Research Article
Print
Research Article
A new species of redfin (Teleostei, Cyprinidae, Pseudobarbus) from the Verlorenvlei River system, South Africa
expand article infoAlbert Chakona, Ernst R Swartz, Paul H. Skelton
† South African Institute for Aquatic Biodiversity, Grahamstown, South Africa
Open Access

Abstract

Pseudobarbus verloreni, a new species, is described from material collected in the Verlorenvlei River system on the west coast of South Africa. It differs from its congeners (except P. skeltoni, P. burchelli, and P. burgi) by the presence of two pairs of oral barbels. Pseudobarbus verloreni sp. n. can be distinguished from the three currently described double barbeled Pseudobarbus species by the following combination of characters: pigment pattern, generally deeper body relative to standard length, a longer intestine associated with the deeper body form, shorter snout relative to head length, and much shorter anterior barbels relative to head length. The new species is distinguished from P. burgi in the neighbouring Berg River system by its longer head and longer pre-dorsal length. It seems as if Pseudobarbus verloreni sp. n. has been extirpated from the Langvlei River system and face several threats to its survival in the Verlorenvlei River system.

Keywords

Freshwater fish, endemic hotspot, threatened, double barbeled redfins

Introduction

Species of the cyprinid genus Pseudobarbus (commonly referred to as “redfins”) are distinctly pigmented small-to-medium sized riverine fishes endemic to southern Africa (Skelton 1988). Pseudobarbus was described by Smith (1841) as a subgenus of Barbus. Nearly 150 years later, the subgenus was raised to a full generic status (Skelton 1988). The monophyly of Pseudobarbus is supported by molecular data and morphological characters (Swartz et al. 2009). The most prominent diagnostic characters for members of this tetraploid genus (Naran et al. 2006) are the presence of bright red fins, a soft or flexible primary dorsal spine, and males develop prominent head and body tubercles during the breeding season. During his taxonomic revision of Pseudobarbus, Skelton (1988) recognised seven species, namely P. afer (Peters, 1864), P. asper (Boulenger, 1911), P. burchelli (Smith, 1841), P. phlegethon (Barnard, 1938), P. quathlambae (Barnard, 1938), and P. tenuis (Barnard, 1938). Two decades later, following genetic studies and a resurgence of field surveys in the Cape Floristic Region, a new redfin species P. skeltoni was described from the Breede River system (Chakona and Swartz 2013), bringing the number of nominal species to eight. Based on insights from molecular studies, several other taxa of this genus remain to be described (Bloomer and Impson 2000, Swartz et al. 2007, 2009, 2014, Chakona et al. 2013). Herein, we describe a ninth species of Pseudobarbus from the Verlorenvlei River system, which was identified as a unique genetic lineage of P. burgi following a phylogeographic study by Bloomer and Impson (2000).

The Verlorenvlei and Berg lineages of Pseudobarbus burgi, three lineages of P. burchelli (see Chakona et al. 2013 and Swartz et al. 2014), and P. skeltoni have two pairs of oral barbels and form a monophyletic group within Pseudobarbus (Swartz et al. 2009). The taxonomic history of the double barbeled redfins has been complex and confusing. The first double barbeled redfin was described by Smith (1841) as Barbus (Pseudobarbus) burchelli. This was followed by descriptions of Gnathendalia vulnerata Castelnau, 1861 and Barbus multimaculatus Steindachner, 1870, both from the Breede River system. Valenciennes (Cuvier and Valenciennes 1842) described Barbus gobionides but this species was later synonymised with Gnathendalia vulnerata by Günther (1868). Barnard (1943) subsequently declared Barbus gobionides Valenciennes, 1842 a nomen dubium, while Boulenger (1905) placed Barbus multimaculatus Steindachner, 1870 in synonymy with Gnathendalia vulnerata. This decision was subsequently accepted by Barnard (1943), Jubb (1965), and Skelton (1988). Boulenger (1911) described Barbus (Pseudobarbus) burgi from the Berg River system, but Barnard (1943) placed this species in synonymy with Barbus (Pseudobarbus) burchelli, and recognised Barbus vulneratus for the Breede River system. Jubb (1965) later reversed this decision and considered Gnathendalia vulnerata to be a synonym of Barbus (Pseudobarbus) burchelli. Skelton (1988) accepted Jubb’s (1965) nomenclatural changes to maintain taxonomic stability in his taxonomic revision of redfin minnows.

Thus, Pseudobarbus burchelli, P. burgi, and the recently described P. skeltoni are the only double barbeled Pseudobarbus species that are presently recognised. The known distribution of P. burchelli sensu lato spans four river systems (Heuningnes, Breede, Duiwenhoks, and Goukou) on the south coast of South Africa (Skelton 1988), while P. skeltoni is restricted to the Breede River system (Chakona and Swartz 2013). The historical distribution of P. burgi sensu lato included the Langvlei, Verlorenvlei, Berg, and Eerste river systems on the west coast of South Africa (Skelton 1988). The Eerste population is thought to be extinct due to a combination of impacts including introduction of non-native species (Gaigher et al. 1980). Recent surveys suggest that the Langvlei population has also been lost. Skelton (1988) noted that specimens of P. burgi from the Verlorenvlei River system had a longer intestine and longer predorsal length compared to specimens from the Berg River system. Bloomer and Impson (2000) discovered high levels of genetic differentiation (5.3–7.0% for the mitochondrial control region) between populations of P. burgi from the Verlorenvlei and Berg river systems, indicating a long history of isolation. The differentiation between these two lineages was confirmed by Swartz et al. (2009) and Chakona and Swartz (2013). The purpose of the present study is to describe the Verlorenvlei Pseudobarbus population as a new species, Pseudobarbus verloreni sp. n.

