Research Article |
Corresponding author: Wilson J.E.M. Costa ( wcosta@acd.ufrj.br ) Academic editor: Peter Bartsch
© 2018 Wilson J.E.M. Costa, Pedro F. Amorim, José Leonardo O. Mattos.
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:
Costa WJEN, Amorim PF, Mattos JLO (2018) Diversity and conservation of seasonal killifishes of the Hypsolebias fulminantis complex from a Caatinga semiarid upland plateau, São Francisco River basin, northeastern Brazil (Cyprinodontiformes, Aplocheilidae). Zoosystematics and Evolution 94(2): 495-504. https://doi.org/10.3897/zse.94.29718
|
A high concentration of endemic species of seasonal killifishes has been recorded for a small area encompassing the highland plateaus associated with the upper section of the Carnaúba de Dentro River drainage and adjacent drainages of the middle section of the São Francisco River basin, northeastern Brazil. The present study is primarily directed to the taxonomy of the H. fulminantis species complex in this region, and describes habitat decline and extirpation of natural killifish populations recorded in field studies between 1993 and 2017. Both morphological characters and molecular species delimitation methods using single-locus models (GMYC and bPTP) support recognition of two closely related endemic species, H. fulminantis and H. splendissimus Costa, sp. n. The new species is distinguished from other congeners of the H. fulminantis complex by having a red pectoral fin in males, well-developed filamentous rays on the tips of the dorsal and anal fins in adult males, and the second proximal radial of the dorsal fin between the neural spines of the 8th and 9th vertebrae in males. Most recent field inventories indicated possible local extinction of populations of H. fulminantis and H. splendissimus in the studied area, but additional field studies should be made in other parts of the upper Carnaíba de Dentro River basin to evaluate the current conservation status of these species.
Biodiversity, species delimitation, systematics, taxonomy.
In the last three decades, field studies of cynolebiine killifishes in temporary pools of the Caatinga, a semi-arid phytogeographical province of northeastern Brazil, have continuously revealed spectacular species diversity (e.g.,
In spite of the great morphological diversity exhibited by different endemic lineages of seasonal killifishes, several cryptic species have been recently recognised in the Caatinga using molecular species delimitation analyses (e.g.,
An uncommonly high concentration of endemic species of seasonal killifishes has been recorded for a small area encompassing the highland plateaus associated with the upper sections of the Carnaúba de Dentro and the Verde Pequeno river drainages, in the middle section of the São Francisco River basin (
Hypsolebias fulminantis since its description in 1993, has become a popular aquarium fish due to the colouration exhibited by males. It was often collected by aquarists and amateur ichthyologists and consequently appears in numerous aquarium fish websites. However, field studies in the region have shown a sharp decline in natural populations (person. observation by WJEMC). In the past, H. fulminantis was frequently sampled around the town of Guanambi, in pools situated in the northeastern and southern parts of the town’s periphery, at altitudes between about 525 and 555 m asl. However, during field studies in January 2010, after a severe environmental change in the region caused by the expansion of the Guanambi urban area, it was noted that all temporary pools sampled in previous years, inhabited by H. fulminantis, had been extirpated. On the other hand, new populations of seasonal killifishes were found just west from Guanambi, including a population with specimens similar to H. fulminantis but exhibiting some distinct morphological traits, suggesting that they may be a new species, which is here supported by molecular species delimitation methods. The objectives of this paper are to describe the new species and to provide a report on distribution and conservation of species of the H. fulminantis complex in the upper Carnaíba de Dentro River basin based on field studies made between February 1993 and March 2017.
Methods for fish capture, euthanasia, fixation, and preservation in collections follow methods described by
Descriptions of colouration in living fish were based on photographs of both sides of individuals. Photographs were taken in small aquaria about 24 hours or less after collections. Additional direct observations were made with fish in small transparent plastic bottles just after collection. Measurements and counts follow
List of specimens used in the molecular analysis, with their respective catalog numbers, coordinates of the collecting site, and GenBank accession numbers for cytb sequences. Asterisk indicates sequences not published previously.
