | JA1946 | PQ451521 | n/a | |
Rhamdia nicaraguensis |
|
JA1936-42 | JA1939 | n/a | PQ458980 | |||||||
JA1940 | PQ451514 | n/a | ||||||||||
Quebrada Altamira | 10°44'01"N, 85°03'34"W | Bijagua | Alajuela | Río Zapote | Atlantic | Rhamdia laticauda |
|
JA1804-11 | JA1804 | PQ451496 | PQ458955 | |
Quebrada Palma | 10°29'54"N, 84°41'19"W | Palma | Alajuela | Río San Carlos | Atlantic | Rhamdia nicaraguensis |
|
JA1734-38 | JA1734 | PQ451498 | PQ458965 | |
Rhamdia laticauda |
|
JA1729-33 | n/a | n/a | n/a |
To document patterns of phenotypic and genetic variation, and to shed light on the taxonomic nature of the cave-dwelling populations of Rhamdia reported herein, we generated meristic and morphometric data from hypogean samples as well as DNA sequence data from both hypogean and epigean samples. Morphometric measurements and meristic counts follow previous taxonomic studies of Rhamdia (
Our sampling efforts in the surveyed caves (Corredores and Gabinarraca) resulted in the discovery of three cave-dwelling populations of Rhamdia, identified as members of the species R. guatemalensis (Corredores cave; n = 8) (Figs
Photographs of hypogean Rhamdia nicaraguensis from Gabinarraca cave A totality of specimens collected (n = 13), immediately postmortem and before tissuing and preservation B lateral view of live specimen in aquarium C lateral view of specimen immediately postmortem. Metacercariae (two) of the parasitic fluke Clinostomum sp. are visible at the base of the anal fin D live specimens (in aquarium) of hypogean (Gabinarraca, yellow) and epigean (Quebrada El Túnel, dark brown) R. nicaraguensis. Scale bar: 1 cm.
Photographs of preserved representatives of the populations of cave-dwelling Rhamdia from Costa Rica reported in this study A R. guatemalensis from Corredores cave (
Phylogenetic relationships of Middle American Rhamdia inferred from comparative COI data. Colored circles on nodes indicate degree of clade support as determined by bootstrap values: black > 95, 95 ≥ blue ≥ 75, red < 75. Terminal names as follow: Species name + GenBank accession or catalog/voucher (for new/unpublished sequences) + country, basin (in parenthesis). Terminals corresponding to samples from populations of Costa Rican hypogean Rhamdia (documented herein) in red. Terminals corresponding to samples from Costa Rican epigean Rhamdia collected in this study in blue. Outgroup taxon (Rhamdia quelen) not shown. The dashed rectangle indicates the R. guatemalensis clade, whereas the light gray rectangle indicates the “R. laticauda-group” clade, inclusive of R. nicaraguensis, R. parryi, and the four Mexican stygobitic species.
Phylogenetic relationships of Middle American Rhamdia inferred from comparative CYTB data. Colored circles on nodes indicate degree of clade support as determined by bootstrap values: black > 95, 95 ≥ blue ≥ 75, red < 75. Terminal names as follow: Species name + GenBank accession or catalog/voucher (for new/unpublished sequences) + country, basin (in parenthesis). Terminals corresponding to samples from populations of Costa Rican hypogean Rhamdia (documented herein) in red. Terminals corresponding to samples from Costa Rican epigean Rhamdia collected in this study in blue. Outgroup taxon (Rhamdia quelen) not shown. The dashed rectangle indicates the R. guatemalensis clade, whereas the light gray rectangle indicates the “R. laticauda-group” clade, inclusive of R. nicaraguensis, R. parryi, and the four Mexican stygobitic species.
Phylogenetic relationships of Middle American Rhamdia inferred from comparative COI + CYTB data (concatenated). Colored circles on nodes indicate degree of clade support as determined by bootstrap values: black > 95, 95 ≥ blue ≥ 75, red < 75. Terminal names as follow: Species name + GenBank accession or catalog/voucher (for new/unpublished sequences) + country, basin (in parenthesis). Terminals corresponding to samples from populations of Costa Rican hypogean Rhamdia (documented herein) in red. Terminals corresponding to samples from Costa Rican epigean Rhamdia collected in this study in blue. Outgroup taxon (Rhamdia quelen) not shown. The dashed rectangle indicates the R. guatemalensis clade, whereas the light gray rectangle indicates the “R. laticauda-group” clade, inclusive of R. nicaraguensis, R. parryi, and the four Mexican stygobitic species.
