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Dormancy in Aquatic Organisms. Theory, Human Use and Modeling pp 221–246Cite as

The Role of Biotic and Abiotic Interactions in Summer Diapause in Cyclopoids: Conceptual Model and Field Validation in Southern Quebec Boreal Lakes

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Part of the book series: Monographiae Biologicae ((MOBI,volume 92))

Abstract

Cyclopoid copepods are a dominant component of freshwater zooplankton and the Cyclopidae is the most diverse family. Dormancy is a fundamental process of cyclopoid life history in permanent lakes and temporary ponds. In boreal lakes, cyclopoid diapause has been documented mainly in Northern Europe but more rarely in Northern America. We present the first assessment on summer diapausing cyclopoids (SDC) in 22 boreal lakes in southern Québec, which vary in their morphometry, tropic status, and predation pressure by fish or invertebrates. We developed a conceptual model to test the hypothesis that diapausing patterns of SDC in boreal lakes are a complex response depending primarily on morphometric and trophic features and secondly on the intensity of hypolimnetic anoxia and predation by fish or invertebrates. Using morphometric indices, lakes were classified in groups varying by the importance of wind-mixing, the strength of thermal stratification during summer, the potential of meromixis, and the risk of predation by fish or chaoborids. Three cyclopoid species (Diacyclops thomasi, Cyclops scutifer, Mesocyclops edax) dominated in all groups of lakes, while Diacyclops nanus and Acanthocyclops vernalis were found in small abundance and only in few lakes. The highest abundances of SDC (density and biomass) were found in sediments of thermally stratified mesotrophic lakes with intermediate wind-mixing index (Ko) and low potential for meromixis (Pm). Strong positive correlations were found between SDC and meiobenthos abundances in all groups of lakes. High biomass of Chaoborus larvae or presence of large populations of fish negatively affected SDC abundances in meiobenthos. Morphometric features, wind-mixing and thermal stratification, as well as the abundance of Chaoborus and fish predators are the key factors governing species diversity and abundance of summer diapausing cyclopoids in boreal lakes.

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References

  • Alekseev VR (1991) Diapause in crustaceans: ecological and physiological aspects. Academia Publications “Nauka”, Moscow, 143 [In Russian]

    Google Scholar 

  • Alekseev VR (1998) Biochemical and physiological characteristics of crustaceans in diapause: the internal mechanism of reactivation. Archiv für Hydrobiologie 52:463–476

    Google Scholar 

  • Alekseev VR (2007) Chapter 3: Diapause in crustaceans: peculiarities of induction. In: Diapause in aquatic invertebrates. Monographiae Biologicae 84. Springer, pp 29–63

    Google Scholar 

  • Alekseev VR, Starobogatov YI (1996) Types of diapause in Crustacea: definitions, distribution, evolution. Hydrobiologia 320:15–26

    Article  Google Scholar 

  • Alekseev VR, Guissani G, Ravera O, Riccardi N (eds) (2004) Diapause in aquatic invertebrates. J Limnol 63(Suppl 1):97p

    Google Scholar 

  • Alekseev VR, De Stasio BT, Gilbert J (2007) Diapause in Aquatic Invertebrates. Monographiae Biologicae 84. Springer, p 257

    Google Scholar 

  • Anderson RS, Raasveldt LG (1974) Gammarus predation and the possible effects of Gammarus and Chaoborus feeding on the zooplankton composition in some small lakes and ponds in western Canada. Canadian Wildlife Service occasional paper no. 18

    Google Scholar 

  • Arnott SE, Vanni MJ (1993) Zooplankton assemblages in fishless bog lakes: influence of biotic and abiotic factors. Ecology 74:2361–2380

    Article  Google Scholar 

  • Balushkina EV, Winberg GG (1979) Relation between body mass and length in planktonic animals. In: Winberg GG (ed) General bases of research into water ecosystems – Obshchiye Osnovy Izucheniya Vodnykh Ekosistem. Nauka, Leningrad, pp 169–172

