Predator-prey relationships are often perceived simply as a situation in which a predator enhances its own fitness while reducing the fitness of its prey. However, this relationship may become reversed when the prey feeds on the juvenile predator stages. We investigated this phenomenon in a model asp (Leuciscus aspius; predator)-bleak (Alburnus alburnus; prey) relationship. The adhesive asp eggs are available for bleak predation after a spawning event for only tens of seconds before they adhere to the stones, where bleak do not forage. Gut content analysis demonstrated that eggs were utilized in high quantities, especially in the spawning peak of the asp reproductive season. Furthermore, using underwater video, we recorded the bleak feeding efficiency on naturally drifting asp eggs as the percentage of eggs eaten. Within the 40 cm egg trajectory captured by our cameras, total egg mortality was 21.2 ± 2.2% on average. The highest survival chances occurred among eggs drifting in aggregations, since the short drifting distance together with their aggregated distribution satiated bleak and part of the egg aggregation could attach to the spawning ground. This study emphasizes the potential efficiency of predator egg utilization by prey, which may have further consequences in predator-prey dynamics.

Faculty of Economics University of South Bohemia Ceske Budejovice Czech Republic

Faculty of Science University of South Bohemia Ceske Budejovice Czech Republic

Institute of Hydrobiology Biology Centre of the Czech Academy of Sciences Ceske Budejovice Czech Republic

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Kozlowski J. Optimal allocation of resources explains interspecific life-history patterns in animals with indeterminate growth. Proc. R. Soc. B Biol. Sci. 1996;263:559–566. doi: 10.1098/rspb.1996.0084. DOI

Hjelm J, Persson L, Christensen B. Growth, morphological variation and ontogenetic niche shifts in perch (Perca fluviatilis) in relation to resource availability. Oecologia. 2000;122:190–199. doi: 10.1007/PL00008846. PubMed DOI

Sargent RC, Taylor PD, Gross MR. Parental care and the evolution of egg size in fishes. Am. Nat. 1987;129:32–46. doi: 10.1086/284621. DOI

Brett MT, Goldman CR. A meta-analysis of the freshwater trophic cascade. Proc. Natl. Acad. Sci. 1996;93:7723–7726. doi: 10.1073/pnas.93.15.7723. PubMed DOI PMC

Köster FW, Möllmann C. Trophodynamic control by clupeid predators on recruitment success in Baltic cod? ICES J. Mar. Sci. 2000;57:310–323. doi: 10.1006/jmsc.1999.0528. DOI

Duarte CM, Alcaraz M. To produce many small or few large eggs: a size-independent reproductive tactic of fish. Oecologia. 1989;80:401–404. doi: 10.1007/BF00379043. PubMed DOI

Chase JM. Are there real differences among aquatic and terrestrial food webs? Trends Ecol. Evol. 2000;15:408–412. doi: 10.1016/S0169-5347(00)01942-X. PubMed DOI

Winemiller KO, Rose KA. Why do most fish produce so many tiny offspring? Am. Nat. 1993;142:585–603. doi: 10.1086/285559. PubMed DOI

Mcbride RS, et al. Energy acquisition and allocation to egg production in relation to fish reproductive strategies. Fish Fish. 2015;16:23–57. doi: 10.1111/faf.12043. DOI

Kamler E. Parent-egg-progeny relationships in teleost fishes: An energetics perspective. Reviews in Fish Biology and Fisheries. 2005;15:399–421. doi: 10.1007/s11160-006-0002-y. DOI

Tinbergen L. The natural control of insects in pinewoods. Arch. Néerlandaises Zool. 1960;13:265–343. doi: 10.1163/036551660X00053. DOI

Fox CJ, et al. Identification of marine fish egg predators using molecular probes. Mar. Ecol. Prog. Ser. 2012;462:205–218. doi: 10.3354/meps09748. DOI

Power ME. Top-down and bottom-up forces in food webs: do plants have primacy? Ecology. 1992;73:733–746. doi: 10.2307/1940153. DOI

Barkai A, Mcquaid C. Predator-prey role reversal in a marine benthic ecosystem. Science. 1988;242:62–64. doi: 10.1126/science.242.4875.62. PubMed DOI