Species | Catalog number | Coordinates | Cytb |
---|---|---|---|
Hypsolebias carlettoi | UFRJ 6780.1 | 14°13'42"S, 42°55'12"W | MH909076* |
Hypsolebias carlettoi | UFRJ 6780.2 | 14°13'42"S, 42°55'12"W | MH048856 |
Hypsolebias carlettoi | UFRJ 6780.3 | 14°13'42"S, 42°55'12"W | MH909078* |
Hypsolebias carlettoi | UFRJ 6780.4 | 14°13'42"S, 42°55'12"W | MH909079* |
Hypsolebias fulminantis | UFRJ 6726.1 | 14°12'21"S, 42°45'42"W | MH048854 |
Hypsolebias fulminantis | UFRJ 6726.2 | 14°12'21"S, 42°45'42"W | MH909075* |
Hypsolebias hellneri | UFRJ 6700.4 | 15°04'49"S, 44°04'40"W | MH909072* |
Hypsolebias splendissimus | UFRJ 6778.1 | 14°12'54"S, 42°50'22"W | MH909080* |
Hypsolebias splendissimus | UFRJ 6778.2 | 14°12'54"S, 42°50'22"W | MH909081* |
Hypsolebias splendissimus | UFRJ 6778.3 | 14°12'54"S, 42°50'22"W | MH909082* |
Hypsolebias splendissimus | UFRJ 6778.4 | 14°12'54"S, 42°50'22"W | MH909083* |
Hypsolebias picturatus | UFRJ 6708.1 | 11°28'03"S, 43°17'10"W | MH048868 |
Total genomic DNA was extracted from muscle tissue of the right side of the caudal peduncle using the DNeasy Blood & Tissue Kit (Qiagen) according to the manufacturer’s instructions. A fragment of the mitochondrial DNA gene cytochrome b (cytb) was amplified using the primers L14724 and H15149 (
Analyses were conducted with a short cytb fragment (416 bp) that has been efficiently used for delimitating cryptic species of different aplocheiloid killifish groups (
Descriptions of field data relative to habitat conservation were made during collecting trips between 1994 and 2017 (February 1994, February 1999, May 1999, January 2002, January 2005, May 2009, January 2010, January 2017, and April 2017).
The phylogenetic analysis generated a tree with most branches supported by highest posterior probability values (Fig.
Bayesian phylogeny used to delimit species endemic to the upper Carnaíba de Dentro River drainage, inferred by using sequences of the mitochondrial gene cytochrome b, 416 bp. Posterior probability values below 95% are not depicted; asterisk above nodes represents maximum value of posterior probability (100 %); numbers before species names are catalogue numbers for voucher specimens.
UFRJ 6909, male, 42.7 mm SL; Brazil: State of Bahia state: Municipality of Guanambi: temporary pool close to road BR-030, about 1.5 km W from the confluence between the Poço do Magro River and the Carnaíba de Dentro River, São Francisco River basin, and about 3 km W of the town of Guanambi, 14°12'54” S 42°50'22” W, altitude about 505 m asl; W. J. E. M. Costa et al., 30 January 2010.
UFRJ 6779, 1 male, 43.3 mm SL, 2 females, 28.5–30.2 mm SL; UFRJ 6910, 1 male, 42.7 mm SL, 3 females, 26.7–30.5 mm SL (C&S); UFRJ 6778, 2 males, 33.7–36.2 mm SL, 6 females, 28.4 – 29.5 mm SL (DNA); collected with holotype.
Hypsolebias splendissimus differs from H. fulminantis and H. shibattai by having: pectoral fin red in males (vs. hyaline in H. fulminantis and H. shibattai), well-developed filamentous rays on the tips of the dorsal and anal fins in adult males (vs. filamentous rays absent or rudimentary, poorly visible), and the second proximal radial of the dorsal fin between the neural spines of the 8th and 9th vertebrae in males (vs. between the neural spines of the 6th and 7th vertebrae). Also distinguished from H. shibattai by having the dorsal-fin origin posterior to the anal-fin origin in males (vs. anterior), distinctive red bars restricted to the anterior portion of the flank males (vs. extending over the whole flank), and absence of contact organs on the pectoral fin in males (vs. present).
Morphometric data appear in Table
Dorsal and anal fins pointed in males, with two or three filaments on tip, rounded, without filaments, in females. Caudal fin rounded. Pectoral fin sub-lanceolate, posterior tip reaching vertical between base of 5th and 7th anal-fin rays in males, reaching between anus and urogenital papilla in females. Pelvic fin small, tip reaching base of 3rd anal-fin ray in males, reaching between urogenital papilla and anal-fin origin in females; pelvic-fin bases medially united. Dorsal-fin origin on vertical between base of 2nd and 4th anal-fin rays in males, between base of 4th and 6th anal-fin rays in females. Dorsal-fin rays 19–22 in males, 15–16 in females; anal-fin rays 21 in males, 18–19 in females; caudal-fin rays 23–24; pectoral-fin rays 12–13; pelvic-fin rays 6. No contact organs on fins. Second proximal radial of dorsal fin between neural spines of 8th and 9th vertebrae in males, between neural spines of 11th and 12th vertebrae in females; first proximal radial of anal fin between pleural ribs of 8th and 9th vertebrae in males, between pleural ribs of 9th and 10th vertebrae in females; total vertebrae 26–27.
