The impact of temporal patterns of temperature and precipitation on silver Prussian carp (Carassius gibelio) spawning events


Keywords: spawning; temperature; precipitation; principal component analysis; phenology

Abstract

It was revealed that Gibel carp, Carassius gibelio (Bloch, 1782) spawning phenology is determined by regular patterns of variability in temperature and precipitation over the period of time after spawning in the previous year. The sensitivity to temperature of water as a stimulus to spawning was shown as being dependent on the characteristics of the environment and fish development trajectories over the previous year. Information about fish spawning was collected in the Dnipro-Orylskiy Nature Reserve in the following locations: Nikolayev system of water bodies, River Protoch system and the Obukhov floodplain, the channel of the River Dnipro, water bodies of the Taromske ledge. The materials that formed the basis of this research were collected from the waters of the reserve in the years 1997–2018. There are dependencies between the air and water temperatures that have their own characteristics depending on the type of water body. These dependencies are described by a logistic equation. The temperature regime in water bodies of the Taromske ledge is very similar to the temperature regime of Nikolayev system of water bodies. The difference is that the spring period of the temperature increase in water bodies of the Taromske ledge comes earlier – in late February – early March. The air temperature dynamics over the year is described by the fourth degree polynomial. The residuals of the polynomial regression for each year were subjected to principal component analysis. The principal component analysis allowed us to identify 8 principal components of the temperature regimes, which together describe 59.2% of the variation of the residual of the polynomial trend. Deviations from the linear trend of the precipitation are systematic throughout the year, reflecting the uneven nature of rainfall during the year. The residuals of linear trend regression models of cumulative precipitation can be used as indicators of the dynamics characteristic of precipitation during the year. The residuals were used for principal component analysis, which revealed that the dynamics of the precipitation can be divided into five orthogonal principal components. The first five principal components explain 82.6% of the feature space variation. The timing of the onset of C. gibelio spawning in 95% of cases occurs on the 113–139th days of the year (on average, it takes place on the 125th day). Regression analysis revealed that the climate principal components and types of the lake systems can explain 79% of the variation in the timing of the onset of C. gibelio spawning. The water temperature at the time of C. gibelio spawning was exposed to natural dynamics in year aspect. The local minimum of the onset of spawning temperatures occured in the mid 2000s. Total of 69% of the water temperature variation at which spawning begins can be described by climatic predictors and water biotope types. The variation explained by some temperature principal components may be increased considerably after including as covariates such variables as the precipitation principal component and the biotope type. This principal component which represents the high frequency variation of the air temperature regime with a characteristic period 20 and 45 days has the highest explanation ability of all the components and is a constant explanatory predictor for all considered spawning characteristics.

References

Abramenko, M. I., Kravchenko, O. V., & Velikoivanenko, A. E. (1997). Population genetic structure of the goldfish Carassius auratus gibelio diploid-triploid complex from the Don River Basin. Journal of Ichthyology, 37, 56–65.


Antonova, E. I. (2010). Short-term thermal compensatory-adaptive reaction mechanisms of the liver in C. auratus gibelio. Contemporary Problems of Ecology, 3, 57–62.


Aydın, H., Gaygusuz, Ö., Tarkan, A. S., Top, N., Emiroğlu, Ö., & Gürsoy Gaygusuz, Ç. (2011). Invasion of freshwater bodies in Marmara Region (NW-Turkey) by non-native gibel carp, Carassius gibelio (Bloch, 1782). Turkish Journal of Zoology, 35, 829–836.


Balik, S., Özkök, R., & Uysal, R. (2004). Investigation of some biological characteristics of the silver crucian carp, Carassius gibelio (Bloch 1782) population in Lake Egirdir. Turkish Journal of Zoology, 28(1), 19–28.


Berg, L. S. (1949). Ryby presnyh vod SSSR i sopredel’nyh stran [Fishes of fresh waters of the USSR and adjacent countries]. Part 2. Izdatel’stvo Akademii Nauk SSSR, Moscow – Leningrad (in Russian).


Bondarev, D. L., & Zhukov, O. V. (2017). Phenology of the white bream (Blicca bjoerkna) spawning in natural reserve "Dnieper-Orylskiy" in dependence from seasonal temperature dynamic. Biosystems Diversity, 25(2), 67–73.


