Seasonal feeding habits and ontogenetic diet shift of black bullhead (Ameiurus melas) in Lake Sava (Serbia)
DOI:
https://doi.org/10.2298/ABS210909045JKeywords:
non-native fish, opportunistic generalist, trophic niche breadth, diet analysisAbstract
Paper description:
- The black bullhead is one of the most successful non-native fish species in European freshwaters.
- Feeding habits of individuals caught in Lake Sava were analyzed by applying the following indices: vacuity index, frequency of occurrence, numerical abundance, and prominence value; trophic niche breadth and seasonal trophic diversity were calculated using the Shannon index.
- The diet spectrum was comprised of 16 prey categories from five groups: Mollusca, Crustacea, Insecta, Teleostei and plants.
- This species is a generalist and opportunist that enters into competitive and predatory relationships with native fish species.
Abstract: The black bullhead is an invasive species that forms dense populations and has a negative impact on the native ichthyofauna. Recent studies indicate that it is one of the most dominant invasive fish species in Serbian waters. Feeding habits based on stomach contents of individuals caught in Lake Sava were analyzed as a first step towards evaluating its possible negative impact on the native fish fauna of the lake. The following indices for diet analysis were applied: vacuity index, frequency of occurrence, numerical abundance and prominence value. Trophic niche breadth and seasonal trophic diversity were calculated using the Shannon’s index. The diet spectrum comprised 16 different prey categories from five groups: Mollusca, Crustacea, Insecta, Teleostei and plants. Fish were the main prey in all seasons, followed by aquatic invertebrates. Plant material and terrestrial insects were used as food in relatively small quantities. Predation on fish eggs was also detected. Our research confirmed that this species is an opportunistic generalist. An ontogenetic diet shift was also detected. The lowest value of trophic diversity was found in age 1+ individuals (H=1.39), while the highest was found in age 3+ individuals (H=2.00). The widest niche breadth was recorded in spring 2011 (H=2.12).
Downloads
References
IUCN. Guidelines for the prevention of biodiversity loss due to biological invasion [Internet]. IUCN - The World Conservation Union, Gland, Switzerland, 2000. 25 p. [cited 2020 Oct 1] Available from:
https://portals.iucn.org/library/efiles/documents/Rep-2000-052.pdf
Williamson M. Invasions. Ecography. 1999;22:5-12.
https://doi.org/10.1111/j.1600-0587.1999.tb00449.x
Clavero M, García-Berthou E. Invasive species are a leading cause of animal extinctions. Trends Ecol Evol. 2005;20(3):110.
https://doi.org/10.1016/j.tree.2005.01.003
Orchan Y, Chiron F, Shwartz A, Kark S. The complex interaction network among multiple invasive bird species in a cavity-nesting community. Biol Invasions. 2013;15:429-45.
https://doi.org/10.1007/s10530-012-0298-6
Pimentel D, Lach L, Zuniga R, Morrison D. Environmental and economic costs of nonindigenous species in the United States. Bioscience. 2000;50:53-65.
https://doi.org/10.1641/0006-3568(2000)050[0053:EAECON]2.3.CO;2
Shirley SM, Kark S. The role of species traits and taxonomic patterns in alien bird impacts. Glob Ecol Biogeogr. 2009;18:450-59.
https://doi.org/10.1111/j.1466-8238.2009.00452.x
Leprieur F, Beauchard O, Blanchet S, Oberdorff T, Brosse S. Fish invasions in the world's river systems: when natural processes are blurred by human activities. PLOS Biol. 2008;6(12):e28.
https://doi.org/10.1371/journal.pbio.0060028
Cucherousset J, Olden JD. Ecological impacts of non-native freshwater fishes. Fisheries. 2011;36:215-30.
https://doi.org/10.1080/03632415.2011.574578
Declerck S, Louette G, De Bie T, De Meester L. Patterns of diet overlap between populations of non-indigenous and native fishes in shallow ponds. J Fish Biol. 2002;61:1182-97.
https://doi.org/10.1111/j.1095-8649.2002.tb02464.x
Cucherousset J, Paillisson JM, Carpenter A, Eybert, M-MC, Olden JD. Habitat use of an artificial wetland by the invasive catfish Ameiurus melas. Ecol Freshw Fish. 2006;15:589-96.
