Aquatic Ecology

, Volume 32, Issue 3, pp 217–227 | Cite as

Speciation of endemic Lake Tana barbs (Cyprinidae, Ethiopia) driven by trophic resource partitioning; a molecular and ecomorphological approach

  • Ferdinand A. Sibbing
  • Leo A.J. Nagelkerke
  • René J.M. Stet
  • Jan W.M. Osse
Article

Abstract

A unique species flock of large barbs (Barbus spp.) from Lake Tana is presented, from the level of fish stocks to molecules. Evidence is given for the species status of 14 morphotypes of large barbs. They distinctly differ in: (1) head and body morphometrics, (2) food preferences, (3) distribution patterns, (4) maximal body size, (5) spawning area and period, and (6) molecular genetic characters. Most types show early morphological divergence at small size. Major Histocompatibility Complex (MHC) genes, encoding cell membrane proteins involved in defence against pathogens, were found to be diagnostic for the species' genetic identity. A strong selective pressure on particular amino acid positions in the MHC protein sequence most probably arose in response to different pathogen loads from the newly invaded ecological niches after formation of Lake Tana, ca. two million years ago.

Arguments for a sympatric origin of this species flock are discussed. An evolutionary scenario suggests a riverine ancestral Barbus intermedius invading Lake Tana after its formation by volcanic blocking of the Blue Nile river and its isolation by waterfalls. Specialisation for particular food types and disruptive selection on many feeding structures are hypothesized as the evolutionary drive in speciation. The causal relationship between the diversity in feeding structures and food types is explained from experiments and models. As an example, the potential food niche of three barb species is predicted from parameter values measured from a large set of feeding structures and tested against the actual gut contents. The co-occurrence of eight piscivorous barb species is unique for cyprinid fish, which lack oral jaw teeth and a stomach. The significance of this aquatic ecosystem as a multidisciplinary evolutionary laboratory and the need for a wise balance between exploitation and conservation is stressed.

ecomorphology evolution feeding fish stocks major histocompatibility complex molecular genetics species flock 

