Aquaculture International

, Volume 20, Issue 3, pp 525–535 | Cite as

Scoring of the extent and intensity of carp (Cyprinus carpio) skin changes made by cormorants (Phalacrocorax carbo sinensis): relationship between morphometric and histological indices

  • Stefan Skorić
  • Božidar Rašković
  • Vesna Poleksić
  • Zoran Gačić
  • Mirjana Lenhardt
Article

Abstract

Cormorants cause damage to fish in aquaculture not only by consuming large number of fish but also by wounding them. Quantification of the actual damage in fish induced by wounding is important for reliable estimations of the overall loss in aquaculture caused by cormorants. In this study, specimens of mirror and scaly carp (Cyprinus carpio L.) injured by attacks of great cormorant (Phalacrocorax carbo L.) were collected from the “Ečka” fish farm in Serbia. Surfaces of superficial and open subepithelial wounds (expressed as a percent of the total body surface), estimated by computer-assisted image analysis, had mean values 10.66 ± 1.86 and 0.85 ± 0.90, respectively. Histological evaluation of wounds was performed by two scoring systems: system proposed by Bernet et al. (J Fish Dis 22:25–34, 1999) and modified system described by Wahli et al. (Aquaculture 225:371–386, 2003). The most frequent histopathological changes were disturbed epidermal structure and surface cell morphology and increased number of club cells (on more than 75% of specimens); increased number of melanocytes and their distribution in different layers in dermis; and enlarged hypodermis (more than 80% of samples) and myolysis (50% of samples). Comparison of wounds’ surfaces (surface of superficial injures) and histopathological changes, estimated by two scoring systems, revealed significant positive correlation. Bernet’s scoring system showed higher correlation coefficients, when compared with the modified Wahli’s scoring system.

