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Effects of water browning on freshwater biodiversity: the case of the predatory phantom midge Chaoborus nyblaei

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Abstract

Water browning, due to increased runoff of terrestrial dissolved organic carbon (DOC), has recently gained considerable attention. While it is well settled how browning affects light regime and thereby aquatic primary production, other impacts on the aquatic biota is less explored. Water browning shelters against UV radiation, and may thus benefit range expansion of UV sensitive organisms, such as midges. We mapped occurrence of Chaoborids in 148 subalpine and alpine ponds in Norway, and identified an apparent threshold for their presence around 3 mg total organic carbon (TOC) l−1. The field study was complemented with laboratory experiments on Chaoborus nyblaei (Zetterstedt, 1838), to test if this species is able to identify and select water colour (concentrations of DOC) for oviposition. Number of egg rafts on brown water tanks was significantly higher than in clear water tanks, indicating that C. nyblaei performs oviposition habitat selection. Chaoborids are effective predators in planktonic habitats, and our findings support the hypothesis that climate change may cascade through the ecosystem and promote range shifts of species due to alternated habitat frame conditions.

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References

  • Allan, S. A. & D. L. Kline, 1998. Larval rearing water and preexisting eggs influence oviposition by Aedes aegypti and Ae. albopictus (Diptera: Culicidae). Journal of Medical Entomology 35: 943–947.

    Article  CAS  PubMed  Google Scholar 

  • Arts, M. T., H. Rai, & V. P. Tumber, 2000. Effects of artificial UV-A and UV-B radiation on carbon allocation in Synechococcus elongatus (cyanobacterium) and Nitzschia palea (diatom). Verhandlungen Internationale Vereinigung Für Theoretische und Angewandte Limnologie 27: 1–8.

    Google Scholar 

  • Asmare, Y., S. R. Hill, R. J. Hopkins, H. Tekie & R. Ignell, 2017. The role of grass volatiles on oviposition site selection by Anopheles arabiensis and Anopheles coluzzii. Malaria Journal. https://doi.org/10.1186/s12936-017-1717-z.

    PubMed  PubMed Central  Google Scholar 

  • Bentley, M. & J. Day, 1989. Chemical ecology and behavioral aspects of mosquito oviposition. Annual Review of Entomology 34: 401–421.

    Article  CAS  PubMed  Google Scholar 

  • Berendonk, T. U., 1999. Influence of fish kairomones on the ovipositing behavior of Chaoborus imagines. Limnology and Oceanography 44(2): 454–458.

    Article  Google Scholar 

  • Berendonk, T. U. & M. B. Bonsall, 2002. The phantom midge and a comparison of metapopulation structures’. Ecology 83: 116–128.

    Article  Google Scholar 

  • Blaustein, L., M. Kiflawi, A. Eitam, M. Mangel & J. E. Cohen, 2004. Oviposition habitat selection in response to risk of predation in temporary pools: mode of detection and consistency across experimental venue. Oecologia. https://doi.org/10.1007/s00442-003-1398-x.

    PubMed  Google Scholar 

  • Blumthaler, M., W. Ambach & W. Rehwald, 1992. Solar UV-A and UV-B radiation fluxes at two alpine stations at different altitudes. Theoretical and Applied Climatology 46: 39–44.

    Article  Google Scholar 

  • Boeing, W. J., D. M. Leech, C. E. Williamson, S. Cooke & L. Torres, 2004. Damaging UV radiation and invertebrate predation: conflicting selective pressures for zooplankton vertical distribution in the water column of low DOC lakes. Oecologia. https://doi.org/10.1007/s00442-003-1468-0.

    PubMed  Google Scholar 

  • Borkent, A., 1979. Systematics and bionomics of the species of the subgenus Schdonophasma DYAR and SHANNON (Chaoborus, Chaoboridae, Diptera). Quaestiones Entomologicae 15: 122–255.

    Google Scholar 

  • Borkent, A., 1981. The distribution and habitat preferences of the Chaoboridae (Culicomorpha: Diptera) of the Holarctic Region. Canadian Journal of Zoology 59: 122–133.

    Article  Google Scholar 

  • Brandstetter, A., R. S. Sletten, A. Mentler & W. W. Wenzel, 1996. Estimating dissolved organic carbon in natural waters by UV absorbance (254 nm). Journal of Plant Nutrition and Soil Science 159(6): 605–607.

