Home Life Sciences Comparison of molecular and morphometric analysis in species discrimination of larvae among five cyprinids from the subfamily Leuciscinae: A tool for sustainable conservation of riverine ichthyofauna
Article
Licensed
Unlicensed Requires Authentication

Comparison of molecular and morphometric analysis in species discrimination of larvae among five cyprinids from the subfamily Leuciscinae: A tool for sustainable conservation of riverine ichthyofauna

  • Lech Kirtiklis EMAIL logo , Katarzyna Palińska-Żarska , Sławomir Krejszeff , Krzysztof Kupren , Daniel Żarski , Dorota Fopp-Bayat and Aleksandra Szabelska
Published/Copyright: November 23, 2016
Become an author with De Gruyter Brill

Abstract

Fish species from the subfamily Leuciscinae are one of the most abundant and ecologically valuable among riverine cyprinids of Central Europe. In order to support their recruitment or properly manage the restocking operations, there is a need to recognize the recruitment success which relies on the necessity of proper species discrimination among the larvae of those species caught on the spawning and/ or nursery grounds. In the present study a comparative analysis of the morphological and molecular (PCR-RFLP technique with two restriction endonucleases HinfI and TaqI based on mitochondrial DNA fragment encoding cytochrome b) techniques for identification of the species status among larvae of five cyprinid species, the ide (Leuciscus idus), common dace (Leuciscus leuciscus), asp (Leuciscus aspius), roach (Rutilus rutilus) and the European chub (Squalius cephalus) was performed. It was shown that the application of morphometric features solely could create many ambiguities in species discrimination. The use of applied molecular techniques was found to be a great support for the larvae identification, regardless the developmental stage of the fish. Moreover, this molecular method may also be used for the identification of the species even if the preserved fish (e.g., in ethanol), having usually deformed and/ or shrunk body caused by preservation, are about to be investigated.

Acknowledgements

The authors would like to thank Prof. Małgorzata Jankun (UWM, Olsztyn) for carefully reading of the manuscript and giving some valuable comments. The study was supported by the project no. 0208.806 from the University of Warmia and Mazury in Olsztyn, Poland and by the project “Innovations in finfish aquaculture with special reference to reproduction” (acronym: InnovaFish), (OR14-61724-OR1400003/09/10/11).

References

Abe K.T., Mariguela T.C., Avelino G.S., Foresti F. & Oliveira C. 2014. Systematic and historical biogeography of the Bryconidae (Ostariophysi: Characiformes) suggesting a new rearrangement of its genera and an old origin of Mesoamerican ichthyofaunal. BMC Evol. Biol. 14 152. 10.1186/ 1471-2148-14-15210.1186/1471-2148-14-152Search in Google Scholar PubMed PubMed Central

Barinova A., Yadrenkina E., Nakajima M. & Taniguchi M. 2004. Identification and characterization of microsatellite DNA markers developed in ide Leuciscus idus and Siberian roach Rutilus rutilus. Mol. Ecol. Notes 4 (1): 86–88. 10.1046/j.1471-8286.2003.00577.x10.1046/j.1471-8286.2003.00577.xSearch in Google Scholar

Braithwaite V.A. & Salvanes A.G.V. 2010. Aquaculture and restocking: implications for conservation and welfare. Anim. Welfare 19 (2): 139–149.10.1017/S0962728600001391Search in Google Scholar

Brander K. 2001. Modelling the timing of plankton production and its effect on recruitment of cod ( Gadus morhua). ICES J. Mar. Sci. 58 (5): 962–966. 10.1006/jmsc.2001.108610.1006/jmsc.2001.1086Search in Google Scholar

Briolay J., Galtier N., Brito R. M. & Bouvet Y. 1998. Molecular phylogeny of Cyprinidae inferred from cytochrome b DNA sequences. Mol. Phylogenet. Evol. 9 (1): 100–108. 10.1006/mpev.1997.044110.1006/mpev.1997.0441Search in Google Scholar PubMed

