Abstract
In 2019, during spring flood, we collected unusual Lampetra fluviatilis smolts migrating from a small lake, as part of a multi-year survey in the Chernaya River (Gulf of Finland, Baltic Sea). They differed from the ordinary Lampetra fluviatilis individuals in some of the features, mainly size. The emigration occurred at the darkest period of night and during extreme flooding, which significantly worsened the conditions in the Lake Gladyshevskoe and Chernaya River. In these individuals, lacus smolts, emigration occurred in the spring season with the migration of ordinary flumen specimens. Several hypotheses are discussed to explain the observation of large lacus (148–165 mm) individuals: they are seaward migrants, within expected body sizes of European river lamprey species but unusual for Gulf of Finland tributaries; the lake is a transitional habitat, and the postmetamorphic lacus juveniles migrating through it from a tributary; postmetamorphic lacus juveniles spend some time feeding in a lake but emigrated due to environmental conditions; larvae of European river lamprey, developing in the eutrophic lake, reach greater sizes than riverine larvae before transformation and subsequently produce larger juveniles.
Similar content being viewed by others
Data availability
Samples designated IEE are stored in the collection of lampreys in the Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia, and datasets of their geographic positions are deposited in the GBIF. Samples designated NRM are stored in the collection of fish and amphibians of the Swedish Museum of Natural History (Stockholm, Sweden). Data may be shared by the authors upon reasonable request.
References
Adams CE, Bissett N, Newton J et al (2008) Alternative migration and host parasitism strategies and their long-term stability in river lampreys from the River Endrick, Scotland. J Fish Biol 72:2456–2466
Almaça C (1995) Freshwater fish and their conservation in Portugal. Biol Conserv 72:125–127
Applegate VC, Brynildson CL (1952) Downstream movement of recently transformed sea lamprey, Petromyzon marinus, in the Carp Lake River. Michigan Trans Am Fish Soc 81(1):275–290
Appy R, Anderson RC (1981) The parasites of lampreys. The biology of Lampreys, Vol. 3, Eds. Hardisty M.W., Potter I.C., London – New York, Academic Press
Atlas presnovodnykh ryb Rossii (Atlas of Freshwater Fishes of Russia) (2002), Vol. 1, Ed. Reshetnikov, Yu.S., Nauka, Moscow
Baer J, Hartmann F, Brinker A (2018) Abiotic triggers for sea and river lamprey spawning migration and juvenile outmigration in the River Rhine. Germany Ecol Freshw Fish 27(4):988–998
Bartels H, Potter IC (2004) Cellular composition and ultrastructure of the gill epithelium of larval and adult lampreys: implications for osmoregulation in fresh and seawater. J Experimental Biol 207:3447–3462
Beamish RJ, Levings CD (1991) Abundance and freshwater migrations of the anadromous parasitic lamprey, Lampetra tridentata, in a tributary of the Fraser River, British Columbia. Can J Fish Aquat Sci 48(7):1250–1263
Berg OK (2005) Fisker, Amfibier og Krypdyr. Kompetendum IZO2001 – Faunistikk. Inst Biol NTNU, Trondheim
Berg LS (1948) Freshwater fishes of the USSR and adjacent countries. Guide to the fauna of the USSR, No. 27. Vol. 1. Israel Program for Scientific Translations Ltd., Jerusalem
Bills TD, Boogaard MA, Johnson DA et al (2003) Development of a pH/alkalinity treatment model for applications of the lampricide TFM to streams tributary to the Great Lakes. J Great Lakes Res 29:510–520
Bogatov VV, Fedorovski AS (2017) Osnovy gidrologii i gidrobiologii. Dalnauka, Vladivostok. 384
