Research Article |
Corresponding author: Peter Rask Møller ( pdrmoller1@gmail.com ) Academic editor: Kyle Piller
© 2020 Damir Hernández, Peter Rask Møller, Didier Casane, Erik García-Machado.
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:
Hernández D, Møller PR, Casane D, García-Machado E (2020) A new species of the cave-fish genus Lucifuga (Ophidiiformes, Bythitidae), from eastern Cuba. ZooKeys 946: 17-35. https://doi.org/10.3897/zookeys.946.51373
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Recently, a barcoding study and a molecular phylogenetic analysis of the Cuban species of the cave-fish genus Lucifuga Poey, 1858 revealed the existence of different evolutionary lineages that were previously unknown or passed unnoticed by morphological scrutiny (i.e., cryptic candidate species). In the present study, Lucifuga gibarensis is described as a new species restricted to anchialine caves in the northeastern karst region of the main island. The species was earlier described as a variety of Lucifuga dentata, but since the name was introduced as a variety after 1960, it is deemed to be infrasubspecific and unavailable according to the International Code of Zoological Nomenclature Art. 15.2. The new species differs from L. dentata by pigmented eyes vs. eyes absent and lack of palatine teeth vs. present. Lucifuga gibarensis seems to be most similar to the Bahamian species L. lucayana by showing pigmented eyes, 13 or 14 precaudal vertebrae and ten caudal fin rays. However, differs from it by a larger size of the pigmented eye (1.1–1.9 vs. 0.9–1.0% SL) and number of posterior lateral line neuromasts (30–33 vs. 34–35).
Anchialine caves, Gibara, Holguin, speleology, taxonomy, viviparous brotulas
Lucifuga Poey, 1858 is a conspicuous genus of obligate cave-dwelling fishes, currently recognised with six species distributed in Cuba and Bahamas (
Because of the characteristics of the habitats of Lucifuga species (caves, sinkholes and crevices) and the morphological modifications that they show in the evolutionary adaptations to the environment, the genus represents an iconic part of the fish fauna in Cuba. The scientific interest in these fishes, however, has been sporadic. Since the description of the genus and the two first Cuban species by Felipe
A controversial taxon has been Lucifuga dentatus var. holguinensis Díaz-Pérez, Nieto and Abio, 1987 from the Holguin province in eastern Cuba. It was suggested as a valid species name by
The morphological study of the Cuban Lucifuga species was based on the analysis of 214 individuals sampled from several localities covering most of its known distribution areas (Fig.
Abbreviations include:
FMNH Division of Fishes, Department of Zoology, Field Museum of Natural History, Chicago, Illinois, U.S.A.;
MCZ Museum of Comparative Zoology, Harvard University, Ichthyology Department, Cambridge, Massachusetts, U.S.A;
Family Bythitidae
Lucifuga subterranea Poey, 1858 by subsequent designation of Jordan and Evermann, 1896, type locality: El Cajio cave, but not precisely stated for L. subterranea, which was referred originally from caves of San Antonio, middle-south Havana province, Cuba.
Body moderately elongated and compressed mainly from the abdomen to the caudal end. Snout with two nostrils: anterior nostril tube-shape and smaller, placed near to the upper lip; posterior nostril is a larger hole, placed ca. midway between snout and eyes cavity. The mouth is subterminal with the lower jaw only slightly shorter than the upper. Opercular spines absent. Seven branchiostegal rays.
The entire body is covered with small, rounded cycloid scales; fins naked except for scales on pectoral fin basis. Predorsal area and operculum scaled. Branchiostegal membranes, entire underside of the head, snout, interorbital areas and entire course of the cavernous cephalic system are naked. Origin of dorsal fin approximately above the tip of pectoral fins. Pelvic fin is subjugular with a single ray reaching ca. 1/3 to halfway to the anus. Pectoral fin behind the operculum, peduncle short and narrow. Lateral line with two series of sensory neuromasts: upper and anterior series extends from the head to a point ca. midway between dorsal and anal fin origins; and lower and posterior series extends from a point under and slightly in advance of the end of the upper series to the mid side from the caudal base.