Materials and methods

Institutional abbreviations follow Sabaj (2013) and are listed at http://www.asih.org/node/204. Description of the new Pseudobarbus species is based on 47 specimens (holotype and paratypes) that were collected from the Verlorenvlei River system during surveys conducted in January 1999 and March 2012. The type material has been deposited at the South African Institute for Aquatic Biodiversity (SAIAB), MRAC, USNM and BMNH.

Molecular data

Two Pseudobarbus individuals from the Verlorenvlei River system were sequenced to assign a hologenetype and a paragenetype following Chakrabarty (2010) for the mitochondrial cytochrome b gene. The sequences were added to the genetic analysis done by Chakona and Swartz (2013) to show the phylogenetic position of the hologenetype and the paragenetype in relation to all known lineages and species of Pseudobarbus. Methods of DNA extraction, amplification, sequencing and analysis follow Swartz et al. (2009) and Chakona and Swartz (2013). The hologenetype and paragenetype sequences were deposited in GenBank for future reference (GenBank numbers are given below) following the definitions of Chakrabarty (2010).

Morphological data

Meristic and morphological characters were examined following Hubbs and Lagler (1958), Skelton (1988), and Chakona and Swartz (2013). The characters considered for each specimen in the present study (22 morphometric measurements) and (12 meristic counts) are presented in Table 1. In addition, entire branchial baskets were dissected from three specimens to examine and count pharyngeal teeth.

Morphological characters of Pseudobarbus species used in the present study.

Character Description Acronym
Morphometric measurements
Standard length Tip of the snout to the point of flecture of the caudal fin SL
Pre-dorsal length Tip of the snout to the origin of the dorsal fin PDL
Head length Tip of the snout to the posterior bony margin of the operculum HL
Snout length Tip of the snout to the anterior bony edge of the orbit S
Orbit diameter The greatest bony diameter of the orbit OD
Inter-orbit width Shortest distance between bony edges of the orbits IO
Post-orbit length Distance between the posterior bony edge of orbit to the posterior bony edge of operculum PO
Head depth Maximum depth measured from the nape HD
Body depth Maximum depth measured from the anterior base of the dorsal fin BD
Anterior barbel length From base to tip of anterior barbel AB
Posterior barbel length From base to tip of posterior barbel PB
Dorsal fin base Distance between origin of dorsal fin and base of last dorsal fin ray DB
Dorsal fin height From anterior base to tip of dorsal fin DH
Pectoral fin length From anterior base to tip of pectoral fin PtL
Pelvic fin length From anterior base to tip of pelvic fin PvL
Anal fin base Distance between origin of anal fin and base of last anal fin AfB
Anal fin height From anterior base to tip of anal fin AfH
Caudal peduncle length Distance from posterior base of anal fin the point of flecture of the caudal fin CPL
Caudal peduncle depth The least depth of the caudal peduncle CPD
Pectoral to pelvic fin length Distance between the posterior margins of the fin bases PP
Pelvic to anal fin length Distance between posterior base of the pelvic fin to anterior base of the anal fin PA
Body width The greatest width just anterior to the origin of the dorsal fin BW
Meristic counts
Lateral line scales Number of scale rows along the lateral line LL
Lateral line to dorsal fin origin Number of scale rows between lateral line scale row (does not include lateral line scale) and anterior base of the dorsal fin LD
Lateral line to pelvic fin origin Number of scale rows between lateral line scale row (does not include lateral line scale) and anterior base of pelvic fin LP
Lateral line to anal fin origin Number of scale rows between lateral line scale row (does not include lateral line scale) and anterior base of the anal fin LA
Circumpeduncular scales Number of scale rows around the caudal peduncle at narrowest portion of caudal peduncle CP
Predorsal scales Number of scale rows between the supraoccipital and the anterior base (origin) of the dorsal fin PDS
Unbranched dorsal fin rays Number of unbranched primary dorsal rays UdR
Branched dorsal fin rays Number of branched dorsal rays; two last branched rays counted as one BdR
Anal fin rays Includes both simple and branched rays; two last rays counted as one
Pectoral fin rays Includes both simple and branched rays
Pelvic fin rays Includes both simple and branched rays
Total vertebrae Total number of vertebrae in vertebral column (including four Weberian vertebrae and a single ural centrum) TV
Pre-dorsal vertebrae Total number of vertebrae in advance of the leading dorsal fin pterigiophore (including the four Weberian vertebrae) PdV
Pre-caudal vertebrae Total number of vertebrae in advance of the vertebrae with haemal arch opposite the leading anal pterygiophore plus the four Weberian vertebrae PcV
Pre-anal vertebrae Total number of vertebrae in advance of the leading anal pterygiophore (including the four Weberian vertebrae) PaV
Caudal vertebrae Total number of vertebrae posterior to (and including) the vertebra with haemal arch opposite the leading anal pterygiophore plus a single ural centrum CV

We compared morphological and meristic differences among all double barbeled redfins using raw data from Skelton (1980, 1988) and Chakona and Swartz (2013). Specimens were assigned to four groups based on geographic origin and previous genetic results (Bloomer and Impson 2000; Swartz et al. 2009, 2014; Chakona and Swartz 2013; Chakona et al. 2013): P. skeltoni (n=25), P. burchelli (n=128), P. burgi (specimens from the Berg River system only; n=66) and Verlorenvlei Pseudobarbus (specimens from the Verlorenvlei River system only; n=47). A total of 47 specimens of Verlorenvlei Pseudobarbus were radiographed to count skeletal features.