Keywords

Carp Cormorant Histopathological changes Skin injuries Scoring system 

Abbreviations

BW

Body weight

CS

Cyst-like structures in dermis

EC

Excoriation of epidermis

EP

Proliferation of the epidermis

EX

Exudate in dermis

FCC

Fulton’s factor of fish condition

H/E

Hematoxylin and eosin

ML

Myolysis of muscular tissue

NI

Nidus in epidermis

SP

Spongiosis of the epidermal tissue

TL

Total body length

References

  1. Adámek Z, Kortan J, Flajšhans M (2007) Computer-assisted image analysis in the evaluation of fish wounding by cormorant [Phalacrocorax carbo sinensis (L.)] attacks. Aquacult Int 15:211–216CrossRefGoogle Scholar
  2. Banerjee TK, Mittal AK (1999) Histopathological studies on the repair of the excised skin wounds of the air-breathing scalyfish Channa striata (Bloch). Curr Sci India 77:1067–1075Google Scholar
  3. Bernet D, Schmidt H, Meier W, Burkhardt-Holm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22:25–34CrossRefGoogle Scholar
  4. Chivers DP, Wisenden BD, Hindman CJ, Michalak TA, Kusch RC, Kaminskyj SGW, Jack KL, Ferrari MCO, Pollock RJ, Halbgewachs CF, Pollock MS, Alemadi S, James CT, Savaloja RK, Goater CP, Corwin A, Mirza RS, Kiesecker JM, Brown GE, Adrian JC, Krone PH, Blaustein AR, Mathis A (2007) Epidermal ‘alarm substance’ cells of fishes maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation, vol 274. In: Proceedings of the Royal Society B: biological sciences, pp 2611–2619Google Scholar
  5. Davies JM, Feltham MJ, Walsingham MV (1995) Fish wounding by cormorants, Phalacrocorax carbo L. Fish Manag Ecol 2:321–324CrossRefGoogle Scholar
  6. Evgen’eva TP, Nikol’skaya MP, Shagaeva VG (2001) Pathological changes in body wall tissues of juvenile sturgeons bred in fish-rearing ponds in the Astrakhan’ Oblast. Doklady Biol Sci 380:445–447CrossRefGoogle Scholar
  7. Fabacher D, Little E (1998) Photoprotective substance occurs primarily in outer layers of fish skin. Environ Sci Pollut R 5:4–6CrossRefGoogle Scholar
  8. Faragó S, Gosztonyi L, Keresztessy K, Gyói G (2006) Fish consumption by cormorants in Hungary. In: Hanson A et al (eds) Limnology and aquatic birds: abstracts and selected papers from the fourth conference of the societas Internationalis Limnologiae (SIL) aquatic birds working group, vol XII. Canadian wildlife service technical report series no. 474 Atlantic region, pp 61–73Google Scholar
  9. Forlenza M, Walker PD, de Vries BJ, Wendelaar Bonga SE, Wiegertjes GF (2008) Transcriptional analysis of the common carp (Cyprinus carpio L.) immune response to the fish louse Argulus japonicus Thiele (Crustacea: Branchiura). Fish Shellfish Immunol 25:76–83PubMedCrossRefGoogle Scholar
  10. Grémillet D, Enstipp M, Boudiffa M, Liu H (2006) Do cormorants injure fish without eating them? An underwater video study. Mar Biol 148:1081–1087CrossRefGoogle Scholar
  11. Guerra RR, Santos NP, Cecarelli P, Silva JRMC, Hernandez-Blazquez FJ (2008) Healing of skin wounds in the African catfish Clarias gariepinus. J Fish Biol 73:572–583CrossRefGoogle Scholar
  12. Gwiazda R (2004) Fish in the diet of the Cormorant and the Yellow-legged Gull breeding near fish ponds (upper Vistula river valley, southern Poland)—preliminary study. Acta Zool Cracoviensia 47:17–26Google Scholar
  13. Humason GL (1972) Animal tissue techniques. Freeman WH, San FranciscoGoogle Scholar
  14. Iger Y, Abraham M (1990) The process of skin healing in experimentally wounded carp. J Fish Biol 36:421–437CrossRefGoogle Scholar
  15. Kortan J, Adámek Z, Flajšhans M, Piačková V (2008) Indirect manifestation of cormorant (Phalacrocorax carbo sinensis (L.)) predation on pond fish stock. Knowl Managt Aquatic Ecosyst 389:01CrossRefGoogle Scholar
  16. Kortan J, Blahova J, Kruzikova K, Adamek Z (2011) Stress responses of carp pond fish stock upon hunting activities of the great cormorant (Phalacrocorax carbo sinensis L.). Aquacult Res 42:322–330CrossRefGoogle Scholar
  17. Lindell L, Mellin M, Musil P, Przybysz J, Zimmerman H (1995) Status and population development of breeding cormorants Phalacrocorax carbo sinensis of the central European flyway. Ardea 83:81–92Google Scholar
  18. Madetoja J, Nyman P, Wiklund T (2000) Flavobacterium psychrophilum, invasion into and shedding by rainbow trout Oncorhynchus mykiss. Dis Aquat Organ 43:27–38PubMedCrossRefGoogle Scholar
  19. Marchand MJ, van Dyk JC, Pieterse GM, Barnhoorn IEJ, Bornman MS (2009) Histopathological alterations in the liver of the sharptooth catfish Clarias gariepinus from polluted aquatic systems in South Africa. Environ Toxicol 24:133–147PubMedCrossRefGoogle Scholar