There are three symmetric sensory canal series on each side of the head: supraorbital series with three pores (two anterior and one posterior): the anteriormost is at the snout rim, the second open between and above the nasal openings, and the posterior single pore is at the end of the lateral canal above the operculum. The infraorbital series with six pores (three anterior and three posterior): first pore is slightly below the anterior nasal opening, the other five pores (two anterior and three posterior) are along the edge of infraorbital rim. Finally, the mandibular series with six pores (three anterior and three posterior). The first pore is in the fold of skin between the lip and canal series, the second is at the side of the jaw tip on the lower lip, the third is at the anterior end of the mandibular series, the fourth to sixth posterior pores open ventrally along the mandibular series. There is also a large preopercular pore. Teeth are present on the premaxillae, dentaries and vomer; but are present or absent in palatines.
Sexual dimorphism. The male copulatory organ is completely integrated into a fleshy genital hood which projects posteriorly beyond the anus, the lateral end of the hood could be from broad to conical. A fleshy small conical papillae project from the middle of the distal margin of the hood and is enclosed by lateral earlike lobes. Penis is placed underneath the hood.
Lucifuga dentatus
variety holguinensis
Lucifuga dentatus var. holguinensis
Lucifuga holguinensis
Dorsal fin rays 72–90; anal fin rays 58–72; pectoral fin rays 15–17, caudal fin rays 10; palatine teeth absent; rakers on anterior gill arch 17–19 (long gill-rakers 3); occiput and area between lateral canal and preopercular canal scaled; diameter of pigmented eyes 1.1–1.9% SL; total vertebrae 50–53.
Meristic and morphometric characters are given in Tables
Morphometric and meristic characters of Lucifuga spp. (HT: holotype; PT: paratype; ST: syntype).
L. gibarensis sp. nov. | L. dentata | L. simile | L. subterranea | L. lucayana | L. spelaeotes | ||||||
---|---|---|---|---|---|---|---|---|---|---|---|
HT | HT and 3 PT | ST, MCZ 32329 | 2 ST and 126 nontypes | 22 nontypes | HT | HT and 42 nontypes | HT | HT and 5 PTs | HT | HT, PT and 40 nontypes | |
Mean and range | Mean and range | Mean and range | Mean and range | Mean and range | Mean and range | ||||||
SL (mm) | 89.3 | 73.2 (45.0–89.3) | 85.0 | 91.0 (45–124) | 74.5 (57.5–103) | 69.0 | 66.1 (39.7–89.5) | 99.0 | 74.3 (44–99) | 110 | 106.3 (42–166) |
Morphometric characters (% SL) | |||||||||||
Head length | 26.0 | 27.5 (26.0–28.4) | 28.5 | 26.7 (18.4–31.5) | 24.0 (17.1–31.2) | 28.7 | 26.3 (18.8–28.9) | 28.8 | 28.4 (27.1–29.3) | 29.1 | 28.8 (26.2–31.3) |
Jaw length | 13.4 | 14.5 (13.4–15.3) | 14.9 | 14.3 (11.7–20.2) | 14.7 (11.2–17.0) | 13.3 | 12.0 (9.6–14.4) | 14.9 | 14.2 (13.2–14.9) | 16.2 | 14.7 (12.4–16.8) |