    CAS  Google Scholar 

  • Cobbaert, D., S. E. Bayley & J.-L. Greter, 2010. Effects of a top invertebrate predator (Dytiscus alaskanus; Coleoptera: Dytiscidae) on fishless pond ecosystems. Hydrobiologia 644(1): 103–114.

    Article  CAS  Google Scholar 

  • Davidowicz, P., J. Paijanowska & K. Ciechomski, 1990. Vertical migration of Chaoborus larvae is induced by the presence of fish. Limnology and Oceanography 35: 1631–1637.

    Article  Google Scholar 

  • De Wit, H. A., S. Valinia, G. A. Weyhenmeyer, M. N. Futter, P. Kortelainen, K. Austnes, D. O. Hessen, A. Raike, H. Laudon & J. Vuorenmaa, 2017. Current browning of surface water will be further promoted by climate change. Environmental Science & Technology Letters. https://doi.org/10.1021/acs.estlett.6b00396.

    Google Scholar 

  • Eie, J., 1974. A comparative study of the crustacean communities in forest and mountain localities in the Vassfaret area (southern Norway). Norwegian Journal of Zoology 22: 177–205.

    Google Scholar 

  • Erlandsson, M., I. Buffam, J. Fölster, H. Laudon, J. Temnerud, G. A. Weyhenmeyer & K. Bishop, 2008. Thirty-five years of synchrony in the organic matter concentrations of Swedish rivers explained by variation in flow and sulphate. Global Change Biology 14: 1191–1198.

    Article  Google Scholar 

  • Evans, C. D., T. G. Jones, A. Burden, et al., 2012. Acidity controls on dissolved organic carbon mobility in organic soils. Global Change Biology 18: 3317–3331.

    Article  Google Scholar 

  • Fader, J. E. & S. A. Juliano, 2014. Oviposition habitat selection by container-dwelling mosquitos: responses to cues of larval and detritus abundances in the field. Ecological Entomology. https://doi.org/10.1111/een.12095.

    PubMed  PubMed Central  Google Scholar 

  • Finstad, A. G., I. P. Helland, O. Ugedal, T. Hesthagen & D. O. Hessen, 2013. Unimodal response of fish yield to dissolved organic carbon. Ecology Letters. https://doi.org/10.1111/ele.12201.

    PubMed  Google Scholar 

  • Finstad, A. G., T. Andersen, S. Larsen, K. Tominaga, S. Blumentrath, H. A. de Wit, H. Tømmervik & D. O. Hessen, 2016. From greening to browning: catchment vegetation development and reduced S-deposition promote organic carbon load on decadal time scales in Nordic lakes. Scientific Reports. https://doi.org/10.1038/srep31944.

    PubMed  PubMed Central  Google Scholar 

  • Hessen, D. O. & P. Faerövig, 2001. The photoprotective role of humus-DOC for Selenastrum and Daphnia. Plant Ecology 154(1–2): 261–273.

    Article  Google Scholar 

  • Hessen, D. O. & K. Sørensen, 1990. Photoprotective pigmentation in alpine zooplankton populations. Aqua Fennica 20: 165–170.

    CAS  Google Scholar 

  • Hirvenoja, M., 1961. Weitere Studien über Chaoborinen (Diptera: Culicidae). Beschreibung der Larve und der Puppe von Chaoborus (Schadonophasma) nyblaei Zett. Annales Entomologici Fennici 27: 77–83.

    Google Scholar 

  • Hofgaard, A., H. Tømmervik, G. Rees & F. Hanssen, 2013. Latitudinal forest advance in northernmost Norway since the early twentieth century. Journal of Biogeography. https://doi.org/10.1111/jbi.12053.

    Google Scholar 

  • Karlsson, J., P. Byström, J. Ask, P. Ask, L. Persson & M. Jansson, 2009. Light limitation of nutrient-poor lake ecosystems. Nature. https://doi.org/10.1038/nature08179.

    Google Scholar 

  • Kortelainen, P., T. Mattsson, L. Finér, M. Ahtiainen, S. Saukkonen & T. Sallantaus, 2006. Controls on the export of C, N, P and Fe from undisturbed boreal catchments, Finland. Aquatic Sciences 68: 453–468.