Plirú A, et al. Sprat feeding behaviour, selective predation, and impact on plaice egg mortality. ICES J. Mar. Sci. 2012;69:1019–1029. doi: 10.1093/icesjms/fss081. DOI

Levine DS. On the stability of a predator-prey system with egg-eating predators. Math. Biosci. 1981;56:27–46. doi: 10.1016/0025-5564(81)90026-2. DOI

Leggett WC, Deblois E. Recruitment in marine fishes: Is it regulated by starvation and predation in the egg and larval stages? Netherlands J. Sea Res. 1994;32:119–134. doi: 10.1016/0077-7579(94)90036-1. DOI

Choh Y, Ignacio M, Sabelis MW, Janssen A. Predator-prey role reversals, juvenile experience and adult antipredator behaviour. Sci. Rep. 2012;2:1–6. doi: 10.1038/srep00728. PubMed DOI PMC

Bailey KM, Brodeur RD, Merati N, Yoklavich MM. Predation on walleye pollock (Theragra chalcogramma) eggs and yolk-sac larvae by pelagic crustacean invertebrates in the western Gulf of Alaska. Fish. Oceanogr. 1993;2:30–39. doi: 10.1111/j.1365-2419.1993.tb00010.x. DOI

Wizen G, Gasith A. An unprecedented role reversal: Ground beetle larvae (Coleoptera: Carabidae) lure amphibians and prey upon them. PLoS One. 2011;6:e25161. doi: 10.1371/journal.pone.0025161. PubMed DOI PMC

Schaeffer JS, Margraf FJ. Predation on fish eggs by white perch, Morone americana, in western Lake Erie. Environ. Biol. Fishes. 1987;18:77–80. doi: 10.1007/BF00002331. DOI

Chotkowski MA, Ellen Marsden J. Round goby and mottled sculpin predation on lake trout eggs and fry: field predictions from laboratory experiments. J. Great Lakes Res. 1999;25:26–35. doi: 10.1016/S0380-1330(99)70714-8. DOI

Bailey KM, Houde ED. Predation on eggs and larvae of marine fishes and the recruitment problem. Adv. Mar. Biol. 1989;25:1–83. doi: 10.1016/S0065-2881(08)60187-X. DOI

Deblois EM, Leggett WC. Functional response and potential impact of invertebrate predators on benthic fish eggs: analysis of the Calliopius laeviusculus-capelin (Mallotus villosus) predator-prey system. Mar. Ecol. Prog. Ser. 1991;69:205–216. doi: 10.3354/meps069205. DOI

Specziár A, Rezsu ET. Feeding guilds and food resource partitioning in a lake fish assemblage: An ontogenetic approach. J. Fish Biol. 2009;75:247–267. doi: 10.1111/j.1095-8649.2009.02283.x. PubMed DOI

Vašek M, et al. Development of non-lethal monitoring of stable isotopes in asp (Leuciscus aspius): a comparison of muscle, fin and scale tissues. Hydrobiologia. 2016;785:327–335.

Šmejkal, M. et al. Seasonal and daily protandry in a cyprinid fish. Sci. Rep. 7, 4737 (2017). PubMed PMC

Šmejkal, M. et al. Population size, age structure and spawning dynamics of asp (Leuciscus aspius) in Želivka Reservoir (in Czech). (2016).

Vøllestad LA. Resource partitioning of roach Rutilus rutilus and bleak Alburnus alburnus in two eutrophic lakes in SE Norway. Holarct. Ecol. 1985;8:88–92.

Vašek M, Kubečka J. In situ diel patterns of zooplankton consumption by subadult/adult roach Rutilus rutilus, bream Abramis brama, and bleak Alburnus alburnus. Folia Zool. 2004;53:203–214.

