Diet of the endangered spirlin (Alburnoides bipunctatus) at the centre of its distribution in Europe
L. Marszał A B , M. Grzybkowska A , D. Błońska A , J. Leszczyńska A and M. Przybylski AA Department of Ecology and Vertebrate Zoology, Faculty of Biology and Environmental Protection, University of Łódź, 12/16 Banacha Street, PL-90-237 Łódź, Poland.
B Corresponding author. Email: lidia.marszal@biol.uni.lodz.pl
Marine and Freshwater Research 69(11) 1712-1723 https://doi.org/10.1071/MF18013
Submitted: 17 January 2018 Accepted: 12 April 2018 Published: 23 July 2018
Abstract
The feeding habits of spirlin Alburnoides bipunctatus were investigated in a tributary of the River Vistula (Poland). To evaluate size-related patterns of resource use, fish were assigned to three size classes, defined according to size at first maturation: small (29–70-mm total length, TL), medium (71–90 mm TL) and large (91–104 mm TL). There was a significant ontogenetic shift in the feeding pattern among size classes, marked by differences in the proportion of the main taxonomic groups of prey consumed: small spirlin primarily consumed chironomid larvae, whereas medium and large spirlin showed a preference for Coleoptera, Ephemeroptera and imagines of unidentified insects. The proportion of prey taken from the water column was significantly lower for small- than medium- and large-sized spirlin. This difference was attributed to the benthic habits of small spirlin compared with medium and large spirlin. The shift to open water feeding in spirlin corresponded with sexual maturation, with habitat segregation between the smallest size class (comprising juveniles) and larger size classes (mature individuals). Size-specific changes in the diet composition of this species have not previously been documented.
Additional keywords: diet preference, habitat use, Jacobs’ electivity index, ontogenetic niche shift.
References
Abbasi, F., Ghorbani, R., Yelghi, S., Hajimoradloo, A., and Molaei, M. (2013). Comparative analyses of the diet of the spirlin (Alburnoides eichwaldii) in the Tilabad, Shirabad and Kaboodval Streams Golestan Province, Iran. World Journal of Fish and Marine Sciences 5, 79–83.Allan, J. D., and Castillo, M. M. (2007). ‘Stream Ecology. Structure and Function of Running Waters’, 2nd edn. (Springer: Dordrecht, Netherlands.)
Amundsen, P. A., Gabler, H. M., and Staldvik, F. J. (1996). A new approach to graphical analysis of feeding strategy from stomach contents data – modification of the Costello (1990) method. Journal of Fish Biology 48, 607–614.
| A new approach to graphical analysis of feeding strategy from stomach contents data – modification of the Costello (1990) method.Crossref | GoogleScholarGoogle Scholar |
Backiel, T. (1964). ‘Pstrągi.’ (Państwowe Wydawnictwo Rolnicze i Leśne: Warszawa, Poland.) [‘The Trouts’].
Bless, R. (1996). Reproduction and habitat preference of the threatened spirlin (Alburnoides bipunctatus Bloch) and soufie (Leuciscus souffia Risso) under laboratory conditions (Teleostei: Cyprinidae). In ‘Conservation of Endangered Freshwater Fish in Europe’. (Eds A. Kirchhofer and D. Hefti.) pp. 249–258. (BirkhauserVerlag: Basel, Switzerland.)
Bournaud, M., Tachet, H., Berly, A., and Cellot, B. (1998). Importance of microhabitat characteristics in the macrobenthos microdistribution of a large river reach. Annales de Limnologie – International. Journal of Limnology 34, 83–98.
| Importance of microhabitat characteristics in the macrobenthos microdistribution of a large river reach.Crossref | GoogleScholarGoogle Scholar |
Brylińska, M. (2000). ‘Ryby słodkowodne Polski.’ (Wydawnictwo Naukowe PWN: Warszawa, Poland.) [‘Freshwater Fishes of Poland’].
Copp, G. H., Kováč, V., and Siryová, S. (2010). Microhabitat use by stream-dwelling spirlin Alburnoides bipunctatus and accompanying species: implications for conservation. Folia Zoologica 59, 240–256.
| Microhabitat use by stream-dwelling spirlin Alburnoides bipunctatus and accompanying species: implications for conservation.Crossref | GoogleScholarGoogle Scholar |
Cortés, E. (1997). A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Canadian Journal of Fisheries and Aquatic Sciences 54, 726–738.
| A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes.Crossref | GoogleScholarGoogle Scholar |
Cranston, P. S., Oliver, D. R., and Saether, O. A. (1983). The larvae of Orthocladiinae (Diptera: Chironomidae) of the Holarctic region – keys and diagnoses. Entomologica Scandinavica 19, 149–291.