Maximum height | 20.4 | 19.1 (17.8–20.4) | – | 19.8 (13.1–24.5) | 20.8 (14.4–26.0) | – | 16.9 (13.2–21.7) | – | – | – | – |
Diameter of pigmented eye | 1.5 | 1.4 (1.1–1.9) | 0.0 | 0.02 (0.0–0.2) | 0.0 | 0.0 | 0.1 (0.0–0.3) | 1.0 | 1.0 (0.9–1.0) | 1.3 | 1.3 (0.7–1.8) |
Predorsal length | 39.1 | 37.6 (35.9–39.1) | 39.6 | 40.1 (31.5–50.7) | 40.2 (32.9–45.3) | 40.8 | 39.9 (36.3–44.0) | 37.0 | 36.4 (35.5–37.0) | 39.9 | 38.1 (34.7–41.1) |
Preanal length | 58.2 | 55.7 (52.6–58.3) | 53.7 | 54.6 (50.0–65.8) | 54.7 (44.0–61.3) | 55.4 | 54.0 (48.2–59.4) | 55.6 | 55.0 (51.7–57.6) | 54.1 | 54.2 (48.2–60.5) |
Pectoral fin length | 11.2 | 13.7 (11.2–15.3) | 11.4 | 10.6 (7.5–15.7) | 10.2 (8.0–12.5) | 10.3 | 8.9 (7.8–12.0) | 13.3 | 12.6 (11.3–13.3) | 12.5 | 12.7 (11.1–14.4) |
Base of pelvic fin to anal fin origin | 35.9 | 35.6 (32.2–38.7) | 31.5 | 31.5 (23.0–38.1) | 28.9 (20.3–33.8) | 31.6 | 31.6 (26.9–35.5) | 34.9 | 33.7 (29.4–36.9) | 31.3 | 31.2 (27.0–36.9) |
Dorsal fin origin to anal fin origin | 17.8 | 18.2 (17.8–18.9) | – | 14.3 (9.4–18.4) | 14.6 (12.3–16.9) | – | 14.2 (9.3–18.8) | – | – | – | – |
Meristic characters | |||||||||||
Dorsal fin rays | 72 | 82.3 (72–90) | – | 90.5 (82–102) | 72.9 (67–80) | 87 | 82.8 (70–87) | 91 | 89.2 (84–91) | 92 | 97.5 (86–109) |
Anal fin rays | 58 | 65.5 (58–72) | – | 72.4 (66–80) | 58.4 (54–70) | 71 | 64.2 (53–70) | 67 | 66.2 (63–69) | 71 | 73.8 (66–82) |
Caudal fin rays | 10 | 10 | – | 8 | 8 | 8 | 8 | 10 | 10 | 10 | 10 |
Pectoral fin rays | 16 | 16.0 (15–17) | 15 | 16.1 (15–17) | 14.4 (13–17) | 13 | 11.9 (10–13) | 17 | 17.2 (17–18) | 18 | 18.5 (17–20) |
Precaudal vertebrae | 14 | 13.5 (13–14) | – | 11.1(11–12) | 11 | 11 | 11.3 (11–12) | 13 | 12.8 (12–13) | 13 | 13.2 (13–14) |
Caudal vertebrae | 36 | 36.5 (36–37) | – | 35.9(34–37) | 34–35 | 37 | 35.8 (34–37) | 39 | 38.6 (37–39) | 39 | 39.5 (38–42) |
Total vertebrae | 50 | 51.0 (50–53) | – | 47.0(46–48) | 46 | 48 | 46.9 (46–48) | 52 | 51.3 (50–52) | 52 | 52.7 (51–55) |
Rakers on anterior gill arch | 18 | 18.0 (17–19) | 20 | 18.4 (15–22) | 17.6 (15–20) | 16 | 14.2 (12–17) | 16 | 15.3 (13–17) | 21 | 18.8 (15–23) |
Premaxillary teeth rows | 5 | 6.0 (5–7) | 6 | 4.3 (3–6) | 3.9 (3–5) | 8 | 4.0 (3–8) | 7 | 6.0 (5–7) | 8 | 6.8 (4–10) |
Palatine teeth rows | 0 | 0 | 3 | 2.1 (1–4) | 2.2 (1–4) | 0 | 0 | 0 | 0 | 5 | 3.7 (1–7) |
Lateral line neuromasts | 15/ 30 |
13–15/ 30–33 |
– | 12–18/ 22–33 |
12–15/ 24–27 |
– | 12–19/ 26–33 |
13/ 35 |
12–13/34–35 | 14/38 | 12–19/30–47 |
Occiput squamation | Yes | Yes | – | No 79%/Yes 21% | No | Yes | Yes | Yes |
Uniformly brown or light brown, with lighter fins and naked parts on the head. Nevertheless, one juvenile specimen (
Lucifuga gibarensis shows a very restricted known distribution, in a lithographically isolate karst patch of caves at the north of Gibara municipality, Holguín province, without any overlap with other Cuban species of the genus (Fig.
