TAXONOMIC REVIEW OF THE GENUS LUCIOBARBUS HECKEL, 1843 (ACTINOPTERYGII, CYPRINIDAE) FROM NORTHWESTERN MOROCCO WITH THE DESCRIPTION OF THREE NEW SPECIES

Miriam Casal-Lopez1, Silvia Perea1, Ahmed Yahyaoui2 & Ignacio Doadrio1*

1Biodiversity and Evolutionary Group. National Museum of Natural Sciences. CSIC. C/ José Gutiérrez Abascal, 2. 28006. Madrid. Spain

MC-L: urn:lsid:zoobank.org:author:84DEBB1B-A34C-412A-B03B-C3492A4E59BE

SP: urn:lsid:zoobank.org:author:75C3112F-5BE9-4512-A9DB-DDA2A10497C7

ID: urn:lsid:zoobank.org:author:1514FE9E-2AA2-46D1-BB43-51F5E8EF1566

2Laboratory of Zoology and General Biology, Faculty of Sciences, Mohammed V University. B.P. 1014. Rabat. Morocco

urn:lsid:zoobank.org:author:EA344560-E0FA-4D5D-A51C-23771D124D4B

* Corresponding author: doadrio@mncn.csic.es

 

ABSTRACT

The genus Luciobarbus in Morocco presents high diversification, in contrast to the generally impoverished freshwater fish fauna from North Africa. Within Morocco the northern area is one of the least studied territories, due to both its historical background and the limited accessibility of many regions. Previous phylogenetic studies identified Luciobarbus populations that are morphologically and genetically differentiated, to the same extent as others already recognized as separate species. The aim of this work is to describe these populations as distinct species, based on morphological, meristic, and genetic traits.

urn:lsid:zoobank.org:pub:8FC4B423-104C-4097-A468-ED3D2664A15A

Key words: Cyprinidae; Luciobarbus; taxonomic review; new species; Morocco.

 

RESUMEN

Revisión taxonómica del género Luciobarbus Heckel, 1843 (Actinopterygii, Cyprinidae) del noroeste de Marruecos con la descripción de tres nuevas especies

En Marruecos el género Luciobarbus está altamente diversificado, en comparación con la empobrecida fauna de peces de agua dulce del norte de África. Dentro de Marruecos la región norte es una de las áreas menos estudiadas, por motivos históricos y también por la poca accesibilidad en algunas de sus regiones. Los estudios filogenéticos previos para esta área han señalado la existencia de poblaciones pertenecientes al género Luciobarbus tan diferenciadas morfológica y genéticamente como otras que ya habían sido reconocidas como diferentes especies. En este trabajo describimos estas poblaciones como diferentes taxa, en base a caracteres morfológicos, merísticos y genéticos.

Palabras clave: Cyprinidae; Luciobarbus; revisión taxonómica; nuevas especies; Marruecos.

 

Recibido/Received: 06/04/2015; Aceptado/Accepted: 08/05/2015; Publicado en línea/Published online: 19/08/2015

Cómo citar este artículo/Citation: Casal-Lopez, M., Perea, S., Yahyaoui, A. & Doadrio, I. 2015. Taxonomic review of the genus Luciobarbus Heckel, 1843 (Actinopterygii, Cyprinidae) from northwestern Morocco with the description of three new species. Graellsia, 71(2): e027. http://dx.doi.org/10.3989/graellsia.2015.v71.135.

Copyright: © 2015 SAM y CSIC. Salvo indicación contraria, todos los contenidos de la edición electrónica de Graellsia se distribuyen bajo licencia de uso y distribución Creative Commons Reconocimiento no Comercial 3.0. España (cc-by-nc).


 

CONTENT

IntroductionTOP

The genus Barbus sensu lato includes more than 800 species and it is one of the genera with the highest number of species among vertebrates. It is a polyphyletic assemblage with different genetic and morphologic features. In fact, in recent years, Barbus phylogenetic studies have led to its division into different genera (Karaman, 1971; Machordom & Doadrio, 2001a; Yang et al., 2015).

European and North African species previously included in the genus Barbus Cuvier & Cloquet, 1843 are presently included in the genera Barbus and Luciobarbus Heckel, 1843 (Kottelat & Freyhof, 2007). The genus Luciobarbus was initially assigned to the Asian species Luciobarbus esocinus Heckel, 1843 but was long considered as a synonym of Barbus Cuvier & Cloquet, 1843. Notwithstanding, a phylogenetic study using morphological characters revealed that most limnophilic circum-Mediterranean species occurring in northern Africa, the Mediterranean peninsulas, and the Near East were monophyletic (Doadrio, 1990). This monophyletic clade was included within the subgenus Luciobarbus (Doadrio, 1990), which with the advent of molecular studies, was better defined and recognized at the generic level (Machordom & Doadrio, 2001b; Tsigenopoulos et al., 2003; Griffiths et al., 2004; Kottelat & Freyhof, 2007; Yang et al., 2015).

Molecular studies of the genus Luciobarbus have, so far, been based on isoenzyme analysis (Machordom et al., 1995, 1998; Doadrio et al., 1998) and sequencing of mitochondrial genes (Zardoya & Doadrio, 1999; Zardoya et al., 1999; Machordom & Doadrio 2001b; Doadrio et al., 2002; Tsigenopoulos et al., 2003). The sequencing of nuclear genes has been constrained by the tetraploid condition of the species of this genus (Yang et al., 2015).

Results of previous molecular studies have revealed a strong Luciobarbus population structure in North Africa (Berrebi et al., 1995; Doadrio et al., 1998; Machordom et al., 1998; Machordom & Doadrio, 2001b). Sixteen populations, genetically isolated during the late Miocene and Pliocene, were recognized in North Africa, some of them assigned to different species (Machordom & Doadrio, 2001b). Within North African populations, those of northwestern Morocco, inhabiting areas ranging from the basins of the Laou River (on the Mediterraenan slope in the North) to the Kasab River (on the Atlantic slope in the southwest), have been clustered together by genetic studies (Machordom & Doadrio, 2001b; Geiger et al., 2014). However, there are few taxonomic studies focusing on Luciobarbus populations of northwestern Morocco, due to its traditional isolation and limited accessibility (Almaça, 1966, 1968, 1970; Doadrio, 1990). For these reasons northern Morocco was ignored, when taxonomic African ichthyological studies were conducted by the French Geographical Society, in the early twentieth century.

Some Luciobarbus populations, mainly from Laou, Grou and Sebou Basins, belonging to northwestern Morocco present high genetic differentiation in several molecular markers, such as isozymes and the mitochondrial cytochrome b gene, compared to other populations of the genus and constitute a monophyletic group (Machordom et al., 1998; Machordom & Doadrio, 2001b; Geiger et al., 2014). Nonetheless, only morphological works have been carried out for the Sebou Basin (Almaça, 1966, 1968, 1970; Doadrio, 1990). The aim of our study was to extend the molecular and morphological works to other populations from northwestern Morocco. Thus, our goal was to clarify, with a more complete sampling, the taxonomy of Luciobarbus in northwestern Morocco with an integrative approach and unravel whether the diversity found corresponds to new taxa that may not have been formally described so far. In this case, we will formally describe these new taxa.

Material and MethodsTOP

MORPHOLOGICAL ANALYSESTOP

The taxonomy of the population of northwestern Morocco was based on 47 specimens from Laou Basin, 43 specimens from Loukos Basin, 22 specimens from Hachef Basin, 55 specimens from Sebou Basin, 33 specimens from Bou Regreg Basin and 23 specimens from Kasab Basin (Fig. 1, Table 1).

Fig. 1.— Geographic distribution of Luciobarbus spp. and sampling localities. The numbers on map correspond to localities in Table 1.
Fig. 1.— Distribución geográfica de Luciobarbus spp. y localidades muestreadas. La correspondencia entre números y localidades se puede ver en la Tabla 1.