Cummins, K. W. (1962). An evaluation of some techniques for the collection and analysis of benthic samples with special emphasis on lotic waters. American Midland Naturalist 67, 477–504.
| An evaluation of some techniques for the collection and analysis of benthic samples with special emphasis on lotic waters.Crossref | GoogleScholarGoogle Scholar |
Cummins, K. W. (1974). Structure and function of stream ecosystems. Bioscience 24, 631–641.
| Structure and function of stream ecosystems.Crossref | GoogleScholarGoogle Scholar |
Dukowska, M., and Grzybkowska, M. (2014). Coexistence of fish species in a large lowland river: food niche partitioning between small-sized percids, cyprinids and sticklebacks in submersed macrophytes. PLoS One 9, e109927.
| Coexistence of fish species in a large lowland river: food niche partitioning between small-sized percids, cyprinids and sticklebacks in submersed macrophytes.Crossref | GoogleScholarGoogle Scholar |
Dukowska, M., Grzybkowska, M., Kruk, A., and Szczerkowska-Majchrzak, E. (2013). Food niche partitioning between perch and ruffe: combined use of a self-organising map and the IndVal index for analysing fish diet. Ecological Modelling 265, 221–229.
| Food niche partitioning between perch and ruffe: combined use of a self-organising map and the IndVal index for analysing fish diet.Crossref | GoogleScholarGoogle Scholar |
Filipović, D., and Janković, D. (1978). Relation between the bottom fauna and fish diet of the upland streams of East Serbia. Ichthyologia 10, 29–40.
Gabler, H. M., and Amundsen, P. A. (2010). Feeding strategies, resource utilisation and potential mechanisms for competitive coexistence of Atlantic salmon and alpine bullhead in a sub-Arctic river. Aquatic Ecology 44, 325–336.
| Feeding strategies, resource utilisation and potential mechanisms for competitive coexistence of Atlantic salmon and alpine bullhead in a sub-Arctic river.Crossref | GoogleScholarGoogle Scholar |
Galat, D. L., and Zweimuller, I. (2001). Conserving large-river fishes: is the highway analogy an appropriate paradigm? Journal of the North American Benthological Society 20, 266–279.
| Conserving large-river fishes: is the highway analogy an appropriate paradigm?Crossref | GoogleScholarGoogle Scholar |
Grzybkowska, M., and Witczak, J. (1990). Distribution and production of Chironomidae (Diptera) in the lower course of the Grabia River (Central Poland). Freshwater Biology 24, 519–531.
| Distribution and production of Chironomidae (Diptera) in the lower course of the Grabia River (Central Poland).Crossref | GoogleScholarGoogle Scholar |
Grzybkowska, M., and Zalewski, M. (1983). The food of roach, bream and white bream in the Sulejów Dam Reservoir. In ‘Proceedings of the Conference of the Polish Hydrobiological Society’, 20–23 September 1983, Lublin, Poland. (Ed. S. Radwan.) pp. 71–72. (Polish Hydrobiological Society: Lublin, Poland.)
Grzybkowska, M., Kurzawski, M., and Dukowska, M. (2012). Response of Chironomidae (Diptera) to impoundments in small lowland rivers. Fauna Norvegica 31, 25–33.
| Response of Chironomidae (Diptera) to impoundments in small lowland rivers.Crossref | GoogleScholarGoogle Scholar |
Hammer, Ø., Harper, D. A. T., and Ryan, P. D. (2001). PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 9.
Hyatt, K. B. (1979). Feeding strategy. In ‘Fish Physiology’. Vol. VIII. (Eds W. S. Hoar, D. J. Randall, and J. R. Brett.) pp. 71–119. (Academic Press: New York, NY, USA.)