Morphological and meristic data from the specimens collected at the surveyed caves are presented in Tables
Meristic comparative data from samples of hypogean populations of Rhamdia spp. from Gabinarraca and Corredores caves. Meristic traits abbreviations as follows: PFR = pectoral-fin rays, PvFR = pelvic-fin rays, DFR = dorsal-fin rays, ARF = anal-fin rays, uCFR = upper caudal-fin rays, and lCFR = lower caudal-fin rays. Caudal-fin rays numbers (x,y,z) correspond to unsegmented (x), unbranched segmented (y), and branched segmented (z) rays.
Cave | Species | Catalog | Voucher | PFR | PvFR | DFR | AFR | uCFR | lCFR |
---|---|---|---|---|---|---|---|---|---|
Gabinarraca | Rhamdia laticauda |
|
3323-01-A | I-9 | 6 | I-6 | 9 | 3,2,8 | 3,2,9 |
JA1906 | I-9 | 7 | I-6 | 9 | 3,2,9 | 3,2,9 | |||
JA1902 | I-9 | 7 | I-5 | 10 | 3,2,9 | 3,2,8 | |||
3323-01-B | I-9 | 7 | I-6 | 9 | 3,2,8 | 3,2,10 | |||
Rhamdia nicaraguensis |
|
JA1903 | I-9 | 7 | I-5 | 9 | 3,2,6 | 3,2,8 | |
JA1904 | I-9 | 7 | I-6 | 10 | 3,2,9 | 3,2,10 | |||
JA1905 | I-9 | 7 | I-6 | 9 | 3,2,8 | 3,2,9 | |||
JA1907 | I-9 | 7 | I-6 | 9 | 3,2,9 | 3,2,9 | |||
JA1908 | I-9 | 8 | I-6 | 9 | 3,2,8 | 3,2,8 | |||
JA1909 | I-9 | 7 | I-6 | 9 | 3,2,9 | 3,2,9 | |||
JA1910 | I-9 | 7 | I-6 | 9 | 3,2,9 | 3,2,9 | |||
JA1911 | I-9 | 7 | I-6 | 9 | 3,2,7 | 3,2,9 | |||
JA1912 | I-9 | 7 | I-6 | 9 | 3,2,9 | 3,2,8 | |||
Corredores | Rhamdia guatemalensis |
|
3330-01-A | I-7 | 6 | I-6 | 9 | 3,2,9 | 3,2,10 |
JA2068 | I-8 | 7 | I-6 | 9 | 3,2,9 | 3,2,10 | |||
JA2069 | I-9 | 7 | I-6 | 9 | 3,2,9 | 3,2,10 | |||
JA2070 | I-9 | 6 | I-6 | 8 | 3,2,8 | 3,2,9 | |||
JA2071 | I-8 | 7 | I-6 | 8 | 3,2,9 | 3,2,9 | |||
JA2072 | I-7 | 6 | I-7 | 8 | 3,2,9 | 3,2,7 | |||
JA2073 | I-9 | 7 | I-6 | 9 | 3,2,9 | 3,2,9 | |||
JA2074 | I-9 | 7 | I-6 | 9 | 3,2,8 | 3,2,9 |
Morphometric comparative data from samples of hypogean populations of Rhamdia spp. from Gabinarraca and Corredores caves. Measurements abbreviations as follows: SL = Standard Length, HL = Head Length, HL = Head Length, BW = Body Width, DFH = Dorsal Fin Height, DSH = Dorsal-fin Spine Height, AFL = Anal Fin Length, AdFL = Adipose Fin Length, PFL = Pectoral Fin Length, PSL = Pectoral-fin Spine Length, PvFL = Pelvic Fin Length, ISL = Interdorsal Space Length, CPL = Caudal Peduncle Length, CPD = Caudal Peduncle Depth, IOW = Interorbital Width, ORB = Orbital Diameter, SNT = Snout Length, MBL = Maxillary Barbel Length, MdBL = Mandibular Barbel Length, MeBL = Mental Barbel Length.