Bracken FSA, Lucas MC (2013) Potential impacts of small-scale hydroelectric power generation on downstream moving lampreys. River Res Appl 29:1073–1081
Budy P, Thiede GP, Bouwes N et al (2002) Evidence linking delayed mortality of Snake River salmon to their earlier hydrosystem experience. North Am J Fish Manage 22(1):35–51
Chernova NV, Lajus DL (2018) Sea lamprey. In: Red Data Book of Leningrad Oblast. Animals. Saint-Petersburg, Russia: Papirus. 337–338
Clemens BJ, Arakawa H, Baker C, Coghlan S et al (2021) Management of anadromous lampreys: common challenges, different approaches. J Great Lakes Res 46(Supplement 1):S129–S146. https://doi.org/10.1016/j.jglr.2020.09.005
Dawson HA, Quintella BR, Almeida PR et al (2015) The ecology of larval and metamorphosing lampreys. In: MF Docker, editor. Lampreys: biology, conservation and control. Dordrecht, Germany: Springer; p. 75–137. (Fish and Fisheries series 37; vol. 1)
Degerman E (2002) Fisk, fiske och miljö i de fyra stora sjöarna från istid till nutid. PM till Naturvårdsverket, 249 s
Docker MF, Potter IC (2019) Life history evolution in lampreys: alternative migratory and feedings types. In: Docker, M.F. (Ed.), Lampreys: biology, conservation and control. Vol. 2. Fish and Fisheries Series, Vol. 38. Springer, Dordrecht, The Netherlands. 287–410
Ducasse J, Leprince Y (1980) Etude preliminaire de la biologie des lamproies dans les bassins de la Garonne et de la Dordogne. Bordeaux: CTGREF–Div. ALA, 151
Eneqvist P (1938) The brook lamprey as an ecological modification of the river lamprey. On the river and brook lampreys of Sweden. Arkiv for Zoologi 29A:1–22
Fodale MF, Bronte CR, Bergstedt RA et al (2003) Classification of lentic habitat for sea lamprey (Petromyzon marinus) larvae using a remote seabed classification device. J Great Lakes Research 29(1):190–203
Goodman DH, Reid SB, Som NA et al (2015) The punctuated seaward migration of pacific lamprey (Entosphenus tridentatus): environmental cues and implications for streamflow management. Can J Fish Aquat Sci 72(12):1817–1828
Goodwin CE, Dick JTA, Rogowski DL et al (2008) Lamprey (Lampetra fluviatilis and Lampetra planeri) ammocoetes habitat associations at regional, catchment and microhabitat scales in Northern Ireland. Ecol Freshwater Fish 17(4):542–553
Goodwin CE, Griffits D, Dick JTA et al (2006) A freshwater-feeding Lampetra fluviatilis L. population in Lough Neagh. Northern Ireland J Fish Biol 68:628–633
Hansen MJ, Madenjian CP, Slade JW et al (2016) Population ecology of the sea lamprey (Petromyzon marinus) as an invasive species in the Laurentian Great Lakes and an imperiled species in Europe. Rev Fish Biol Fisheries 26:509–535
Hammer Ø, Harper DAT, Ryan PD (2001) Past: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 4(1):9–18
Hardisty MW (1944) The life history and growth of the brook lamprey (Lampetra planeri). J Animal Ecol 13:110–122
Hardisty MW (1986) Petromyzontiforma. In: Holcik J (ed) The freshwater fishes of Europe. Aula-Verlag, Wiesbaden
Hardisty MW, Potter IC (1971) The general biology of adult lampreys. In: Hardisty MW, Potter IC (eds) The Biology of Lampreys. Academic Press, London
Hume JB (2011) Adult lamprey survey of the Endrick Water SSSI and SAC 2009–2010. Scottish Natural Heritage Commissioned Report No. 480
Hume JB (2013) The evolutionary ecology of lampreys (Petromyzontiformes). PhD thesis. University of Glasgow, Glasgow. 278 p. http://theses.gla.ac.uk/4125/
Hume JB, Adams CE, Mable B et al (2013) Post-zygotic hybrid viability in sympatric species pairs – a case study from European lampreys. Biol J Linn Soc 108:378–383