    Google Scholar 

  • Berger F (1971) Zur Morphometrie der Caranthia II, Special Issue 31:29–39

    Google Scholar 

  • Birge EA, Juday C (1908) A summer resting stage in development of Cyclops bicuspidatus Claus. Trans Wis Acad Sci Arts Lett 16:1–9

    Google Scholar 

  • Boers JJ, Carter JCH (1978) The life history of Cyclops scutifer Sars (Copepoda, Cyclopoida) in a small lake of the Matamek River System, Québec. Can J Zool 56:2603–2607

    Article  Google Scholar 

  • Boxshall GA, Defaye D (2008) Global diversity of copepods (Crustacea: Copepoda) in freshwater. Hydrobiologia 595:195–207

    Article  Google Scholar 

  • Brendonck L, De Meester L (2003) Egg banks in freshwater zooplankton: evolutionary and ecological archives in the sediment. Hydrobiologia 491:65–84

    Article  Google Scholar 

  • Brendonck L, De Meester L, Hairston N Jr (eds) (1998) Evolutionary and ecological aspects of crustacean diapause: proceedings of the Symposium “Diapause in the Crustacea – with Invited Contributions on Non-Crustacean Taxa” held in Gent, August 24–29, 1997. Archiv für Hydrobiologie, Special Issues: Advances in Limnology 52: 561p

    Google Scholar 

  • Charlton MN (1980) Hypolimnion oxygen consumption in lakes: discussion of productivity and morphometry effects. Can J Fish Aquat Sci 37:1531–1539

    Article  Google Scholar 

  • Dahms H-U (1995) Dormancy in the copepods – an overview. Hydrobiologia 306:199–211

    Article  Google Scholar 

  • Dussart BH, Defaye D (1985) Répertoire mondial des Copépodes Cyclopoïdes. Centre National de la Recherche Scientifique (CNRS), Bordeaux/Paris. 236 pp

    Google Scholar 

  • Elgmork K (1967) Ecological aspects of diapause in copepods. In: Proceedings of the Syrup. Crustacea. III. Marine Biological Association of India, symposium. series 2, pp 947–954

    Google Scholar 

  • Elgmork K (1973) Bottom resting stages of planktonic cyclopoid copepods in meromictic lakes. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 18:1474–1478

    Google Scholar 

  • Elgmork K (1980) Evolutionary aspects of diapause in freshwater copepods. In: Kerfoot WC (ed) Evolution and ecology of zooplankton communities. The University Press of New England, Hanover/London, pp 411–417

    Google Scholar 

  • Elgmork K (1981) Extraordinary prolongation on the life cycle in a freshwater planktonic copepod. Holarct Ecol 4:278–290

    Google Scholar 

  • Elgmork K (1996) Variation in torpidity of diapause in freshwater cyclopoid copepods. Hydrobiologia 320:63–70

    Article  Google Scholar 

  • Elgmork K (2004) Life cycles of the freshwater, planktonic copepod Cyclops scutifer Sars on a north-south gradient in North America. Hydrobiologia 529:37–48

    Google Scholar 

  • Elgmork K, Langeland A (1980) Cyclops scutifer Sars – one and two-year life cycles with diapause in the meromictic lake Blank vatn. Archiv für Hydrobiologie 88:178–201

    Google Scholar 

  • Elgmork K, Lie S (1998) Diapause in the life cycle of Cyclops scutifer (Copepoda) in a meromictic lake and the problem of termination by an internal clock. Archiv für Hydrobiol, Special Issue Advances in Limnology 52: 371–381

    Google Scholar 

  • Elgmork K, Nilssen JP (1978) Equivalence of copepod and insect diapause. Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 20:2511–2517

    Google Scholar 

  • Elgmork K, Halvorsen G, Eie JA, Langeland A (1990) Coexistence with similar life cycles in two species of freshwater copepods (Crustacea). Hydrobiologia 208:187–199