https://doi.org/10.1111/j.1600-0633.2006.00199.x
Savini D, Occhipinti-Ambrogi A, Marchini A, Tricatico E, Gherardi F, Olenin S, Gollasch S. The top 27 animal alien species introduced into Europe for aquaculture and related activities. J Appl Ichthyol. 2010;26:1-7.
https://doi.org/10.1111/j.1439-0426.2010.01503.x
Novomeská A, Kováč V. Life-history traits of non-native black bullhead Ameiurus melas with comments on its invasive potential. J Appl Ichthyol. 2009;25:79-84.
https://doi.org/10.1111/j.1439-0426.2008.01166.x
Scott WB, Crossman EJ. Freshwater fishes in Canada. Bulletin of the Fisheries Research Board of Canada. 1973. 184 p.
Rutkayová J, Biskup R, Harant R, Šlechta V, Koščo J. Ameiurus melas (black bullhead): morphological characteristics of new introduced species and its comparison with Ameiurus nebulosus (brown bullhead). Rev Fish Biol Fisher. 2012;22:1-18.
https://doi.org/10.1007/s11160-012-9274-6
Louette G, Declerck S. Assessment and control of non-indigenous brown bullhead Ameiurus nebulosus populations using fyke nets in shallow ponds. J Fish Biol. 2006;68:522-31. https://doi.org/10.1111/j.0022-1112.2006.00939.x
Cvijanović G, Cvijanović M, Jarić I, Lenhardt M. Use of shape analysis in the investigation of disputable meristic characters for Ameiurus melas (Rafinesque, 1820) and Ameiurus nebulosus (Lesueur, 1819). J Appl Ichthyol. 2012;28:617-22.
https://doi.org/10.1111/j.1439-0426.2012.02009.x
Holčík J. Fish introductions in Europe with particular reference to its Central and Eastern part. Can J Fish Aquat Sci. 1991;48:13-23. https://doi.org/10.1139/f91-300
Copp GH, Tarkan AS, Masson G, Godard MJ, Koščo J, Kováč V, Novomeská A, Miranda R, Cucherousset J, Pedicillo G, Blackwell BG. A review of growth and life-history traits of native and nonnative European populations of black bullhead Ameiurus melas. Rev Fish Biol Fisher. 2016;26:441-69.
https://doi.org/10.1007/s11160-016-9436-z
Fijan N, Petrinec Z, Đorđević V. Taxonomy and production of North American catfishes of the genus Ictalurus. Ribar Jugosl. 1989;44:109-13. Croatian.
Glamužina B, Tutman P, Nikolić V, Vidović Z, Pavličević J, Vilizzi L, Copp GH, Simonović P. Comparison of taxon-specific and taxon-generic risk screening tools to identify potentially invasive non-native fishes in the River Neretva catchment (Bosnia & Herzegovina and Croatia). River Res Appl. 2017;33(5):670-9.
https://doi.org/10.1002/rra.3124
Bódis E, Borza P, Potyó I, Puky M, Weiperth A, Guti G. Invasive mollusc, crustacean, fish and reptile species along the Hungarian stretch of the River Danube and some connected waters. Acta Zool Acad Sci Hung. 2012;58 (Suppl.):29-45.
Păpuc T, Ladoşi D, Boaru A. The black bullhead (Ameiurus melas, Rafinesque 1820) - a new invasive fish species in Someş river, Romania. ELBA Bioflux. 2018;10(1):18-24.
Povž M, Jakšić G, Piria M. The updated list of the non-native freshwater fishes in Slovenia with note of their potential impact in inland Waters. Pak J Zool. 2018;13:1-7.
Piria M, Povž M, Vilizzi L, Zanella D, Simonović P, Copp GH. Risk screening of non-native freshwater fishes in Croatia and Slovenia using FISK (Fish Invasiveness Screening Kit). Fish Manag Ecol. 2016;23:21-31.
https://doi.org/10.1111/fme.12147
Piria M, Svjetiličić S, Poljak A, Jakovlić I. Natural diet of topmouth gudgeon, pumpkinseed and black bullhead with note on their invasive potential in Croatia. In: 52nd Croatian and 12th International symposium on agriculture: proceedings; 2017 Feb 12-17; Dubrovnik, Croatia. Osijek, Croatia: Faculty of Agriculture, Josip Juraj Strossmayer, University of Osijek; 2017. p 428-32.