 
Table 1.— Sampling localities for Luciobarbus spp. Code is the number on the phylogenetic tree. G= Genetic, M= Morphometry.
Tabla 1.— Localidades muestreadas de las especies de Luciobarbus estudiadas. El código es el número que aparece en el árbol filogenético. G= análisis genético. M= análisis morfométrico.
Species River Locality Basin Analyses Code GenBank Map
L. ksibi Kasab Essaouira Kasab G,M K6-K10 KT003951-55 1
L. ksibi Reraia Asni Tensift G K1-K5 KT003956-60 2
L. sp1 Tizguit Ifrane Sebou M 4
L. sp1 Ifrane Ouad Ifrane Sebou G,M S1-S6 KT003941-45 5
L. sp2 Tattofte Ouled Soltane Loukos M 6
L. sp2 Loukos Mouries Loukos M 7
L. sp2 Loukos Souk Had, Laghdir Loukos G RK1-RK5 KT003936-40 8
L. sp2 Hachef Dar Chaoui Hachef G,M RH1-RH5 KT003931-35 9
L. sp2 Laou Derdara Laou G,M RL1-RL5 KT003926-30 10
L. sp2 Laou Beni Ferten Laou M 11
L. sp3 Bou Regreg Sebt Ait Rahhou Grou G B1-B5 KT003946-50 3
L. capito Terek Kizlyar Terek (Russia) G L. capito AF045975

The material studied comsisted of the following locations and number of specimens: 25 adult specimens from the Laou River, Laou Basin, Derdara, (35.118986, -5.288900), Morocco (Voucher numbers: MNCN 290.639-290.652, 290.655, 290.657-663, 290.665-667); 22 specimens from the Laou River, Laou Basin, Beni Ferten (35.353254, -5.184840), Morocco (Voucher numbers: MNCN 284.939-940, 284.942-945, 284.947-284.948, 284.950-951, 284.953-964); 43 specimens from the Loukos River, Loukos Basin, Souk Had, Laghdir (35.02624,-5.404660), Morocco (Voucher numbers: MNCN: 280.162-163, 280.165, 280.168, 280.170, 280.172-174, 280.176-181, 280.183, 280.185-186, 290.671-696); 22 specimens from the Hachef River, Hachef Basin, Dar Chaoui (35.526763,-5.713771), Morocco (MNCN 290.707-714; 290.716-722; 290.725-731); 32 specimens from the Ifrane River, Sebou Basin, Ouad Ifrane, (33.296957, -5.492639) Morocco (voucher numbers: MNCN 279.711-729, 290.731, 279.733-744); 23 specimens from the Tizguit River, Sebou Basin, Ifrane (33.549241, -5.097144), Morocco (Voucher number: MNCN 71675-697); and 33 specimens from the Grou River, Bou Regreg Basin, Sebt Ait Rahhou (33.164678, -6.366963), Morocco (Voucher numbers: MNCN 71725-746, 71918-28). For comparative purposes, we analyzed 23 specimens of Luciobarbus ksibi Boulenger 1905 from species type locality in the Kasab River, Kasab Basin, Essaouira (31.465857,-9.759850) Morocco (Voucher numbers: MNCN 105.460-65, 105.469, 234.925-29, 280.483-485, 71220-21, 71223-26, 71230, 290.670). All sampling sites (Fig. 1) presented similar riverine morphology, with clear water and fast current and gravel bottom, with the exception of the Kasab River, in Essaouira, which showed a more marked seasonal regime and poorer water conditions.

Twenty-three morphometric measurements (in mm) and nine meristic variables were recorded from digital photographs using TpsDig v.1.4 (Rohlf, 2003). The following abbreviations were used for morphometric and meristic characters: A, anal fin rays; AFH, anal fin height; AFL, anal fin length; APL, anal peduncle length; BL1, first barbel length; BL2, second barbel length; BD, body depth; LBD, lowest body depth; C, central caudal fin rays; CFL, caudal fin length; CPL, caudal peduncle length; D, dorsal fin rays, DFL dorsal fin length; DFH dorsal fin height; ED, eye diameter; HL, head length; LL lateral line scales; P, pectoral fin rays; PFL, pectoral fin length; PrAD, pre-anal distance; PrDD, pre-dorsal distance; PrOL, pre-orbital length; PrPD, pre-pectoral distance; PrVD, pre-ventral distance; PsOL, postorbital length; PVL, pectoral-ventral length; RSA, scale rows above lateral line; RSB scale rows below lateral line; SL, standard length; V, ventral fin rays; VFL, ventral fin length; VE, Number of vertebrae. The number of vertebrae was obtained by direct counting on X-ray images of individuals from all populations sampled.

After constructing the measurement matrix, Burnaby’s method was used to correct size effect (Burnaby, 1966; Rohlf & Bookstein, 1987). All analyses were conducted with the corrected matrix. Morphometric and meristic characters were analyzed independently. A two-way analysis of variance (ANOVA) comparing morphometric characters was conducted to test for sexual dimorphism and variation among populations. To identify the variables that contributed most to the variation between populations, a principal components analysis (PCA) was performed using the covariance matrix for morphometric characters.

MOLECULAR ANALYSESTOP

For the molecular approach, we analyzed samples corresponding to individuals of Luciobarbus spp. from Sebou, Laou, Hachef, Loukos and Bou Regreg basins; and Luciobarbus ksibi from the Kasab Basin (Table 1). The species Luciobarbus capito (Güldenstädt, 1773) was selected as outgroup based on previous phylogenetic analyses (Zardoya & Doadrio, 1999). Total genomic DNA was extracted from fin-clip tissue using the commercial kit Biosprint 15 for tissue and blood (Qiagen). For each specimen, the complete region (1140bp) of the mitochondrial cytochrome b (cytb) was amplified. Primers and protocols used for PCR for cytb followed Machordom & Doadrio (2001b). After checking PCR products on 1% agarose gels, they were purified by ExoSAP-IT™ (USB) and directly sequenced on MACROGEN service using a 3730XL DNA sequencer. All sequences were deposited in the GenBank database (Accession Numbers: KT003926-KT003960).

PHYLOGENETIC ANALYSESTOP

Phylogenetic analyses were performed using Bayesian inference (BI) implemented in MrBayes v.3.2 (Ronquist et al., 2012). The Akaike Information Criterion (Akaike, 1973) implemented in jModeltest (Posada, 2008) was used to determine the evolutionary model that best fit the data. In this case TrN+I model was selected (R(a) [AC] =1.0000, R(b) [AG] =92.1342, R(c) [AT] =1.0000, R(d) [CG] =1.0000, R(e) [CT] =20.3361, R(f) [GT] =1.0000, p-inv =0.7900). BI was performed using two independent runs of four Markov Montecarlo coupled chains (MCMC) of 106 generations each, to estimate the posterior probability distribution. Topologies were sampled every 100 generations, and majority-rule consensus tree was estimated after discarding the first 10% of generations. Robustness of clades was assessed using Bayesian posterior probabilities. The average genetic distances among Luciobarbus populations were calculated for each gene using MEGA package v.6.0 (Tamura et al., 2013) according to the uncorrected-p distances.

Results and DiscussionTOP

COMPARISON OF MORPHOLOGY AMONG POPULATIONSTOP

Two-way analysis of variance (ANOVA), testing for sexual dimorphism and differentiation among populations, showed significant differences (p<0.05) for the variables standard length, postorbital length, and anal fin size (Table 2). In absolute values all variables were greater in females, but proportionally to the standard length postorbital length was longer in males (Table 3). A non-biological interpretation could explain the differences in postorbital length by sex, therefore we performed a test of Mann-Whitney-Wilcoxon at p<0.05, with postorbital length and sex as variables, for each population independently. The null hypothesis for identical postorbital length between males and females for each population was not rejected in all populations (Sebou Basin z=−0.810; Bou Regreg Basin z=−0.868; Kasab Basin z=−1.692; Loukos Basin z=−0.480; Laou Basin z=−0.343; Hachef Basin z=−0.032). Therefore, the differences in postorbital length were not explained by sex and were an effect of population differences.

Table 2.— Two-way analysis of variance (ANOVA) for sexual dimorphism, population variation, and their interaction. Significant differences p<0.05 (*); p<0.01 (**). N=163 males and n=60 females. Acronyms are defined in the Material and Methods.
Tabla 2.— Análisis de la varianza (ANOVA) de dos vías para dimorfismo sexual, variación poblacional y su interacción. Diferencias significativas p<0,05 (*); p<0,01 (**). N=163 machos and N=60 hembras. Las abreviaturas se describen en el epígrafe de Material y Métodos.
Variables Sexual dimorphism (f/p-value) Population Variation (f/p-value) Sex/pop variation (f/p-value)
SL 4.51/* 53.38/** 2.37/
HL 3.06/ 26.74/** 1.94/
PrOL 1.45/ 13.36/** 2.08/
ED 0.22/ 11.32/** 0.57/
PsOL 22.32/** 469.5/** 7.58/**
B1L 3.45/ 10.09/** 2.17/
B2L 1/ 21.07/** 0.19/
PrDD 1.66/ 78.49/** 2.14/
PrPD 0.01/ 44.54/** 4/**
PrVD 3.18/ 68.28/** 3.55/*
PrAD 1.75/ 56.71/** 3.5/*
CPL 0.96/ 11.14/** 1.92/
APL 0.51/ 3.68/* 4.39/**
PVL 0.01/ 12.71/** 0.51/
BD 3.13/ 9.64/** 1.34/
BLD 0.001/ 6.93/** 1.61/
DFL 2.04/ 2.9/ 0.137/
DFH 3.31/ 27.42/** 2.32/
PFL 0.10/ 23.08/* 1.8/
VFL 2.42/ 14.26 /** 0.19/
AFL 4.26/* 16.61/ 2.37/
AFH 11.46/** 29.88/** 2.06/
CFL 0.87/ 16.08/** 1.41/
Table 3.— Morphometric variables showing significant sexual dimorphism (p<0.05). Values are mean (minimum-maximum). Acronyms are defined in the Material and Methods.
Tabla 3.— Variables morfométricas que muestran dimorfismo sexual significativo (p<0.05). Los valores son medias y entre paréntesis valores máximos y mínimos. Las abreviaturas están descritas en el epígrafe de Material y Métodos.
Variables (mm) Males n=163 Females n=60
SL 106.2 (53.1-232.8-75) 157.7 (82.1-240.1)
PsOL 13.5 (6.6-30.8) 18.9 (9.6-29.6)
AFL 8.3 (3.74-17.8) 12.3 (6.2-19.3)
AFH 18.3 (10-41.6) 27.5 (15-44.8)

Females had proportionally higher and longer anal fins (Table 3). Sex differences in the size of anal fins have been found in other Luciobarbus species, and are probably associated with the female’s use of the anal fin to excavate nests in the riverbed (Banarescu & Bogutskaya, 2003). Nuptial tubercles were present in the snout and head of males, particularly around the preorbital region.