Bondarev, D., Kunah, O., & Zhukov, O. (2018). Assessment of the impact of seasonal patterns climatic conditions on spawning events of the white bream Blicca bjoerkna (Linnaeus, 1758) in astronomical and biological time. Acta Biologica Sibirica, 4(2), 48–64.


Bone, Q., Marshall, N. B., & Blaxter, J. H. S. (1995). Biology of fishes. Blackie Academic and Professional, Glasgow.


Bugay, K. S., & Koval, N. V. (1976). Reproduction biology of the silver crucian carp (Carassius auratus gibelio Bloch) in the reservoirs of the Dnieper-Bug region [K biologii razmnozheniya serebryanogo karasya (Carassius auratus gibelio Bloch) vodoemov Dneprovsko-Bugskoy oblasti]. Hydrobiological Journal, 5(12), 53–58.


Chu, C., Mandrak, N. E., & Minns, C. K. (2005). Potential impacts of climate change on the distributions of several common and rare freshwater fishes in Canada. Diversity and Distributions, 11, 299–310.


Crivelli, A. (1995). Are fish introductions a threat to endemic freshwater fishes in the Northern Mediterranean region? Biological Conservation, 72, 311–319.


Cushing, D. H. (1990). Plankton production and year-class strength in fish populations: An update of the match/mismatch hypothesis. Advances in Marine Biology, 26, 249–292.


Elger, M., & Hentschel, H. (1981). The glomerulus of a stenohaline fresh-water teleost, Carassius auratus gibelio, adapted to saline water. A scanning and transmission electron-microscopic study. Cell and Tissue Research, 220(1), 73–85.


Elgin, E. L., Tunna, H. R., & Jackson, L. J. (2014). First confirmed records of Prussian carp, Carassius gibelio (Bloch, 1782) in open waters of North America. BioInvasions Records, 3(4), 275–282.


Emiroğlu, Ö., Tarkan, A. S., Top, N., Başkurt, S., & Sülün, Ş. (2012). Growth and life history traits of a highly exploited population of non-native gibel carp, Carassius gibelio from a large eutrophic lake (Lake Uluabat, NW Turkey): Is reproduction the key factor for establishment success? Turkish Journal of Fisheries and Aquatic Sciences, 12, 925–936.


Erdogan, Z., Torcu Koc, H., Serkan, K. G., & Ulunehir, G. (2014). Age, growth and reproductive properties of an invasive species Carassius gibelio (Bloch, 1782) (Cyprinidae) in the Ikizcetepeler Dam Lake (Balikesir), Turkey. Periodicum Biologorum, 116(3), 285–291.


Ficke, A. D., Myrick, C. A., & Hansen, L. J. (2007). Potential impacts of global climate change on freshwater fisheries. Reviews in Fish Biology and Fisheries, 17, 581–613.


Gaygusuz, Ö., Tarkan, A. S., & Gürsoy Gaygusuz, Ç. (2007). Changes in the fish community of the Ömerli Reservoir (Turkey) following the introduction of nonnative gibel carp Carassius gibelio (Bloch, 1782) and other human impacts. Aquatic Invasions, 2, 117–120.


Hänfling, B., Bolton, P., Harley, M., & Carvalho, G. R. (2005). A molecular approach to detect hybridisation between crucian carp (Carassius carassius) and nonindigenous carp species (Carassius spp. and Cyprinus carpio). Freshwater Biology, 50, 403–417.


Heina, К. (2017). Biological characteristics of Prussian carp (Carassius auratus gibelio (Bloch, 1782) commercial stock of the Dnieper-Bug estuary. Fisheries Science of Ukraine, 41, 37–49.


Holčík, J. (1980). Possible reason for the expansion of Carassius auratus (Linnaeus, 1758) (Teleostei, Cyprinidae) in the Danube River Basin. International Revue Gesamten Hydrobiologi, 65, 673–679.


Japoshvili, B., Mumladze, L., & Murvanidze, L. (2015). The population of Carassius gibelio (Bloch, 1782) and its parasites in Madatapa Lake (South Georgia). Iranian Journal of Fisheries Sciences, 16(2), 793–799.


Kallemeyn, L. W. (1987). Correlations of regulated lake levels and climatic factors with abundance of young-of-the-year walleye and yellow perch in four lakes in Voyageurs National Park. North American Journal of Fisheries Management, 7, 513–521.


Liasko, R., Koulish, A., Pogrebniak, A., Papiggioti, O., Taranenko, L., & Leonardos, I. (2011). Influence of environmental parameters on growth pattern and population structure of Carassius auratus gibelio in Eastern Ukraine. Hydrobiologia, 658, 317–328.