    Article  Google Scholar 

  • Filion J-M, Chain P, Futter M (1993) Cantilevering vertical tow nets to reduce two-line induced zooplankton avoidance. J Plankton Res 15:581–587

    Article  Google Scholar 

  • Frisch D (2002) Dormancy, dispersal and the survival of cyclopoid copepods (Cyclopoida, Copepoda) in a lowland floodplain. Freshw Biol 47:1269–1281

    Article  Google Scholar 

  • Fryer G (1996) Diapause, a potent force in the evolution of freshwater crustaceans. Hydrobiologia 320:1–14

    Article  Google Scholar 

  • George DG (1973) Diapause in Cyclops vicinus. Oikos 24:136–142

    Article  Google Scholar 

  • Gliwicz ZM, Rowan MG (1984) Survival of Cyclops abyssorum tatricus (Copepoda, Crustacea) in alpine lakes stocked with planktivorous fish. Limnol Oceanogr 29:1290–1299

    Article  Google Scholar 

  • Gyllström M, Hansson L-A (2004) Dormancy in freshwater zooplankton: induction, termination and the importance of benthic-pelagic coupling. Aquat Sci 66:274–295

    Article  Google Scholar 

  • Hairston NG (1987) Diapause as a predator-avoidance adaptation: Chapter 18. In: Kerfoot WC, Sih A (eds) Predation: direct and indirect impacts on aquatic communities. University Press of New England, Hanover, pp 281–290

    Google Scholar 

  • Hairston NG Jr, Hansen A-M, Schaffner WR (2000) The effect of diapause emergence on the seasonal dynamics of a zooplankton assemblage. Freshw Biol 45:133–145

    Article  Google Scholar 

  • Hakala A (2004) Meromixis as a part of lake evolution- observations and a revised classification of true meromictic lakes in Finland. Boreal Environ Res 9:37–53

    CAS  Google Scholar 

  • Halvorsen G, Elgmork K (1976) Vertical distribution and seasonal cycle of Cyclops scutifer Sars (Crustacea, Copepoda) in two oligotrophic lakes in southern Norway. Nor J Zool 24:143–160

    Google Scholar 

  • Hanazato T, Yasuno M (1989) Zooplankton community structure driven by vertebrate and invertebrate predators. Oecologia 81:450–458

    Article  Google Scholar 

  • Hansen A-M (1996) Variable life history of a cyclopoid copepod: the role of food availability. Hydrobiologia 320:223–227

    Article  Google Scholar 

  • Hansen A-M, Hairston NG (1998) Food limitation in a wild cyclopoid copepod population: direct and indirect life history responses. Oecologia 115:320–330

    Article  Google Scholar 

  • Husson F, Josse J, Le S, Mazet J (2011) FactoMineR: Multivariate exploratory data analysis and data mining with R. R. package version 1.16

    Google Scholar 

  • Keller W, Conlon M (1994) Crustacean zooplankton communities and lake morphometry in Precambrian Shield lakes. Can J Fish Aquat Sci 51:2424–2434

    Article  Google Scholar 

  • Kerfoot WC, Sih A (1987) Predation: direct and indirect impacts on aquatic communities. University Press, Hanover

    Google Scholar 

  • Kobari T, Ban S (1998) Life cycles of two limnetic cyclopoid copepods, Cyclops vicinus and Thermocyclops crassus, in two different habitats. J Plankton Res 20:1073–1086

    Article  Google Scholar 

  • Krylov PI, Alekseev VR, Frenkel OA (1996) Feeding and digestive activity of cyclopoid copepods in active diapause. Hydrobiologia 320:71–79

    Article  Google Scholar 

  • Le Jeune A-H, Bourdiol F, Aldamman L, Perron T, Amyot M, Pinel-Alloul B (2012) Factors affecting methylmercury biomagnification by a widespread aquatic invertebrate predator, the phantom midge larvae Chaoborus. Environ Pollut 165:100–108