Prchalová M, et al. The effect of depth, distance from dam and habitat on spatial distribution of fish in an artificial reservoir. Ecol. Freshw. Fish. 2009;18:247–260. doi: 10.1111/j.1600-0633.2008.00342.x. DOI

Krpo-Ćetković J, Hegediš A, Lenhardt M. Diet and growth of asp, Aspius aspius (Linnaeus, 1758), In the Danube River near the confluence with the Sava River (Serbia) J. Appl. Ichthyol. 2010;26:513–521. doi: 10.1111/j.1439-0426.2010.01456.x. DOI

McGurk MD. Natural mortality of marine pelagic fish eggs and larvae: role of spatial patchiness. Mar. Ecol. Prog. Ser. 1986;34:227–242. doi: 10.3354/meps034227. DOI

Alheit J. Egg cannibalism versus egg predation: their significance in anchovies. South African J. Mar. Sci. 1987;5:467–470. doi: 10.2989/025776187784522694. DOI

Ellis T, Nash RDM. Predation by sprat and herring on pelagic fish eggs in a plaice spawning area in the Irish Sea. J. Fish Biol. 1997;50:1195–1202. doi: 10.1111/j.1095-8649.1997.tb01647.x. DOI

Roseman EF, Taylor WW, Hayes DB, Jones AL, Francis JT. Predation on walleye eggs by fish on reefs in western Lake Erie. J. Great Lakes Res. 2006;32:415–423. doi: 10.3394/0380-1330(2006)32[415:POWEBF]2.0.CO;2. DOI

Silbernagel JJ, Sorensen PW. Direct field and laboratory evidence that a combination of egg and larval predation controls recruitment of invasive common carp in many lakes of the upper Mississippi River basin. Trans. Am. Fish. Soc. 2013;142:1134–1140. doi: 10.1080/00028487.2013.788889. DOI

Hamilton WD. Geometry for the selfish herd. J. Theor. Biol. 1971;31:295–311. doi: 10.1016/0022-5193(71)90189-5. PubMed DOI

Turchin P, Kareiva P. Aggregation in Aphis varians: an effective strategy for reducing predation risk. Ecology. 1989;70:1008–1016. doi: 10.2307/1941369. DOI

Ims RA. On the adaptive value of reproductive synchrony as a predator-swamping strategy. Am. Nat. 1990;136:485–498. doi: 10.1086/285109. DOI

Targoñska K, Zarski D, Kucharczyk D. A review of the artificial reproduction of asp, Aspius aspius (L.), and nase, Chondrostoma nasus (L.) Arch. Polish Fish. 2008;16:341–354.

Billard R, Cosson J, Perchec G, Linhart O. Biology of sperm and artificial reproduction in carp. Aquaculture. 1995;129:95–112. doi: 10.1016/0044-8486(94)00231-C. DOI

Andersen KH, Jacobsen NS, Jansen T, Beyer JE. When in life does density dependence occur in fish populations? Fish Fish. 2016;0:00–00.

Bajer PG, Chizinski CJ, Silbernagel JJ, Sorensen PW. Variation in native micro-predator abundance explains recruitment of a mobile invasive fish, the common carp, in a naturally unstable environment. Biol. Invasions. 2012;14:1919–1929. doi: 10.1007/s10530-012-0203-3. DOI

Hladík M, Kubečka J. Fish migration between a temperate reservoir and its main tributary. Hydrobiologia. 2003;504:251–266. doi: 10.1023/B:HYDR.0000008525.46939.42. DOI

Fuiman LA, Connelly TL, Lowerre-Barbieri SK, Mcclelland JW. Egg boons: Central components of marine fatty acid food webs. Ecology. 2015;96:362–372. doi: 10.1890/14-0571.1. PubMed DOI

Křížek, J. & Vostradovský, J. Population dynamics of the rapacious carp (Aspius aspius L.) in the Želivka Reservoir in 1972–1992. 4thInt. Conf. Reserv. Limnol. waterQual. ČeskéBudějovice, CzechRepublic, B. Abstr. 180–182 (2002).

Říha M, et al. Patterns in diel habitat use of fish covering the littoral and pelagic zones in a reservoir. Hydrobiologia. 2015;747:111–131. doi: 10.1007/s10750-014-2124-x. DOI

Vašek M, et al. The use of pelagic habitat by cyprinids in a deep riverine impoundment: Římov Reservoir, Czech Republic. Folia Zool. 2008;57:324–336.

R Core Team. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2015).

Esri. Working with ArcMap. ArcGIS Help 10.2.2. http://desktop.arcgis.com/en/arcmap/ (2016).

Nocturnal spawning as a way to avoid egg exposure to diurnal predators