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.


Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.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.
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.
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.
Bentley, M. & J. Day, 1989. Chemical ecology and behavioral aspects of mosquito oviposition. Annual Review of Entomology 34: 401–421.
Berendonk, T. U., 1999. Influence of fish kairomones on the ovipositing behavior of Chaoborus imagines. Limnology and Oceanography 44(2): 454–458.
Berendonk, T. U. & M. B. Bonsall, 2002. The phantom midge and a comparison of metapopulation structures’. Ecology 83: 116–128.
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.
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.
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.
Borkent, A., 1979. Systematics and bionomics of the species of the subgenus Schdonophasma DYAR and SHANNON (Chaoborus, Chaoboridae, Diptera). Quaestiones Entomologicae 15: 122–255.
Borkent, A., 1981. The distribution and habitat preferences of the Chaoboridae (Culicomorpha: Diptera) of the Holarctic Region. Canadian Journal of Zoology 59: 122–133.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Hessen, D. O. & P. Faerövig, 2001. The photoprotective role of humus-DOC for Selenastrum and Daphnia. Plant Ecology 154(1–2): 261–273.
Hessen, D. O. & K. Sørensen, 1990. Photoprotective pigmentation in alpine zooplankton populations. Aqua Fennica 20: 165–170.
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.
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.
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.
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.
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.
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.
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.
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.
Lynch, M., 1979. Predation, competition, and zooplankton community structure: an experimental study. Limnology & Oceanography 24(2): 253–272.
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.
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.
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.
Neill, W. E., 1981. Impact of Chaoborus predation upon the structure and dynamics of a crustacean zooplankton community. Oecologia 48(2): 164–177.
Nilssen, J. P., 1974. On the ecology and distribution of the Norwegian larvae of Chaoborus (Diptera, Chaoboridae). Norsk Entomologisk Tidsskrift 21: 37–44.
Persaud, A. D., & N. D. Yan, 2003. UVR sensitivity of Chaborus Larvae. Ambio 32(3): 219–224.
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.
Pritchard, G., 1965. Prey capture by dragonfly larvae (Odonata; Anisoptera). Candian Journal of Zoology 43(2): 271–289.
Rautio, M. & B. Tartarotti, 2010. UV radiation and freshwater zooplankton: damage, protection and recovery. Freshwater Reviews 3: 105–131.
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.
Resetarits, W. J., 1996. Oviposition site choice and life history evolution. American Zoologist 36: 205–215.
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.
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.
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.
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.
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.
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.
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.
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.
Van Buskirk, J., 1988. Interactive effects of dragonfly predation in experimental pond communities. Ecology 69(3): 857–867.
Wiklund, C. & M. Friberg, 2008. Enemy-free space and habitat-specific host specialization in a butterfly. Oecologia 157: 287–294.
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.
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.
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.
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.
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling editor: John M. Melack
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-017-3503-x