    Article  Google Scholar 

  • Legendre P, Legendre L (2012) Numerical ecology. Elsevier Science, Amsterdam

    Google Scholar 

  • Maier G (1994) Patterns of life history among cyclopoid copepods of Central Europe. Freshw Biol 31:77–86

    Article  Google Scholar 

  • Masson S, Pinel-Alloul B (1998) Spatial distribution of zooplankton biomass size fractions in a bog lake: abiotic and (or) biotic regulation. Can J Zool 76:805–823

    Article  CAS  Google Scholar 

  • Masson S, Pinel-Alloul B, Dutilleul P (2004) Spatial heterogeneity of zooplankton biomass and size structure in southern Québec lakes: variation among lakes and within lake among epi-, meta- and hypolimnion strata. J Plankton Res 26:1441–1458

    Article  Google Scholar 

  • Medland VL, Taylor BE (2001) Strategies of emergence from diapause for cyclopoid copepods in a temporary pond. Archiv für Hydrobiol 150:329–349

    Article  Google Scholar 

  • Naess T, Nilssen JP (1991) Diapausing fertilized adults: A new pattern of copepod life cycle. Oecologia 86:368–371

    Article  Google Scholar 

  • Naess T, Nilssen JP, Demmo R (1993) Individual lake characteristics modify the life cycle and diapause habitat of two neighbouring populations of the cyclopoid copepod Thermocyclops oithonoides. Can J Zool 71:1663–1672

    Article  Google Scholar 

  • Nilssen J, Elgmork K (1977) Cyclops abyssorum – life cycle dynamics and habitat selection. Memorie dell Istituto Italiano di Idrobiologia 34:197–238

    Google Scholar 

  • Nürnberg GK (1988) A simple method for predicting the date of fall turnover in thermally stratified lakes. Limnol Oceanogr 32:1160–1164

    Article  Google Scholar 

  • Nürnberg GK (1995) Quantifying anoxia in lakes. Limnol Oceanogr 40:1100–1111

    Article  Google Scholar 

  • Paquette M, Pinel-Alloul B (1982) Cycles de développement de Skistodiaptomus oregonensis, Tropocyclops prasinus et Cyclops scutifer dans la zone limnétique du lac Cromwell, Saint-Hippolyte, Québec. Can J Zool 60:139–151

    Article  Google Scholar 

  • Pinel-Alloul B (1995a) Chapitre 18: Les invertébrés prédateurs du zooplancton. In: Pourriot R, Meybeck M (eds) Limnologie Générale. Collection d’écologie 25. Masson, Paris, pp 541–564

    Google Scholar 

  • Pinel-Alloul B (1995b) Chapitre 21: Impacts des prédateurs invertébrés sur les communautés aquatiques. In: Pourriot R, Meybeck M (eds) Limnologie Générale. Collection d’écologie 25. Masson, Paris, pp 628–647

    Google Scholar 

  • Pinto-Coelho R, Pinel-Alloul B, Méthot G, Havens KE (2005) Crustacean zooplankton in lakes and reservoirs of temperate and tropical regions: variation with trophic status. Can J Fish Aquat Sci 62:348–361

    Article  CAS  Google Scholar 

  • Prepas E (1978) Sugar frosted Daphnia: an improved fixation technique for Cladocera. Limnol Oceanogr 23:557–559

    Article  Google Scholar 

  • Radzikowski J (2013) Resistance of dormant stages of planktonic invertebrates to adverse environmental conditions. J Plankton Res 35:707–723

    Article  Google Scholar 

  • Reckhow KH (1977) Phosphorus model for lake management. PhD dissertation. Harvard University

    Google Scholar 

  • Rivier IC (1996) Ecology of diapausing copepodids of Cyclops kolensis Lill. in reservoirs of the Upper Volga. Hydrobiologia 320:235–241

    Article  Google Scholar 

  • Santer B, Boldt E (1998) The seasonal patterns of lipids in the life cycle of the summer-diapausing freshwater copepod Cyclops kolensis (Lilljeborg). Archiv für Hydrobiol, Special Issues Advanced Limnology 52: 477–492

