Multiscale oscillations of the annual course of temperature affect the spawning events of rudd (Scardinus erythrophthalmus)

  • O. M. Kunakh Oles Honchar Dnipro National University
  • D. L. Bondarev “Dnipro-Orylskiy” Nature Reserve
  • N. L. Gubanova Dnipro State Agrarian and Economic University
  • A. V. Domnich Zaporizhzhia National University
  • O. V. Zhukov Bogdan Khmelnitsky Melitopol State Pedagogical University
Keywords: temporal pattern; phenology; climate change; oscilation dynamic; hierahy; temporal scales; biological rhythm


Identifying climate impacts on ecosystems and their components requires observing time series of sufficient length to ensure adequate statistical power and reasonable coverage of the historical range of variability inherent in the system. The complexity of the hierarchy of climate effects reflected in temporal patterns in time series creates a need to be accurately modeled. The life cycle phenomena of living organisms, including fish spawning, have the character of one-time or time-limited events in time. An approach to finding the relationship between continuous components of time dynamics of environment properties and life cycle events of living organisms was proposed. This approach allowed us to evaluate the role of temperature patterns in the phenology of spawning rudd (Scardinus erythrophthalmus Linnaeus, 1758) in the Dnipro River basin water bodies. The atmospheric temperature time series may be decomposed into the following components: trend, annual cycle, episodic component, harmonic component, extreme events, and noise. Systematically low water temperatures at the beginning of the spawning period were observed in the Protoka River system and the Obukhov floodplain, and systematically elevated temperatures were recorded in the Dnipro River. The annual temperature dynamics was shown to be presented as a composition of oscillatory processes of different scale levels. The sinusoidal trend was previously extracted from the temperature series data. The average annual temperature, amplitude, and phase shift were calculated on the basis of the sinusoidal regression model. The residuals of the sinusoidal trend were processed by means of redundancy analysis with variables derived from symmetric distance-based Moran’s eigenvector maps as explanatory predictors. A set of 104 orthogonal dbMEM variables was extracted from the annual time series. These temporal variables were divided into the broad-, medium-, and fine-scale components. The parameters of temperature dynamics and biotope type are able to explain 51–72% of variability of spawning event. The time of spawning in water bodies corresponds to the time of spawning start: the earlier spawning starts, the earlier it ends. The duration of the spawning season is influenced by the patterns of different scale levels, as well as the amplitude and shift of phases. In this case, the duration of spawning in all water bodies does not differ. Spawning temperature depends on medium- and fine-scale temperature patterns, but does not depend on the characteristics of the sinusoidal annual trend. The annual temperature variation has been shown to be such that it can be decomposed into a sinusoidal trend, patterns of a multiscale nature, and a random fraction. Over the time range studied, the trend of increasing mean annual temperature was not statistically significant for spawning events. The sinusoidal trend explains 78.3–87.6% of the temperature variations and depends on the mean annual temperature, the amplitude of temperature variations during the year, and the earlier or later seasons of the year. Amplitude and phase shift play a role in describing spawning phenology. The residuals of the sinusoidal trend have been explained using dbMEM variables. This variation was decomposed into large-scale, medium-scale, and small-scale components. Winter and spring temperature fluctuations prior to spawning initiation had the greatest effect on spawning. Water temperature determines the lower possible limit for the start of spawning, but the actual start of spawning is determined by the preceding temperature dynamics. The results of the study have implications for understanding the dynamics of fish populations and assessing the influence of environmental conditions on the harmonization of the various components of ecosystems.


Alavi, S. M. H., & Cosson, J. (2005). Sperm motility in fishes. I. Effects of temperature and pH: A review. Cell Biology International, 29(2), 101–110.

Allen, C. R., Angeler, D. G., Garmestani, A. S., Gunderson, L. H., & Holling, C. S. (2014). Panarchy: Theory and application. Ecosystems, 17(4), 578–589.

Angeler, D. G., Viedma, O., & Moreno, J. M. (2009). Statistical performance and information content of time lag analysis and redundancy analysis in time series modeling. Ecology, 90(11), 3245–3257.

Avtaeva, T., Petrovičová, K., Langraf, V., & Brygadyrenko, V. (2021). Potential bioclimatic ranges of crop pests Zabrus tenebrioides and Harpalus rufipes during climate change conditions. Diversity, 13(11), 559.

Baho, D. L., Futter, M. N., Johnson, R. K., & Angeler, D. G. (2015). Assessing temporal scales and patterns in time series: Comparing methods based on redundancy analysis. Ecological Complexity, 22, 162–168.