Jacobs, J. (1974). Quantitative measurement of food selection: a modification of the forage ratio and Ivlev’s electivity index. Oecologia 14, 413–417.
| Quantitative measurement of food selection: a modification of the forage ratio and Ivlev’s electivity index.Crossref | GoogleScholarGoogle Scholar |
Jamet, J. L. (1994). Feeding activity of adult roach (Rutilus rutilus (L.)), perch (Perca fluviatilis L.) and ruffe (Gymnocephalus cernuus (L.)) in eutrophic Lake Aydat (France). Aquatic Sciences 56, 376–387.
| Feeding activity of adult roach (Rutilus rutilus (L.)), perch (Perca fluviatilis L.) and ruffe (Gymnocephalus cernuus (L.)) in eutrophic Lake Aydat (France).Crossref | GoogleScholarGoogle Scholar |
Jażdżewski, M., Błońska, D., Marszał, L., Przybylski, M., Janic, B., Pietraszewski, D., Tybulczuk, S., Zieliński, P., Grabowska, J., and Zięba, G. (2012). Monitoring of fish fauna in the Skrwa Prawa River system: continuation in 2010 and 2011. Scientific Annual of the Polish Angling Association 25, 5–29.
Jelonek, M., and Amirowicz, A. (1987). Density and biomass of fish in the Rożnów Reservoir (Southern Poland). Acta Hydrobiologica 29, 243–251.
Kottelat, M., and Freyhof, J. (2007). ‘Handbook of European Freshwater Fishes.’ (Publications Kottelat: Cornol, Switzerland.)
Kováč, V. (2015). Current status of fish communities in the Danube. In ‘The Danube River Basin. Handbook of Environmental Chemistry’. (Ed. I. Liska.) Vol. 39, pp. 359–389. (Springer-Verlag: Berlin, Germany.)
Kováč, V., Katina, S., Copp, G. H., and Siryová, S. (2006). Ontogenetic variability in external morphology and microhabitat use of spirlin Alburnoides bipunctatus from the River Rudava (Danube catchment). Journal of Fish Biology 68, 1257–1270.
| Ontogenetic variability in external morphology and microhabitat use of spirlin Alburnoides bipunctatus from the River Rudava (Danube catchment).Crossref | GoogleScholarGoogle Scholar |
Kukuła, K., and Bylak, A. (2011). Wpływ czynników antropogenicznych na faunę karpackich dopływów Wisły. Roczniki Bieszczadzkie 19, 207–222.
Lammens, E. H. R. R., and Hoogenboezem, W. (1991). Diets and feeding behaviour. In ‘Cyprinid Fishes: Systematics, Biology and Exploitation’. (Eds I. J. Winfield and J. S. Nelson.) pp. 353–376. (Chapman & Hall: London, UK.)
Levins, R. (1968). ‘Evolution in Changing Environments: Some Theoretical Explorations.’ (Princeton University Press: Princeton, NJ, USA.)
Lik, J., Dukowska, M., Grzybkowska, M., and Leszczyńska, J. (2017). Summer co-existence of small-sized cyprinid and percid individuals in natural and impounded reaches of a lowland river: food niche partitioning between fish. Journal of Fish Biology 90, 1609–1630.
| Summer co-existence of small-sized cyprinid and percid individuals in natural and impounded reaches of a lowland river: food niche partitioning between fish.Crossref | GoogleScholarGoogle Scholar |
Losos, B., Peňáz, M., and Kubičkova, J. (1980). Food and growth of fishes of the Jihlava River. Acta Scientarum Naturalium Academiae Scientiarum Bohemicae Brno 14, 1–46.
Lusk, S., Hanel, L., and Lusková, V. (2004). Red List of the ichthyofauna of the Czech Republic: development and present status. Folia Zoologica 53, 215–226.
Magurran, A. E. (2004). ‘Measuring Biological Diversity.’ (Blackwell Publishing: Oxford, UK.)
Makino, W., Kato, H., Takamura, N., Mizutani, H., Katano, N., and Mikami, H. (2001). Did chironomid emergence release Daphnia from fish predation and lead to Daphnia-driven clear-water phase in Lake Towada, Japan? Hydrobiologia 442, 309–317.
| Did chironomid emergence release Daphnia from fish predation and lead to Daphnia-driven clear-water phase in Lake Towada, Japan?Crossref | GoogleScholarGoogle Scholar |
Mann, R. H. K. (1996). Environmental requirements of European non-salmonid fish in rivers. Hydrobiologia 323, 223–235.
| Environmental requirements of European non-salmonid fish in rivers.Crossref | GoogleScholarGoogle Scholar |
Mann, R. H. K., Bass, J. A. B., Leach, D., and Pinder, A. C. (1997). Temporal and spatial variations in the diet of 0 group roach (Rutilus rutilus) larvae and juveniles in the river Great Ouse in relation to prey availability. Regulated Rivers: Research and Management 13, 287–294.