Burrow J.F., Horwood J.W. & Pitchford J.W. 2011. The importance of variable timing and abundance of prey for fish larval recruitment. J. Plankton Res. 33 (8): 1153–1162. 10.1093/plankt/fbr01510.1093/plankt/fbr015Search in Google Scholar

Chakraborty A., Aranishi F. & Iwatsuki Y. 2006. Genetic differences among three species of the genus Trichiurus (Perciformes: Trichiuridae) based on mitochondrial DNA analysis. Ichthyol. Res. 53 (1): 93–96. 10.1007/s10228-005-0313-310.1007/s10228-005-0313-3Search in Google Scholar

Copp G.H. 1992. Comparative microhabitat use of cyprinid larvae and juveniles in a lotic floodplain channel. Environ. Biol. Fish. 33 (1): 181–193. 10.1007/BF0000256310.1007/978-94-011-2544-4_16Search in Google Scholar

Geiger M.F., Herder F., Monaghan M.T. & Almada V., Barbieri R., Bariche M., Berrebi P., Bohlen J., Casal-Lopez M., Delmastro G.B., Denys G.P., Dettai A., Doadrio I., Kalogianni E., Kärst H., Kottelat M., Kovačić M., Laporte M., Lorenzoni M., Marčić Z., Özuluğg M., Perdices A., Perea S., Persat H., Porcelotti S., Puzzi C., Robalo J., Šanda R., Schneider M., Šlechtová V., Stoumboudi M., Walter S. & Freyhof J. 2014. Spatial heterogeneity in the Mediteranean Biodiversity Hotspot affects barcoding accuracy of its freshwater fishes. Mol. Ecol. Resour. 14 (6): 1210–1221. 10.1111/17550998.1225710.1111/1755-0998.12257Search in Google Scholar PubMed

Gisbert E. 1999. Early development and allometric growth patterns in Siberian sturgeon and their ecological significance. J. Fish Biol. 54 (4): 852–862. 10.1111/j.1095-8649.1999.tb02037.x10.1111/j.1095-8649.1999.tb02037.xSearch in Google Scholar

Gisbert E., Asgari R., Rafiee Gh., Agh N., Eagderi S., Eshaghzadeh H. & Alcaraz C. 2014. Early development and allometric growth patterns of beluga Huso huso (Linnaeus, 1758). J. Appl. Ichthyol. 30 (6): 1264–1272. 10.1111/jai.1261710.1111/jai.12617Search in Google Scholar

Gleason L.U. & Burton R.S. 2012. High-throughput molecular identification of fish eggs using multiplex suspension bead arrays. Mol. Ecol. Resour. 12 (1): 57–66. 10.1111/j.17550998.2011.03059.x10.1111/j.1755-0998.2011.03059.xSearch in Google Scholar PubMed

Gómez M.I., Sánchez S. & Fuentes C.M. 2014. Shrinkage of Prochilodus lineatus (Valenciennes, 1847) larvae preserved in either ethyl-alcohol or formalin in relation to their developmental stage and feeding condition. J. Appl. Ichthyol. 30 (1): 140–144. 10.1111/jai.1230810.1111/jai.12308Search in Google Scholar

Gozlan R.E., Copp G.H. & Tourenq J.N. 1999. Comparison of growth plasticity in the laboratory and field, and implications for the onset of juvenile development in sofie, Chondrostoma toxostoma Environ. Biol. Fish. 56 153–165. 10.1007/978-94-017-3678-7 1110.1007/978-94-017-3678-7_11Search in Google Scholar

Hall T.A. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41 95–98.Search in Google Scholar

HELCOM 2011 Salmon and Sea Trout Populations and Rivers in the Baltic Sea – HELCOM assessment of salmon (Salmo salar) and sea trout (Salmo trutta) populations and habitats in rivers flowing to the Baltic Sea. B. S. E. P. 126A. Helsinki Commission, Baltic Marine Environment Protection Commission, 79 pp.Search in Google Scholar

Humphries P., Richardson A., Wilson G. & Ellison T. 2013. River regulation and recruitment in a protracted-spawning riverine fish. Ecol. Appl. 23 (1): 208–225. 10.1890/11-2255.110.1890/11-2255.1Search in Google Scholar PubMed