Statistical analyses were performed with the programs InfoStat (Di Rienzo et al. 2012), PAST and STATISTICA 12. Prior to analyses, morphometric data were normalised using procedures described by Lleonart et al. (2000). Analyses of meristic characters were performed using the raw data.

Principal component analysis (PCA) was performed using the correlation matrix to explore the separation of the specimens based on the normalised morphometric data (Lleonart et al. 2000) and raw meristic characters. Invariant characters (such as the number of pelvic fin rays) were excluded from analysis. All scores (including PC1) were considered, because the normalisation approach allows for size free comparisons (Lleonart et al. 2000).

Discriminant Function Analysis (DFA) was performed to visualise the degree of morphological separation among the species and to identify the most important characters that contribute to the differentiation. DFA also provides jacknifed measurements of re-classification success of individuals to their original group, as well as identifying the group to which individuals were assigned if misclassified. Separate DFAs were performed for the morphometric and meristic characters, as well as for these two data sets combined.

Results

Figure 1 is a re-analysis of the phylogeny done by Chakona and Swartz (2013) to include the genetypes of Pseudobarbus verloreni sp. n. sequenced in the present study. It shows the phylogenetic relationships among double barbeled redfins based on the mitochondrial cytochrome b data, and shows the position of the new species that is distinct from the three described double barbeled redfin species, including the three previously identified lineages of P. burchelli (Swartz et al. 2009, 2014). The model corrected genetic distances show deep divergences (6.6–12.3%) between the new species and the other members of the double barbeled redfin group.

Figure 1.

Bayesian phylogenetic tree showing genetic distances between Pseudobarbus verloreni sp. n. compared to all other Pseudobarbus species/lineages. Bayesian posterior probabilities are shown on the branches.

Principal components analysis (PCA) of normalised morphometric and raw meristic characters shows Pseudobarbus specimens from the Verlorenvlei River system, herein described as the new species P. verloreni sp. n., form a cluster that is clearly separated from P. skeltoni and marginally overlaps with P. burchelli and P. burgi (Figure 2). The most important factor loadings are presented in Table 2. PCI was mainly defined by differences in head length, head depth, predorsal length, number of lateral line scales, number of scale rows between lateral line and dorsal fin, number of scale rows around the caudal peduncle and the number of predorsal scale rows (Table 2). PCII primarily contrasted differences in body depth, length of anterior barbel, and snout length. PCIII was mainly defined by caudal peduncle depth and body width. Specimens of P. verloreni sp. n. were associated positively with PCII, describing individuals characterised by deeper bodies relative to standard length. Specimens of the new species are separated from those of P. burgi, which were associated positively with PCI, describing individuals characterised by deeper heads relative to head length. Note also that the syntypes of P. burgi are clearly not conspecific with specimens of P. verloreni (Figure 2).

Figure 2.

Scatter plot of PC1 against PC2 for a PCA carried out on 15 normalised morphometric and seven raw meristic characters for all examined specimens (n=266) of double barbeled redfins from the Cape Floristic Region of South Africa. The figure shows clear separation of Pseudobarbus verloreni sp. n. from to all the other Pseudobarbus species/lineages.

Factor loadings for the first three principal component (PC) axes of a PCA carried out on morphometric and meristic characters of double barbeled Pseudobarbus specimens (n=266) from the Cape Floristic Region of South Africa.

Character PCI PCII PCIII
Head length -0.769 0.408 -0.077
Head depth 0.669 0.194 -0.276
Inter orbit 0.514 0.297 -0.421
Snout length 0.205 -0.727 0.040
Post orbit 0.325 -0.387 -0.067
Predorsal length -0.721 0.418 0.218
Dorsal fin base 0.507 -0.115 0.296
Body depth 0.148 0.796 0.269
Body width -0.463 0.153 0.620
Caudal peduncle length 0.478 -0.431 0.107
Caudal peduncle depth -0.335 0.178 0.752
Anterior barbel -0.405 -0.729 0.418
Posterior barbel -0.250 -0.477 0.520
Unbranched dorsal fin rays -0.215 -0.477 0.111
Lateral line scales -0.650 -0.340 -0.153
Scale rows between lateral line and dorsal fin -0.853 0.024 -0.100
Scale rows between lateral line and pelvic fin -0.575 0.248 -0.191
Scale rows between lateral line and anal fin -0.180 0.165 0.114
Scale rows around caudal peduncle -0.687 -0.103 -0.194
Predorsal scale rows -0.758 -0.352 0.095

The Discriminant Function Analysis (DFA) performed using combined morphometric and meristic characters correctly classified all individuals of the new species (Table 3). Similar to PCA results, the discriminant scores showed that the new species was clearly separated from the three previously described species of Pseudobarbus with two pairs of oral barbels (results not shown).