Gabinarraca Cave | Corredores Cave | ||||||||
---|---|---|---|---|---|---|---|---|---|
Rhamdia laticauda (n = 4) | Rhamdia nicaraguensis (n = 9) | Rhamdia guatemalensis (n = 8) | |||||||
Range | Mean | SD | Range | Mean | SD | Range | Mean | SD | |
mm | |||||||||
SL | 119.94–198.00 | 150.45 | 34.85 | 107.16–171.00 | 132.82 | 21.23 | 124.41–237.00 | 193.43 | 45.70 |
HL | 29.75–43.29 | 34.45 | 6.04 | 24.80–40.43 | 31.32 | 5.50 | 28.60–52.92 | 43.10 | 10.27 |
% SL | |||||||||
HL | 21.46–24.99 | 23.14 | 1.74 | 22.64–24.64 | 23.53 | 0.67 | 20.49–22.99 | 22.30 | 0.78 |
BW | 16.35–17.92 | 17.19 | 0.64 | 15.48–18.14 | 16.56 | 0.76 | 18.00–18.91 | 18.48 | 0.32 |
DFH | 13.25–14.75 | 14.00 | 0.64 | 10.17–14.88 | 13.34 | 1.28 | 12.48–15.64 | 13.93 | 1.03 |
DSH | 5.32–6.20 | 5.81 | 0.37 | 4.19–5.05 | 4.55 | 0.29 | 5.98–6.72 | 6.35 | 0.28 |
AFL | 17.29–18.80 | 17.95 | 0.63 | 18.32–21.42 | 20.15 | 1.05 | 17.61–19.60 | 18.59 | 0.60 |
AdFL | 40.80–42.41 | 41.93 | 0.75 | 39.90–45.58 | 43.84 | 1.99 | 36.54–38.39 | 37.74 | 0.57 |
PFL | 10.49–13.89 | 12.22 | 1.50 | 12.45–13.79 | 13.15 | 0.45 | 12.16–13.89 | 12.95 | 0.57 |
PSL | 6.67–8.58 | 7.45 | 0.89 | 7.02–8.89 | 7.88 | 0.62 | 7.30–9.24 | 8.41 | 0.62 |
PvFL | 9.90–12.61 | 11.32 | 1.40 | 11.43–12.94 | 12.08 | 0.47 | 11.01–13.12 | 11.63 | 0.83 |
ISL | 4.61–4.78 | 4.69 | 0.08 | 1.46–2.43 | 1.67 | 0.30 | 5.27–7.75 | 6.67 | 0.85 |
CPL | 16.35–18.94 | 17.47 | 1.22 | 17.79–18.96 | 18.24 | 0.41 | 17.90–20.23 | 18.48 | 0.75 |
CPD | 9.95–10.35 | 10.11 | 0.17 | 9.78–11.12 | 10.30 | 0.40 | 9.71–11.36 | 10.83 | 0.55 |
% HL | |||||||||
IOW | 36.13–42.67 | 38.94 | 2.72 | 35.02–39.45 | 37.13 | 1.46 | 40.05–46.97 | 43.71 | 2.14 |
ORB | 17.39–20.10 | 18.65 | 1.23 | 15.94–20.24 | 17.98 | 1.44 | 9.01–16.09 | 12.07 | 2.16 |
SNT | 37.75–41.49 | 39.48 | 1.60 | 35.54–41.75 | 38.15 | 1.77 | 32.72–41.85 | 36.82 | 2.73 |
MBL | 100.11–117.27 | 111.31 | 7.64 | 88.97–136.11 | 121.53 | 14.67 | 124.49–228.91 | 158.01 | 33.37 |
MdBL | 47.62–54.66 | 50.70 | 3.01 | 54.28–74.97 | 60.26 | 5.95 | 62.72–90.31 | 72.73 | 9.92 |
MeBL | 27.66–36.79 | 32.88 | 3.97 | 32.69–46.50 | 35.71 | 4.21 | 41.76–55.44 | 47.45 | 5.06 |
GenBank accession numbers corresponding to the DNA sequence data generated in this study (COI and CYTB) are presented in Table
In the most recent and comprehensive review of Costa Rican cave-dwelling fauna,
Remarkably, among our findings is the discovery of syntopic hypogean populations from two different Rhamdia species (R. laticauda and R. nicaraguensis) inhabiting the Gabinarraca cave system. This finding is noteworthy because it represents the first taxonomically verified record of a cave-dwelling population of R. nicaraguensis. Furthermore, the population of R. laticauda from Gabinarraca cave constitutes the latest addition to the extensive list of hypogean records for this epigean species—which includes five populations from the karstic Sierra de Zongolica in the state of Veracruz (
Given the ample taxonomic and geographic coverage, the resulting phylogenies (Figs
Phylogeographic structure in R. guatemalensis and R. laticauda appears generally consistent with a latitudinal gradient and the expectations from catchment hydrology (
This pattern, also documented for numerous cave-dwelling populations of Rhamdia catfishes in southern Mexico (
In conclusion, this study adds to a body of work showcasing the continued discovery of cave-dwelling populations of Rhamdia catfishes during targeted ichthyological surveys in karstic regions of Middle America (
This research was financially supported by the Universidad Nacional Autónoma de México (UNAM) through a “Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT)” grant (IN214922) to JA, the Vicerrectoría de Investigación de la Universidad de Costa Rica (