Scales small, cycloid. Body and head entirely scaled, except anterior ventral surface of head. Body squamation extending over anterior 20 % of caudal-fin base; scales slightly extending on middle part of anal-fin base in males. Frontal scales E-patterned. Longitudinal series of scales 25–26; transverse series of scales 11; scale rows around caudal peduncle 12. One prominent contact organ on each flank scale in males. Cephalic neuromasts: supraorbital 12–16; parietal 2; anterior rostral 1, posterior rostral 1; infraorbital 3 + 22–24; preorbital 3–4; otic 2, post-otic 2; supratemporal 1; median opercular 1, ventral opercular 1–2; pre-opercular 15–16; mandibular 10–13; lateral mandibular 4, paramandibular 1.
Males. Flank intense red to pink on middle portion and metallic yellow ochre on anteroventral part; small, vertically elongated bright blue spot on centre of each scale; central portion of flank often with distinctive red bars, alternating with faint green bars, sometimes inconspicuous. Dorsum pale yellowish brown, venter yellowish white. Side of head metallic light blue, with red scale margins on dorsal portion and intense metallic yellow ochre on opercular, post-orbital and infra-orbital regions; snout and jaws light grey. Iris light yellow to pale orange, with dark brown bar through orbit centre. Unpaired fins red, with alternating short and long metallic blue lines to greenish golden lines, depending on angle of light incidence, parallel to fin rays; dorsal and anal fin filaments dark grey to black. Pelvic fin red with light blue rays. Pectoral fin red.
Females. Flank light brownish grey, to yellowish grey on dorsal portion and pale golden on anteroventral portion; two or three oval black spots on antero-central portion of flank; smaller specimens, about 28 mm SL or less, with dark grey bars, often interrupted; larger specimens above 28 mm SL, with dark grey spots on whole flank, often arranged in vertical rows, becoming dark grey to black around antero-central spots. Dorsum yellowish grey, venter white. Side of head yellowish grey, pale greenish golden on opercular and post-orbital regions; jaws light grey. Iris light yellow to pale orange, with dark brown bar through orbit centre. Fins yellowish hyaline.
Trunk and head pale brown, with faint grey bars on anterior portion of flank in males, and grey spots on flank in females. Fins grey in males, hyaline in females. No vestige of red pigmentation and blue iridescent marks.
Hypsolebias splendissimus is known from a single collection at the type locality, a temporary pool in a flat plains area about 1.5 km W from the confluence between the Poço do Magro and Carnaíba de Dentro rivers, middle São Francisco River basin, Bahia, Brazil (14°12'54” S 42°50'22” W, altitude about 505 m asl; Fig.
From the Latin splendissimus (very splendid), an allusion to the bright colours in males of the new species, which is among the most colourful South American aplocheiloid killifishes.
Holotype | Paratypes | ||
---|---|---|---|
Male | Males (2) | Females (5) | |
Standard length (mm) | 42.7 | 42.9–43.3 | 27.0–30.5 |
Percent of standard length | |||
Body depth | 36.0 | 35.0–36.8 | 35.8–38.8 |
Caudal peduncle depth | 16.1 | 15.5–16.0 | 14.9–15.6 |
Pre-dorsal length | 45.2 | 47.3–48.0 | 58.0–62.3 |
Pre-pelvic length | 42.2 | 42.7–43.6 | 49.9–52.0 |
Length of dorsal-fin base | 42.9 | 39.6–40.1 | 24.3–28.8 |
Length of anal-fin base | 42.1 | 40.0–43.8 | 23.2–26.7 |
Caudal-fin length | 40.2 | 40.0–41.3 | 34.7–37.8 |
Pectoral-fin length | 28.2 | 28.8–29.1 | 24.1–25.7 |
Pelvic-fin length | 10.7 | 10.4–11.6 | 10.6–12.2 |
Head length | 27.1 | 26.5–27.7 | 28.3–31.1 |
Percent of head length | |||
Head depth | 109.9 | 111.9–114.3 | 102.5–97.6 |
Head width | 63.9 | 67.1–68.7 | 65.2–74.4 |
Snout length | 14.7 | 12.9–15.5 | 13.8–14.8 |
Lower jaw length | 19.9 | 17.7–18.0 | 14.9–16.5 |
Eye diameter | 28.4 | 29.3–32.0 | 31.3–37.1 |
Cynolebias fulminantis Costa & Brasil, 1993: 194 (type locality: swamp near Guanambi [road BR-122], Estado da Bahia, northeastern Brazil [14°15'16"S, 42°46'56"W, altitude about 555 m]; MZUSP 43674).