Classification results of discriminant function analysis using (a) combined morphometric and meristic characters, (b) morphometric characters and (c) meristic characters of double barbeled Pseudobarbus species from the Cape Floristic Region of South Africa.

Species Predicted count Total Error (%)
1 2 3 4
Combined data 1. P. burchelli 128 0 0 0 128 0.00
2. P. burgi 0 66 0 0 66 0.00
3. P. skeltoni 0 0 24 1 25 4.00
4. P. verloreni sp. n. 0 0 0 47 47 0.00
Morphometrics 1. P. burchelli 124 1 3 0 128 3.13
2. P. burgi 0 66 0 0 66 0.00
3. P. skeltoni 1 0 22 2 25 12.00
4. P. verloreni sp. n. 0 0 0 47 47 0.00
Meristics 1. P. burchelli 99 9 5 15 128 22.66
2. P. burgi 0 65 0 1 66 1.52
3. P. skeltoni 0 0 25 0 25 0.00
4. P. verloreni sp. n. 1 2 0 44 47 12.41

The DFA using morphometric measurements revealed morphological shape differences between the new species and the other previously described species of Pseudobarbus with two pairs of oral barbels. This analysis correctly classified all individuals of the new species, P. verloreni sp. n., as well as P. burgi sensu stricto while three individuals of P. skeltoni and four individuals of P. burchelli were misclassified (Table 3).

In contrast, the DFA using meristic characters showed poor classification of individuals of the four species, with three individuals of the new species, 29 individuals of P. burchelli and one individual of P. burgi being misclassified (Table 3).

Based on the deep genetic and significant morphological divergence between individuals from the Verlorenvlei River system and other members of the double barbeled redfin group, the Verlorenvlei population represents a new species.

Pseudobarbus verloreni sp. n.

Figure 3, Table 4

Proposed common names

Verlorenvlei redfin (English), Verlorenvlei rooivlerkie (Afrikaans).

Holotype

South Africa: Western Cape Province: SAIAB186092, mature male, 70.8 mm standard length (SL), collected from the Verlorenvlei River, 20 m upstream from railway at the Het Kruis bridge on R365 (32.60179000 S, 18.75039000 E) on 13 March 2012 by E. Swartz and W. Bronaugh, using a seine net. Hologenetype: GenBank number KM366106.

Paratypes

(n=46). South Africa: Western Cape Province: SAIAB192542 (n=3, 53.3–70.8 mm SL), same data as for holotype; SAIAB59808 (n=10, 40.1–46.9 mm SL), collected from the Verlorenvlei River (32.74560165 S, 18.81780052 E) on 22 January 1999 by R. Bills and D. Naran using a seine net and D-net; BMNH2014.2.26.1-2 (n=2, 52.8–58.2 mm SL), USNM427302 (n=2, 53.4–56.8 mm SL), MRAC-B4-03-P-1-2 (n=2, 53.0–54.5 mm SL), same data and collectors as SAIAB59808, SAIAB121038 (n=10, 34.0–68.0 mm SL) collected from the Verlorenvlei River in 1973 by P. Skelton, C. Gaigher and D. Heard; SAIAB121039 (n=17, 41–57 mm SL) collected from the Kruis River, Verlorenvlei, in 1973 by P. Skelton, C. Gaigher and D. Heard. Paragenetype: SAIAB192542, GenBank number: KM366107.

Diagnosis

The new species can be distinguished from its congeners by distinct linear speckles above and below the lateral line, anterior barbels minute and much smaller than eye diameter, lips unretracted, and a cartilaginous fig absent.

Description

Proportional measurements and meristic characters are presented in Table 4. The body is fusiform, more or less laterally compressed, with a conspicuous lateral stripe from the posterior edge of the head terminating in a dark spot at the base of the caudal peduncle. The lateral band is more pronounced in juveniles and sub-adults, but is less conspicuous in adults. Distinct linear speckles are present on the abdomen. The head is relatively small and slightly depressed; head length is almost equal to body depth. Two pairs of barbels, rostral (anterior) barbels minute and much smaller than eye diameter; maxillary barbels are rooted at the corner of the mouth are longer than rostral barbels and are equal or smaller than eye diameter. Eyes are relatively large, located dorsolaterally, closer to the tip of the snout than the caudal margin of the operculum, interorbital space is flat. Mouth is sub-terminal, lower lip is unretracted and lacks a cartilaginous fig. Snout is relatively short, only few nuptial tubercles present (observed in only one individual; Figure 4) or tubercles are completely lacking.

Comparisons of the morphometric measurements and meristic counts of Pseudobarbus species with two pairs of barbels. For meristics, the mode is given first, with the range in parentheses. Values are expressed as mean ± SE.