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References

  1. Alekseyev SS, Dgebuadze YuYu, Mina MV and Mironovsky AN (1996) Small ‘large barbs’ spawning in tributaries of Lake Tana: what are they? Folia Zool 45 (Suppl. 1): 85-96Google Scholar
  2. Banister KE (1973) A revision of the large Barbus(Pisces, Cyprinidae) of East and Central Africa. Studies on African Cyprinidae, part 2. Bull Br Mus nat Hist (Zool) 26: 1-148Google Scholar
  3. Barel CDN (1983) Towards a constructional morphology of cichlid fishes (Teleostei, Perciformes). Neth J Zool 33: 357-424Google Scholar
  4. Barel CDN, Ligtvoet W, Goldschmidt T, Witte F and Goudswaard P C (1991) The haplochromine cichlids in Lake Victoria: an assessment of biological and fisheries interests. In: Cichlid fishes. Behaviour, ecology and evolution. In: Keenleyside MHA (ed.), Fish & Fisheries series 2. Chapman & Hall, London, pp. 258-279Google Scholar
  5. Bernatchez L, Vuorinen JA, Bodaly RA and Dodson JL (1996) Genetic evidence for reproductive isolation and multiple origins of sympatric trophic ecotypes of whitefish (Coregonus). Evolution 50: 624-635Google Scholar
  6. Berrebi P and Ráb P (1998) Barbus intermediusspecies flock in Lake Tana (Ethiopia) III. Cytogenetics and molecular genetics data. Italian J Zool (in press)Google Scholar
  7. Bini G (1940) I pesci del Lago Tana. Missione di Studio al Lago Tana richerge limnologiche. B. Chimicae Biologica, vol. 3, Reale Accademia d'Italia 18: 137-179Google Scholar
  8. Boulenger GA (1902). Descriptions of new fishes from the collection made by Mr. E. Degen in Abyssinia. Ann Mag N Hist Ser 7, 10: 421-437Google Scholar
  9. Boulenger GA (1907). Zoology of Egypt: Fishes of the Nile. Published for the Egyptian government. Hugh Rees, London, 578 ppGoogle Scholar
  10. Dgebuadze YuYu (1995) The land/inland-water ecotones and fish population of Lake Valley (West Mongolia). Hydrobiologia 303: 235-245Google Scholar
  11. Dixon B, Nagelkerke LAJ, Sibbing FA, Egberts E and Stet RJM (1996). Evolution of MHC class II ß chain-encoding genes in the Lake Tana barbel species flock (Barbus intermediuscomplex). Immunogenetics 44: 419-431Google Scholar
  12. Eldredge N (1985) Unfinished synthesis. Oxford University Press, Oxford, 237 ppGoogle Scholar
  13. Golubtsov AS and Krysanov EYu (1993) Karyological study of some cyprinid species from Ethiopia. The ploidy differences between large and small Barbusof Africa. J Fish Biol 42: 445-455Google Scholar
  14. Greenwood PH (1984) What is a species flock? In: Echelle, AA and Kornfield, I (eds), Evolution of fish species flocks. University of Maine at Orono Press, Orono, Maine, pp. 13-19Google Scholar
  15. Hofer R (1988) Morphological adaptations of the digestive tract of tropical cyprinids and cichlids to diet. J Fish Biol 33: 399-408Google Scholar
  16. Klein D, Ono H, O'hUigin C, Vincek V, Goldschmidt T and Klein J (1993) Extensive MHC variability in cichlid fishes of Lake Malawi. Nature 364: 330-334Google Scholar
  17. Kondrashov AS and Mina MV (1986) Sympatric speciation: when is it possible? Biol J Linn Soc 27: 201-223Google Scholar
  18. Kornfield I and Carpenter KE (1984) Cyprinids of Lake Lanao, Philippines: taxonomic validity, evolutionary rates and speciation scenarios. In: Echelle, A.A. and Kornfield, I. (eds),Evolution of fish species flocks. University of Maine at Orono Press, Orono, Maine, pp. 69-83Google Scholar
  19. Krysanov EYu and Golubtsov AS (1996) Karyotypes of some Ethiopian Barbusand Varicorhinusfrom the Nile basin including Lake Tana morphotypes. Folia Zool 45 (Suppl. 1): 67-75Google Scholar
  20. Leeuwen JL van and Muller M (1984) Optimum sucking techniques for predatory fish. Trans Zool Soc Lond 37: 137-169Google Scholar
  21. Lévêque C (1995) Role and consequences of fish diversity in the functioning of African freshwater ecosystems: a review. Aquat Living Res 8: 59-78Google Scholar
  22. Meyer A (1987) Phenotypic plasticity and heterochrony in Cichlasoma managuense(Pisces, Cichlidae) and their implications for speciation in cichlid fishes. Evolution 41: 1357-369Google Scholar
  23. Meyer A (1993) Phylogenetic relationships and evolutionary processes in East African cichlid fishes. Trends Ecol Evol 8: 279-284Google Scholar
  24. Mina MV (1992) Microevolution of fishes. Russian translation series 79. A.A. Balkema, Rotterdam, 215 ppGoogle Scholar
  25. Mina MV, Mironovsky AN and Dgebuadze YuYu (1996) Lake Tana large barbs: phenetics, growth and diversification. J Fish Biol 48: 383-404Google Scholar
  26. Mohr PA (1962) The geology of Ethiopia. University college of Addis Ababa Press, Addis Ababa, 268 ppGoogle Scholar
  27. Muller M and Osse JWM (1984) Hydrodynamics of suction feeding in fish. Trans zool Soc Lond 37: 51-135Google Scholar