Kamler E. & Wolnicki J. 2006. The biological background for the production of stocking material of 11 European rheophilic cyprinids. A review. Arch. Hydrobiol. (Suppl.) 158 (4): 667–687. 10.1127/lr/16/2006/66710.1127/lr/16/2006/667Search in Google Scholar

Kirtiklis L., Boroń A., Ptasznik P., Luskova V. & Lusk S. 2011. Molecular differentiation of three loach species (Pisces, Cobitidae) based on the nuclear 5S rDNA marker. Folia biol. – Krakow 59 (3-4): 141–145. 10.3409/fb59 3-4.141-14510.3409/fb59_3-4.141-145Search in Google Scholar PubMed

Kirtiklis L., Grzymkowska M. & Boroń A. 2013. Characterization of three species from the subfamily Leuciscinae (Pisces, Cyprinidae) using the nuclear ITS-1 rDNA spacer. Folia Biol. – Krakow 61 (1-2): 53–57. 10.3409/fb59 3-4.141-14510.3409/fb61_1-2.53Search in Google Scholar PubMed

Kirtiklis L., Żarski D., Krejszeff S. & Kupren K. 2012. Molecular technique support for the species identification of larvae between the ide Leuciscus idus and the common dace Leuciscus leuciscus (Teleostei, Cypriniformes), pp. 33–36. In: Kucharczyk D. (eds), Domestication in Finfish Aquaculture, ElSet, 23.–25.10.2012 Olsztyn and Mrąagowo, 124 pp. ISBN: 978-8362863-31-0Search in Google Scholar

Knebelsberger T., Dunz A.R., Neumann D. & Geiger M.F. 2015. Molecular diversity of Germany’s freshwater fishes and lampreys assessed by DNA barcoding. Mol. Ecol. Resour. 15 562–572. 10.1111/1755-0998.1232210.1111/1755-0998.12322Search in Google Scholar PubMed

Ko H-L., Wang Y-T., Chiu T-S., Lee M-A., Leu M-Y., Chang K-Z., Chen W-Y. & Shao K-T. 2013. Evaluating the accuracy of morphological identification of larval fishes by applying DNA barcoding. PLoS One 8 (1): e53451. 10.1371/jour-nal.pone.005345110.1371/journal.pone.0053451Search in Google Scholar PubMed PubMed Central

Kottelat M. & Freyhof J. 2007. Handbook of European Freshwater Fishes. Kottelat, Cornol and Freyhof, Berlin, 646 pp. ISBN: 978-2-8399-0298-4Search in Google Scholar

Koumoundouros G., Divanach P. & Kentouri M. 1999. Ontogeny and allometric plasticity of Dentex dentex (Osteichthyes: sparidae) in rearing conditions. Mar. Biol. 135 (3): 561–572. 10.1007/s00227005065710.1007/s002270050657Search in Google Scholar

Kováč V. 1994. Early ontogeny of three Gymnocephalus species (Pisces: Percidae): reflections on the evolution of the genus. Environ. Biol. Fish. 40 (3): 241–253. 10.1007/BF0000 251110.1007/BF00002511Search in Google Scholar

Krejszeff S., Targońska K., Żarski D. & Kucharczyk D. 2009. Domestication affects spawning of the ide (Leuciscus idus)-preliminary study. Aquaculture 295 (1-2): 145–147. 10.1016/j.aquaculture.2009.06.03210.1016/j.aquaculture.2009.06.032Search in Google Scholar

Krejszeff S., Targońska K., Zarski D. & Kucharczyk D. 2010. Artificial reproduction of two different spawn-forms of the chub. Reprod. Biol. 10 (1): 67–74. 10.1016/S1642-431X(12)60038-210.1016/S1642-431X(12)60038-2Search in Google Scholar

Kress W.J., Garcia-Robledo C., Uriarte M. & Erickson D.L. 2015. DNA barcodes for ecology, evolution, and conservation. Trends Ecol. Evol. 30 (1): 25–35. 10.1016/j.tree. 2014.10.00810.1016/j.tree.2014.10.008Search in Google Scholar PubMed