Cvijanović G, Lenhardt M, Hegediš A. The first record of black bullhead Ameiurus melas (Pisces, Ictaluridae) in Serbian waters. Arch Biol Sci. 2005;57(4):21-2.
https://doi.org/10.2298/ABS0504307C
Lenhardt M, Marković G, Hegediš A, Maletin S, Ćirković M, Marković Z. Non-native and translocated fish species in Serbia and their impact on the native ichthyofauna. Rev Fish Biol Fisher. 2011;21:407-21.
https://doi.org/10.1007/s11160-010-9180-8
Blaženčić J. Floristic characteristics of the macrophytic vegetation in Lake Savsko near Belgrade (Serbia. Yugoslavia). Glasn Inst Bot Botan Bašte Univ Beograd. 1995;29:167-73. Serbian.
Janković MM, Janković IM. Contribution to the knowledge and problem-solving of eutrophication and overgrowing the Sava Lake (Ada Ciganlija) in Belgrade. Glasn Ins Bot Botan Bašte Univ Beograd. 1987;16:1-42. Serbian.
Simić V, Simić S, Petrović A, Radojković N, Veličković T, Matejić B, Mitrović A, Vlajković M. Program upravljanja ribarskim područjem "Kolubara" za period 2017-2026. Kragujevac: Prirodno-matematički fakultet Univerzitet; 2018. 41 p. Serbian.
Zakon o zaštiti i održivom korišćenju ribljeg fonda "Sl. glasnik RS", br. 128/14 i 95/2018 [Internet] [cited 2020 Nov 23]. Available from: https://www.paragraf.rs/propisi/zakon_o_zastiti_i_odrzivom_koriscenju_ribljeg_fonda.html Serbian.
Kottelat M, Freyhof J. Handbook of European freshwater fishes. Cornol, Switzerland: Publications Kottelat. 2007. 646p.
AVMA. Guidelines for the euthanasia of animals: 2013 edition. [Internet]. Schaumburg: American Veterinary Medical Association. 2013, version 2013.0.1. [cited 2020 Nov 26]. Available from:
https://www.avma.org/KB/Policies/Documents/euthanasia.pdf
Ricker WE. Handbook of computations for biological statistics of fish populations. Ottawa: Fisheries Research Board of Canada; 1958. 119 p. (Bulletin (Fisheries Research Board of Canada); No. 119).
Bartoo NW, Parker KR. Stochastic age-frequency estimation using the Von Bertalanffy growth equation. Fish Bull. 1983;81:91-6.
Secor DH, Dean JM, Laban EH. Otolith removal and preparation for microstructural examination. In: Stevenson DK, Campana SE, editors. Otolith microstructure examination and analysis. Ottawa: Department of Fisheries and Oceans; 1992. p. 19-57. (Canadian Special Publication of Fisheries and Aquatic Science; No. 117).
https://doi.org/10.2307/1446235
Hyslop EJ. Stomach contents analysis - a review of methods and their application. J Fish Biol. 1980;17:411-29.
https://doi.org/10.1111/j.1095-8649.1980.tb02775.x
Hickley P, North R, Muchiri SM, Harper DM. The diet of largemouth bass, Micropterus salmoides, in Lake Naivasha, Kenya. J Fish Biol. 1994;44(4):607-19.
https://doi.org/10.1111/j.1095-8649.1994.tb01237.x
Lorenzoni M, Corboli M, Dörr AJM, Giovinazzo G, Selvi S, Merelli M. Diets of Micropterus salmoides Lac. and Esox lucius L. in lake Trasimeno (Umbria, Italy) and their diet overlap. Knowl Manag Aquat Ecol. 2002;365-366:537-47.
https://doi.org/10.1051/kmae:2002050
Krebs CJ. Ecology: The Experimental Analysis of Distribution and Abundance. San Francisco: Benjamin/Cummings; 2011. 801 p.
Leunda PM, Oscoz J, Elvira B, Agorreta A, Perea S, Miranda R. Feeding habits of the exotic black bullhead Ameiurus melas (Rafinesque) in the Iberian Peninsula; first evidence of direct predation on native fish species. J Fish Biol. 2008;73:96-114.
https://doi.org/10.1111/j.1095-8649.2008.01908.x
Bowen SH. Quantitative description of the diet. In: Murphy BR, Willis DW, editors. Fisheries Techniques. 2nd ed. Bethesda, MD: American Fisheries Society; 1996. p. 513-32.