Hume JB, Recknagel H, Bean CW et al (2018) RADseq and mate choice assays reveal unidirectional gene flow among three lamprey ecotypes despite weak assortative mating: insights into the formation and stability of multiple ecotypes in sympatry. Mol Ecol 27:4572–4590
Igoe F, Quigley DTG, Marnell F et al (2004) The sea lamprey Petromyzon marinus (L.), river lamprey Lampetra fluviatilis (L.) and brook lamprey Lampetra planeri (Bloch) in Ireland: general biology, ecology, distribution and status with recommendations for conservation. Biol Environ Proc Roy Irish Acad 104B(3):43–56
Ivanova-Berg MM (1966) Morfologicheskie otlichiya ladozhskoy minogi ot nevskoy (Morphological differences between lampreys from Ladoga Lake and Neva River). Vopr Ikhtiol 6(3):561–566
Kelly FL, King JJ (2001) Distribution of three lamprey species, Lampetra fluviatilis (L.), Lampetra planeri (Bloch), Petromyzon marinus (L.): a context for conservation and biodiversity considerations in Ireland. Biol Environ Proc Royal Irish Acad 101B(3):165–185
King JJ, O’Gorman N (2018) Initial observations on feeding juvenile sea lamprey (Petromyzon marinus L.) in Irish lakes. Biol Environ Proc Royal Irish Acad 118(2):1–8
Kirillova VA, Raspopov IM (1971) Ozyora Leningradskoy Oblasti (Lakes of the Leningrad Region). Lenizdat, Leningrad
Kirillova E, Kirillov P, Kucheryavyy A et al (2016) Common behavioral adaptations in lamprey and salmonids. In: Jawless Fishes of the World. Orlov A, Beamish R (Eds). Cambridge: Cambr. Schol. Publ. V. 2. Ch. 23. P. 196–213
Koli L (1990) Suomenkalat. [Fishes of Finland]. Werner Söderström Osakeyhtiö, Helsinki. 357
Kucheryavyy AV (2021) Sea lamprey Petromyzon marinus Linnaeus, 1758. In: Red Data Book of the Russian Federation. Animals. Moscow: Ministry of Natural Resources and Ecology of the Russian Federation, Russian Academy of Sciences. 304–305
Kucheryaviy AV, Tsimbalov IA, Nazarov DYu et al (2017) Biological characteristics of smolts of European river lamprey Lampetra fluviatilis from the Chernaya River basin (Gulf of Finland, Baltic Sea). J Ichthyol 57(2):276–286
Kucheryavyi AV, Tsimbalov IA, Kostin VV et al (2016) Polymorphism of spawners of the resident form of European river lamprey Lampetra fluviatilis (Petromyzontidae). J Ichthyol 56(5):744–751
Kucheryavyy A, Tsimbalov I, Kirillova E et al (2016) The need for a new taxonomy for lampreys. In: Jawless Fishes of the World. Orlov A., Beamish R (Eds) Cambridge: Cambr. Schol. Publ., V. 1. Ch. 10. P. 251–278
Laaskonen R (1972) Järvisgvänteet vesiviranomaisen 1965–1970 maaliskuussa tekemienien havaintojen valossa Helsinki. Vesientutkimuslaitoksen jukaisuja 4, 80
Land J, Costello MJ, Bailly N et al (2001) Pisces –Agnatha. In: Costello M.J. et al. (Ed.). European register of marine species: a check-list of the marine species in Europe and a bibliography of guides to their identification. Collection Patrimoines Naturels. Vol. 50. 358
Lee DS, Weise JG (1989) Habitat selection of lentic larval lampreys: preliminary analysis based on research with a manned submersible. J Great Lakes Research 15:156–163
Lind EA (1977) A review of pike-perch (Stizostedion lucioperca), Eurasian perch (Perca fluviatilis) and ruff (Gymnocephalus cemua) in Finland. J Fish Res Board Can 34(10):1684–1695
Ljunggren N, Soderman M (2007) Inventering av flodnejonoga i gotlandska vattendrag 2006. Lansstyrelsen i Gotlands lan. Rapporter om natur och miljo. No 2007:8, 113
Lucas M, Bracken F (2010) Potential impacts of hydroelectric power generation on downstream-mowing lampreys of Howsham. Durh Univ School Biol Biomed Sci, Durham, Yorkshire Derwent, p 29
Maitland PS (2003) Ecology of the river, brook and sea lamprey. Conserving Natura 2000 Rivers Ecology. English Nature, Peterborough