Kruk A. & Penczak T. 2013. Natural regeneration of fish assemblages in the Pilica River after a reduction of point-source pollution. River Res.Appl. 29 502–511. 10.1002/rra.256210.1002/rra.2562Search in Google Scholar

Kucharczyk D., Targońska K., Żarski D., Kujawa R. & Mamcarz A. 2008. A review of the reproduction biotechnology for fish from the genus Leuciscus. Arch. Pol. Fish. 16 (4): 319–340. 10.2478/s10086-008-0021-510.2478/s10086-008-0021-5Search in Google Scholar

Kupren K., Mamcarz A. & Kucharczyk D. 2011. Effect of variable and constant thermal conditions on embryonic and early larval development of fish from the genus Leuciscus (Cyprinidae, Teleostei). Czech J. Anim. Sci. 56 (2): 70–80.10.17221/312/2009-CJASSearch in Google Scholar

Kupren K., Mamcarz A., Kucharczyk D. & Prusińnska M. 2008. Changes in morphometric parameters in selected early stages of three fish species from the genus Leuciscus (Teleostei, Cyprinidae). Arch. Pol. Fish. 16 (4): 421–436. 10.2478/s10086-008-0029-x10.2478/s10086-008-0029-xSearch in Google Scholar

Kupren K., Nowosad J., Żarski D., Targońska K., Hakuć-Błażzowska A. & Kucharczyk D. 2015a. Early development and allometric growth in laboratory-reared European Chub Leuciscus cephalus (Linnaeus, 1758). Turk. J. Fish. Aquat. Sci. 15 385–392. 10.4194/1303-2712-v15 2 24Search in Google Scholar

Kupren K., Prusińska M., Żarski D., Krejszeff S. & Kucharczyk D. 2014a. Early development and allometric growth in Nannacara anomala Regan, 1905 (Perciformes: Cichlidae) under laboratory conditions. Neotrop. Ichthyol. 12 (3): 659–665. 10.1590/1982-0224-2013010410.1590/1982-0224-20130104Search in Google Scholar

Kupren K., Rams I., Żarski D. & Kucharczyk D. 2016. Early development and allometric growth patterns of rheophilic cyprinid common dace Leuciscus leuciscus (Cyprinidae: Leuciscinae). Ichthyol. Res. 63 (3): 382–390. 10.1007/ s10228-016-0508-910.1007/s10228-016-0508-9Search in Google Scholar

Kupren K., Trąbska I., Żarski D., Krejszeff S., Palińska- Żarska K. & Kucharczyk D. 2014b. Early development and allometric growth patterns in burbot Lota lota L. Aquacult. Int. 22 (1): 29–39. 10.1007/s10499-013-9680-310.1007/s10499-013-9680-3Search in Google Scholar

Kupren K., Żarski D. & Kucharczyk D. 2015b. Early development and allometric growth patterns in ide Leuciscus idus (Linnaeus 1758). J. Appl. Ichthyol. 31 (3): 509–517. 10.1111/jai.1274710.1111/jai.12747Search in Google Scholar

Lima A.C. & Araujo-Lima C.A.R.M. 2004. The distributions of larval and juvenile fishes in Amazonian rivers of different nutrient status. Freshwater Biol. 49 (6): 787–800. 10.1111/j.1365-2427.2004.01228.x10.1111/j.1365-2427.2004.01228.xSearch in Google Scholar

Mann R.H.K. 1996. Environmental requirements of European non-salmonid fish in rivers. Hydrobiologia 323 (3): 223–235. 10.1007/BF0000784810.1007/BF00007848Search in Google Scholar

Moku M., Mori K. & Watanabe Y. 2004. Shrinkage in the body length of myctophid fish (Diaphus slender-type spp.) larvae with various preservatives. Copeia 2004 (3): 647–651. 10.1643/CI-03-113R10.1643/CI-03-113RSearch in Google Scholar

Nikolioudakis N., Koumoundouros G., Kiparissis S. & Somarakis S. 2010. Defining length-at-metamorphosis in fishes: a multi-character approach. Mar. Biol. 157 (5): 991–1001. 10.1007/s00227-009-1379-710.1007/s00227-009-1379-7Search in Google Scholar

