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Characterization of two Synodontis (Siluriformes: Mochokidae) in the White Nile and Lake Nubia

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Elagba Mohamed University of Khartoum

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All in-text references underlined in blue are linked to publications on ResearchGate, Available from: Elagba Mohamed letting you access and read them immediately. Retrieved on: 02 May 2016 Environ Biol (2010) 88:17–23 DOI 10.1007/s10641-010-9585-1

Characterization of two Synodontis (Siluriformes: Mochokidae) catfish species in the White Nile and Lake Nubia

Elagba Haj Ali Mohamed

Received: 23 July 2008 /Accepted: 13 January 2010 /Published online: 16 March 2010 # Springer Science+Business Media B.V. 2010

Abstract I found that cluster analysis of body Keywords Allele . Genetics . Heterozygosity. Lake weight, 25 morphometric measurements and seven Nubia . Morphology . Synodontis meristic counts separated most of the population of Synodontis schall, from the Jebel Aulia area, Khar- toum along the White Nile, from the population of Lake Nubia, the southern part of a large reservoir on Introduction the River Nile at the northern borders of the Sudan, above the Aswan High Dam in Egypt. Analysis of Lake Nubia is the southern part of a large reservoir variance revealed significantly higher mean numbers established on the River Nile after the construction of of gill rakers and mandibular teeth in Lake Nubia for Aswan High Dam in Egypt in 1964. The whole S. schall and S. serrata,comparedtothetwospecies reservoir, Lake Nasir and Lake Nubia, extends ′– ′ in the White Nile. Higher numbers of anal fin rays between latitudes 20°27 23° 58 N and longitudes ′– ′ were also found in S. serratus from Lake Nubia 30°35 33°14 E through the Nubian Desert (Abu- compared to the White Nile. Females of both species Gideiri and Ali 1975). Lake Nubia has a maximum exhibited isometric growth in the White Nile and length of 190 km and an average width of about allometric growth in Lake Nubia. Females of S. schall 10 km and 1,000 km² surface area within the borders and both sexes of S. serrata in Lake Nubia had higher of the Sudan. A change in the dynamics of fish condition factors compared to individuals in the White population in the Lake was observed 20 years after its Nile. I detected differences in allele frequency of nine establishment, where the number of species dropped out of 17 loci between the populations of the two from 45 to 20, with an increase in fish size and localities. The average heterozygosity values were populations (George 1971). An increase in the annual lower for the two species from Lake Nubia compared yield of fish and in density of algal growth was also to both species in the White Nile. The inter-population observed (Dumont et al. 1984). These observations genetic distance was 0.02 for both species. This study suggested that morphological changes and divergence should be applied to other species in Lake Nubia for within species in Lake Nubia might have occurred due rational fishery management and aquaculture. to the environmental changes in their habitats. As stated by Goncalves et al. (1996); Froese and Pauly (1998) morphological change and divergence within species E. H. A. Mohamed (*) are expected to take place when fishes are exposed to Natural History Museum, Faculty of Science, new developmental and evolutionary forces that University of Khartoum, P.O. Box 321, Khartoum, Sudan determine their body forms. A change could take e-mail: [email protected] place, either through natural hybridization or the effect 18 Environ Biol Fish (2010) 88:17–23 of the environmental factors that operate in early stages mandibular barbels. To obtain the best possible of development (Nei 1987; Currens et al. 1989). discrimination between the populations of the two In the present study I compared the morphomer- species in the two sampling sites, I used multivariate istic characteristics of two sympatric : Syno- analysis- for the combined morphomertic measurement dontis schall Bloch & Schneider 1801 and Synodontis according to Sokal and Rohlf (1969). serrata Ruppell 1829 in the White Nile and Lake The meristic counts included: the number of Nubia. Synodontis schall and S. serrata are the only dorsal, pectoral, pelvic and anal fin rays- number of Synodontis species that have successfully adapted to mandibular teeth- number of gill rakers on the first the new environmental conditions in Lake Nubia, and arch and number of vertebrae. I made observations on have attained large sizes and numbers (Ali 1984). the general osteological features and vertebrae count They are important as significant components of both on skeletal preparations after boiling fish in 10% local subsistence and commercial freshwater fishery NaOH. The counts included all free vertebrae and one landings in the Sudan. I also investigated the genetic of the fused vertebrae, and excluded those that were characteristics of both species from Lake Nubia and fused to form the Webberian complex. I compared compared my results to their populations from White data between the two species and between the Nile (Mohammed 2005). populations of each species from the two sampling sites by sex. I tested difference in mean value by means of analysis of variance. In all cases I accepted Materials and methods p<0.05 as indicating statistical difference. I determined the length–weight relationship and Specimen collection type of growth by the regression formula (W=aLb), where W represents the weight, L represents the I collected 150 specimens of each of Synodontis standard length, SL, and b is an exponent with a schall −160 to 310 mm, SL- and S. serrata −160 to value always between 3 and 4, often close to three 335 mm, SL- from local fishermen at the Jebel Aulia following the procedure of Eason and Gettinby area, 45 km south of Khartoum along the White Nile. (1980). The value b≥3 indicates that the fish has They fished with a “drive-in surround net” which was grown symmetrically or isometrically (provided its usually about 150 m long by 1 m deep- made of specific gravity remains constant). Values of b<3 cotton twine with a mesh size of 5 cm. I collected indicate allometric growth; if b>3, the fish becomes another 150 specimens of each species- 160–315 mm, heavier for its length and grows larger. It is convenient SL- and 160–400 mm, SL- by the same method from to plot log weight against log length and calculate the Lake Nubia, on the river Nile at the northern borders regression line by the method of least square. The of the Sudan. regression coefficient is b and the intercept of the line with the Y-axis is log a. These coefficients differ Morphological measurements between different species and different populations within a species (Vaznetsov 1953). The length–weight I recorded body weight and 25 morphometric measure- relationship may also vary in different sexes, season, ments and seven meristic counts for all specimens (150 habitats and developmental stages. specimens of each species) following definitions in IusedFulton’s condition factor (K)- calculated from Lagler et al. (1962) and Bagenal (1978). The morpho- the formula (K=100W/Lb)- to investigate the fatness or metric measurements included: total length- standard general well-being of different populations and sexes length- head length- head width- snout length- inter- of the same species in different habitats following the orbital width- eye diameter- body depth- pre-dorsal procedure of Eason and Gettinby (1980), where, W length- pre-adipose length- pre-pelvic length- pre-anal represents the weight, L represents SL and b is the length- dorsal—to—adipose length- length of dorsal value obtained from the above length–weight formula. fin base- adipose fin length- pelvic fin length- anal fin I used cluster analysis to test for homogeneity length- length of dorsal and pectoral spines- caudal within and between populations of S. schall in the two peduncle length and depth- mouth width- length of localities following the procedure of Clifford and maxillary and the length of the outer and inner Stephenson (1975). Average linkage (between groups) Environ Biol Fish (2010) 88:17–23 19 was estimated, based on differences of the body the two sampling sites according to the procedure of weight and 25 morphometric measurements and Ayala and Kiger (1984). I used allele frequency data seven meristic. I obtained a hierarchical cluster of to calculate the inter-population genetic distance (D) individuals in a distance dendrogram using the according to Nei’s formula (Nei 1972). Statistical Package (SPSS/PC 1986).