To deal with the presence of sexual dimorphism in anal fin size, we removed AFL and AFH from posterior analyses. Most morphometric variables showed significant differences between populations in the two-way ANOVA analysis (Table 2). An analysis of body proportions based on Kruskal-Wallis and Mann-Whitney post hoc comparisons, was used to detect differences in body shape that can masked if only linear untransformed measurements are taken into account (Appendix 1). We grouped the populations from the Rif Mountains (Laou, Loukos, and Hachef Basins) based on mitochondrial DNA analysis and previous genetic studies (Machordom et al., 1998, Machordom & Doadrio, 2001b; Geiger et al., 2014). The populations from Sebou Basin showed a shorter predorsal distance and a longer caudal peduncle than the other Luciobarbus populations studied, due to the more anterior position of the dorsal fin (Fig. 2, Table 4).

Fig. 2.— Comparison of two females of similar standard length from (A) Sebou Basin and (B) Laou Basin (Rifian population) showing differing position of the dorsal fin with respect to ventral fin insertion.
Fig. 2.— Comparación entre dos hembras de similar longitud estándar de las cuencas del Sebou (A) y del río Laou (población del Rif) (B) mostrando la diferente posición de la aleta dorsal con respecto al origen de la aleta ventral.

 
Table 4.— Ratios of morphometric variables and scale count. Values are mean (minimum and maximum). Acronyms are defined in the Material and Methods.
Tabla 4.— Valores de la media, y entre paréntesis valores mínimos y máximos, para diferentes proporciones de las variables morfométricas y número escamas. Las abreviaturas están descritas en el epígrafe de Material y Métodos.
Measurements Rif populations (n=112) Sebou (n=55) Bou Regreg (n=33) Luciobarbus ksibi (n=23)
SL/PrDD 1.87 (1.79-1.95) 1.93 (1.79-2.03) 1.85 (1.78-1.96) 1.85 (1.73-1.98)
SL/CPL 2.81 (2.56-3.06) 2.7 (2.54-2.91) 2.79 (2.63-2.91) 2.82 (2.63-3.17)
HL/PsOL 2.21 (1.65-2.50) 1.61 (1.29-1.81) 2.04 (2.47-3.41) 2.23 (2.03-2.57)
HL/PrOL 2.74 (2.35-3.23) 2.82 (2.48-3.49) 2.97 (2.47-3.5) 2.78 (2.4-3.1)
SL/BLD 9.11 (7.48-10.92) 8.72 (7.57-10) 8.38 (8.06-8.7) 7.8 (7.36-8.27)
CPL/BLD 3.24 (2.46-3.83) 3.24 (2.67-3.75) 3 (2.81-3.26) 2.78 (2.6-2.99)
APL/BLD 1.64 (1.25-2.07) 1.58 (1.37-1.83) 1.55 (1.39-1.67) 1.5 (1.29-1.87)
HL/L1B 4.16 (2.78-6.87) 3.96 (3.03-5.27) 4.11 (3.8-4.5) 3.5 (2.93-4.05)
HL/L2B 3.27 (2.48-5) 3.1 (2.4-4.74) 3.29 (3.05-3.52) 2.65 (2.26-3.25)
LL 43.9 (46-42) 43.7 (41-47) 46.5 (45-50) 43.7 (41-47)
RSA 8.8 (8.5-9.5) 7.5 (7.5-8.5) 9.6 (8.5-10.5) 8.3 (6.5-8.5)
RSB 4.7 (3.5-5.5) 5.5 (4.5-6.5) 6.74 (6.5-7.5) 4.98 (4.5-5.5)

The Sebou population exhibited greater postorbital length with respect to the other studied populations, and therefore the ratio SL/PsOL in the Sebou population was the lowest (Table 4). The caudal peduncle was higher in Luciobarbus ksibi (Kasab population) than in the other studied populations, and the ratios CPL/CPI and APL/BLD, were the lowest-. Barbels were longest in Luciobarbus ksibi. Preorbital length was significantly shorter in the Bou Regreg population compared to the other populations studied.

Lateral line scales were more numerous in the Bou Regreg population than in other populations. Scales numbers on the superior transverse line were higher in Bou Regreg and Rifian populations than in L. ksibi and Sebou populations, while the number of scales on the inferior transverse line was lower in Rifian populations and L. ksibi (Table 4).

The principal component analysis divided the populations into three groups corresponding to Luciobarbus ksibi and populations of the Rifian and the Sebou Basins. The population of the Bou Regreg Basin was included in the morphometric variability of Rifian populations (Fig. 3). Nevertheless, the Bou Regreg population could be discriminated from the other studied populations by the number of scales on the body (Fig. 4).

Fig. 3.— Variables that most contributed to the PCA analysis. Dots, Rifian populations. Squares, Luciobarbus ksibi from Kasab Basin. X, Population from Bou Regreg Basin. Circles, population from Sebou Basin. Abbreviations are defined in Materials and Methods.
Fig. 3.— Variables que más contribuyen al ordenamiento en el PCA. Puntos poblaciones del Rif. Cuadrados Luciobarbus ksibi de la cuenca del Kasab. Equis población de la cuenca del Bou Regreg. Círculos población de la cuenca del Sebou. Las abreviaturas están descritas en el epígrafe de Material y Métodos.

 

Fig. 4.— Box-plots of lateral line scale numbers. A, Rifian population; B, Sebou Basin population; C, Bou-Regreg Basin population.
Fig. 4.— Box-plots para el número de escamas en la línea lateral. A, Población del Rif; B, Población de la Cuenca del Sebou; C, Población de la Cuenca del Bou Regreg.

 

The eigenvalues of the two first principal components, with the Burnaby-corrected matrix, explained most of the variance (Table 5). The highest values for eigenvectors in both males and females, and, consequently, the variables that contributed most to the ordination in the PCA were: postorbital and preorbital length, caudal and dorsal fin size, and barbel length (Table 5).

Table 5.— Eigenvalues and eigenvectors for the first three principal components (PC1-PC3) of 21 morphometric variables for all Luciobarbus populations. Acronyms are defined in the Material and Methods. In bold, variables with the highest eigenvectors for each PC.
Tabla 5.— Eigenvalores y eigenvectores para los tres primeros componentes principales (PC1-PC3) de 21 variables morfométricas para todas las poblaciones del género Luciobarbus. Las abreviaturas están descritas en el epígrafe de Material y Métodos. En negrita, variables con los eigenvectores más altos para cada CP.
Variables PCI PCII PCIII
Eigenvalue 0.0073 0.0044 0.0029
% variance 29.1 17.56 11.48
Eigenvectors
SL −0.1416 −0.0053 0.0137
PrDD −0.1419 −0.0904 0.0254
PrPD −0.1741 −0.0915 −0.0420
PrVD −0.2401 −0.0236 −0.0667
PrAD −0.1961 0.0014 −0.0377
PVL −0.2772 0.0095 −0.0804
CPL −0.1750 0.1154 0.0243
APL −0.1185 0.0260 0.1110
BD −0.1550 −0.1024 −0.0021
BLD −0.0296 −0.0078 −0.0763
HL −0.0841 −0.0731 −0.0450
PrOL −0.1817 −0.1536 −0.0761
ED 0.0442 −0.1513 −0.1591
PsOL 0.1385 0.7205 −0.3674
B1L 0.5001 −0.2952 0.4918
B2L 0.3794 −0.2658 −0.1933
PFL 0.2412 0.0068 0.2772
VFL 0.2282 0.1219 0.1780
DFL −0.0322 −0.2115 −0.0283
DFH 0.1795 0.3645 0.4958
CFL 0.2966 0.2586 0.4046

OSTEOLOGICAL FEATURESTOP

The hardness of the last single ray of the dorsal fin (DFR) and its number of denticulations frequently has been used in the taxonomy of Luciobarbus (Almaça, 1970). As Doadrio (1990) pointed out, there is ontogenetic variability in DFR, and comparison of the characteristics of DFR among species, for taxonomic purposes, must be done using adult specimens (Appendix 2-1). We found L. ksibi presents strong denticulations but only over 2/3 of the DFR length. Denticulations of the DFR in specimens of the Bou Regreg population were deep and the length of these denticulations was greater than the width of the ray. Dorsal fin rays of the Rifian and Sebou basins populations were similar, slightly stronger in Rifian populations than in the Sebou population.