Number of dorsal fin rays | ||||||||||||||||||||||||||||||||||||||||
6 7 | 6 9 | 7 0 | 7 1 | 7 2 | 7 4 | 7 5 | 7 6 | 7 7 | 7 8 | 7 9 | 8 0 | 8 1 | 8 2 | 8 3 | 8 4 | 8 5 | 8 6 | 8 7 | 8 8 | 8 9 | 9 0 | 9 1 | 9 2 | 9 3 | 9 4 | 9 5 | 9 6 | 9 7 | 9 8 | 9 9 | 1 0 0 | 1 0 1 | 1 0 2 | 1 0 3 | 1 0 4 | 1 0 5 | 1 0 6 | 1 0 9 | N | |
L. dentata | 1 | 3 | 1 | 1 | 2 | 6 | 5 | 5 | 5 | 5 | 6 | 5 | 7 | 3 | 2 | 1 | 1 | 61 | ||||||||||||||||||||||
L. gibarensis sp. nov. | 1 | 1 | 1 | 1 | 4 | |||||||||||||||||||||||||||||||||||
L. simile | 1 | 2 | 2 | 2 | 1 | 2 | 2 | 3 | 2 | 1 | 18 | |||||||||||||||||||||||||||||
L. subterranea | 1 | 1 | 5 | 4 | 5 | 7 | 3 | 3 | 7 | 2 | 2 | 1 | 41 | |||||||||||||||||||||||||||
L. lucayana | 1 | 1 | 4 | 6 | ||||||||||||||||||||||||||||||||||||
L. spelaeotes | 1 | 1 | 2 | 2 | 1 | 6 | 2 | 3 | 2 | 5 | 2 | 6 | 1 | 2 | 1 | 1 | 2 | 1 | 1 | 42 | ||||||||||||||||||||
Number of anal fin rays | ||||||||||||||||||||||||||||||||||||||||
5 3 | 5 4 | 5 5 | 5 6 | 5 7 | 5 8 | 6 0 | 6 1 | 6 2 | 6 3 | 6 4 | 6 5 | 6 6 | 6 7 | 6 8 | 6 9 | 7 0 | 7 1 | 7 2 | 7 3 | 7 4 | 7 5 | 7 6 | 7 7 | 7 8 | 7 9 | 8 0 | 8 1 | 8 2 | N | |||||||||||
L. dentata | 4 | 3 | 3 | 4 | 5 | 6 | 6 | 7 | 4 | 4 | 4 | 3 | 3 | 2 | 3 | 61 | ||||||||||||||||||||||||
L. gibarensis sp. nov. | 1 | 1 | 1 | 1 | 4 | |||||||||||||||||||||||||||||||||||
L. simile | 2 | 2 | 3 | 3 | 3 | 1 | 1 | 1 | 1 | 1 | 18 | |||||||||||||||||||||||||||||
L. subterranea | 1 | 2 | 6 | 7 | 8 | 4 | 6 | 3 | 3 | 1 | 41 | |||||||||||||||||||||||||||||
L. lucayana | 1 | 2 | 1 | 1 | 5 | |||||||||||||||||||||||||||||||||||
L. spelaeotes | 1 | 1 | 1 | 1 | 2 | 7 | 6 | 4 | 4 | 2 | 2 | 2 | 2 | 4 | 1 | 1 | 1 | 42 | ||||||||||||||||||||||
Number of pectoral fin rays | ||||||||||||||||||||||||||||||||||||||||
1 0 | 1 1 | 1 2 | 1 3 | 1 4 | 1 5 | 1 6 | 1 7 | 1 8 | 1 9 | 2 0 | N | |||||||||||||||||||||||||||||
L. dentata | 22 | 48 | 24 | 94 | ||||||||||||||||||||||||||||||||||||
L. gibarensis sp. nov. | 1 | 1 | 1 | 3 | ||||||||||||||||||||||||||||||||||||
L. simile | 5 | 8 | 4 | 3 | 1 | 21 | ||||||||||||||||||||||||||||||||||
L. subterranea | 3 | 7 | 25 | 10 | 45 | |||||||||||||||||||||||||||||||||||
L. lucayana | 5 | 1 | 6 | |||||||||||||||||||||||||||||||||||||
L. spelaeotes | 2 | 18 | 20 | 2 | 42 | |||||||||||||||||||||||||||||||||||
Number of posterior lateral line neuromasts | ||||||||||||||||||||||||||||||||||||||||
2 0 | 2 2 | 2 3 | 2 4 | 2 5 | 2 6 | 2 7 | 2 8 | 2 9 | 3 0 | 3 1 | 3 2 | 3 3 | 3 4 | 3 5 | 3 6 | 3 7 | 3 8 | 3 9 | 4 0 | 4 1 | 4 2 | 4 3 | 4 4 | 4 5 | 4 6 | 4 7 | N | |||||||||||||