Paine M.A., McDowell J.R. & Graves J.E. 2008. Specific identification using COI sequence analysis of scombrid larvae collected off the Kona coast of Hawaii Island. Ichthyol. Res. 55 (1): 7–16. 10.1007/s10228-007-0003-410.1007/s10228-007-0003-4Search in Google Scholar

Paragamian V.L. & Hansen M.J. 2011. Stocking for rehabilitation of burbot in the Kootenai River, Idaho, USA and British Columbia, Canada. J. Appl. Ichthyol. 27 (s1): 22–26. 10.1111/j.1439-0426.2011.01839.x10.1111/j.1439-0426.2011.01839.xSearch in Google Scholar

Penczak T., Galicka W., Głowacki ŁL., Koszaliński H., Kruk A., Zięba G., Kostrzewa J. & Marszał, L. 2004. Fish assemblage changes relative to environmental factors and time in the Warta River, Poland, and its oxbow lakes. J. Fish Biol. 64 (2): 483–501. 10.1111/j.0022-1112.2004.00316.x10.1111/j.0022-1112.2004.00316.xSearch in Google Scholar

Penczak T. & Kruk A. 2000. Threatened obligatory riverine fishes in human-modified Polish rivers. Ecol. Freshwater Fish. 9 (12): 109–117. 10.1034/j.1600-0633.2000.90113.x10.1034/j.1600-0633.2000.90113.xSearch in Google Scholar

Perea S., Bohme M., Zupancic P, Freyhof J., Sanda R., Ozulug M., Abdoli A. & Doadrio I. 2010. Phylogenetic relationships and biogeographical patterns in circum-Mediterranean subfamily Leuciscinae (Teleostei, Cyprinidae) inferred from both mitochondrial and nuclear data. BMC Evol. Biol. 10: 265. 10.1186/1471-2148-10-26510.1186/1471-2148-10-265Search in Google Scholar PubMed PubMed Central

Santos J.N.S., Araújo F.G. & Silva D.S. 2009. Length correction for early-juvenile Brazilian herring Sardinella janeiro (Eigenmann, 1894) after preservation in formalin, ethanol and freezing. Neotrop. Ichthyol. 7 (1): 87–92. 10.1590/S1679-6225200900010001110.1590/S1679-62252009000100011Search in Google Scholar

Skinner K., Shields D. & Harrison S. 2008. Measures of Success: Uncertainty and Defining the Outcomes of River Restoration Schemes, Chapter 10, pp. 187–208. 10.1002/978047086 7082.ch10 ch10. In: Darby S. & Sear D. (eds), River Restoration: Managing the Uncertainty in Restoring Physical Habitat, John Wiley & Sons, Ltd., Chichester, UK, 328 pp. ISBN: 978-0-470-86706-810.1002/9780470867082.ch10Search in Google Scholar

Snyder D.E., Bestgen K.R. & Seal S.C. 2005. Native cyprini-form fish larvae of the Gila River Basin – morphological descriptions, comparisons, and computer-interactive keys. Final report of Colorado State University Larval Fish Laboratory to U.S. Department of the Interior Bureau of Reclamation in Phoenix, Arizona, 180 pp. http://www.usbr.gov/lc/phoenix/biology/azfish/pdf/Snydere2005GilaGuFnlRptr.pdf (accessed 06.04.2016).Search in Google Scholar

Strauss R.E. & Bond C.E. 1990. Taxonomic methods: morphology, Chapter 4, pp. 109–140. In: P. Moyle P. & Schreck C. (eds), Methods for Fish Biology, American Fisheries Society, Bethesda, 684 pp. ISBN: 091323558X, 9780913235584Search in Google Scholar

Targońska K., Kucharczyk D., Kujawa R., Mamcarz A. & Żarski D. 2010. Controlled reproduction of asp, Aspius aspius (L.) using luteinizing hormone releasing hormone (LHRH) analogues with dopamine inhibitors. Aquaculture 306 (1-4): 407–410. 10.1016/j.aquaculture.2010.05.02710.1016/j.aquaculture.2010.05.027Search in Google Scholar