  28. Nagelkerke LAJ (1997) The barbs of Lake Tana, Ethiopia: morphological diversity and its implications for taxonomy, trophic resource partitioning and fisheries. PhD thesis, Agricultural University, Wageningen, The Netherlands, 296 ppGoogle Scholar
  29. Nagelkerke LAJ and Sibbing FA (1996a) Reproductive segregation among the Barbus intermediuscomplex of Lake Tana, Ethiopia. An example of intralacustrine speciation? J Fish Biol 49: 1244-1266Google Scholar
  30. Nagelkerke LAJ and Sibbing FA (1996b) Efficiency of feeding on zebra mussel (Dreissena polymorpha) by common bream (Abramis brama), white bream (Blicca bjoerkna) and roach (Rutilus rutilus): the effects of morphology and behavior. Can J Fish Aquat Sc 53: 2847-2861Google Scholar
  31. Nagelkerke LAJ and Sibbing FA (1997) A revision of the large barbs (Barbusspp., Cyprinidae, Teleostei) of Lake Tana, Ethiopia, with a description of seven new species. In: The barbs of Lake Tana, Ethiopia: morphological diversity and its implications for taxonomy, trophic resource partitioning and fisheries: 105-170. PhD thesis, Agricultural University, Wageningen, The Netherlands, 296 ppGoogle Scholar
  32. Nagelkerke LAJ, Sibbing FA, van den Boogaart JGM, Lammens EHRR and Osse JWM (1994) The barbs (Barbusspp.) of Lake Tana: a forgotten species flock? Env Biol Fish 39: 1-22Google Scholar
  33. Nagelkerke LAJ, Mina MV, Wudneh T, Sibbing, FA and Osse JWM (1995a) In Lake Tana, a unique fish fauna needs protection. Bioscience 45: 772-775Google Scholar
  34. Nagelkerke LAJ, Sibbing FA and Osse JWM (1995b) Morphological divergence during growth in the large barbs (Barbusspp.) of Lake Tana, Ethiopia. Neth J Zool 45: 431-454Google Scholar
  35. Osse JWM, Sibbing FA and van den Boogaart JGM (1997) Intraoral food manipulation of carp and other cyprinids: adaptations and limitations. Acta Physiol Scand 161 (Suppl.638): 47-57Google Scholar
  36. Ricklefs RE and Miles DB (1994) Ecological and evolutionary inferences from morphology: an ecological perspective. In: Wainwright, P.C. and S.M. Reilly (eds.), Ecological morphology University of Chicago Press, Chicago, 13-41 ppGoogle Scholar
  37. Rüppell E (1836) (Neuer Nachtrag von) Beschreibungen und Abbildungen neuer Fische im Nil entdeckt. Museum Senckenbergianum, Abhandlungen aus dem Gebiete der Beschreibenden Naturgeschichte 2: 1-28Google Scholar
  38. Sibbing FA (1988) Specializations and limitations in the utilization of food resources by the carp, Cyprinus carpio: a study of oral food processing. Env Biol Fish 22: 161-178Google Scholar
  39. Sibbing FA (1991a) Food capture and oral processing. In: Winfield, I.J. and Nelson, J.S. (eds.), Cyprinid fishes: systematics, biology and exploitation. Chapman & Hall, London, pp. 377-412Google Scholar
  40. Sibbing FA (1991b) Food processing by mastication in cyprinid fish. In: Vincent, J.F.V. and Lillford, P.J. (eds) Feeding and the texture of food. SEB Seminar series 43. Cambridge University Press, Cambridge, pp. 57-92Google Scholar
  41. Sibbing FA, Osse JWM and Terlouw A (1986) Food handling in the carp (Cyprinus carpio): its movements patterns, mechanisms and limitations. J Zool Lond (A) 210: 161-203Google Scholar
  42. Sibbing FA, Nagelkerke LAJ and Osse JWM (1994) Ecomorphology as a tool in fisheries: identification and ecotyping of Lake Tana barbs (Barbus intermediuscomplex), Ethiopia. Neth J Agr Sc 42: 77-85Google Scholar
  43. Stearns SC (1989) The evolutionary significance of phenotypic plasticity. BioScience 39: 436-445Google Scholar
  44. Wainwright PC and Richard BA (1995) Predicting patterns of prey use from morphology of fishes. Env Biol Fishes 44: 97-113Google Scholar
  45. Werner EE (1974) The fish size, prey size, handling time relation in several sunfishes and some implications. J Fish Res Bd Can 31: 1531-1536Google Scholar
  46. West-Eberhard MJ (1989). Phenotypic plasticity and the origin of diversity. Ann Rev Ecol Syst 20: 249-278Google Scholar
  47. Witte F, Barel CDN and Hoogerhoud RJC (1990) Phenotypic plasticity of anatomical structures and its ecomorphological significance. Neth J Zool 40: 278-298Google Scholar
  48. Wudneh T (1998) Biology and management of the fish stocks in Bahir Dar Gulf, Lake Tana, Ethiopia. PhD Thesis, Agricultural University, Wageningen, The Netherlands, 143 ppGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • Ferdinand A. Sibbing
    • 1
  • Leo A.J. Nagelkerke
    • 1
  • René J.M. Stet
    • 1
  • Jan W.M. Osse
    • 1
  1. 1.Wageningen Institute of Animal Sciences (WIAS)Agricultural University, Experimental Zoology Group, Cell Biology and Immunology GroupWageningenThe Netherlands

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