    Article  CAS  Google Scholar 

  • Larsen, S., T. Andersen & D. O. Hessen, 2011. Climate change predicted to cause severe increase of organic carbon in lakes. Global Change Biology. https://doi.org/10.1111/j.1365-2486.2010.02257.x.

    Google Scholar 

  • Laurion, I., D. R. S. Lean & W. F. Vincent, 1998. UVB effects on a plankton community: results from a large-scale enclosure assay. Aquatic Microbial Ecology 16: 189–198.

    Article  Google Scholar 

  • Lindholm, M., R. Wolf, A. G. Finstad & D. O. Hessen, 2016. Water browning mediates decimation of the Arctic fairy shrimp Branchinecta paludosa. Freshwater Biology. https://doi.org/10.1111/fwb.12712.

    Google Scholar 

  • Lopez-Martinez, G., M. A. Elnitsky, J. B. Benoit, R. E. Lee Jr. & D. L. Denlinger, 2008. High resistance to oxidative damage in the Antarctic midge Belgica Antarctica, and developmentally linked expression of genes encoding superoxide dismutase, catalase and heat shock proteins. Insect Biochemistry and Molecular Biology 38: 796–804.

    Article  CAS  PubMed  Google Scholar 

  • Lynch, M., 1979. Predation, competition, and zooplankton community structure: an experimental study. Limnology & Oceanography 24(2): 253–272.

    Article  Google Scholar 

  • Meyer-Jacob, C., N. Michelutti, A. M. Paterson, D. Monteith, H. Yand, J. Weckström, J. P. Smol & R. Bindler, 2017. Inferring past trends in lake water organic carbon concentrations in northern lakes using sediment spectroscopy. Environmental Science & Technology 51: 13248–13255.

    Article  CAS  Google Scholar 

  • Monteith, D. T., J. L. Stoddard, C. D. Evans, H. A. de Wit, M. Forsius, T. Høgåsen, et al., 2007. Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry. Nature 450: 537–540.

    Article  CAS  PubMed  Google Scholar 

  • Nagiller, K. & R. Sommaruga, 2009. Differential tolerance of UV radiation between Chaoborus species and role of photoprotective compounds. Journal of Plankton Research. https://doi.org/10.1093/plankt/fbn133.

    Google Scholar 

  • Neill, W. E., 1981. Impact of Chaoborus predation upon the structure and dynamics of a crustacean zooplankton community. Oecologia 48(2): 164–177.

    Article  PubMed  Google Scholar 

  • Nilssen, J. P., 1974. On the ecology and distribution of the Norwegian larvae of Chaoborus (Diptera, Chaoboridae). Norsk Entomologisk Tidsskrift 21: 37–44.

    Google Scholar 

  • Persaud, A. D., & N. D. Yan, 2003. UVR sensitivity of Chaborus Larvae. Ambio 32(3): 219–224.

    Article  PubMed  Google Scholar 

  • Petranka, J. W. & K. Fakhoury, 1991. Evidence of a chemically-mediated avoidance response of ovipositing insects to blue-gills and green frog tadpoles. Copeia 1: 234–239.

    Article  Google Scholar 

  • Pritchard, G., 1965. Prey capture by dragonfly larvae (Odonata; Anisoptera). Candian Journal of Zoology 43(2): 271–289.

    Article  Google Scholar 

  • Rautio, M. & B. Tartarotti, 2010. UV radiation and freshwater zooplankton: damage, protection and recovery. Freshwater Reviews 3: 105–131.

    Article  PubMed  PubMed Central  Google Scholar 

  • Reiskind, M. H. & M. L. Wilson, 2004. Culex restuans (Diptera: Culicidae) oviposition behavior determined by larval habitat quality and quantity in southeastern Michigan. Journal of Medical Entomology. https://doi.org/10.1603/0022-2585-41.2.179.

    Google Scholar 

  • Resetarits, W. J., 1996. Oviposition site choice and life history evolution. American Zoologist 36: 205–215.

    Article  Google Scholar 

  • Resetarits, W. J. & A. Silberbush, 2015. Local contagion and regional compression: habitat selection drives spatially explicit, multiscale dynamics of colonization in experimental metacommunities. Ecology Letters. https://doi.org/10.1111/ele.12553.