Penczak T, Kusto E, Krzyånowska D, Moliński M, Suszycka E. Food consumption and energy transformations by fish populations in two small lowland rivers in Poland. Hydrobiologia. 1984;108:135-44.
https://doi.org/10.1007/BF00014873
Sotirov SK. Ekologija američkog somića (Ictalurus nebulosus nebulosus Le Sueur, 1819) [dissertation]. Belgrade: University of Belgrade; 1968. 186 p.
Ruiz-Navarro A, Britton JR, Jackson MC, Davies GD, Sheath D. Reproductive ecology and diet of a persistent Ameiurus melas (Rafinesque, 1820) population in the UK. J Appl Ichthyol. 2015;31:201-3.
https://doi.org/10.1111/jai.12644
Lien L. Biology of the minnow Phoxinus phoxinus and its interactions with brown trout Salmo trutta in Øvre Heimdalsvatn, Norway. Holarctic Ecol. 1981;4:191-200.
https://doi.org/10.1111/j.1600-0587.1981.tb00997.x
Blanc TJ, Margraf FJ. Effects of nutrient enrichment on channel catfish growth and consumption in Mount Storm Lake, West Virginia. Lakes Reserv: Res Manag 2002;7:109-23.
https://doi.org/10.1046/j.1440-169X.2002.00184.x
Grubačević M. Kvalitet životne sredine grada Beograda u 2012. godini.. Beograd: Gradska uprava grada Beograda - Sekretarijat za zaštitu životne sredine, Gradski zavod za javno zdravlje, Regional Environmental Center (REC); 2013. 368 p. Serbian.
Kreutzenberger K, Leprieur F, Brosse S. The influence of the invasive black bullhead Ameiurus melas on the predatory efficiency of pike Esox lucius L. J Fish Biol. 2008;73:196-205.
https://doi.org/10.1111/j.1095-8649.2008.01926.x
Braig EC, Johnson DL. Impact of black bullhead (Ameiurus melas) on turbidity in a diked wetland. Hydrobiologia. 2003;90:11-21.
Reid SM, Fox MG, Whillans TH. Influence of turbidity on piscivory in largemouth bass (Micropterus salmoides). Can J Fish Aquat Sci. 1999;56(8):1362-69.
https://doi.org/10.1139/f99-056
Utne-Palm AC. Visual feeding of fish in a turbid environment: physical and behavioural aspects. Mar Freshw Behav Physiol. 2002;5:111-28.
https://doi.org/10.1080/10236240290025644
García-Berthou E, Moreno-Amich R. Food of introduced pumpkinseed sunfish: ontogenetic diet shift and seasonal variation. J Fish Biol. 2000;57:29-40.
https://doi.org/10.1111/j.1095-8649.2000.tb00773.x
Haubrock PJ, Balzani P, Johović I, Inghilesi AF, Nocita A, Tricarico E. The diet of the alien channel catfish Ictalurus punctatus in the River Arno (Central Italy). Aquat Invasions. 2018;13(4):575-85.
https://doi.org/10.3391/ai.2018.13.4.14
Oscoz J, Leunda PM, Campos F, Escala MC, García-Fresca C, Miranda R. Spring diet composition of Rainbow Trout, Oncorhynchus mykiss (Walbaum, 1792) in the Urederra River (Spain). Ann Limnol Int J Lim. 2005;41:27-34.
https://doi.org/10.1051/limn/2005003
Oscoz J, Leunda PM, Miranda R, Escala MC. Summer feeding relationships of the co-occurring Phoxinus phoxinus and Gobio lozanoi (Cyprinidae) in an Iberian river. Folia Zool. 2006; 55: 418-32.
Jaćimović M, Lenhardt M, Krpo-Ćetković J, Jarić I, Gačić Z, Hegediš A. Boom-bust like dynamics of invasive black bullhead (Ameiurus melas) in Lake Sava (Serbia). Fish Manag Ecol. 2019;26:153-64.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2021 Archives of Biological Sciences
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Authors grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution 4.0 International License that allows others to share the work with an acknowledgment of the work’s authorship and initial publication in this journal.