The skulls of L. ksibi and Sebou populations are shorter and wider than those of the Bou Regreg and Rifian populations. The ethmoid bone in the Sebou population is narrower than in other studied populations, especially pronounced compared to the Rifian population (Append. 2-2). In the skull lateral view, the opercular bone appeared longer in the Sebou population than in other populations (Append. 2-3). Infraorbital bones are larger in L. ksibi than in other populations, and the second infraorbital bone is longer in Rifian than in other populations and usually exhibits four pores (Append. 2-4). The pharyngeal bone is thinner in the Bou Regreg populations and wider in L. ksibi. The dorsal branch of the pharyngeal bone forms a closed angle with respect to inferior branch in Rifian population and L. ksibi (Append. 2-5).

MOLECULAR DATATOP

Phylogenetic analyses based on the cytb gene supported four main clades in the tree, corresponding to the populations of the Rif, Sebou, and Bou Regreg Basins and Luciobarbus ksibi (Fig. 5). The genetic distances found among populations are presented in Table 6. Genetic distances within Sebou, Bou Regreg, and Rifian populations and L. ksibi ranged between 0-0.6% but between these populations were 1.7-3.9%. The minimum value was found between L. ksibi and Bou Regreg populations (Table 6).

Fig. 5.— Phylogenetic tree rendered by Bayesian Inference of the cytochrome b gene. Numbers on branches indicate posterior probability values. Abbreviations of localities are defined in Table 1.
Fig. 5.— Árbol filogenético obtenido por Inferencia Bayesiana para el gen citocromo b. Los números en las ramas indican los valores de probabilidad posterior. Las abreviaturas de las localidades se muestran en la Tabla 1.

 
Table 6.— Genetic distances for complete mitochondrial cytb gene. Uncorrected genetic distances between populations are presented below diagonal. In the diagonal uncorrected genetic distances within populations are shown.
Tabla 6.— Distancias genéticas. Por debajo de la diagonal distancias genéticas no corregidas entre poblaciones para el gen mitocondrial cytb. En la diagonal distancias genéticas no corregidas dentro de poblaciones.
Laou (Rif) Hachef (Rif) Loukos (Rif) Sebou Bou Regreg
Hachef 0.0
Loukos 0.2 0.2
Sebou 3.2 3.2 3.2
Bou Regreg 3.9 3.9 3.9 3.1
L. ksibi 3.8 3.8 3.9 3.7 1.7

The distances are of similar range as those between well recognized species of cyprinid fishes (Doadrio et al., 2002, 2007a, 2007b; Doadrio & Carmona, 2003, 2006; Doadrio & Madeira, 2004; Robalo et al., 2005; Doadrio & Elvira, 2007; Domínguez-Domínguez et al., 2007, 2009). These results confirm the differences found with allozyme analyses (Machordom et al., 1998). Allozyme studies found 23 polymorphic loci, four of which (MPI, GPI-5, IDHP-2, CK) were diagnostic, with a probability criterion of 99% of correct assignment to Rifian populations with respect to the Sebou Basin. Between the Sebou Basin (Ifrane population) and Grou Basin three diagnostic loci were found (GPI-2*, GPI-5* and PGDH-1). The population of the Grou River (Bou Regreg Basin) exhibited a unique diagnostic locus (GPI-2* 118) with respect to all Luciobarbus populations (Machordom et al., 1998). Populations from Sebou, Rif and Bou Regreg basins were identified as different taxa by other authors based on the molecular differences found, but were not formally described as new so far (Machordom et al., 1998).

TAXONOMY OF LUCIOBARBUS LABIOSUS (PELLEGRIN, 1920)TOP

Initially the population from Sebou Basin in Morocco was considered to belong to Barbus setivimensis Valenciennes, 1842, which was originally described for populations of the Setif Basin in Algeria (Pellegrin, 1920). Within the Sebou population of B. setivimensis, Pellegrin (1920) found specimens with well-developed lips that this author described as a variety, B. setivimensis var. labiosa Pellegrin, 1920. This development of the lips in some specimens of the former genus Barbus sensu lato, currently within Luciobarbus, is common, and Pellegrin (1922) described another variety as Barbus massaensis var. labiosa Pellegrin, 1922. As Almaça (1968, 1970) stated, Pellegrin (1920) did not describe the var. labiosa as a subspecific category or geographic form because he found typical specimens of B. setivimensis and some specimens with more developed lips in the same locality. For this reason Article 45.6.4 of the International Code of Zoological Nomenclature is not applicable:

“45.6.4. it is subspecific if first published before 1961 and its author expressly used one of the terms “variety” or “form” (including use of the terms “var.”, “forma”, “v.” and “f.”), unless its author also expressly gave it infrasubspecific rank, or the content of the work unambiguously reveals that the name was proposed for an infrasubspecific entity, in which case it is infrasubspecific”

Subsequent molecular studies showed that populations of L. setivimensis of the Setif Basin in Algeria and those of the Sebou Basin in Morocco were not monophyletic. Thus, mitochondrial genes of species of Luciobarbus showed that L. setivimensis from the Setif Basin is a sister group of the Iberian species, while populations of L. setivimensis from the Sebou Basin were closer to North African species (Machordom & Doadrio, 2001b). For this reason, and in the absence of another valid name for the populations of the Sebou Basin, molecular studies have referred to Sebou populations as Luciobarbus labiosa (Machordom & Doadrio, 1993, 2001b; Doadrio, 1994; Geiger et al., 2014).

Hence, populations from the Sebou Basin do not have a valid specific name at the present time, and we describe here this population as a new species.

DESCRIPTION OF LUCIOBARBUS POPULATIONSTOP

The high degree of morphological and genetic differentiation of Luciobarbus populations endemic to the region of the Strait of Gibraltar in North Africa justifies the consideration of these populations as distinct species. No available name for these populations exists, and therefore three new species are described in this study.

Luciobarbus maghrebensis Doadrio, Perea & Yahyaoui, sp. nov.

urn:lsid:zoobank.org:act:3FE3F718-F050-44F5-93DC-C5ABFE3C8674

TYPE MATERIAL: Holotype: Fig. 6, Table 7. MNCN 279.718 female, 135.6 mm (SL); Ifrane River, Sebou Basin, Ouad Ifrane, Atlantic slope in Morocco (33.296957, -5.492639) (Fig. 1); 27/3/2013. Collected by (Coll.) Doadrio, I.; Garzón, P.; Yahyaoui, A; González, E. G.; Perea, S.

Paratypes: Table 7. MNCN 279.711-717, 279.719-29, 279.731, 279.733-744: Thirty-one specimens from the Ifrane River, Sebou Basin, Ouad Ifrane, Atlantic slope in Morocco (33.296957,-5.492639); 27/3/2013. Coll. Doadrio, I; Yahyaoui, A.; Garzón, P.; González, E. G.; Perea, S. MNCN 71675-697: Twenty-three specimens from Tizguit River, Sebou Basin, Ifrane, Atlantic slope in Morocco (33.549241,-5.097144). 19/4/1991. Doadrio, I; Garzón, P.

Holotype and a series of paratypes (55 specimens) have been deposited at the Fish Collection of the Museo Nacional de Ciencias Naturales, (Madrid, Spain).

SUPPLEMENTARY MATERIAL: Lectotype of Barbus setivimensis var. labiosa Pellegrin, 1920: MNHN-IC-1920-0215, Fez, Morocco. Coll. M. CH. Allaud. Paralectotypes of Barbus setivimensis var. labiosa Pellegrin, 1920: MNHN-IC-1920-0212 and MNHN-IC-1920-0214, Fez, Morocco.

DIAGNOSIS: Differs from other known species of Luciobarbus by the following combination of characters: 41-47 scales on the lateral line (x=43.7 Median=44); 7.5-8.5 (x=7.5 Median=7.5) above lateral line and 4.5-6.5 (x=5.47, Median=5.5) below lateral line. Insertion of the ventral fin is posterior to dorsal fin origin. The last single fin ray is strongly ossified and densely denticulated along its length (Append. 2-1). Postorbital length is longer than that of other studied populations. The PrOL/PsOL ratio ranged from 0.69 to 0.84 (x=0.77). In adult specimens, the lower lip is thick with a retracted medial lobe revealing the dentary. The ethmoid bone is narrower than its length. Vertebrae 41-43 (x=42.1, n=12), Gill Rakers (GR) 13-15 (x=14.1 Median=14). Differences in diagnostic characters among analyzed Luciobarbus populations are presented in Table 10.