Blood sampling and electrophoresis Results

I collected blood in a centrifuge tube from the severed Although the numbers of gill rakers, mandibular teeth caudal peduncle of 100 live specimens from Lake and vertebrae overlapped between the population of Nubia. I allowed the blood to clot and then centri- both species from the two sampling sites (Table 1) fuged it at 5,000 g for 10 min. I pipetted the serum analysis of variance revealed significantly (p<0.05) and stored it at −20°C. I prepared the haemolysate of higher numbers of gill rakers, mandibular teeth and erythrocytes from a freshly drawn heparanized blood, vertebrae in Lake Nubia. Higher numbers of anal fin centrifuged it and then washed the red cells three rays were also found in S. serrata from Lake Nubia. times in saline solution (0.9% NaCl) and then stored No significant difference was found between sexes. them at −20°C. I carried out electrophoresis within In the cluster analysis of 25 specimens of S. schall, 2 weeks of sampling. 160–310 mm- SL from the White Nile and 35 I used horizontal starch–gel electrophoresis for specimens, 160–315 mm- SL from Lake Nubia the hemoglobin and erythrocyte enzymes following the first major dichotomy separated one specimen of Lake procedure of Shaw and Prasad (1970). Detection of Nubia from the remaining pooled individuals (Fig. 1). phenotypes and nomenclature of gene loci followed The second major dichotomy grouped most speci- the standards recommended by Shaklee et al. (1990). I mens (29 specimens) from the White Nile and one analyzed serum proteins on a gradient gel (5–15%) by specimen from Lake Nubia, while the other sub- vertical slab SDS-polyachrylamide gel electrophoresis cluster included 22 specimens from the White Nile. for 5 h. I used Commassie Blue to visualize the Females of both species exhibited isometric growth general serum proteins. in the White Nile (b>3) and allometric growth in I calculated phenotype and gene frequency distri- Lake Nubia (Table 2) while males exhibited allome- butions for each locus and tested for deviation from tric growth in the two localities. The value of Fulton’s Hardy–Weinberg equilibrium within and between condition factor was higher for females of S. schall populations by contingency (χ2), according to Emery and both sexes of S. serrata from Lake Nubia. (1976). I used the genetic data for the Nile popula- Nine loci, HB*, G6PD-1*, 6PGD*, MDH-1*, tions already described in Mohammed (2005) for PGM-1*, GPI-2*, SOD*, CAT* and G3PD*of17 comparison purposes. presumptive loci scored, were polymorphic in the