| Temporal and spatial variations in the diet of 0 group roach (Rutilus rutilus) larvae and juveniles in the river Great Ouse in relation to prey availability.Crossref | GoogleScholarGoogle Scholar |
Mark, W., Hofer, R., and Wieser, W. (1987). Diet spectra and resource partitioning in the larvae and juveniles of three species and six cohorts of cyprinids from a subalpine lake. Oecologia 71, 388–396.
| Diet spectra and resource partitioning in the larvae and juveniles of three species and six cohorts of cyprinids from a subalpine lake.Crossref | GoogleScholarGoogle Scholar |
Marshall, S., and Elliott, M. (1997). A comparison of univariate and multivariate numerical and graphical techniques for determining inter- and intraspecific feeding relationships in estuarine fish. Journal of Fish Biology 51, 526–545.
| A comparison of univariate and multivariate numerical and graphical techniques for determining inter- and intraspecific feeding relationships in estuarine fish.Crossref | GoogleScholarGoogle Scholar |
Marszał, L., and Błońska, D. (2015). Reproductive traits of spirlin Alburnoides bipunctatus in the Vistula River basin. Reproductive Biology 15, 184–187.
| Reproductive traits of spirlin Alburnoides bipunctatus in the Vistula River basin.Crossref | GoogleScholarGoogle Scholar |
Marszał, L., Grzybkowska, M., Kostrzewa, J., and Kruk, A. (1998). Food resource partitioning between spined loach (Cobitis taenia L.) and golden loach (Sabanejewia aurata (Fil.)) in a lowland river. Scientific Annual of the Polish Angling Association 11, 5–18.
Marszał, L., Zięba, G., Przybylski, M., Grabowska, J., and Kaczkowski, Z. (2004). Monitoring of fish fauna in the Skrwa Prawa River system. Scientific Annual of the Polish Angling Association 17, 77–98.
Moller Pillot, H. K. M. (2009). ‘Chironomidae Larvae of the Netherlands and Adjacent Lowlands: Biology and Ecology of the Chironomini.’ (KNNV Publishing: Zeist, Netherlands.)
Nunn, A. D., Harvey, J. P., and Cowx, I. G. (2007). The food and feeding relationships of larval and 0+ year juvenile fishes in lowland rivers and connected waterbodies. I. Ontogenetic shifts and interspecific diet similarity. Journal of Fish Biology 70, 726–742.
| The food and feeding relationships of larval and 0+ year juvenile fishes in lowland rivers and connected waterbodies. I. Ontogenetic shifts and interspecific diet similarity.Crossref | GoogleScholarGoogle Scholar |
Olivier, J.-M., Carrel, G., Lamouroux, N., Dole-Olivier, M.-J., Malard, F., Bravard, J.-P., and Amoros, C. (2009). The Rhône River Basin. In ‘Rivers of Europe’. (Eds K. Tockner, U. Uehlinger, and C. T Robinson.) pp. 247–295. (Academic Press: London, UK.)
Peňáz, M. (1996). Chondrostoma nasus – its reproduction strategy and possible reasons for a widely observed population decline – a review. In ‘Conservation of Endangered Freshwater Fish in Europe’. (Eds A. Kirchhofer and D. Hefti.) pp. 279–285. (BirkhauserVerlag: Basel, Switzerland.)
Penttinen, O.-P., and Holopainen, I. J. (1992). Seasonal feeding activity and ontogenetic dietary shifts in crucian carp, Carassius carassius. Environmental Biology of Fishes 33, 215–221.
| Seasonal feeding activity and ontogenetic dietary shifts in crucian carp, Carassius carassius.Crossref | GoogleScholarGoogle Scholar |
Petersen, R. C., Cummins, K. W., and Ward, G. M. (1989). Microbial and animal processing of detritus in a woodland stream. Ecological Monographs 59, 21–39.
| Microbial and animal processing of detritus in a woodland stream.Crossref | GoogleScholarGoogle Scholar |
Pinkas, L., Oliphant, M. S., and Iverson, L. R. (1971). Food habits of albacore, bluefin tuna, and bonito in California waters. Fish Bulletin 152, 1–105.
Piria, M., Treer, T., Aničič, I., Safner, R., and Odak, T. (2005). The natural diet of five cyprinid fish species. Agriculturae Conspectus Scientificus 70, 21–28.
Polačik, M., and Kováč, V. (2006). Fecundity and annual course of maturation in spirlin, Alburnoides bipunctatus. Folia Zoologica 55, 399–410.