DESCRIPTION: D IV 8, A III 5, P I 15-16, V I 8, C 18; LL 41-47 (x=43.7, Median=44), RSA 7.5-8.5 (x=7.5, Median=7.5), RSB 4.5-6.5 (x=5.4, Median=5.5). Pharyngeal teeth in adults 4.3.2/4.3.2., GR 13-15 (x=14.1 X=14), VE 41-43 (x=42.1, n=12). A medium-sized species, rarely reaching 500 mm. The body is elongated relative to maximum body depth and compared to other Luciobarbus species. The head is large with respect to the body with head length 22-28% of SL. Infraorbital bones are narrow. The first barbel did not reach the anterior edge of the eye, but, in some specimens, barbels reached the rim of the eye and extended to half the width of the eye. The second barbel usually extended beyond the posterior rim of the eye, rarely reaching the preopercle. The anterior barbel is 19.3-33.3%, and the second 21.2-41%, of HL. The lips are thick with the inferior usually retracted in adults revealing the dentary bone. In some specimens, lips are not retracted and exhibited a well-developed medial lobe. The lacrimal bone has a medium-sized manubrium. The snout is prominent, marked in some specimens, with preorbital length 7.8-10.3% of SL; postorbital length ranged from 9-13.6% SL. The iris, as in other Moroccan species of Luciobarbus is yellow pigmented at the superior border but is less conspicuous than in other species. The jugal space closes at the same plane of the vertical of the eye, and 11-12 pores were present in the inferior branch of the pre-operculum. The dorsal fin is posterior on the body with a predorsal distance of 48.2-55.8% SL. The profile of the dorsal fin is straight or slightly concave, with the last single ray ossified and profusely denticulated (Fig. 7). The caudal peduncle is slightly more elongated than that in Rifian populations, with a height of 30-39.3% SL. The height of the caudal peduncle is 1.4 to 1.98 times the length of the anal peduncle. The pectoral and ventral fins are longer in males, and the anal fin is longer in the females. Males exhibit nuptial tubercles in the preorbital space. Ventral fins are inserted forward to dorsal fin insertion. The caudal fin is 16.6-27.3% SL. Morphometric and meristic measurements for the holotype and paratypes of Luciobarbus maghrebensis are represented in Table 7. The coloration of L. maghrebensis is silver-yellowish with darker fins (Fig. 6). Some specimens exhibit a darker longitudinal band in the center of the body. Juveniles present blotches, as in other Luciobarbus species. The skull is wide with a narrow ethmoid bone and a large opercle; the pharyngeal bone is wide with a long inferior process. The lacrimal bone is well developed, and infraorbital bones are narrow. The dentary has a long anterior process, and the maxilla has a small palatine process. The basioccipital plate is wide and triangular.

ETYMOLOGY: The species name “maghrebensis” has been selected because it is mainly distributed in the northwestern area of the Maghreb region.

DISTRIBUTION: This species is endemic to north-central Morocco, inhabiting Sebou Basin and rivers flowing into the Moulay Bouselham Lagoon on the Atlantic slope (Fig. 1).

COMMON NAME: We propose using the English common name “Maghreb barbel” for this new species.

HABITAT AND BIOLOGY: The species can inhabit rivers of varying typology within its distribution range. Upstream it is substituted for the trout, and in the lower courses of rivers and calm currents it is locally highly abundant. From April to May the species migrates upstream to headwaters for spawning. The species is also present in reservoirs.

CONSERVATION: Luciobarbus maghrebensis spawning migration has been affected by dams, which present physical barriers to upstream migration. The presences of exotic species in reservoirs, as well as poor water quality in the lower courses, due to fertilizers and pesticides, have probably been primary causes of the decline in its population in recent years. No quantification of the decline in numbers is available, but the species is still abundant and thriving locally. We suggest that this species should be included in the IUCN category of Least Concern (LC).

GENETICS: Uncorrected genetic distances of mitochondrial gene cytb between Luciobarbus maghrebensis and the other analyzed species are represented in Table 6. L. maghrebensis shows 12 diagnostic positions in the cytb gene. A previous allozyme study found three diagnostic loci between L maghrebensis (GP1-2*, GP15* and PGDH-1*) and Grou population (Machordom et al., 1998).

Fig. 6.— Holotype of Luciobarbus maghrebensis from the Ifrane River, Sebou Basin, Ouad Ifrane, Morocco. MNCN 279.718.
Fig. 6.— Holotipo de Luciobarbus maghrebensis del río Ifrane, Cuenca del Sebou, en Ouad Ifrane, Marruecos. MNCN 279.718.

 
Table 7.— Morphometric and meristic measurements of the holotype and paratypes of Luciobarbus maghrebensis.
Tabla 7.— Medidas morfométricas y merísticas del holotipo y paratipos de Luciobarbus maghrebensis.
Morphometric
variables
Holotype MNCN 279718 Paratypes n=54
Measurements (mm) Range Mean Standard Deviation
SL 135.6 70-170.6 109.9 25.2
PrDD 68.8 33.4-85.7 56.8 12.2
PrPD 36.2 18.6-43.6 28.2 6.4
PrVD 75.6 40.2-93.2 59.7 14.3
PrAD 104.9 54.7-130.7 84.1 22.3
PVL 39.9 19.2-52 32.6 8.4
CPL 51.3 24.2-67.6 41.4 10.6
APL 25.2 12.1-32.9 20.5 5.0
BD 34.7 18.7-43.6 28.0 6.4
BLD 16.1 7.7-18.5 12.3 2.6
HL 33.7 17.1-38.8 26.6 5.3
PrOL 12.2 6.0-14.4.1 9.4 2.1
ED 7.7 4.2-8.2 5.7 1.1
PsOL 14.4 6.8-19.1 13.7 2.4
B1L 10.0 3.6-11.2 7.0 1.8
B2L 14.4 4.6-15.6 9.2 2.6
PFL 24.4 10.7-30.9 20.2 4.3
VFL 21.5 11.5-26 17.6 3.5
DFL 17.8 9.1-3.1 15.0 3.1
DFH 24.8 11.2-30.6 18.6 4.8
AFL 8.7 5.1-26.8 8.6 3.0
AFH 24.4 10.9-31 18.6 4.2
CFL 32.6 17.3-40.1 25.7 5.3
LL 44 41-47 43.7 1.2
RSA 7.5 7.5-8.5 7.6 0.2
RSB 5.5 4.5-6.5 5.5 0.4

Fig. 7.— Denticulated last single ray of the dorsal fin in specimen of Luciobarbus maghrebensis from the Ifrane River.
Fig. 7.— Aleta dorsal con el ultimo radio sencillo denticulado en un individuo de Luciobarbus maghrebensis del río Ifrane.

 

Luciobarbus rifensis Doadrio, Casal-Lopez & Yahyaoui, sp. nov.

urn:lsid:zoobank.org:act:F32CCBDD-7C77-4584-889E-1DAA0733AF43

TYPE MATERIAL: Holotype: Fig. 8, Table 8. MNCN 290.642; female, 177.2 mm (SL); Laou River, Laou Basin, Derdara, Chefchauen Province, Mediterranean slope in Morocco; (35.118986-5.288900) (Fig. 1); 6/6/2013. Coll: Doadrio, I; Yahyaoui, A; Casal-Lopez, M; Perea, S.

Paratypes: Table 8. MNCN 290.639-641, 290.643-652, 290.655, 290.657-663, 290.665-667: Twenty-four specimens from Laou River, Laou Basin, Derdara, Chefchaouen Province, Mediterranean slope in Morocco; (35.118986, -5.288900); 6/6/2013; Coll: Doadrio, I; Yahyaoui, A; Casal-Lopez, M.; Perea, S. MNCN 284.939-940, 284.942-945, 284.947-948, 284.950-951, 284.953-964: Twenty-two specimens from Laou River, Laou Basin, Beni Ferten, Tétouan Province, Mediterranean slope in Morocco (35.353254, -5.184840); 8/4/2007. Coll: Doadrio, I; Doadrio I jr; Perea, S. MNCN 280.162-163, 280.165, 280.168, 280.170, 280.172-174, 280.176-181, 280.183, 280.185-186; 290.671-696: Forty-three specimens from Loukos River, Loukos Basin, Souk Had, Laghdir, Chefchaouen Province, Atlantic slope in Morocco (35.02624, -5.404660) 30/10/2011. Coll: Doadrio, I; Yahyaoui, A; Casal-Lopez, M; Garzon, P. MNCN 290.707-714, 290.716-722, 290.725-731. Twenty-two specimens from Hachef River, Hachef Basin, Dar Chaoui, Tétouan Province, Atlantic slope in Morocco (35.526763, -5.713771); 6/6/2013. Coll: Doadrio, I; Yahyaoui, A; Casal-Lopez, M; Perea, S.

Holotype and a series of paratypes (112 specimens) have been deposited in the Fish Collection of the Museo Nacional de Ciencias Naturales, Madrid, Spain.

DIAGNOSIS: Differs from other known species of Luciobarbus by the following combination of characters: 42-46 scales on the lateral line (x=43.9, Median=44), 8.5-9.5 scales above lateral line (x=8.8, Median=8.5), and 3.5-5.5 scales below lateral line (x=4.7, Median=4.5). Insertions of dorsal fin and ventral fin were situated similarly on the body or the insertion of the dorsal fin is slightly anterior to the ventral fin origin. Last single fin ray is ossified and denticulated along its length. The denticulations at mid-height of the ray are shorter than the ray width. In adult specimens, the lower lip is well developed with retracted medial lobe revealing the dentary. The ethmoid bone is wider than long. Vertebrae 41-42, (x=42, n=12); gill rakers 10-15 (x=13.6 Median=13). Diagnostic characters of the studied Luciobarbus populations are presented in Table 10.