P. verloreni sp. n. P. burgi P. skeltoni P. burchelli
Holotype Paratypes
No. of specimens 1 46 66 25 128
Standard length (SL) (mm) 70.0 34.0–70.8 42.0–109.0 28.5–163.4 30.0–151.7
Head length (HL) (mm) 18.9 10.0–19.6 10.9–25.0 8.6–51.7 8.1–45.8
Percentage of SL (%)
Head length 27.0 28.1±0.2 24.9±0.1 30.5±1.5 26.8± 1.0
Predorsal length 54.0 53.1±0.4 47.6±0.1 53.3± 1.7 51.2± 1.4
Dorsal fin base 12.9 13.2±0.1 13.7±0.1 12.0± 0.8 13.4± 0.7
Dorsal fin height 25.3 25.6±0.3 24.2±0.1 21.2± 1.8 22.9± 1.4
Body depth 27.6 29.1±0.2 26.9±0.3 25.6± 1.3 25.6± 1.6
Body width 16.1 16.4±0.2 15.2±0.3 17.9± 1.5 17.1± 1.6
Caudal peduncle length 20.9 23.5±0.2 25.7±0.1 22.4± 0.8 25.0± 1.2
Percentage of HL (%)
Head depth 72.5 73.0±0.4 74.1± 0.3 64.2± 3.1 70.1± 2.6
Inter-obit 36.0 34.4±0.3 33.1±0.3 28.1± 2.1 31.3± 2.1
Snout length 31.2 31.0±0.4 36.6±0.4 38.0± 2.2 36.5± 1.9
Post orbit 46.0 47.6±0.5 46.4±0.3 45.4± 1.8 45.2± 1.9
Anterior barbel length 6.3 3.3±0.3 5.1±0.2 20.3± 9.5 16.5± 4.3
Posterior barbel length 30.7 20.8±0.8 19.3±0.3 27.5± 11.9 28.4± 5.6
Orbit diameter 31.2 31.5±0.4 28.8±0.4 21.5± 4.4 27.7± 2.8
Percentage of caudal peduncle length (%)
Caudal peduncle depth 61.0 52.6±0.8 46.9± 4.0 53.4± 3.6 49.4± 3.5
Unbranched dorsal fin rays iv iii (iii-v) iii (iii–iv) iii (iii–iv) iv (iii–iv)
Branched dorsal fin rays 7 7 (7–8) 7 (6–7) 7 (7–8) 7 (6–8)
Unbranched anal fin rays iii iii (iii-iv) iii (ii-iv) iii (iii-iv) iii (iii-iv)
Branched anal fin rays 5 5 5 (5–6) 5 (4–5) 5 (4–6)
Pectoral fin rays 14 15 (13–16) 14 (13–16) 13 (13–16) 14 (13–16)
Pelvic fin rays 8 8 (7–9) 8 (8–9) 8 (7–8) 8 (7–8)
Lateral line scales 33 32 (29–36) 32 (28–37) 38 (36–39) 35 (29–37)
Scale rows between lateral line and dorsal fin 6 6 (5–6) 5 (4–6) 7 (6–7) 6 (5–7)
Scale rows between lateral line and pelvic fin 4 5 (4–5) 4 (3–5) 5 (5–7) 4 (4–5)
Scale rows between lateral line and anal fin 4 4 (4–5) 4 (3–4) 5 (4–6) 4 (4–6)
Caudal peduncle scale rows 12 12 (12–16) 12 (12–13) 16 (15–18) 12 (12–16)
Predorsal scale rows 16 16 (13–18) 15 (12–16) 19 (17–21) 17 (14–22)
Total vertebrae 36 36 (34–37) 37 (35–38) 37 (36–38) 36 (35–37)
Pre-caudal vertebrae 19 19 (18–21) 19 (18–20) 20 (19–21) 19 (17–20)
Caudal vertebrae 17 17 (16–19) 18 (16–19) 17 (16–18) 18 (17–20)
Predorsal vertebrae 11 11 (10–13) 11 (10–12) 12 12 (11–13)
Pre-anal vertebrae 20 20 (19–21) 20 (19–22) 21 (20–22) 19 (18–21)

Counts for the holotype are given in a separate column in Table 4. Dorsal fin of the new species has 3 unbranched and 7 or 8 branched rays, distal margin almost straight, anterior base of dorsal fin inserted directly above or slightly in front of the origin of pelvic fins. Origin of dorsal fin inserted almost midway between tip of snout and base of caudal fin. Pectoral fins with 13 to 16 rays, shorter than head length, reaching beyond halfway to pelvic fin origin. Pelvic fin with 7 to 9 rays, shorter than head, posterior edge gently rounded, reaching the anus in males and within one or two scale rows to the anus in females. Anal fin with 3 or 4 unbranched and 5 branched rays, distal margin almost straight or gently rounded, origin inserted closer to origin of pelvic fin than base of caudal fin. Caudal fin forked, shorter than head length. Genital opening situated adjacent to anterior base of anal fin.

Scales moderately large; lateral line complete, majority of specimens have 32 scales along lateral line (range 29–36); 5–6 (mode 6) scale rows between dorsal fin origin and lateral line; 4–5 (mode 5) scale rows between pelvic fin origin and lateral line; 4–5 (mode 4) scale rows between lateral line and anal fin origin; 12–16 (mode 12) circumpeduncular scale rows. Predorsal scale rows 13–18 (mode 16), embedded in skin, smaller than flank scales. Patch between head and posterior base of pectoral fins naked; scales between posterior base of pectoral fins and anterior base of pelvic fins smaller than flank scales and embedded. Pelvic fins lack prominent or elongate axillary scales. Scales radiately striated.

Nuptial tubercles have only been observed in one individual of P. verloreni (Figure 4). The bilateral placement of tubercles on the snout is typical for Pseudobarbus, but the low number (only 4 tubercles in total) of the P. verloreni individual in Figure 4 is unusual. The other members of the double barbeled redfin group develop multiple prominent conical tubercles on the snout and head dorsum during the breeding season (see Chakona and Swartz 2013). Additional sampling during the breeding season is required to determine whether this is a consistent development pattern for P. verloreni.