Hypsolebias fulminantis is a member of the H. fulminantis complex, differing from H. splendissimus by: the presence of hyaline pectoral fins in males (vs. red), presence of rudimentary or absence of filamentous rays on the tips of the dorsal and anal fins in adult males (vs. well-developed filamentous rays present), and the second proximal radial of the dorsal fin situated between the neural spines of the 6th and 7th vertebrae in males (vs. between the neural spines of the 8th and 9th vertebrae); and from H. shibattai by having the dorsal-fin origin posterior to the anal-fin origin in males (vs. anterior); distinctive red bars restricted to the anterior portion of the flank males (vs. extending over the whole flank); and absence of contact organs on the pectoral fin in males (vs. present).
Hypsolebias fulminantis has been recorded from several localities in the upper Carnaíba de Dentro River basin, close to the town of Guanambi, in altitudes between 525–555 m asl (Fig.
For a full description, see
Brazil: State of Bahia: Municipality of Guanambi: São Francisco River basin, upper Carnaíba de Dentro River drainage: MZUSP 43674, holotype, male, 38.9 mm SL; MZUSP 43675, 2 paratypes; UFRJ 685, 2 paratypes; UFRJ 686, 3 paratypes; Guanambi, road BR-122, 14°15'16"S, 42°46'56"W, altitude about 555 m; G. C. Brasil, 1 Jan. 1992. – UFRJ 6068, 6; UFRJ 6069, 2; UFRJ 6726, 3; Guanambi, road BR-030, 14°12'21"S, 42°45'42"W, altitude about 545 m; W. J. E. M. Costa et al., 13 Jan. 2005. – UFRJ 4802, 1; temporary pool about 4.5 km S from Guanambi, Rio road BR-122,14°16'49"S, 42°47'01"W, altitude about 525 m; W. J. E. M. Costa et al., 11 Feb. 1999. – UFRJ 4847, 2; same locality as UFRJ 4802; W. J. E. M. Costa et al., 4 May 1999. – UFRJ 3809, 6; UFRJ 5864, 4 (C&S); temporary pool 4.5 km S from Guanambi; A. L. F. Cyrino et al., 27 Jan. 1996.
Hypsolebias splendissimus is presently known from a single locality just 8 km west from the geographical area inhabited by H. fulminantis (Fig.
Field studies in the Caatinga have shown that H. carlettoi is also endemic to the upper Carnaíba de Dentro River drainage, but it was never found in sympatry with H. fulminantis or H. splendissimus. Its distribution range is situated in a different subdrainage of the Upper Carnaíba de Dentro River drainage, the Mutula River subdrainage, and is separated by a distance of about 7 km from the type locality of H. splendissimus and about 15 km from the recorded geographical range of H. fulminantis (Fig.
The present study reports an accentuated decline in seasonal killifish habitats in the upper Carnaíba de Dentro River drainage around the town of Guanambi, possibly causing local extinction of H. fulminantis and H. splendissimus. However, most parts of the Carnaíba de Dentro River drainage are still not easily accessible and field studies to detect the occurrence of seasonal killifishes have never been conducted. So at this time it is not possible to evaluate the conservation status of H. fulminantis and H. splendissimus. On the other hand, satellite images indicate that these unsampled areas are extensively modified for agriculture, an environmental impact that usually has negatively affected seasonal killifish habitats (
Thanks are due to Claudia Bove and Bruno Costa for accompanying the first author in most collecting trips, and Anaïs Barbosa and Axel Katz for help in collecting trips. This study was supported by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, Ministério de Ciência e Tecnologia) and FAPERJ (Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro). We are grateful to Donald Taphorn, Felipe Ottoni and Peter Bartsch for the critical review, corrections and suggestions.