Targońska K., Żarski D. & Kucharczyk D. 2008. A review of the artificial reproduction of asp, Aspius aspius (L.) and nase, Chondrostoma nasus (L.). Arch. Pol. Fish. 16 341–354. 10.2478/s10086-008-0022-410.2478/s10086-008-0022-4Search in Google Scholar

Walsh P.S., Metzger D.A. & Higuchi R. 1991. Chelex 100 as a medium for sample extraction of DNA for PCR-based typing from forensic material. BioTechniques 10 (4): 506–513. 10.2144/000113897Search in Google Scholar

Woynarovich E. & Woynarovich A. 1980 Modified technology for elimination of stickiness of common carp Cyprinus carpio eggs. Aquacult. Hung. 2: 19–21.Search in Google Scholar

Yokoyama R. & Goto A. 2005. Evolutionary history of freshwater sculpins, genus Cottus (Teleostei; Cottidae) and related taxa, as inferred from mitochondrial DNA phylogeny. Mol. Phyl. Evol. 36 (3): 654–668. 10.1016/j.ympev.2005.06. 00410.1016/j.ympev.2005.06.004Search in Google Scholar PubMed

Zhang Z., Schwartz S., Wagner L. & Miller W. 2000. A greedy algorithm for aligning DNA sequences. J. Comput. Biol. 7 (1-2): 203–214. 10.1089/1066527005008147810.1089/10665270050081478Search in Google Scholar PubMed

Żarski D., Kucharczyk D., Targonska K., Jamróz M., Krejszeff S. & Mamcarz A. 2009. Application of Ovopel, Ovaprim and their combination in artificial reproduction of two rheophilic cyprinid fishes. Pol. J. Natur. Sci. 24 (4): 235–244. 10.2478/v10020-009-0022-x10.2478/v10020-009-0022-xSearch in Google Scholar

Received: 2016-4-4
Accepted: 2016-9-14
Published Online: 2016-11-23
Published in Print: 2016-10-1

© 2016 Institute of Zoology, Slovak Academy of Sciences

Articles in the same Issue

  1. Section Cellular and Molecular Biology
  2. Pigments from fungi, an opportunity of production for diverse applications
  3. Section Zoology
  4. Morphological view on the evolution of the immunity and lymphoid organs of vertebrates, focused on thymus
  5. Section Cellular and Molecular Biology
  6. p53-Fibrinolytic system and acute lung injury
  7. Section Cellular and Molecular Biology
  8. The multipotent action of electromagnetic field
  9. Section Cellular and Molecular Biology
  10. Prescreening, identification and harvesting of microalgae with antibacterial activity
  11. Section Botany
  12. Cloning and molecular characterization of Myb transcription factors from Leymus (Poaceae: Trticeae)
  13. Section Botany
  14. Hydrological soil behavior in areas with semi-arid vegetation (Beni Chougrane Mountains, Algeria)
  15. Section Botany
  16. Extent and persistence of water repellency in two Iranian soils
  17. Section Botany
  18. The impact of the permanent grass cover or conventional tillage on hydraulic properties of Haplic Cambisol developed on paragneiss substrate
  19. Section Zoology
  20. Species composition of tetranychoid mites (Acari: Trombidiformes: Prostigmata: Tetranychoidea) in main landscapes of Tehran and modelling ecological niche of Tetranychoidea in main climates of Tehran Province, Iran
  21. Section Zoology
  22. Abiotic factors affect the occurrence of different morphological characteristics in Erebia medusa (Lepidoptera: Nymphalidae)
  23. Section Zoology
  24. Comparison of molecular and morphometric analysis in species discrimination of larvae among five cyprinids from the subfamily Leuciscinae: A tool for sustainable conservation of riverine ichthyofauna
  25. Section Zoology
  26. Values of three branched plasma amino acids of farmed rainbow trout, Oncorhynchus mykiss
Downloaded on 8.12.2025 from https://www.degruyterbrill.com/document/doi/10.1515/biolog-2016-0139/pdf
Scroll to top button