Colouration

Live colouration is golden-tan dorsally and laterally, becoming lighter and more silver ventrally (Figure 3c). In adults (above 40 mm SL), base of fins is pale red or yellowish-orange in some specimens. Alcohol preserved specimens have conspicuous linear speckles above and below the lateral line.

Figure 3.

a Habitus of Pseudobarbus verloreni sp. n. (holotype, SAIAB186092). Drawing by R. Palmer b Radiograph of Pseudobarbus verloreni sp. n. (holotype, SAIAB186092) c Live colours of Pseudobarbus verloreni sp. n. (SAIAB186108). Picture by W. Bronaugh d Preserved colours of Pseudobarbus verloreni sp. n. (holotype, SAIAB186092).

Figure 4.

Lateral and dorsal view of Pseudobarbus verloreni sp. n. from site 4 in Figure 5. The figure shows a different pattern of tubercule expression compared to other members of the double barbeled redfin group (see Chakona and Swartz 2013).

Osteology

Radiographs of the holotype (SAIAB 186092) and paratypes show that the species has osteology typical of all Pseudobarbus species. Compared to other cyprinids, particularly those within the genus Barbus, supraneural bones are less developed or extremely vestigial in all members of the genus Pseudobarbus (Skelton, 1988). Skelton (1988) did not record any supraneural bones in Pseudobarbus specimens (n=53) from the Verlorenvlei River system (herein described as Pseudobarbus verloreni sp. n.). Vertebrae counts for the holotype are given in a separate column in Table 4. Total number of vertebrae in 47- specimens investigated in the present study ranged from 34–37: 34 (n=1), 35 (n=3), 36 (n=31) or 37 (n=12) comprising 18–21 (mode 19) precaudal, 19–22 (mode 20) pre-anal, 10–13 (mode 11) predorsal and 16–19 (mode 17) caudal vertebrae (Table 4).

Additional information

SAIAB59813, juveniles (n=68, 13.5–28.4 mm SL) and adults (n=3, 59.3–64.6 mm SL), collected from the Verlorenvlei River, near Grootfontein farm (32.39830017 S, 18.47419930 E) on 23 January 1999 by R. Bills and D. Naran using a seine net and D-net. Juveniles and sub-adults of P. verloreni have a conspicuous lateral band, while the lateral band is either less prominent or interrupted by linear spots in juveniles and sub-adults of the other double barbeled Pseudobarbus species. The new species has three rows of pharyngeal teeth, teeth pattern 2.3.5–5.3.2 (observed in 3 adults; SAIAB59813); teeth with asymmetrical crowns and hooked at their tips. Pseudobarbus verloreni sp. n. has the longest intestine relative to standard length compared to all the Pseudobarbus species (Skelton 1988: Figure 25Bc).

Comparisons

Pseudobarbus verloreni sp. n. is distinguished from all other species of Pseudobarbus (except P. skeltoni, P. burchelli and P. burgi) by the presence of two pairs of oral barbels. The new species is distinguished from P. skeltoni, P. burchelli and P. burgi by having a deeper body relative to standard length, smaller anterior barbels and shorter snout relative to head length (Table 4). The new species is distinguished from P. skeltoni by having a sub-terminal mouth (versus terminal in adults of the latter species) and a smaller head relative to standard length (Table 4). Pseudobarbus verloreni is distinguished from P. burchelli and P. skeltoni by a deeper head, wider distance between the eyes (inter-orbit), larger eye relative to head length, shorter posterior barbel relative to head length, wider post-orbit distance, shallower caudal peduncle and generally fewer scales along the lateral line. Pseudobarbus verloreni is distinguished from P. burchelli and P. burgi by lack of cartilaginous fig on lower lip and having unretracted lips. The new species is distinguished from P. burgi by its longer head, longer pre-dorsal length, shorter caudal peduncle and larger eye (Table 4).

Reproduction

Unknown, but spawning possibly occurs around October-December, based on the general patterns of congeners.

Distribution and habitat

Pseudobarbus verloreni is a lowland species that is restricted to the Verlorenvlei River system on the west coast of South Africa (Figure 5). The morphological features of two juvenile specimens of Pseudobarbus collected from the Langvlei River by Thorne and Cambray in 1986 (SAIAB 130464) are consistent with juveniles of the new species, and are thus assigned to P. verloreni. The Langvlei River population is likely to have been extirpated, as no specimens of Pseudobarbus have been collected during more recent surveys (2001–2012). The major impact on this river is excessive water extraction that causes the river to dry up completely during the dry season. The Verlorenvlei River system has a gentle gradient and slow to moderate flow for much of the year. The water is highly turbid during the rain season (winter months) when water volume and flow velocity is high, but it becomes less turbid during low flow periods. Most sections of the river system recede into a series of isolated pools during the dry season, especially during late summer and autumn. The bottom substratum is predominantly sand, silt and mud. This is in contrast with the majority of the streams in the CFR that are associated with the Cape Fold Mountains with steeper gradients, clear water, moderate to fast flow throughout the year and rocky substratum. The species was possibly widespread throughout the Verlorenvlei and Langvlei River systems in the past, but numbers likely declined during the last century due to predation and competition from introduced fish species and habitat degradation (see below).