I calculated average heterozygosity (He) of inves- populations of both species. The corresponding tigated loci for the population of each species from allozymes revealed the same electrophoretic patterns,

Table 1 Range and (mean) of seven meristic counts in Character S. schall S. serrata S. schall and S. serrata from the White Nile and Lake White Nile Lake Nubia White Nile Lake Nubia Nubia rays 7 (7) 7 (7) 7 (7) 7 (7) Anal fin rays 11–13 (12) 11–12 (12) 11–12 (11) 12–13 (13)* Ventral fin rays 7 (7) 7 (7) 7 (7) 7 (7) Pectoral fin rays 8–9 (9) 8–9 (9) 10 (10) 10 (10) Gill rakers 21–23 (22) 23–25 (24)* 23–25 (24)* 24–29 (26)* Mandibular teeth 27–36 (30) 20–38 (32)* 28–42 (36) 36–44 (40)* *Significant difference Vertebrae 33–36 (35) 34–36 (35) 35–40 (38) 37–39 (38) (P<0.05) 20 Environ Biol Fish (2010) 88:17–23

G6PD-1* and G3PD* was low in S. serrata and high in S. schall from Lake Nubia. The average heterozygosity value of 0.15 was observed in the population of S. schall and 0.16 in S. serrata from Lake Nubia compared to the value of 0.26 for both species from the White Nile. Nei’s inter- population genetic distance was D=0.022 for S. schall and D=0.019 for S. serrata.

Discussion

The present results must be interpreted within the context of other changes observed in these species such as the differences in the morphological charac- teristics (Mohammed 1990) and the increase of sizes and numbers (Ali 1980, 1987) in Lake Nubia. The same observations were recorded by Goncalves et al (1996); Froese and Pauly (1998) in anadromous fishes. But it is not easy to determine exactly the environmental factors behind these differences. Variation in length–weight relationship and mor- phology was also recorded for fish species from geographically distinct revrine drainages (Colless 1980; Galman and Avtalion 1982; Goncalves et al. 1996; Jerry and Cairns 1998). Since the body form of the fish is determined both genetically and environ- mentally (Colless 1980; Jerry and Cairns 1998), the morphological differences between the populations of the two localities might be an evolutionary response to environmentally induced changes that lead to divergence from original phenotypes (Beacham 1990; Papaconstantinou et al. 1992; Fleming et al. Fig. 1 A cluster dendrogram based on body weight, morpho- 1994; Stergiou and Politou 1995). This may occur logical measurements and meristic counts of Synodontis schall because the fish will be exposed to new developmen- from the White Nile (open circle) and Lake Nubia (filled circle), using average linkage (between groups) method tal and evolutionary forces that may shape their phenotypes (Currens et al. 1989). The results could also be interpreted in a previous context of cline where two alleles were observed for each locus. The variation, which was affected by the onset of the new G6PD-2*, MDH-2*, PGM-2*, GPI-1*, ALB*, HP*, lakustrine conditions and change in environmental TF* and CP* loci were monomorphic. Allele fre- conditions. The effect was generalized and not quencies at the polymorphic loci for both species restricted, because it was detected in the two species. from Lake Nubia were compared with allele frequen- The differences observed could also be interpreted cy data reported by Mohammed (2005) in the White in terms of selection pressures that took place since Nile (Table 3). The frequency of allele A of HB*, the appearance of Lake Nubia more than 40 years MDH-1*, GPI-2*, and CAT* was low for both species ago. This might have been strong enough for in Lake Nubia and allele A of 6PGD*, PGM-1* and successful interaction of underlying genotypes with SOD* was high for S. serrata and low for S. schall the new environmental conditions to produce pheno- from Lake Nubia compared to White Nile. Allele A of types with higher fitness, during such short period of Environ Biol Fish (2010) 88:17–23 21

Table 2 Length-weight relationship and type of growth in the populations of S. schall and S. serrata of the White Nile and Lake Nubia, according to sex

Species Standard length range (mm) Body weight range (g) Regression equationa Fulton’s(Kb) Growth type