Berg, L. S. (1949). Fishes of fresh waters of the USSR and adjacent countries. Vol. 2. AN SSSR, Moscow, Leningrad.

Billard, R. (1986). Spermatogenesis and spermatology of some teleost fish species. Reproduction Nutrition Développement, 26(4), 877–920.

Billard, R., Breton, B., Fostier, A., Jalabert, B., & Weil, C. (1978). Endocrine control of the teleos reproductive cycle and its relation to external factors: Salmonid and cyprinid models. In: Gaillard, H. H. B. P. J. (Ed.). Comparative endocrinology. North Holland Biomedical Press, Amsterdam. Pp. 37–47.

Black, B. A., Schroeder, I. D., Sydeman, W. J., Bograd, S. J., & Lawson, P. W. (2010). Wintertime ocean conditions synchronize rockfish growth and seabird reproduction in the Central California current ecosystem. Canadian Journal of Fisheries and Aquatic Sciences, 67(7), 1149–1158.

Blanchet, F. G., Bergeron, J. A. C., Spence, J. R., & He, F. (2013). Landscape effects of disturbance, habitat heterogeneity and spatial autocorrelation for a ground beetle (Carabidae) assemblage in mature boreal forest. Ecography, 36(5), 636–647.

Bondarev, D. L., Fedyushko, M. P., Gubanova, N. L., & Zhukov, O. V. (2020). The temporal dynamic of young fish communities in the water bodies of the “Dnipro-Orylskiy” Nature Reserve. Agrology, 3(3), 145–159.

Bondarev, D., Fedushko, M., Hubanova, N., Novitskiy, R., Kunakh, O., & Zhukov, O. (2022). Temporal dynamics of the fish communities in the reservoir: The influence of eutrophication on ecological guilds structure. Ichthyological Research, in press.

Bondarev, D., Kunakh, 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), 61.

Borcard, D., & Legendre, P. (2002). All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecological Modelling, 153, 51–68.

Boznak, E. I. (2008). The rudd Scardinius erythrophthalmus from tributaries of the Northern Dvina. Journal of Ichthyology, 48(5), 408–410.

Breton, B., Horoszewicz, L., Billard, R., & Bieniarz, K. (1980). Temperature and reproduction in tench: Effect of a rise in the annual temperature regime on gonadotropin level, gametogenesis and spawning. I. The male. Reproduction Nutrition Développement, 20(1A), 105–118.

Brett, J. R. (1979). Environmental factors and growth. In: Hoar, W. S., Randall, D. J., & Brett, J. R. (Eds.). Fish physiology. Vol. 8: Bioenergetics and growth. Academic Press, New York, London. Pp. 599–675.

Bulakhov, V. L., Novitsky, R. O., Pakhomov, O. E., & Khristov, O. O. (2008). Biological diversity of Ukraine. Dnipropetrovsk region. Cyclostomes (Cyclostomata). Fishes (Pisces). Dnipropetrovsk University Press, Dnipropetrovsk.

Bulla, M., Oudman, T., Bijleveld, A. I., Piersma, T., & Kyriacou, C. P. (2017). Marine biorhythms: Bridging chronobiology and ecology. Philosophical Transactions of the Royal Society B: Biological Sciences, 372(1734), 20160253.

Chavez, F. P., Ryan, J., Lluch-Cota, S. E., & Ñiquen, C. M. (2003). From anchovies to sardines and back: Multidecadal change in the Pacific Ocean. Science, 299(5604), 217–221.

Cooper, S. D., Diehl, S., Kratz, K., & Sarnelle, O. (1998). Implications of scale for patterns and processes in stream ecology. Austral Ecology, 23(1), 27–40.

Domagała, J., Kirczuk, L., & Pilecka-Rapacz, M. (2013). Annual development cycle of gonads of Eurasian ruffe (Gymnocephalus cernuus L.) females from lower Odra River sections differing in the influence of cooling water. Journal of Freshwater Ecology, 28(3), 423–437.

Dray, S., Legendre, P., & Peres-Neto, P. R. (2006a). Spatial modelling: A comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecological Modelling, 196, 483–493.

Fedushko, M. P., Bondarev, D. L., Gubanova, N. L., & Zhukov, O. V. (2021). Effects of eutrophication on the long-term dynamics of juvenile fish communities. Agrology, 4(4), 149–164.

Forrest, J., & Miller-Rushing, A. J. (2010). Toward a synthetic understanding of the role of phenology in ecology and evolution. Philosophical Transactions of the Royal Society B: Biological Sciences, 365(1555), 3101–3112.