Figure 5.

Map of a part of the west coast of South Africa. The map shows the likely present distribution of Pseudobarbus verloreni in the Verlorenvlei River system (green line), based on available accurate museum data (green circles; site 1=59813; site 2=SAIAB 59804, 130461 and 186108; site 3=SAIAB 121039, 128824, 186092 and 192542; site 4=SAIAB 130453 and 59808). Also shown is site 5 where the species was collected in the Langvlei River system in 1986 (red circle; site 5=SAIAB 130464), but have not been found in subsequent surveys. The insert map shows the study area in relation to Cape Town, Cape Agulhas (most southern point in Africa) and neighbouring major river systems.

Etymology

The species is named after the Verlorenvlei River system to which it is now confined.

Conservation

The Verlorenvlei redfin was listed as Endangered during the most recent IUCN assessment by Tweddle et al. (2009). The presence of non-native predatory black bass Micropterus spp and potential competitors, banded tilapia Tilapia sparrmanii, Mozambique tilapia Oreochromis mossambicus and common carp Cyprinus carpio, habitat degradation and excessive water withdrawal for agricultural purposes pose the greatest threat to the survival of this species. Protection of critical habitats and establishment of sanctuaries are some of the most immediate conservation measures required to prevent further decline. The effectiveness of current protected areas in conserving Pseudobarbus verloreni is limited because they largely encompass upland areas where this species does not occur. Long-term measures to protect and prevent extinction of this species may have to include eradication of alien fishes and the construction of barriers to prevent re-invasion where feasible and restoration of existing habitats to facilitate recovery.

Key to double barbeled redfin species of the genus Pseudobarbus

1 Mouth terminal, 36–39 lateral scale series Pseudobarbus skeltoni
Mouth sub-terminal 2
2 Lower lip unretractable, cartilaginous fig absent, conspicuous linear speckles above and below lateral line P. verloreni sp. n.
Lower lip retractable, cartilaginous fig present 3
3 Anterior barbels less than 30% of orbit diameter P. burgi
Anterior barbels more than 30% of orbit diameter P. burchelli

Discussion

Specimens of Pseudobarbus from the Verlorenvlei River system show clear genetic and morphological differences when compared with the three currently described double barbeled Pseudobarbus species (P. burchelli, P. burgi, and P. skeltoni) and are thus described as a new species. The morphological differentiation between P. verloreni sp. n. and P. burgi reported here is consistent with the findings of Skelton (1988) who reported considerable ‘intraspecific’ morphological variation between Verlorenvlei and Berg populations. The most informative characters that distinguish P. verloreni sp. n. from P. burgi are body depth, head length, predorsal length, snout length and anterior barbel length. However, P. verloreni sp. n. and P. burgi cannot be distinguished based on meristic characters because considerable overlap exists between the two species.

Phylogenetic results from the present study, Swartz et al. (2009) and Chakona and Swartz (2013) show that the relationships among P. verloreni sp. n. (referred to as Verlorenvlei lineage in latter two studies), P. burgi sensu stricto, P. burchelli sensu lato and P. skeltoni are not well resolved, with a polytomy linking the new species and the other taxa. This is further evidence that the Pseudobarbus from Verlorenvlei represents a separate species as it does not clearly group with one of the other species or lineages. Our review of available material of double barbeled redfins confirmed that P. verloreni sp. n. is restricted to the Verlorenvlei River system and likely have been extirpated from the adjacent Langvlei River system.

Reduced tubercle occurrence in P. verloreni could represent a different breeding strategy or behaviour compared to other redfins. Further research is required to better describe the ecology, biology, population size, distribution and conservation status of this species. There are serious conservation concerns, because this species is associated with pool habitats, which are also favourable habitats for non-native fish predators and competitors. This species is also threatened by proposed mining activities and excessive water withdrawal in the Verlorenvlei catchment. Improved understanding of the conservation status, distribution and ecology is a critical requirement for developing effective conservation measures to prevent extinction of this species. The current protected areas are unlikely to be effective for the conservation of Pseudobarbus verloreni as the known distribution range of this species falls outside protected areas. Expansion of protected areas and education of landowners may be necessary to ensure survival of this species.

Acknowledgements

This work was supported by the National Research Foundation (NRF) of South Africa under the Foundational Biodiversity Information Programme: Biodiversity surveys in priority inland areas (IBIP) grants (grant reference no. IBIP-BS13100251309). We thank Roger Bills, Daksha Naran and Whit Bronaugh for field collections, Rose Palmer for the illustration of P. verloreni, Dr Phil Heemstra for providing equipment and Nkosinathi Mazungula for taking the radiographs. CapeNature provided permits for undertaking field surveys and specimen collections. The authors acknowledge that opinions, findings and conclusions or recommendations expressed in this publication generated by the NRF supported research are that of the authors and that the NRF accepts no liability whatsoever in this regard.