Quinn, J. M., and Hickey, C. W. (1990). Magnitude of effects of substrate particle size, recent flooding, and catchment development on benthic invertebrates in 88 New Zealand rivers. New Zealand Journal of Marine and Freshwater Research 24, 387–409.
| Magnitude of effects of substrate particle size, recent flooding, and catchment development on benthic invertebrates in 88 New Zealand rivers.Crossref | GoogleScholarGoogle Scholar |
Ricciardi, A., and Rasmussen, J. B. (1999). Extinction rates of North American fauna. Conservation Biology 13, 1220–1222.
| Extinction rates of North American fauna.Crossref | GoogleScholarGoogle Scholar |
Rincón, P. A., Barrachina, P., and Bernat, Y. (1992). Microhabitat use by 0+ juvenile cyprinids during summer in a Mediterranean river. Archiv für Hydrobiologie 125, 323–337.
Seifali, M. (2011). Population biology of Alburnoides Jeitteles 1861 (Actinopterygii: Cyprinidae) in Iran. Ph.D. Thesis, Universiti Putra, Selangor, Malaysia.
Skóra, S. (1972). Piekielnica (Alburnus bipunctatus Bloch) z dorzeczy górnego Sanu i Dunajca. Acta Hydrobiologica 14, 173–204.
Szczerkowska-Majchrzak, E., Grzybkowska, M., and Dukowska, M. (2010). Effect of flow fluctuations on patch dynamics and chironomid distribution in a medium-sized lowland river. Journal of Freshwater Ecology 25, 437–448.
| Effect of flow fluctuations on patch dynamics and chironomid distribution in a medium-sized lowland river.Crossref | GoogleScholarGoogle Scholar |
Tallman, R. F., and Gee, J. H. (1982). Intraspecific resource partitioning in a headwaters stream fish, pearl dace Semotilus margarita (Cyprinidae). Environmental Biology of Fishes 7, 243–249.
| Intraspecific resource partitioning in a headwaters stream fish, pearl dace Semotilus margarita (Cyprinidae).Crossref | GoogleScholarGoogle Scholar |
Townsend, C. R. (1989). The patch dynamics concept of stream community ecology. Journal of the North American Benthological Society 8, 36–50.
| The patch dynamics concept of stream community ecology.Crossref | GoogleScholarGoogle Scholar |
Treer, T., Piria, M., Aničić, I., Safner, R., and Tomljanović, T. (2006). Diet and growth of spirlin, Alburnoides bipunctatus in the barbel zone of the Sava River. Folia Zoologica 55, 97–106.
Tszydel, M., Grzybkowska, M., and Kruk, A. (2009). Influence of dam removal on trichopteran assemblages in the lowland Drzewiczka River, Poland. Hydrobiologia 630, 75–89.
| Influence of dam removal on trichopteran assemblages in the lowland Drzewiczka River, Poland.Crossref | GoogleScholarGoogle Scholar |
Vannote, R. L., Minshall, G. W., Cummins, K. W., Sedell, J. R., and Cushing, C. E. (1980). The river continuum concept. Canadian Journal of Fisheries and Aquatic Sciences 37, 130–137.
| The river continuum concept.Crossref | GoogleScholarGoogle Scholar |
Vuković, T. (1968). Das Variieren der Länge des digestive Traktesbeieinigen Cyprinidenaus den Nebenflüssen des Oberlaufes der Bosna. Ribarstvo Jugoslavije 23, 84–86.
Vuković, T., and Ivanović, B. (1971). ‘Slatkovodne ribe Jugoslavije.’ (Zemaljski muzej B&H: Sarajevo, Yugoslavia.) [‘Freshwater Fishes from Jugoslavia’].
Werner, E. E., and Gilliam, J. F. (1984). The ontogenetic niche and species interactions in size-structured populations. Annual Review of Ecology and Systematics 15, 393–425.
| The ontogenetic niche and species interactions in size-structured populations.Crossref | GoogleScholarGoogle Scholar |
Witkowski, A., Kotusz, J., and Przybylski, M. (2009). Stopień zagrożenia słodkowodnej ichtiofauny Polski: Czerwona Lista minogów i ryb – stan 2009. Chrońmy Przyrodę Ojczystą 65, 33–52.
Wołos, A., and Wiśniewolski, W. (2002). Program restytucji gatunków łososiowatych i reofilnych karpiowatych w rzece Skrwie Prawej. Komunikaty Rybackie 6, 4–8.
Wootton, R. J. (1998). ‘Ecology of Teleost Fishes.’ (Kluwer Academic Publishers: London, UK.)