DESCRIPTION: D IV 8, A III 5, P I 15-16, V I 8, C 18. LL 42-46 (x=43.9, Median=44); RSA 8.5-9.5 (x=8.8, Median=8.5); RSB 3.5-5.5 (x=4.7, Median=4.5). Pharyngeal teeth in adults 4.3.2/4.3.2. GR 10-15 (x=13.6 Median=13); VE 41-42 (x=42 n=12). A medium-sized species that rarely reaches 500 mm. The body is short and deep in comparison with other Luciobarbus species with maximum body depth 22-28% SL. The head is large with respect to the body with head length 23.2-27.8% SL. Circumorbital bones are narrow. The barbels were long with the first barbel not reaching the anterior edge of the eye. The second barbel usually extended to the posterior edge of the eye, but did not reach the preopercle. In females, the first barbel is 14.5-36% HL and the second 20-40.3% HL. The lips are thick with the inferior usually retracted in adults making the dentary bone visible. Some specimens do not exhibit inferior lip retraction and show well developed lips (Fig. 9). The lacrimal bone has a short manubrium. The eye is placed anteriorly in the head; preorbital length is 7.1-10.6% SL, and postorbital length is 10.2-12.5% SL. The snout is characteristically rounded. The iris, as in other Moroccan species of Luciobarbus, is yellow pigmented at the superior border but is less conspicuous than in other species. The jugal spacious closes at the same vertical plane of the eye and from 11 to 12 pores were present in the inferior branch of the preopercular. The dorsal fin was located posterior on the body, with the predorsal distance being 51.2-55.9% SL. The profile of the dorsal fin was slightly concave, and presents the last single ray strongly ossified and denticulated. The caudal peduncle (CPL) is high and short with a height of 32.6-39% SL. The height of the caudal peduncle is 1.2 to 2 times the length of the anal peduncle. The pectoral and ventral fins are longer in males, and the anal fin is longer in females. Males have nuptial tubercles in the preorbital space, but not as well developed as in other Luciobarbus species. Ventral fins are inserted in the same vertical plane as the origin of the dorsal fin or slightly posterior to the dorsal fin. The length of the caudal fin is 14.9-26.5% SL. Morphometric and meristic measurements for the holotype and the paratypes of the newly described species are represented in Table 8. The coloration of L. rifensis is brown-yellowish with darker fins, with the body becoming progressively paler in the ventral region (Fig. 8). Juveniles present black blotches as in other Luciobarbus species. The skull is long and narrow with a wide ethmoid bone. Infraorbitals are narrow with a large lacrimal bone. The basioccipital plate is triangular. The palatine process of maxilla is small. The superior branch of the pharyngeal bone forms a closed angle with respect to inferior branch.

ETYMOLOGY: The species name “rifensis” has been selected because the distribution range comprises the Rifian Mountains of Morocco.

DISTRIBUTION: The new species is endemic to north Morocco, inhabiting waters from the Loukos Basin on the western Atlantic slope to the Laou Basin on the eastern Mediterranean slope (Fig. 1).

COMMON NAME: We propose the English common name “Rifian barbel” for this newly identified species.

HABITAT AND BIOLOGY: The species is ubiquitous and inhabits streams and rivers with substrata ranging from sandy to stony, being absent only in small streams near the sources of rivers and in shallow waters. The species is present in reservoirs. The spawning period is variable, but usually takes place in April and May. The species migrates upstream to spawn in cold and oxygenated waters where the females excavate a nest in the gravel.

CONSERVATION: Luciobarbus rifensis is a common species. However, its distribution area has been extensively transformed in recent years due to construction of dams, which also hamper upstream migration during the spawning period. In addition, reservoirs can harbor exotic species, some piscivorous, which could be a potential threat to barbels. The area where the species occurs has and increasing interest for tourism activities, which increases water abstraction for recreational use, leading to decreased water levels in summer as well as water oxygen depletion. The species is currently common and locally abundant. For this reason, we suggest that it should be included in the IUCN category as Least Concern (LC).

GENETICS: Uncorrected genetic distance based on mitochondrial gene cytb between Luciobarbus rifensis populations and the other analyzed populations are represented in Table 6. L. rifensis shows 6 diagnostic positions in the cytb gene. An earlier allozyme study found four diagnostic loci to L. rifensis (MPI, GPI-5, IDHP-2 and CK) with respect to Sebou populations (Machodom et al., 1998).

Fig. 8.— Holotype of Luciobarbus rifensis from Laou river, Laou Basin, in Derdara, Morocco. MNCN 290.641.
Fig. 8.— Holotipo de Luciobarbus rifensis del río Laou, Cuenca del Laou, en Derdara, Marruecos. MNCN 290.641.

 
Table 8.— Morphometric and meristic measurements of holotype and paratype series of Luciobarbus rifensis.
Tabla 8.— Medidas morfométricas y merísticas del Holotipo y Paratipos de Luciobarbus rifensis.
Morphometric
variables
Holotype MNCN 290642 Paratypes n=111
Measurement (mm) Range Mean Standard Deviation
SL 177.2 77.2-226 127.2 41.6
PrDD 90.4 41.4-122.8 69.4 22.5
PrPD 45.3 20.9-63.3 34.1 11.4
PrVD 94.6 43.4-126.2 71.2 23.1
PrAD 135.3 58.4-173.4 98.4 32.1
PVL 50.7 21.9-65.4 37.5 12.0
CPL 68.6 26.9-86.0 46.7 15.9
APL 33.2 13.2-43.5 23.6 8.3
BD 45.4 18.4-58.2 32.5 10.6
BLD 19.1 8.4-21.8 13.6 3.7
HL 41.1 19.3-56.7 31.9 10.1
PrOL 15.7 6-20.3 11.2 3.5
ED 7.0 3.7-11.4 6.6 1.9
PsOL 18.6 8-27.1 14.4 5.0
B1L 8.1 3.0-16.3 7.6 3.3
B2L 13.3 4.1-22 10.0 4.2
PFL 28.4 12.3-42.2 22.3 7.5
VFL 23.9 11.1-32.3 18.5 5.5
DFL 23.2 9.5-28.7 16.1 4.8
DFH 31.9 11.2-41.9 21.7 7.1
AFL 12.5 4.8-17.3 9.4 3.1
AFH 31.1 11.7-42.1 20.8 7.7
CFL 36.7 16.2-49.2 26.9 8.3
LL 44 42-46 43.8 0.8
RSA 9.5 8.5-9.5 8.7 0.4
RSB 5.5 3.5-5.5 4.7 0.4

Fig. 9.— Well developed lips with medial lobe in a specimen of Luciobarbus rifensis from the Loukos River on the left and lips retracted revealing dentary in one specimen of Luciobarbus rifensis from Laou River on the right.
Fig. 9.— A la izquierda un individuo de Luciobarbus rifensis del río Loukos con labios bien desarrollados y lóbulo medial. A la derecha un individuo de Luciobarbus rifensis del río Laou con los labios retraídos dejando ver el dentario.

 

Luciobarbus rabatensis Doadrio, Perea & Yahyaoui, sp. nov.

urn:lsid:zoobank.org:act:45CC4380-B532-4AEC-9050-692042FF0365

TYPE MATERIAL: Holotype: Fig. 10, Table 9. MNCN 71920, male, 129.9 mm (SL); Grou River, Bou Regreg Basin, Sebt Ait Rahhou, Atlantic slope of Morocco (33.164678, -6.366963) (Fig. 1). Coll: P. Garzón, I. Doadrio, and A. Yahyaoui. 17/04/1991.

Paratypes: MNCN 71725-746, 71918-919, 71921-928; Thirty-two specimens from the Grou River, Bou Regreg Basin, Sebt Ait Rahhou (33.164678, -6.366963) Morocco. Coll: P. Garzón, I. Doadrio and A. Yahyaoui. 17/04/1991

Holotype and the series of paratypes (33 specimens) have been deposited in the Fish Collection of the Museo Nacional de Ciencias Naturales (Madrid, Spain).

DIAGNOSIS: Differs from other known species of Luciobarbus by the following combination of characters: Number of scales on LL 45-50 (x=46.5, Median=46); number of scales above lateral line 8.5-10.5 (x=9.6, Median=9.6). Number of scales below lateral line 6.6-7.5 (x=6.7, Median=6.5). Insertion of dorsal and ventral fins is in the same vertical plane. Last single fin ray is ossified, with deep denticulations along its length. Denticulations at mid-height of the ray are equal to or longer than ray width. In adult specimens, the inferior lip is retracted revealing the dentary. The ethmoid bone is wider than its length. The maxilla showed a large palatine process. Vertebrae 41-42 (x=42, n=6); gill rakers 14-12 (x=12.9). Diagnostic characters of the analyzed Luciobarbus populations are presented in Table 10.