L. dentata | 1 | 1 | 1 | 3 | 5 | 7 | 1 | 4 | 3 | 1 | 27 | |||||||||||||||||||||||||||||
L. gibarensis sp. nov. | 2 | 1 | 3 | |||||||||||||||||||||||||||||||||||||
L. simile | 2 | 2 | 2 | 6 | ||||||||||||||||||||||||||||||||||||
L. subterranea | 1 | 7 | 4 | 8 | 2 | 4 | 3 | 29 | ||||||||||||||||||||||||||||||||
L. lucayana | 1 | 1 | 2 | |||||||||||||||||||||||||||||||||||||
L. spelaeotes | 1 | 2 | 1 | 1 | 2 | 5 | 6 | 1 | 2 | 1 | 1 | 23 | ||||||||||||||||||||||||||||
Number of rakers on anterior gill arch | ||||||||||||||||||||||||||||||||||||||||
1 2 | 1 3 | 1 4 | 1 5 | 1 6 | 1 7 | 1 8 | 1 9 | 2 0 | 2 1 | 2 2 | 2 3 | N | ||||||||||||||||||||||||||||
L. dentata | 2 | 3 | 6 | 11 | 10 | 7 | 2 | 1 | 42 | |||||||||||||||||||||||||||||||
L. gibarensis sp. nov. | 1 | 1 | 1 | 3 | ||||||||||||||||||||||||||||||||||||
L. simile | 1 | 1 | 3 | 2 | 2 | 1 | 10 | |||||||||||||||||||||||||||||||||
L. subterranea | 3 | 9 | 10 | 9 | 2 | 1 | 36 | |||||||||||||||||||||||||||||||||
L. lucayana | 1 | 1 | 1 | 3 | ||||||||||||||||||||||||||||||||||||
L. spelaeotes | 3 | 3 | 6 | 3 | 9 | 5 | 8 | 1 | 1 | 39 |
The specific epithet refers to the village of Gibara, where the three caves inhabited by this species are located. We do not follow variety epithet used by
Among Cuban species,
Based on external appearance, Lucifuga gibarensis sp. nov. resembles the Cuban species L. dentata (from which it was designated as variety, see Díaz et al. 1987b) and L. simile. Nonetheless, it differs in several characters: e.g., number of caudal fin rays (10 vs. 8), diameter of the pigmented eyes (1.1–1.9 vs. 0.0–0.2% SL), lack of palatine teeth vs. present and scaled occiput vs. naked or weakly scaled occiput. It also differs in dorsal and anal fin rays mean number (fewer than L. dentata and more than L. simile) (Table
Lucifuga gibarensis sp. nov. also resembles L. subterranea in the lack of palatine teeth and the scaled occiput, but it differs in the body moderately elevate behind the head vs. little elevated (see maximum height in Table
Finally, Lucifuga gibarensis resembles both Bahamian species in the head profile, the number of caudal fin rays (10), the occiput scales (similar to L. spelaeotes and less scaled than L. lucayana) and in the presence of relatively large pigmented eyes (Table
It has been demonstrated that L. gibarensis is not phylogenetically close to L. dentata. The estimate of mtDNA genetic divergence between these two lineages is huge (P = 30.5%) and several diagnostic nucleotide changes at the intron 4 of calmoduline gene and intron 1 of the homeodomain EVX gene were described (