    PubMed  Google Scholar 

  • Saether, O., 1972. Chaoboridae. In Elster, H. J. & W. Ohle (eds), Die Binnengewässer. Einzeldarstellungen aus der Limnologie und ihren Nachbargebieten. Band 26, 1.Teil. Stuttgart.

  • Scully, N. M. & D. R. S. Lean, 1994. The attenuation of ultraviolet radiation in temperate lakes, Archive für Hydrobiologie, Beihefte. Ergebnisse der Limnologie 43: 135–144.

    Google Scholar 

  • Segev, O., R. Verster & C. Weldon, 2016. Testing the link between perceived and actual risk of predation: mosquito oviposition site selection and egg predation by native and introduced fish. Journal of Applied Ecology. https://doi.org/10.1111/1365-2664.12789.

    Google Scholar 

  • Solomon, C. T., S. E. Jones, B. C. Weidel, I. Buffam, M. L. Fork, J. Karlsson, et al., 2015. Ecosystem consequences of changing inputs of terrestrial dissolved organic matter to lakes: current knowledge and future challenges. Ecosystems 28: 376–389. https://doi.org/10.1007/s10021-015-9848-y.

    Article  Google Scholar 

  • Sommaruga, R., R. Psenner, E. Schafferer, K. A. Koinig & S. Sommaruga-Wögrath, 1999. Dissolved organic carbon concentration and phytoplankton biomass in high-mountain lakes of the Austrian Alps: potential effect of climatic warming on UV underwater attenuation. Arctic, Antarctic, and Aline Research 31(3): 247–253.

    Article  Google Scholar 

  • Sommaruga, R., 2001. The role of solar UV radiation in the ecology of alpine lakes. Journal of Photochemistry and Photobiology B: Biology 62: 35–42.

    Article  CAS  Google Scholar 

  • Taylor, D. J., M. J. Ballinger, A. S. Medeiros & A. A. Kotov, 2015. Climate-associated tundra thaw pond formation and range expansion of boreal zooplankton predators. Ecography 39: 45–53. https://doi.org/10.1111/ecog.01514.

    Google Scholar 

  • Thrane, J.-E., D. O. Hessen & T. Andersen, 2014. The Absorption of light in lakes: negative impact of dissolved organic carbon on primary productivity. Ecosystems. https://doi.org/10.1007/s10021-014-9776-2.

    Google Scholar 

  • Van Buskirk, J., 1988. Interactive effects of dragonfly predation in experimental pond communities. Ecology 69(3): 857–867.

    Article  Google Scholar 

  • Wiklund, C. & M. Friberg, 2008. Enemy-free space and habitat-specific host specialization in a butterfly. Oecologia 157: 287–294.

    Article  PubMed  Google Scholar 

  • Williamson, C. E., D. P. Morris, M. L. Pace & A. G. Olson, 1999. Dissolved organic carbon and nutrients as regulators of lake ecosystems: resurrection of a more integrated paradigm. Limnology and Oceanography 44: 795–803.

    Article  CAS  Google Scholar 

  • Wolf, R., T. Andersen, D. O. Hessen & K. Hylland, 2017. The influence of dissolved organic carbon and ultraviolet radiation on the genomic integrity of Daphnia magna. Functional Ecology. https://doi.org/10.1111/1365-2435.12730.

    Google Scholar 

  • Yan, N. D., W. Keller, H. J. MacIsaac & L. J. McEachern, 1991. Regulation of zooplankton community structure of an acidified lake by Chaoborus. Ecological Applications 1(1): 52–65.

    Article  PubMed  Google Scholar 

  • Zahiri, N. & M.-E. Rau, 1998. Oviposition attraction and repellency of Aedes aegypti (Diptera: Culicidae) to waters from conspecifics larvae subjected to crowding, confinement, starvation, or infection. Journal of Medical Entomology 35: 782–787.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was funded by the Norwegian Research Council Project ECCO (224779/E10), and by NIVA’s. Strategic Institute Initiative “Climate effects from mountains to fjords” (Research Council of Norway, Contract No. 208279). We are indebted to Jon Arne Eie for field work assistance.

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Correspondence to Markus Lindholm.

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Lindholm, M., Eie, M., Hessen, D.O. et al. Effects of water browning on freshwater biodiversity: the case of the predatory phantom midge Chaoborus nyblaei. Hydrobiologia 813, 33–40 (2018). https://doi.org/10.1007/s10750-017-3503-x

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