Gao, J., Hu, J., & Wen Tung, W. (2011). Facilitating joint chaos and fractal analysis of biosignals through nonlinear adaptive filtering. PLoS One, 6(9), e24331.

Gao, J., Hu, J., Mao, X., & Perc, M. (2012). Culturomics meets random fractal theory: Insights into long-range correlations of social and natural phenomena over the past two centuries. Journal of The Royal Society Interface, 9(73), 1956–1964.

Garcia, A. M., Vieira, J. P., Winemiller, K. O., Moraes, L. E., & Paes, E. T. (2012). Factoring scales of spatial and temporal variation in fish abundance in a subtropical estuary. Marine Ecology Progress Series, 461, 121–135.

Goto, S. G., & Takekata, H. (2015). Circatidal rhythm and the veiled clockwork. Current Opinion in Insect Science, 7, 92–97.

Gwinner, E. (1986). Evidence for circannual rhythms. In: Bradshaw, S. D., Burggren, W., Heller, H. C., Ishii, S., Langer, H., Randall, D. J., & Neuweiler, G. (Eds.). Zoophysiology. Springer. Pp. 11–38.

Herzig, A., & Winkler, H. (1986). The influence of temperature on the embryonic development of three cyprinid fishes, Abramis brama, Chalcalburnus chalcoides mento and Vimba vimba. Journal of Fish Biology, 28(2), 171–181.

Jafri, S. (1989). The effects of photoperiod and temperature manipulation on reproduction in the roach, Rutilus rutilus (L.) (Teleostei). Pakistan Journal of Zoology, 213, 289–299.

Jobling, M. (2003). The thermal growth coefficient (TGC) model of fish growth: A cautionary note. Aquaculture Research, 34(7), 581–584.

Kennedy, M., & Fitzmaurice, P. (1974). Biology of the rudd Scardinius erythrophthalmus (L.) in Irish Waters. Proceedings of the Royal Irish Academy. Section B: Biological, Geological, and Chemical Science, 74(18), 245–303.

Kodba, S., Perc, M., & Marhl, M. (2005). Detecting chaos from a time series. European Journal of Physics, 26(1), 205.

Korzelecka, A., & Winnicki, A. (1998). Peculiarities of embryogenesis in Scardinius erythrophthalmus L. Electronic Journal of Polish Agricultural Universities. Series Fisheries, 1, 1.

Koshelev, O., Koshelev, V., Fedushko, M., & Zhukov, O. (2021). Annual course of temperature and precipitation as proximal predictors of birds’ responses to climatic changes on the species and community level. Folia Oecologica, 48(2), 118–135.

Kottelat, M., & Freyhof, J. (2007). Handbook of European freshwater fishes. Maurice Kottelat, Cornol, Switzerland.

Lahnsteiner, F., & Mansour, N. (2012). The effect of temperature on sperm motility and enzymatic activity in brown trout Salmo trutta, burbot Lota lota and grayling Thymallus thymallus. Journal of Fish Biology, 81(1), 197–209.

Legendre, P., & Legendre, L. (2012). Canonical analysis. Developments in Environmental Modelling, 24(C), 625–710.

Levin, S. A. (1992). The problem of pattern and scale in ecology: The Robert H. Mac Arthur award lecture. Ecology, 73(6), 1943–1967.

Marques, L. V., Short, F. T., & Creed, J. C. (2015). Sunspots drive seagrasses. Biological Rhythm Research, 46(1), 63–68.

McGowan, J. A., Cayan, D. R., & Dorman, L. M. (1998). Climate-ocean variability and ecosystem response in the Northeast Pacific. Science, 281(5374), 210–217.

Morisette, J. T., Richardson, A. D., Knapp, A. K., Fisher, J. I., Graham, E. A., Abatzoglou, J., Wilson, B. E., Breshears, D. D., Henebry, G. M., Hanes, J. M., & Liang, L. (2009). Tracking the rhythm of the seasons in the face of global change: Phenological research in the 21st century. Frontiers in Ecology and the Environment, 7(5), 253–260.

Nash, K. L., Allen, C. R., Angeler, D. G., Barichievy, C., Eason, T., Garmestani, A. S., Graham, N. A. J., Granholm, D., Knutson, M., Nelson, R. J., Nyström, M., Stow, C. A., & Sundstrom, S. M. (2014). Discontinuities, cross-scale patterns, and the organization of ecosystems. Ecology, 95(3), 654–667.