Lushchak, V. I., Luschchak, L. P., Mota, A. A., & Hermes-Lima, M. (2001). Oxidative stress and antioxidant defenses in goldfish C. auratus during anoxia and reoxygenation. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 280(1), R100–R107.


Lusk, M. R., Luskova, V., & Hanel, L. (2010). Alien fish species in the Czech Republic and their impact on the native fish fauna. Folia Zoologica, 59, 57–72.


Luskova, V., Lusk, S., Halacka, K., & Vetesnik, L. (2010). Carassius auratus gibelio – the most successful invasive fish in waters of the Czech Republic. Russian Journal of Biological Invasions, 1(3), 176–180.


Mertz, G., & Myers, R. (1994). Match/mismatch predictions of spawning duration versus recruitment variability. Fisheries Oceanography, 3, 236–245.


Migaud, H., Fontaine, P., Sulistyo, I., Kestemont, P., & Gardeur, J. N. (2002). Induction of out-of-season spawning in Eurasian perch Perca fluviatilis: Effects of rates of cooling and cooling durations on female gametogenesis and spawning. Aquaculture, 205(3–4), 253–267.


Mikheev, V. M. (2006). Ekologiya serebryanogo karasya Carassius auratus gibelio Bloch tsentralnoy chasti Kuybyishevskogo vodohranilischa [Ecology silver crucian carp Carassius auratus gibelio Bloch in the central part of the Kuibyshev water reservoir]. Kazan (in Russian).


Nathanailides, C., Perdikaris, C., Gouva, E., & Paschos, I. (2003). Gibel carp (Carassius gibelio) growth under increased ammonia concentration. In: Proceedings of the 11th Panhellenic conference of ichthyologists. Chania. Pp. 178–181.


Özcan, G. (2007). Distribution of non-indigenous fish species, Prussian carp Carassius gibelio (Bloch, 1782) in the Turkish freshwater systems. Pakistan Journal of Biological Sciences, 10, 4241–4245.


Özdilek, Ş. Y., & Jones, R. I. (2014). The diet composition and trophic position of introduced Prussian carp Carassius gibelio (Bloch, 1782) and native fish species in a Turkish river. Turkish Journal of Fisheries and Aquatic Sciences, 14, 769–776.


Pankhurst, N. W., & Munday, P. L. (2011). Effects of climate change on fish reproduction and early life history stages. Marine and Freshwater Research, 62, 1015–1026.


Pankhurst, N. W., & Porter, M. J. R. (2003). Cold and dark or warm and light: Variations on the theme of environmental control of reproduction. Fish Physiology and Biochemistry, 28, 385–389.


Paschos, I., Nathanailides, C., Tsoumani, M., Perdicaris, C., Gouva, E., & Leonardos, I. (2004). Intra- and interspecific mating options for gynogenetic reproduction of Carassius gibelio (Bloch, 1783) in Lake Pamvotis (NW Greece). Belgian Journal of Zoology, 134, 55–60.


Paulovits, G., Tatrai, I., Matyas, K., Korponai, J., & Kovats, N. (1998). Role of Prussian carp (Carassius auratus gibelio Bloch) in the nutrient cycle of the Kis-Balaton Reservoir. Internationale Revue der Gesamten Hydrobiologie, 83, 467–470.


Pauly, D., & Pullin, R. S. V. (1988). Hatching time in spherical pelagic marine eggs in response to temperature and egg size. Environmental Biology of Fishes, 22, 261–271.


Penaz, M., & Kokes, J. (1981). Notes on the diet, growth and reproduction of Carassius auratus gibelio in two localities in southern Slovakia. Folia Zoologica, 30, 83–94.


Perdikaris, C., Ergolavou, A., Gouva, E., Nathanailides, C., Chantzaropoulos, A., & Paschos, I. (2012). Carassius gibelio in Greece: The dominant naturalised invader of freshwaters. Reviews in Fish Biology and Fisheries, 22, 17–27.


Scott, S. G., & Pankhurst, N. W. (1992). Interannual variation in the reproductive cycle of the New Zealand snapper Pagrus auratus (Bloch & Schneider) (Sparidae). Journal of Fish Biology, 41, 685–696.