DESCRIPTION: D IV 8, A III 5, P I 15-16, V I 8, C 18; LL 46-50 (x=46.5, Median=46), RSA 8.5-10.5 (x=9.6, Median=9.6), RSB 6.5-7.5 (x=6.7, Median=6.5). Pharyngeal teeth in adults 4.3.2/4.3.2. GR 12-14 (x=12.9 Median=13). VE 41-42 (x=42 n=6). It is a medium-sized species that rarely reaches 500 mm. The body is slightly more elongated in comparison with L. rifensis and L. maghrebensis with maximum body depth ranging from 24.4-28.5% SL. The head is large relative to the body, similar to other Luciobarbus species, with head length 23.5-26.8% SL. The preorbital distance is short and the proportion with respect to head length is 29.2-40.5% SL. The circumorbitals bones are narrow. The barbels are similar in size to those of L. maghrebensis and L. rifensis, but, due to a shorter snout, the first barbel usually reaches the anterior edge of the eye. The second barbel usually extends to the posterior edge of the eye, but does not reach the preopercle. The anterior barbel is 22.1-26.3% HL and the second 22.3-32.8% HL. The lips of adult individuals are usually retracted, and the dentary bone is visible. The lacrimal bone has a short and high manubrium. As in other Moroccan Luciobarbus species, the iris is yellow pigmented at the superior border. The dorsal fin is placed posteriorly on the body with a predorsal lenght of 50.9-56.3% SL. The profile of the dorsal fin is concave with the last single ray ossified with pronounced denticulation. The caudal peduncle (CPL) is slightly more elongated than in L. maghrebensis and L. rifensis, with a height from 34.7 to 38% SL. The height of the caudal peduncle is 1.4 to 1.7 times the anal peduncle length. The pectoral and ventral fins are longer in males, and the anal fin is longer in females. Males present nuptial tubercles in the preorbital space. The caudal fin is long, with a lenght of 20.4-24.2% SL. Morphometric and meristic measurements for the holotype and the paratypes of the newly described species are presented in Table 9. The colour is slightly yellow, brownish in the dorsal region and more silver in the ventral area. The skull is long and narrow with the ethmoid bone wider than its length. The lacrimal bone is short. The basioccipital bone has a wide pentagonal plate. The palatine process of the maxilla is more conspicuous and the pharyngeal bone is narrower than in specimens of the other populations studied.

ETYMOLOGY: The species name “rabatensis” has been selected because its distribution area mainly comprises the Bou Regreg Basin, which flows through Rabat City.

DISTRIBUTION: This new species is endemic to north Morocco, inhabiting the Bou Regreg Basin (Fig. 1).

COMMON NAME: We propose the English common name “Rabat barbel” for this species.

HABITAT AND BIOLOGY: As other barbels of Morocco, with the exception of L. magniatlantis, L. rabatensis inhabits rivers of differing typologies. The species is present in reservoirs. Spawning takes places at the end of April and the beginning of May. At that time, individuals migrate upstream for spawning in cold and oxygenated waters where the females excavate a nest in the gravel.

CONSERVATION: The habitat of Luciobarbus rabatensis has been extensively transformed with the growth of Rabat City, urban development, water usage, increased pollution linked to agriculture, construction of dams and reservoirs, and introduction of exotic species. Although, an abundant population of this species is still found, it is suffering a slight decline. For this reason, we suggest that this species should be included in the IUCN category of Near Threatened (NT).

GENETICS: Uncorrected genetic distances between Luciobarbus rabatensis and the sister population of Luciobarbus ksibi to mitochondrial gene cytb was 1.7%. Luciobarbus rabatensis shows 6 diagnostic positions in the cytb gene. A previous allozyme study found one diagnostic locus (GPI-2* 118) with respect to other African Luciobarbus.

Fig. 10.— Holotype of Luciobarbus rabatensis from Grou River, Bou Regreg Basin, Sebt Ait Rahhou, (Morocco). MNCN 71920.
Fig. 10.— Holotipo de Luciobarbus rabatensis del río Grou, cuenca del Bou Regreg en Sebt Ait Rahhou, Marruecos. MNCN 71920.

 
Table 9.— Morphometric and meristic measurements of holotype and paratypes of Luciobarbus rabatensis.
Tabla 9.— Medidas morfometicas y merísticas del Holotipo y Paratipos de Luciobarbus rabatensis.
Morphometric variables Holotype MNCN 71920 Paratypes n=32
Measurement in mm Range Mean Standard Deviation
SL 129.9 53.1-113.6 74.8 14.5
PrDD 66.1 29.1-59.9 40.4 7.3
PrPD 33.8 14.4-30.4 19.5 4.3
PrVD 68.2 28.8-60.7 39.8 8
PrAD 96.5 39.1-84.5 55.5 10.8
PVL 34.7 14.3-30.8 20.8 4
CPL 49.5 18.9-40.5 26.8 5.4
APL 24.7 9.1-21.7 13.8 2.8
BD 31.7 14.9-28.8 16.7 3.5
BLD 15.2 6.3-14.1 8.9 1.8
HL 32.1 14.2-27.3 18.8 3.4
PrOL 12.8 4.1-11-1 6.3 1.6
ED 6.3 3.5-5.6 4.4 0.6
PsOL 16.3 6.6-13.7 9.2 1.7
B1L 8.2 3.1-6.7 4.6 0.8
B2L 9.9 4.1-8.4 5.7 1.1
PFL 25.8 11.4-22.5 15.4 2.7
VFL 21.6 9.2-18.6 12.7 2.2
DFL 16.5 7.4-15 10.1 1.9
DFH 24.5 10.3-21.9 14.3 2.8
AFL 9.3 3.7-8.1 5.2 1.1
AFH 24.3 10-21.1 13.9 2.5
CFL 26.5 12.7-24 17.1 2.7
LL 46 45-50 46.5 1.3
RSA 9.5 8.5-10.5 9.6 0.4
RSB 6.5 6.5-7.5 6.7 0.4
Table 10.— Diagnostic morphological characters for the four species studied.
Tabla 10.— Caracteres morfológicos diagnósticos para las cuatro especies estudiadas.
Last Dorsal Fin Ray Scales Origin dorsal fin Postorbital length Ethmoid bone Pharyngeal bone Infraorbitals
L. rifensis Highly ossified and densely denticulate
Denticulations are pesent most of the ray length
Denticulations are shorter than the width of the ray
LL≤46
RSA≤8.5
RSB≤5.5
Vertical to the origin of pelvic fin Short Wider than long Upper branch hooked
Lower branch wide
Lachrymal large
Infraorbital narrow
Second infraorbital large
L. maghrebensis Highly ossified and densely denticulate
Denticulations are pesent along the entire length of the ray
Denticulations are shorter than the width of the ray
LL≤46
RSA≤7.5
RSB≤5.5
Anterior to the origin of pelvic fin Large Longer than wide Upper branch not hooked
Lower branch wide
Lachrymal large
Infraorbitals narrow
Second infraorbital short
L. rabatensis Ossified with deep well-separated denticulations
Denticulations length are equal to or greater than the width of the ray
LL≥46
RSA≥5.5
RSB≥6.5
Vertical to the origin of ventral fin Short Wider than long
Lower branch thin
Upper branch not hooked
Infraorbitals narrow
Lachrymal short
Second infraorbital short
L. ksibi Ossified and feebly sawn
Denticulations are absent from the upper third of the ray
LL≤46
RSA≤8.5
RSB≤5.5
Vertical to the origin of ventral fin Short Wider than long Upper branch hooked
Lower branch wide
Pharyngeal bone robust
Lachrymal short
Infraorbitals wide
Second infraorbital short

AcknowledgmentsTOP

Many persons have participated in the field sampling trips. We warmly thank J. Cubo, M. Merino, J. L. González, P. Garzón, I. Doadrio Jr., A. Doadrio, A. Perdices, Y. Bernat, and S. El Gharbi. We would also like to thank L. Alcaraz, involved in lab work, the curator of the ichthyological collection of National Museum of the Natural Sciences (MNCN-CSIC), G. Solís and also C. Parejo for her technical assistance at the lab of non-destructive techniques with the computerized Tomography scan (CTscan) at the MNCN-CSIC. This project was funded by MESRSFC and the CNRST from Morocco to the Project N°PPR/2015/2 “Impact des changements climatiques sur la diversité génétique des poissons des eaux douces du Maroc”. Permission for fish collection was provided by the High Commissioner for Water, Forest and the Fight Against Dessertification (HCEFLCD) of Morocco.