References

  • Barnard KH (1938) Notes on the species of Barbus from the Cape Province, with descriptions of new species. Annals and Magazine of Natural History (Series 11) 2(7): 80−88.
  • Barnard KH (1943) Revision of the indigenous freshwater fishes of the S.W. Cape Region. Annals of the South African Museum 36: 101–263.
  • Bloomer P, Impson ND (2000) Mitochondrial DNA differentiation in the Critically Endangered Berg River Redfin (Pseudobarbus burgi). The Journal of Heredity 91: 122–127. doi: 10.1093/jhered/91.2.122
  • Boulenger GA (1905) A list of freshwater fishes of Africa. Annals and Magazine of Natural History 7: 36–60. doi: 10.1080/03745480509443651
  • Boulenger GA (1911) Catalogue of freshwater fishes of Africa in the British Museum (Natural History). British Museum (Natural History) 2: 1–529.
  • Castelnau FL (1861) Mémoire sur les poissons de l’Afrique australe. Baillière et Fils, Paris. doi: 10.5962/bhl.title.3819
  • Cambray JA (1994) Seasonal occurrence and distribution of nuptial tubercles in two African minnows, Pseudobarbus afer (Peters, 1864) inhabiting clear water, and Pseudobarbus asper (Boulenger, 1911) inhabiting turbid water (Cypriniformes, Cyprinidae). Annals of the Cape Provincial Museums (Natural History) 19: 149–170.
  • Chakona A, Swartz ER (2013) A new redfin species, Pseudobarbus skeltoni (Cyprinidae, Teleostei), from the Cape Floristic Region, South Africa. Zootaxa 3686: 565–577. doi: 10.11646/zootaxa.3686.5.5
  • Chakona A, Swartz ER, Gouws G (2013) Evolutionary drivers of diversification and distribution of a southern temperate stream fish assemblage: testing the role of historical isolation and spatial range expansion. PLoS ONE 8(8): e70953. doi: 10.1371/journal.pone.0070953
  • Chakrabarty P (2010) Genetypes: a concept to help integrate molecular phylogenetics and taxonomy. Zootaxa 2632: 67–68.
  • Cuvier G, Valenciennes A (1842) Histoire naturelle des poissons. Tome seizième. Livre dix-huitième. Les Cyprinoïdes. v. 16: i-xx + 1–472, Pls. 456–487.
  • Gaigher IG, Hamman KCD, Thorne SC (1980) The distribution, conservation status and factors affecting the survival of indigenous freshwater fishes in the Cape Province. Koedoe 23: 57–88. doi: 10.4102/koedoe.v23i1.636
  • Jubb RA (1965) Freshwater fishes of the Cape Province. Annals of the Cape Provincial Museum 4: 1–72.
  • Lleonart J, Salat J, Torres GJ (2000) Removing allometric effects of body size in morphological analysis. Journal of Theoretical Biology 205: 85–93. doi: 10.1006/jtbi.2000.2043
  • Peters WCH (1864) Über eine neue Percoidengattung, Plectroperca, aus Japan und eine neue Art von Haifischen, Crossorhinus tentaculatus, aus Neuholland. Monatsberichte der Königlichen Preussische Akademie der Wissenschaft zu Berlin 1864: 121–126.
  • Sabaj PMH (2013) Standard symbolic codes for institutional resource collections in herpetology and ichthyology: an Online Reference. Version 4.0 (28 June 2013). Electronically accessible at http://www.asih.org/, American Society of Ichthyologists and Herpetologists, Washington, D.C.
  • Skelton PH (1980) Systematics and biogeography of the redfin Barbus species (Pisces, Cyprinidae) from southern Africa. PhD thesis, Rhodes University, Grahamstown.
  • Skelton PH (1988) A taxonomic revision of the redfin minnows (Pisces, Cyprinidae) from southern Africa. Annals of the Cape Provincial Museum (Natural History) 16: 201–307.
  • Smith A (1841) Pisces. Illustrations of the Zoology of South Africa. Smith, Elder and Col., London.
  • Steindachner F (1870) Ichthyologiesche Notizen (X). Sitzungsberichte Der Akademie Der Wissenschaften Wien 61: 623–642.
  • Swartz ER, Skelton PH, Bloomer P (2007) Sea-level changes, river capture and the evolution of populations of the Eastern Cape and fiery redfins (Pseudobarbus afer and Pseudobarbus phlegethon, Cyprinidae) across multiple river systems in South Africa. Journal of Biogeography 34: 2086–2099. doi: 10.1111/j.1365-2699.2007.01768.x
  • Swartz ER, Skelton PH, Bloomer P (2009) Phylogeny and biogeography of the genus Pseudobarbus (Cyprinidae): Shedding light on the drainage history of rivers associated with the Cape Floristic Region. Molecular Phylogenetics and Evolution 51: 75–84. doi: 10.1016/j.ympev.2008.10.017
  • Swartz ER, Chakona A, Skelton PH, Bloomer P (2014) The genetic legacy of lower sea-levels: does the confluence of rivers during the last glacial maximum explain the contemporary distribution of a primary freshwater fish (Pseudobarbus burchelli, Cyprinidae) across isolated river systems? Hydrobiologia 726: 109–121. doi: 10.1007/s10750-013-1755-7
  • Tweddle D, Bills R, Swartz E, Coetzer W, Da Costa L, Engelbrecht J, Cambray J, Marshall B, Impson D, Skelton PH (2009) The status and distribution of freshwater fishes. In: Darwall WRT, Smith KG, Tweddle D, Skelton PH (Eds) The Status and Distribution of Freshwater Biodiversity in Southern Africa. IUCN, Gland, Switzerland and SAIAB, Grahamstown, South Africa, 21–37.