S. schall (WN) Males 160–290 125–800 W=0.21 L2.282 3.19 Allometric : Females 160–310 115–1,116 W¼7:7 10 6 L3 25 2.25 Isometric S. schall (LN) Males 160–300 440–1,350 W=0.015 L1.91 3.16 Allometric Females 160–315 515–1,460 W=0.013 L1.95 2.92 Allometric S. serrata (WN) : Males 160–315 120–630 W¼7:4 10 6 L2 32 2.14 Allometric : Females 160–335 90–555 W¼2:7 10 3 L3 27 2.50 Isometric S. serrata (LN) Males 160–315 800–1,300 W=0.049 L1.69 3.05 Allometric Females 305–400 700–1,350 W=0.22 L1.83 3.20 Allometric a W=aLb b (K)=100W/Lb time. However, the increase in the number of teeth Low value of heterozygosity reflected less advantage and gill rakers might, probably, indicate that these of heterozygous individuals in LN. Reduction in species have gradually changed their feeding habits heterozygosity is known to exist when the habitat is from herbivorous to carnivorous. disturbed (Jean et al. 1996) and such disturbance is

Table 3 Allele frequencies at nine polymorphic loci for Gene Locus Genotype Allele frequency S. schall and S. serrata from a the White Nile and Lake White Nile Lake Nubia Nubia S. schall S. serrata S. schall S. serrata

HBa A 0.56 0.62 0.52 0.51 B 0.44 0.38 0.48 0.49 G6PD-1a A 0.50 0.57 0.52 0.52 B 0.50 0.43 0.48 0.48 6PGDa A 0.52 0.31 0.46 0.33 B 0.48 0.69 0.54 0.67 MDH-1a A 0.54 0.54 0.44 0.37 B 0.46 0.46 0.56 0.63 PGM-1a A 0.55 0.47 0.40 0.49 B 0.45 0.53 0.60 0.51 GPI-2a A 0.57 0.51 0.39 0.41 B 0.43 0.49 0.61 0.59 SODa A 0.53 0.62 0.44 0.75 B 0.47 0.38 0.56 0.25 CATa A 0.59 0.55 0.42 0.42 B 0.41 0.45 0.58 0.58 G3PDa A 0.53 0.54 0.59 0.53 a Source, Mohammed B 0.47 0.46 0.41 0.47 (2005) 22 Environ Biol Fish (2010) 88:17–23 thought to be related to a frequent local extinction and Ali MT (1987) On the fisheries and biology of four recolonization (Fleming et al. 1994). Low heterozy- commercially important fish species from Lake Nubia. Ph.D thesis, University of Khartoum gosity values may also derive from stochastic fluctua- Ayala FJ (1982) Population and evolutionary genetics, a primer. The tions or from past demographic events such as strong Benjamin Cummings Publishing Company Inc, California bottlenecks or founder effects. However, individuals of Ayala FJ, Kiger JA (1984) Modern genetics, 2nd edn. The both species successfully survived the new environ- Benjamin Cummings Publihing Company Inc, California Bagenal TB (1978) Methods for assessment of fish production mental conditions and reproduced in Lake Nubia. in freshwater, 3rd edn. Blackwell, Oxford Natural selection was a factor responsible for change Beacham TD (1990) A genetic analysis of meristic and and shift in allele frequencies among the populations of morphometric variation in chum salmon (Oncorhynchus the two localities. Factors such as mutation, gene flow keta) at three different temperature. Ca J Zool 6:225–229 Clifford HT, Stephenson W (1975) An introduction to were unlikely the causes of differences observed numerical classification. Academic, New York because heritable mutation is a rare event and needs Colless DH (1980) Congruence between morphological and long time to manifest itself (Emery and Muller 1988). allozyme data for Menidia species, a reappraisal. Sys Zool Moreover, drift forces and natural selection usually 29:288–299 Currens KP, Sharpe CS, Hjort R, Schreck CB, Li HW (1989) affect mutations. Gene flow was excluded as a cause of Effects of different regimes on the morphometrics of change because, of absence of any other water drainage chinook salmon (Oncorhynchus tshawytscha) and rainbow connected to the Nile-Lake Nubia system. There might trout (O. mykiss). Copeia 1989:689–695 be certain amount of assortative mating besides the Dumont H, Moghrapy AI, Desougi LA (1984) Limnology and marine biology in the Sudan. Dr. W Junk Publisher, The random mating, going on simultaneously, since there is Hague an increase of homozygous individuals in Lake Nubia. 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Investi- Sci 51:2808–2824 gation of other species might support the effect of the Froese R, Pauly D (1998) Fishbase: concepts, design and data environmental changes on the Nile fishes, and deter- sources. Naga, 293 pp mine whether change detected in Synodontis is a Galman OR, Avtalion RR (1982) A preliminary investigation of the characteristics of red Tilapia from the Philippine and general attribute of fish in Lake Nubia. Nonetheless, Taiwan. International symposium on Tilapia Aquaculture, a good correspondence between biochemical and Philippine, pp 291–301 morphological characters is expected (Shaklee and George TT (1971) Preliminary account of the fish of Lake Tamaru 1981; Kelsch and Hendricks 1986). More Nubia during 1967. 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