 

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APPENDIXTOP


Appendix 1.— Kruskal-Wallis test and Non-parametric Mann-Whitney’s pairwise comparisons for all populations. Values of Kruskal-Wallis test (H) below variables. Values of Mann-Whitney test are below the diagonal. Median in the diagonal of each variable. Significant differences p<0.05 (*); p<0.01 (**). Acronyms are defined in the Material and Methods.
Apéndice 1.— Test de Kruskal-Wallis y análisis no paramétrico de Mann-Whitney para todas las poblaciones. Valores para el test de Kruskal-Wallis (H) debajo de las variables. Valores de Mann-Whitney por debajo de la diagonal. Valor de la Mediana en la diagonal de cada variable. Diferencias significativas p<0,05 (*); p<0,01 (**). Las abreviaturas están descritas en el epígrafe de Material y Métodos.
Variables Populations Rif (n=112) Sebou (n=55) Bou Regreg (n=33) L. ksibi (n=23)
SL (H=65.99**) Rif 140.46
Sebou 0.018* 106.13
Bou-Regreg <0.0001** <0.0001** 71.88
Kasab <0.0001** 0.005** 0.0006** 88.97
SL/PrDD (H=55.87**) Rif 1.876
Sebou <0.0001** 1.934
Bou-Regreg 0.005* <0.0001** 1.843
Kasab 0.206 <0.0001** 0.624 1.863
SL/PrPD (H=20.44**) Rif 3.768
Sebou <0.001** 3.682
Bou-Regreg 0.021* 0.379 3.818
Kasab 0.002** 0.8084 0.34 3.88
SL/PrVD (H=97.1**) Rif 1.793
Sebou <0.0001** 1.828
Bou-Regreg <0.0001** <0.0001** 1.87
Kasab <0.0001** <0.0001** <0.0001* 1.919
SL/PrAD (H=86.63**) Rif 1.304
Sebou 0.183 1.311
Bou-Regreg <0.0001** <0.0001** 1.346
Kasab <0.0001** <0.0001** 0.938 1.347
PrVD/PrDD (H=89.65**) Rif 1.045
Sebou 0.051 1.065
Bou-Regreg <0.0001** <0.0001** 0.981
Kasab <0.0001** <0.0001** 0.02* 0.964
SL/PVL (H=22.62**) Rif 3.474
Sebou 0.277 3.415
Bou-Regreg 0.002** <0.0001** 3.601
Kasab 0.005** <0.0001** 0.414 3.63
SL/CPL (H=41.94**) Rif 2.818
Sebou <0.0001** 2.699
Bou-Regreg 0.301 <0.0001** 2.798
Kasab 0.928 <0.0001** 0.481 2.804
SL/APL (H=19.43**) Rif 5.561
Sebou 0.648 5.587
Bou-Regreg 0.003** 0.06 5.39
Kasab <0.0001** 0.003** 0.093 5.31
CPL/BLD (H=68.72**) Rif 3.275
Sebou 0.662 3.187
Bou-Regreg <0.0001** <0.0001** 3.003
Kasab <0.0001** <0.0001** <0.0001** 2.773
APL/BLD (H=27.44) Rif 1.642
Sebou 0.008** 1.576
Bou-Regreg <0.0001** 0.205 1.546
Kasab <0.0001** 0.006 0.04* 1.495
SL/BD (H=44.26) Rif 3.999
Sebou 0.752 3.991
Bou-Regreg <0.0001** <0.0001** 3.829
Kasab <0.0001** <0.0001** 0.2001 3.75
SL/BLD (H=44.76**) Rif 9.061
Sebou 0.752 8.719
Bou-Regreg <0.0001** <0.0001** 8.378
Kasab <0.0001** <0.0001** 0.2 7.891
SL/HL (H=10.4*) Rif 3.981
Sebou 0.145 4.044
Bou-Regreg 0.89 0.107 3.992
Kasab <0.0001** <0.0001** <0.0001** 3.811
HL/PrOL (H=27.43) Rif 2.73
Sebou 0.044* 2.788
Bou-Regreg <0.0001** 0.0007** 2.98
Kasab 0.397 0.624 0.002** 2.77
HL/PsOL (H=151.5**) Rif 2.205
Sebou <0.0001** 1.606
Bou-Regreg <0.0001** <0.0001** 2.025
Kasab 0.67 <0.0001** <0.0001** 2.187
SL/PrOL (36.47**) Rif 10.965
Sebou 0.002** 11.364
Bou-Regreg <0.0001** <0.0001** 12.06
Kasab 0.701 <0.0001** <0.0001** 11.122
SL/PsOL (153.8**) Rif 8.867
Sebou <0.0001** 6.491
Bou-Regreg <0.0001** <0.0001** 8.127
Kasab 0.14 <0.0001** <0.0001** 8.622
PsOL/PrOL (H=153.9) Rif 1.248
Sebou <0.0001** 1.727
Bou-Regreg <0.0001** <0.0001** 1.462
Kasab 0.745 <0.0001** <0.0001** 1.265
SL/ED (H=51.66**) Rif 20.004
Sebou 0.936 19.71
Bou-Regreg <0.0001** <0.0001** 17.1
Kasab 0.004** 0.009** 0.303 17.37
HL/L1B (H=22.49**) Rif 4.032
Sebou 0.29 3.9
Bou-Regreg 0.546 0.011* 4.06
Kasab 0.0005** 0.0002** <0.0001** 3.545
PrO/L1B (H=16.57**) Rif 1.459
Sebou 0.114 1.419
Bou-Regreg 0.095 0.365 1.359
Kasab 0.0005** 0.001** 0.007** 1.293
HL/L2B (H=48.31**) Rif 3.154
Sebou 0.037* 3.001
Bou-Regreg 0.085 0.0001 3.29
Kasab <0.0001** <0.0001** <0.0001** 2.571
PsOL/L2B (H=122.3**) Rif 1.434
Sebou <0.0001** 1.872
Bou-Regreg 0.0003** <0.0001** 1.612
Kasab <0.0001** <0.0001** <0.0001** 1.17
HL/PFL (H=104.1**) Rif 1.43
Sebou <0.0001** 1.318
Bou-Regreg <0.0001** <0.0001** 1.221
Kasab <0.0001** <0.0001** 0.104 1.179
HL/VFL (H=133.2**) Rif 1.721
Sebou <0.0001** 1.524
Bou-Regreg <0.0001** 0.2194 1.489
Kasab <0.0001** <0.0001** <0.0001** 1.352
HL/CFL (H=78.93**) Rif 1.185
Sebou <0.0001** 1.032
Bou-Regreg <0.0001** <0.0001** 1.09
Kasab <0.0001** 0.933 0.006** 1.028
LL (H=72.21**) Rif 44
Sebou 0.1428 44
Bou-Regreg <0.0001** <0.0001** 46
Kasab 0.605 0.681 0** 44
RSA (H=145.8**) Rif 8.5
Sebou <0.0001** 7.5
Bou-Regreg <0.0001** <0.0001** 9.5
Kasab 0.0004** <0.0001** <0.0001** 8.5
RSB (H=123.7**) Rif 4.5
Sebou <0.0001** 5.5
Bou-Regreg <0.0001** <0.0001** 6.5
Kasab 0.025 <0.0001** <0.0001** 4.5

Appendix 2.— Osteological features.
Apéndice 2.— Características osteológicas.TOP

Appendix 2-1.— Last single dorsal fin ray in adult specimens (SL>120 mm) of the studied populations. A: Rifian population (Laou River). B: Sebou Basin (Ifrane River). C: Bou Regreg (Grou River). D: Luciobarbus ksibi (Kasab River).
Apéndice 2-1.— Último radio sencillo de la aleta dorsal en individuos adultos (SL>120 mm) de las diferentes poblaciones estudiadas. A: población del Rif (río Laou). B: Cuenca del Sebou (río Ifrane). C: Cuenca del Bou Regreg (río Grou). D: Luciobarbus ksibi (río Kasab).

 

Appendix 2-2.— Dorsal view of the skull of the populations under study. Arrows indicate width of the ethmoid bone. A: Rifian population (Laou River) B: Sebou Basin (Ifrane River) C: Bou Regreg (Grou River), D: Luciobarbus ksibi (Kasab River).
Apéndice 2-2.— Cráneo de las diferentes poblaciones estudiadas. Entre flechas se señala la diferente anchura del etmoides. A: población del Rif (río Laou). B: Cuenca del Sebou (río Ifrane). C: Cuenca del Bou Regreg (río Grou). D: Luciobarbus ksibi (río Kasab).

 

Appendix 2-3.— Lateral view of the skull of the studied populations. Arrows show the length of the opercular bone. A: Rifian population (Laou River). B: Sebou Basin (Ifrane River). C: Bou Regreg (Grou River). D: Luciobarbus ksibi (Kasab River).
Apéndice 2-3.— Cráneo de las diferentes poblaciones estudiadas. Entre flechas se muestra la longitud del opercular. A: población del Rif (río Laou). B: Cuenca del Sebou (río Ifrane). C: Cuenca del Bou Regreg (río Grou). D: Luciobarbus ksibi (río Kasab).

 

Appendix 2-4.— Infraorbital bones of the studied populations. A: Rifian population (Laou River). B: Sebou Basin (Ifrane River). C: Bou Regreg (Grou River). D: Luciobarbus ksibi (Kasab River). Lcr = Lacrymal. 2°-5°: Infraorbitals.
Apéndice 2-4.— Huesos infraorbitarios de las diferentes poblaciones estudiadas. A: población del Rif (río Laou). B: Cuenca del Sebou (río Ifrane). C: Bou Regreg (río Grou). D: Luciobarbus ksibi (río Kasab). Lcr: Lacrimal. 2°-5° Infraorbitales.

 

Appendix 2-5.— Pharyngeal teeth of the studied populations. The arrows show the width of the pharyngeal bone. A: Rifian population (Laou River). B: Sebou Basin (Ifrane River). C: Bou Regreg (Grou River). D: Luciobarbus ksibi (Kasab River).
Apéndice 2-5.— Dientes faríngeos de las diferentes poblaciones estudiadas. Entre flechas la anchura del hueso faríngeo. A: población del Rif (río Laou). B: Cuenca del Sebou (río Ifrane). C: Cuenca del Bou Regreg (río Grou). D: Luciobarbus ksibi (río Kasab).

 



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