    Google Scholar 

  • Santer B, Hansen A-M (2006) Diapause of Cyclops vicinus (Uljanin) in Lake Søbygård: indication of a risk-spreading strategy. Hydrobiologia 560:217–226

    Article  Google Scholar 

  • Santer B, Lampert W (1995) Summer diapause in cyclopoid copepods – adaptive response to a food bottleneck. J Anim Ecol 64:600–613

    Article  Google Scholar 

  • Seebens H, Einsle U, Straile D (2009) Copepod life cycle adaptations and success in response to phytoplankton spring bloom phenology. Glob Chang Biol 6:1394–1404

    Article  Google Scholar 

  • Szlauer L (1963) The resting stages of Cyclopidae in Stary Dwór Lake. Polka Archiv für Hydrobiologie 11:385–394

    Google Scholar 

  • Watson NHF, Smallman BN (1971) The role of photoperiod and temperature in the induction and termination of an arrested development in two species of freshwater cyclopoid copepods. Can J Zool 49:855–862

    Article  Google Scholar 

  • Williams-Howze J (1997) Dormancy in the free-living copepod orders Cyclopoida, Calanoida, and Harpacticoida. Oceanogr Mar Biol Annu Rev 35:257–321

    Google Scholar 

  • Wyngaard GA (1988) Geographical variation in dormancy in a copepod: evidence from population crosses. Hydrobiologia 167/168:367–374

    Article  Google Scholar 

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Acknowledgements

This chapter is a contribution resulting from research collaborations between the Russian Academy of Sciences and the Ministry of Education of Quebec, Canada. Financial support for this first research on diapausing cyclopoid copepods in boreal lakes of Quebec was provided through grants from the Natural Sciences and Engineering Research Council of Canada (NSERC Discovery) and the Fond de Recherche du Québec (FRQ – Regroupement stratégique GRIL: Groupe de Recherche Interuniversitaire en Limnologie et Environnement Aquatique) to Bernadette Pinel-Alloul and from the Russian Foundation for Basic Researches to Victor R. Alekseev. Victor R. Alekseev was awarded by two grants “Excellence in Science” from the Ministry of Education, Quebec, Montreal, in 1998 and 2000. This chapter was written with the partial support from RFBR (grant 17-04-00027). The study was partly supported by the Russian Academy of Science, topics 65.4 and 65.5. Our thanks go to Ginette Méthot and Pierre Marcoux for helpful assistance during field sampling, to Louise Pelletier for SEM photos of encysted diapausing cyclopoids, to Louise Cloutier for valuable assistance in meiobenthos taxa identification, to David Lévesque and El-Amine Mimouni for statistical analysis and figure preparation, and to Antonia Cattaneo and Gwyneth McMillan for helpful comments and English editing on a previous version of the manuscript.

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Authors and Affiliations

  1. GRIL, Département de sciences biologiques, Université de Montréal, Montréal, QC, Canada

    Bernadette Pinel-Alloul

  2. Zoological Institute of Russian Academy of Sciences, St. Petersburg, Russia

    Victor R. Alekseev

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  1. Bernadette Pinel-Alloul
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  2. Victor R. Alekseev
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Correspondence to Bernadette Pinel-Alloul .

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Editors and Affiliations

  1. Zoological Institute of Russian Academy of Sciences, St. Petersburg, Russia

    Victor R. Alekseev

  2. Département de sciences biologiques, Université de Montréal, Montréal, QC, Canada

    Bernadette Pinel-Alloul

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Pinel-Alloul, B., Alekseev, V.R. (2019). The Role of Biotic and Abiotic Interactions in Summer Diapause in Cyclopoids: Conceptual Model and Field Validation in Southern Quebec Boreal Lakes. In: Alekseev, V., Pinel-Alloul, B. (eds) Dormancy in Aquatic Organisms. Theory, Human Use and Modeling. Monographiae Biologicae, vol 92. Springer, Cham. https://doi.org/10.1007/978-3-030-21213-1_14

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