Nõges, P., & Järvet, A. (2005). Climate driven changes in the spawning of roach (Rutilus rutilus (L.)) and bream (Abramis brama (L.)) in the Estonian part of the Narva River basin. Boreal Environment Research, 10(1), 45–55.

Papageorgiou, N., & Neophytou, C. (1982). Age, growth and fecundity of the rudd (Scardinius erythrophthalmus L.) in Lake Kastoria. Thalassographica, 2, 5–15.

Patimar, R., Nadjafypour, E., Yaghouby, M., & Nadjafy, M. (2010). Reproduction characteristics of a stunted population of rudd, Scardinius erythrophthalmus (Linnaeus, 1758) living in the Anzali Lagoon (the Southwest Caspian Sea, Iran). Journal of Ichthyology, 50(11), 1060–1065.

Perry, A. L., Low, P. J., Ellis, J. R., & Reynolds, J. D. (2005). Climate change and distribution shifts in marine fishes. Science, 308(5730), 1912–1915.

Raible, F., Takekata, H., & Tessmar-Raible, K. (2017). An overview of monthly rhythms and clocks. Frontiers in Neurology, 8(5), 1–14.

Rheinberger, V., Hofer, R., & Wieser, W. (1987). Growth and habitat separation in eight cohorts of three species of cyprinids in a subalpine lake. Environmental Biology of Fishes, 18(3), 209–217.

Sandstrom, O., Neuman, E., & Thoresson, G. (1995). Effects of temperature on life history variables in perch. Journal of Fish Biology, 47(4), 652–670.

Scheffer, M., & Van Nes, E. H. (2007). Shallow lakes theory revisited: Various alternative regimes driven by climate, nutrients, depth and lake size. Hydrobiologia, 584(1), 455–466.

Schneider, K. N., Newman, R. M., Card, V., Weisberg, S., & Pereira, D. L. (2010). Timing of walleye spawning as an indicator of climate change. Transactions of the American Fisheries Society, 139(4), 1198–1210.

Shikhshabekov, M. M. (1979). The reproductive biology of the “kutum”, Rutilus frisii kutum, the asp, Aspius aspius, the vimba, Vimba vimba persa, and the rudd, Scardinius erythrophthalmus, in the waters of Dagestan. Journal of Ichthyology, 19, 98–105.

Stehlik, J. (1968). Fecundity of Scardinius erythrophthalmus L. Acta Musei Silesiae, 17, 81–88.

Tarkan, A. S. (2006). Reproductive ecology of two cyprinid fishes in an oligotrophic lake near the southern limits of their distribution range. Ecology of Freshwater Fish, 15(2), 131–138.

Vejříková, I., Vejřík, L., Syväranta, J., Kiljunen, M., Čech, M., Blabolil, P., Vašek, M., Sajdlová, Z., Chung, S. H. T., Šmejkal, M., Frouzová, J., & Peterka, J. (2016). Distribution of herbivorous fish is frozen by low temperature. Scientific Reports, 6(1), 1–11.

Vila-Gispert, A., & Moreno-Amich, R. (2000). Fecundity and spawning mode of three introduced fish species in Lake Banyoles (Catalunya, Spain) in comparison with other localities. Aquatic Sciences, 62(2), 154–166.

Vislocky, R. L., & Fritsch, J. M. (1995). Generalized additive models versus linear regression in generating probabilistic MOS forecasts of aviation weather parameters. Weather and Forecasting, 10(4), 669–680.

Weijerman, M., Lindeboom, H., & Zuur, A. (2005). Regime shifts in marine ecosystems of the North Sea and Wadden Sea. Marine Ecology Progress Series, 298, 21–39.

Zerunian, S., Valentini, L., & Gibertini, G. (1986). Growth and reproduction of rudd and red-eye roach (Pisces, Cyprinidae) in Lake Bracciano. Bolletino Di Zoologia, 53(1), 91–95.

Zhukov, O. V., Bondarev, D. L., Yermak, Y. I., & Fedushko, M. P. (2019). Effects of temperature patterns on the spawining phenology and niche overlap of fish assemblages in the water bodies of the Dnipro River basin. Ecologica Montenegrina, 22, 177–203.

How to Cite
Kunakh, O. M., Bondarev, D. L., Gubanova, N. L., Domnich, A. V., & Zhukov, O. V. (2022). Multiscale oscillations of the annual course of temperature affect the spawning events of rudd (Scardinus erythrophthalmus) . Regulatory Mechanisms in Biosystems, 13(2), 180-188.