Makhrov AA, Artamonova VS (2020) Instability stabilized: mechanisms of evolutionary stasis and genetic diversity accumulation in fishes and lampreys from environments with unstable abiotic factors. Contemp Probl Ecol 13(4):370–381
Makhrov AA, Popov IYu (2015) Life forms of lampreys (Petromyzontidae) as a manifestation of intraspecific diversity of ontogenesis. Russ J Dev Biol 46:196–207
Malmqvist B (1980) The spawning migration of the brook lamprey, Lampetra planeri Bloch, in a south Swedish stream. J Fish Biol 16:105–114
Manzon RG, Youson JH, Holmes JA (2015) Lamprey metamorphosis, in: Docker M.F. (Ed.), Lampreys: biology, conservation and control. Vol. 1. Fish and Fisheries Series, Vol. 37. Springer, Dordrecht, The Netherlands. 139 – 214
Moravec F (1979) Observations on the development of Cucullanus (Truttaedacnitis) truttae (Fabricius, 1794) (Nematoda: Cucullanidae). Folia Parasit 26:295–307
Moore JW, Mallatt JM (1980) Feeding of larval lamprey. Can J Fish Aquatic Sci 37:1658–1664
Moser ML, Jackson AD, Lucas MC et al (2015) Behavior and potential threats to survival of migrating lamprey ammocoetes and macrophtalmia. Rev Fish Biol Fisheries 25:103–116
Muus BJ, Dahlstrøm P (1990) Europasferskvandsfisk. GEC Gads Forlag, København. 224
Müller Y (2004) Faune et flore du littoral du Nord, du Pas-de-Calais et de la Belgique: inventaire. Commission Régionale de BiologieRégion Nord Pas-de-Calais: France. 307
Nijssen H, Groot SJ (1974) Catalogue of fish species of the Netherlands. Beaufortia 21(285):173–207
Ojutkangas E, Aronen K, Laukkanen E (1995) Distribution and abundance of river lamprey (Lampetra fluviatilis) ammocoetes in the regulated river Perhonjoki. Regul Rivers 10:239–245
Pavlov DS, Nazarov DYu, Zvezdin AO et al (2014) Downstream migration of early larvae of the European river lamprey Lampetra fluviatilis. Doklady Biol Sci 459:344–347
Pavlov DS, Zvezdin AO, Kostin VV et al (2017) Temporal characteristics of downstream migration of smolts of the European river lamprey Lampetra fluviatilis in the Chernaya River. Biol Bull 44(3):290–295
Perçin-Paçal F, Sancar-Baş S (2008) An anatomical and morphological study about Gordius aquaticus, Linnaeus, 1758 (Nematomorpha) found in Sarɪyer. Istanbul IUFS J Biology 67(2):123–128
Pestryakov VK (1973) Soils of Leningrad Oblast. Lenizdat, Leningrad
Petrosky CE, Schaller HA (2010) Influence of river conditions during seaward migration and ocean conditions on survival rates of Snake River Chinook salmon and steelhead. Ecol Freshwater Fish 19:520–536
Polyakova NV, Kucheryavyy AV, Movchan EA (2021) The European river lamprey Lampetra fluviatilis (L., 1758) (Petromyzontidae) as a component of the Neva Bay bottom coenoses. Ecosystems Transformation 4(2):111–119
Polyakova NV, Kucheryavyy AV, Pavlov DS et al (2019) Feeding habits of larval European river lamprey Lampetra fluviatilis from the Chernaya River (Baltic Sea Basin). J Ichthyol 59(2):216–224
Popov IYu (2014) “Lake rule” and other regularities in the distribution of the freshwater pearl mussel Margaritifera margaritifera. Transactions of Karelian Research Centre of Russian Academy of Sciences 2:126–139
Potter IC (1980) Ecology of larval metamorphosing lampreys. Can J Fish Aquat Sci 37:1641–1657
Potter IC, Huggins RJ (1973) Observations on the morphology, behaviour and salinity tolerance of downstream migrating river lampreys (Lampetra fluviatilis). J Zool 169:365–379
Quintella BR, Andrade NO, Koed A, Almeida PR (2004) Behavioural patterns of sea lampreys’ spawning migration through difficult passage areas, studied by electromyogram telemetry. J Fish Biol 65:961–972