  20. Marković Z, Mitrović-Tutundžić V, Jeremić S, Poleksić V, Dulić-Stojanović Z, Živić I, Stanković M, Vasiljević M (2005) Monitoring of water quality, biological characteristics of fish farm ecosystems, and fish health—basis for successful production of carp in semi-intensive system. In: Marković Z (ed) II international conference «Fishery», Faculty of Agriculture, University of Belgrade, Belgrade, Serbia pp 33–41Google Scholar
  21. Mikuška J (1986) Prilog poznavanju ishrane velikog kormorana Phalacrocorax carbo L. (1758), na ribnjacima Slavonije i Baranje. Ribarstvo Jugoslavije 1–2:24–26Google Scholar
  22. Opačak A, Florijančić T, Horvat D, Ozimec S, Bodakoš D (2004) Diet spectrum of great cormorants (Phalacrocorax carbo sinensis L.) at the Donji Miholjac carp fishponds in eastern Croatia. Eur J Wildl Res 50:173–178CrossRefGoogle Scholar
  23. Ottesen OH, Amin AB (2011) Mortality and cellular response in the skin and gills of plaice (Pleuronectes platessa L) to parasite and bacteria infection. B Eur Assoc Fish Pat 31:16–22Google Scholar
  24. Pihler I, Popović E, Ćirković M (2000) Štete koje ribnjacima nanose ihtiofagne ptice. Savremeno ribarstvo Jugoslavije, Monografija, Beograd, Novi Sad, pp 117–126Google Scholar
  25. Poleksić V, Mitrović-Tutundžić V (1994) Fish gills as a monitor of sublethal and chronic effects of pollution. In: Muller R, Lloyd R (eds) Sublethal and chronic toxic effects of pollutants on freshwater fish. Blackwell Scientific Publications Ltd, Oxford, pp 339–352Google Scholar
  26. Poleksić V, Dulić-Stojanović Z, Marković Z (2002) Gill structure of carp fingerlings from Baranda fish farm. Acta Biologica Jugoslavica Ichthyologia 34:11–20Google Scholar
  27. Quilhac A, Sire J-Y (1999) Spreading, proliferation, and differentiation of the epidermis after wounding a Cichlid fish, Hemichromis bimaculatus. Anat Rec 254:435–451PubMedCrossRefGoogle Scholar
  28. Rašković B, Poleksić V, Živić I, Spasić M (2010) Histology of carp (Cyprinus carpio L.) gills and pond water quality in semiintensive production. Bulgarian J Agric Sci 16:253–262Google Scholar
  29. Ritchie BW, Wooley RE, Vaughan V (2005) Use of potentiated antimicrobials in treating skin infections In: 36th annual IAAAM conference, international association for aquatic animal medicine, Seward, Alaska, pp 33–41Google Scholar
  30. Roberts RJ (1989) Fish pathology. Baillière Tindall, LondonGoogle Scholar
  31. Silva JRMC, Sinhorini IL, Jensch-Junior BE, Porto-Neto LR, Hernadez-Blazquez FJ, Vellutini BC, Pressinotti LN, Pinto FAC, Cooper EL, Borges JCS (2004) Kinetics of induced wound repair at 0°C in the Antarctic fish (Cabeçuda) Notothenia coriiceps. Polar Biol 27:458–465CrossRefGoogle Scholar
  32. Silva JRMC, Cooper EL, Sinhorini IL, Borges JCS, Jensch-Junior BE, Porto-Neto LR, Hernandez-Blazquez FJ, Vellutini BC, Pressinotti LN, Costa-Pinto FA (2005) Microscopical study of experimental wound healing in Notothenia coriiceps (Cabeçuda) at 0°C. Cell Tissue Res 321:401–410CrossRefGoogle Scholar
  33. Singh SK, Mittal AK (1990) A comparative study of the epidermis of the common carp and the three Indian major carp. J Fish Biol 36:9–19CrossRefGoogle Scholar
  34. Steffens W (2010) Great cormorant—substantial danger to fish populations and fishery in Europe. Bulgarian J Agric Sci 16:322–331Google Scholar
  35. Svobodová Z, Vykusová B, Modrá H, Jarkovský J, Smutná M (2006) Haematological and biochemical profile of harvest-size carp during harvest and post-harvest storage. Aquacult Res 37:959–965CrossRefGoogle Scholar
  36. Van Der Salm AL, Nolan DT, Spanings FAT, Wendelaar Bonga SE (2000) Effects of infection with the ectoparasite Argulus japonicus (Thiele) and administration of cortisol on cellular proliferation and apoptosis in the epidermis of common carp, Cyprinus carpio L., skin. J Fish Dis 23:173–184CrossRefGoogle Scholar
  37. Wahli T, Verlhac V, Girling P, Gabaudan J, Aebischer C (2003) Influence of dietary vitamin C on the wound healing process in rainbow trout (Oncorhynchus mykiss). Aquaculture 225:371–386CrossRefGoogle Scholar
  38. Žydelis R, Kontautas A (2008) Piscivorous birds as top predators and fishery competitors in the lagoon ecosystem. Hydrobiologia 611:45–54CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Stefan Skorić
    • 1
  • Božidar Rašković
    • 2
  • Vesna Poleksić
    • 2
  • Zoran Gačić
    • 1
  • Mirjana Lenhardt
    • 1
  1. 1.Institute for Multidisciplinary ResearchUniversity of BelgradeBelgradeSerbia
  2. 2.Faculty of AgricultureUniversity of BelgradeZemun, BelgradeSerbia

Personalised recommendations