Shimizu, A. (2003). Effect of photoperiod and temperature on gonadal activity and plasma steroid levels in a reared strain of the mummichog (Fundulus heteroclitus) during different phases of its annual reproductive cycle. General and Comparative Endocrinology, 131, 310–324.


Slavík, O., & Bartoš, L. (2004). What are the reasons for the Prussian carp expansion in the Upper Elbe River, Czech Republic? Journal of Fish Biology, 65, 240–253.


Sokolov, S. G., & Zhukov, A. V. (2014). Variation trends in the parasite assemblages of the Chinese sleeper Perccottus glenii (Actinopterygii: Odontobutidae) in its native habitat. Biology Bulletin, 41(5), 468–477.


Sokolov, S. G., & Zhukov, A. V. (2016). The diversity of parasites in the Chinese sleeper Perccottus glenii Dybowski, 1877 (Actinopterygii: Perciformes) under the conditions of large-scale range expansion. Biology Bulletin, 43(4), 374–383.


Sokolov, S. G., & Zhukov, A. V. (2017). Functional diversity of a parasite assemblages of the Chinese sleeper Perccottus glenii Dybowski, 1877 (Actinopterygii: Odontobutidae) and habitat structure of the host. Biology Bulletin, 44(3), 331–336.


Sponaugle, S., & Cowen, R. K. (1996). Larval supply and patterns of recruitment for two Caribbean reef fishes, Stegastes partitus and Acanthurus bahianus. Marine and Freshwater Research, 47, 433–447.


Sundby, S., & Nakken, O. (2008). Spatial shifts in spawning habitats of Arcto-Norwegian cod related to multidecadal climate oscillations and climate change. ICES Journal of Marine Science, 65, 1–10.


Szczerbowski, J. A. (2001). Carassius auratus. In: Banarescu, P., & Paepke, H. J. (Eds.). The freshwater fishes of Europe. Vol. 5. Cyprinidae-2, Part 3. Carassius to Cyprinus: Gasterosteidae. Germany. Pp. 5–41.


Tarkan, A. N., Gaygusuz, Ö., Tarkan, A. S., Gürsoy, Ç., & Acıpınar, H. (2007). Interannual variability of fecundity and egg size of an invasive cyprinid, Carassius gibelio: Effects of density-dependent and density-independent factors. Journal of Freswater Ecology, 22(1), 11–17.


Tarkan, A. S., Copp, G. H., Top, N., Özdemir, N., Önsoy, B., Bilge, G., Filiz, H., Yapici, S., Ekmekçi, G., Kırankaya, Ş., Emiroğlu, Ö., Gaygusuz, Ö., Gürsoy Gaygusuz, Ç., Oymak, A., Özcan, G., & Saç, G. (2012). Are introduced gibel carp Carassius gibelio in Turkey more invasive in artificial than in natural waters? Fisheries Management and Ecology, 19, 178–187.


Vetemaa, M., Eschbaum, R., Albert, A., & Saat, T. (2005). Distribution, sex ratio and growth of Carassius gibelio (Bloch) in coastal and inland waters of Estonia (Northeastern Baltic Sea). Journal of Applied Ichthyology, 21, 287–291.


Wingate, R. L., & Secor, D. H. (2008). Effects of winter temperature and flow on a summer-fall nursery fish assemblage in the Chesapeake Bay, Maryland. Transactions of the American Fisheries Society, 137, 1147–1156.


Ye, L., Yang, G., Van Ranst, E., & Tang, H. (2013). Time-series modeling and prediction of global monthly absolute temperature for environmental decision making. Advances in Atmospheric Sciences, 30, 382–396.


Zhu, X., Xie, S., Zou, Z., Lei, W., Cui, Y., Yang, Y., & Wootton, R. J. (2004). Compensatory growth and food consumption in gibel carp, Carassius auratus gibelio, and Chinese longsnout catfish Leiocassis longirostris, experiencing cycles of feed deprivation and re-feeding. Aquaculture, 241, 235–247.


Zhukov, O. V., & Gubanova, N. L. (2015a). Dynamic stability of communities of amphibians in short-term-floodedforest ecosystems. Visnyk of Dnipropetrovsk University, Biology, Ecology, 23(2), 161–171.


Zhukov, O. V., & Gubanova, N. L. (2015b). Diversity and dynamics of amphibians in floodplain ecosystems of the Samara river. Visnyk of Dnipropetrovsk University, Biology, Ecology, 23(1), 66–73.

Published
2019-05-12
Section
Articles