Quintella BR, Clemens BJ, Sutton T et al (2021) At-sea feeding ecology of parasitic lampreys. J Great Lakes Research. https://doi.org/10.1016/j.jglr.2021.07.008
Raczyński M (2012) Minog rzeczny Lampetra fluviatilis (Linnaeus, 1758). In Monitoring gatunkow zwierząt. Przewodnik metodyczny. Makomaskiej-Juchiewicz M., Baran P. (Eds.). Biblioteka Monitoringu Srodowiska, Warszawa. 70–100
Rask M, Ruuhijärvi J (1990) Pienten Järvien Kalatutkimukset. Suomen Kalatalous 56:101–115
Reshetnikov YS, Bogutskaya NG, Vasil’eva ED et al (1997) An annotated check-list of the freshwater fishes of Russia. J Ichthyol 37(9):687–736
Renaud CB (2011) Lampreys of the World. An annotated and illustrated catalogue of lamprey species known to date. FAO species catalogue for fishery purposes 5. FAO: Rome, Italy. 109 p
Rochard E, Elie P (1994) La macrofaune aquatique de l’estuaire de la Gironde. Contribution au livre blanc de l’Agence de l’Eau Adour Garonne. Etat des connaissances sur l’estuaire de la Gironde. Mauvais J-L, Guillaud J-F (eds). Bordeaux: Bergeret. P. 1–56
Scheuerell MD, Zabel RW, Sandford BP (2009) Relating juvenile migration timing and survival to adulthood in two species of threatened Pacific salmon (Oncorhynchus spp.). J Appl Ecol 46(5):983–990
Sobecka E, Moskal J, Więcaszek B (2009) Checklist of the pathogens of lamprey species of Poland. Int J Oceanography Hydrobiology 38(2):129–137
Spravochnik po gidravlike (1984). V.A. Bolshakov (ed). Kyiv, Visha Shkola 343
Staponkus R, Kesminas V (2014) Confirmation of hybridization between river lamprey L. fluviatilis and brook lamprey L. planeri from in situ experiments. Polish J Natur Sci 29(1):49–54
Taverny C, Elie P (2008) Les lamproies en France – guide pratique d’identification et de determination des ecophases, des especes et des habitats. Etude Cemagref, Groupement de Bordeaux. No 122. 108
Taverny C, Urdaci M (2003) Biologie, ecologie et peche des lamproies migratrices (agnathes amphihalins) – premiere tranche fonctionnelle. Cestas, Cemagref Bordeaux. 53
Thiel R, Salewski V (2003) Verteilung und Wanderung von Neuenaugen im Elbeästuar (Deutschland). Limnologica 33:214–226
Tsimbalov IA, Kucheryuavyi AV, Pavlov DS (2018) Results of hybridization between anadromous and resident forms of European river lamprey Lampetra fluviatilis. J Ichthyol 58(1):122–125
Tsimbalov IA, Kucheryavyi AV, Veselov AE et al (2015) Description of the European river lamprey Lampetra fluviatilis (L., 1758) from the Lososinka River (Onega Lake Basin). Doklady Biol Sci 462:124–127
Tomilin AM (2009) Project of the Gladyshevsky State Natural Complex Reserve of Regional Significance in the Leningrad Region. Vol. 1. Initial data for the design and development of the functional zoning scheme of the territory. Saint Petersburg, Fund for Support and Development of Specially Protected Natural Areas, Protection, Reproduction and Rational Use of Fauna Objects in the Leningrad Region
Tuunainen P, Ikonen E, Auvinen H (1980) Lamprey and lamprey fishing in Finland. Can J Fish Aquat Sci 37:1953–1959
Valovirta EJ (1950) Lamprey (P. fluviatilis) found in the Finnish lakes Paijanne and Leppavesei. Luonnen Tutkija 54:150–151
Vladykov VD (1984) Petromyzonidae. p. 64–67. In PJP. Whitehead, M-L Bauchot, J-C Hureau, J Nielsen, and E Tortonese (eds.) Fishes of the north-eastern Atlantic and Mediterranean. UNESCO, Paris. Vol. 1
Wang CJ, Schaller HA, Coates KC et al (2020) Climate change vulnerability assessment for Pacific lamprey in rivers of the Western United States. J Freshwater Ecol 35(1):29–55
Waterstraat A, Krappe M (2000) Beiträge zur Ökologie und Verbreitung von FFH-Fischarten und Rundmäulern in Mecklenburg-Vorpommern: 1. Das Flußneuenauge (Lampetra fluviatilis L.) im Peenesystem. Natur Natur Mecklenburg-Vorpommern 35:64–79