As a result of the present study, we describe a new species, Lucifuga gibarensis, which is supported by morphology and molecular phylogenetic analysis (
The current key is based on a small number of samples. Measures that overlapping in range were only used when it helps distinguishing between two species.
1 | Diameter of pigmented eyes 0.0–0.3% SL, caudal fin rays 8, number of vertebrae < 50 | 2 |
– | Diameter of pigmented eyes > 0.7% SL, caudal fin rays 10, number of vertebrae ≥ 50 | 4 |
2 | Palatine teeth present, pectoral fin rays 13–17 | 3 |
– | Palatine teeth absent, pectoral fin rays 10–13 | L. subterranea |
3 | Dorsal fin rays < 80 | L. simile |
– | Dorsal fin rays ≥ 80 | L. dentata |
4 | Palatine teeth present, lateral occipital area naked | L. spelaeotes |
– | Palatine teeth absent, lateral occipital area scaled | 5 |
5 | Pigmented eye diameter 0.9–1.0% SL, number of posterior lateral line neuromasts 34–35 | L. lucayana |
– | Pigmented eye diameter 1.1–1.9% SL, number of posterior lateral line neuromasts 30–33 | L. gibarensis sp. nov. |
(38 specimens: 18 females, 20 males).
Holotype
:
(126 specimens: 63 females, 63 males).
MCZ 12415, 32329, 85–90 mm SL, females, Cave of Cajio, Cuba.
Lucifuga dentata has been described as having the caudal fin free from dorsal and anal fins and the occiput naked (Poey, 1858; Cohen and Robins, 1970; Vergara, 1980; Nalbant, 1981;
As mention previously for L. subterranea, the sampling at localities near to those mentioned in Poey’s original description of the species, applied exactly for L. dentata. We also use several exemplars from Juanelo Piedra and Luis Piedra caves which are near to El Cajio cave (ca. 2 km) the type-locality referred by
(22 specimens: 8 females, 14 males).
We examined specimens of L. simile from the two known localities: the type-locality Grieta Punta de Guana cave (Nalbant, 1981) and La Pluma Cave (
Lucifuga lucayana Møller, Schwarzhans, Iliffe & Nielsen, 2006
see
Lucifuga spelaeotes Cohen & Robins, 1970
see
We want to thank Pedro Chevalier, Eduardo Abreu, Majorie Condis, Katrine Worsaae, José Alberto Pino Cuenca and Yosvani Medina, for field assistance, and José Luis Ponce de León, Niurka Hernández, Carlos Arredondo, Alfredo García and Arturo Rojas that supplied valuable specimens. Thanks to Isabelle Germon for laboratory assistance. Thanks to technician Mabel Suares for radiographs assistance. We thank Mark Sabaj Perez (