White JL, Harvey BC (2003) Basin-scale patterns in the drift of embryonic and larval fishes and lamprey ammocoetes in two coastal rivers. Environ BiolFishes 67:369–378
Winter HV, Griffioen AB, van Keeken OA (2014) De Vismigratierivier: Bronnenonderzoek naar gedrag van vis rond zoet-zout overgangen. IMARES Wageningen UR C035/14. 127
Zvezdin AO, Kucheryavyy AV, Tsimbalov IA et al (2018) Influence of illumination on the locomotor activity in smolts of European river lamprey Lampetra fluviatilis (L). Inland Water Biol 11(4):477–484
Zvezdin AO, Pavlov DS, Kucheryavyy AV et al (2019a) Circadian rhythms and locomotor activity of smolts of the European river lamprey Lampetra fluviatilis (L.). Doklady Biol Sci 484:16–18
Zvezdin AO, Pavlov DS, Tsimbalov IA et al (2019b) Experimental study of rheoreaction of the European river lamprey Lampetra fluviatilis (L.) downstream migrating smolts under various illumination. Doklady Biol Sci 487:112–114
Zvezdin AO, Kucheryavyy AV, Kolotei AV et al (2021a) Invasion of the European River Lamprey Lampetra fluviatilis in the Upper Volga. Water 13(1825) https://doi.org/10.3390/w13131825
Zvezdin AO, Polyakova NV, Kucheryavyy AV et al (2021b) Discovery of Eudontomyzon sp. (Petromyzontidae) larvae in lakes and a characterization of their habitats. Nature Conservation 6(3) https://doi.org/10.24189/ncr.2021b.039
Zanandrea GSJ (1959) Speciation among lampreys. Nature 184:380
Acknowledgements
The authors are grateful to the employees of the Reserve Gladyshevsky, and its administration; Skorobogatov M.A. for the assistance in carrying out the research; Krapivin V.A. for his help in identification of parasites and their life stage; Bo Delling, the keeper of the collection of fish and amphibians of the Swedish Museum of Natural History, for the information and photographs of the lampreys, as well as the staff of the laboratory of the behavior of the lower vertebrate IEE RAS Kostin V.V., Kirillov P.I., Kirillova E.A., and Kolotei A.V. for comments on the text of the paper. We are incredibly pleased with the help that Audrey Thompson gave us with the translation, Dr. Benjamin Clemens and Dr. John Hume for their comments to the draft of the paper, and for the very helpful comments and suggestions provided by two anonymous reviewers.
Funding
The work was carried out with the financial support of the Russian Science Foundation (19–14-00015).
Author information
Authors and Affiliations
Contributions
A.V.K., A.O.Z., and N.V.P. designed and performed the field works, observations, and data analysis; N.V.P estimated the Nematodes. All authors wrote the paper, read, and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval
The authors report no conflicts of interest. All animal experiments were performed in accordance with guidelines approved by the Institute of Ecology and Evolution (Moscow, Russia) Animal Committee and handled in accordance with the 1986 Animals (Scientific Procedures) Act and Helsinki Declaration.
Consent to participate
Not applicable as this research did not involve human participants.
Consent for publication
The authors give explicit consent to submit for publication.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kucheryavyy, A.V., Zvezdin, A.O., Polyakova, N.V. et al. A new element in the migration cycle of the European river lamprey Lampetra fluviatilis: downstream migration from a lake. Environ Biol Fish 105, 1857–1871 (2022). https://doi.org/10.1007/s10641-022-01249-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10641-022-01249-1