in

Short term fluctuating temperature alleviates Daphnia stoichiometric constraints

  • 1.

    Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. & West, G. B. Toward a metabolic theory of ecology. Ecology 85, 1771–1789 (2004).

    Article 

    Google Scholar 

  • 2.

    Dillon, M. E., Wang, G. & Huey, R. B. Global metabolic impacts of recent climate warming. Nature 467, 704–706. https://doi.org/10.1038/nature09407 (2010).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 3.

    Elser, J. J. et al. Biological stoichiometry from genes to ecosystems. Ecol. Lett. 3, 540–550 (2000).

    Article 

    Google Scholar 

  • 4.

    Elser, J., Obrien, W., Dobberfuhl, D. & Dowling, T. The evolution of ecosystem processes: growth rate and elemental stoichiometry of a key herbivore in temperate and arctic habitats. J. Evol. Biol. 13, 845–853 (2000).

    Article 

    Google Scholar 

  • 5.

    Hessen, D. O., Elser, J. J., Sterner, R. W. & Urabe, J. Ecological stoichiometry: An elementary approach using basic principles. Limnol. Oceanogr. 58, 2219–2236 (2013).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 6.

    Hessen, D. O., Faerovig, P. J. & Andersen, T. Light, nutrients, and P : C ratios in algae: Grazer performance related to food quality and quantity. Ecology 83, 1886–1898 (2002).

    Article 

    Google Scholar 

  • 7.

    Moody, E. K., Rugenski, A. T., Sabo, J. L., Turner, B. L. & Elser, J. J. Does the growth rate hypothesis apply across temperatures? Variation in the growth rate and body phosphorus of neotropical benthic grazers. Front. Environ. Sci. https://doi.org/10.3389/fenvs.2017.00014 (2017).

    Article 

    Google Scholar 

  • 8.

    Prater, C., Wagner, N. D. & Frost, P. C. Seasonal effects of food quality and temperature on body stoichiometry, biochemistry, and biomass production in Daphnia populations. Limnol. Oceanogr. 63, 1727–1740. https://doi.org/10.1002/lno.10803 (2018).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 9.

    Boersma, M. et al. Temperature driven changes in the diet preference of omnivorous copepods: No more meat when it’s hot?. Ecol. Lett. 19, 45–53. https://doi.org/10.1111/ele.12541 (2016).

    Article 
    PubMed 

    Google Scholar 

  • 10.

    Wojewodzic, M. W., Kyle, M., Elser, J. J., Hessen, D. O. & Andersen, T. Joint effect of phosphorus limitation and temperature on alkaline phosphatase activity and somatic growth in Daphnia magna. Oecologia 165, 837–846. https://doi.org/10.1007/s00442-010-1863-2 (2011).

    ADS 
    Article 
    PubMed 

    Google Scholar 

  • 11.

    Starke, C. W. E., Jones, C. L. C., Burr, W. S. & Frost, P. C. Interactive effects of water temperature and stoichiometric food quality on Daphnia pulicaria. Freshwat. Biol. 66, 256–265. https://doi.org/10.1111/fwb.13633 (2020).

    CAS 
    Article 

    Google Scholar 

  • 12.

    Ruiz, T. et al. U-shaped response Unifies views on temperature dependency of stoichiometric requirements. Ecol. Lett. 23, 860–869. https://doi.org/10.1111/ele.13493 (2020).

    Article 
    PubMed 

    Google Scholar 

  • 13.

    Persson, J., Wojewodzic, M. W., Hessen, D. O. & Andersen, T. Increased risk of phosphorus limitation at higher temperatures for Daphnia magna. Oecologia 165, 123–129. https://doi.org/10.1007/s00442-010-1756-4 (2011).

    ADS 
    Article 
    PubMed 

    Google Scholar 

  • 14.

    Malzahn, A. M., Doerfler, D. & Boersma, M. Junk food gets healthier when it’s warm. Limnol. Oceanogr. 61, 1677–1685. https://doi.org/10.1002/lno.10330 (2016).

    ADS 
    Article 

    Google Scholar 

  • 15.

    Cross, W. F., Hood, J. M., Benstead, J. P., Huryn, A. D. & Nelson, D. Interactions between temperature and nutrients across levels of ecological organization. Glob. Change Biol. 21, 1025–1040. https://doi.org/10.1111/gcb.12809 (2015).

    ADS 
    Article 

    Google Scholar 

  • 16.

    Woods, H. A. et al. Temperature and the chemical composition of poikilothermic organisms. Funct. Ecol. 17, 237–245. https://doi.org/10.1046/j.1365-2435.2003.00724.x (2003).

    Article 

    Google Scholar 

  • 17.

    Cotner, J. B., Makino, W. & Biddanda, B. A. Temperature affects stoichiometry and biochemical composition of Escherichia coli. Microb. Ecol. 52, 26–33. https://doi.org/10.1007/s00248-006-9040-1 (2006).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 18.

    Hessen, D. O. et al. Changes in stoichiometry, cellular RNA, and alkaline phosphatase activity of Chlamydomonas in response to temperature and nutrients. Front. Microbiol. 8, 18. https://doi.org/10.3389/fmicb.2017.00018 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 19.

    Van Geest, G. J., Sachse, R., Brehm, M., van Donk, E. & Hessen, D. Maximizing growth rate at low temperatures: RNA:DNA allocation strategies and life history traits of Arctic and temperate Daphnia. Polar Biol. 33, 1255–1262 (2010).

    Article 

    Google Scholar 

  • 20.

    Prater, C., Wagner, N. D. & Frost, P. C. Interactive effects of genotype and food quality on consumer growth rate and elemental content. Ecology 98, 1399–1408. https://doi.org/10.1002/ecy.1795 (2017).

    Article 
    PubMed 

    Google Scholar 

  • 21.

    Lampert, W. The adaptive significance of diel vertical migration of zooplankton. Funct. Ecol. 3, 21–27 (1989).

    Article 

    Google Scholar 

  • 22.

    Williamson, C. E., Fischer, J. M., Bollens, S. M., Overholt, E. P. & Breckenridge, J. K. Towards a more comprehensive theory of zooplankton diel vertical migration: Integrating ultraviolet radiation and water transparency into the biotic paradigm. Limnol. Oceanogr. 56, 1603–1623 (2011).

    ADS 
    Article 

    Google Scholar 

  • 23.

    Dawidowicz, P. & Loose, C. J. Metabolic costs during predator-induced diel vertical migration of Daphnia. Limnol. Oceanogr. 37, 1589–1595 (1992).

    ADS 
    Article 

    Google Scholar 

  • 24.

    Mikulski, A., Grzesiuk, M., Rakowska, A., Bernatowicz, P. & Pijanowska, J. Thermal shock in Daphnia: cost of diel vertical migrations or inhabiting thermally-unstable waterbodies?. Fund. Appl. Limnol. 190, 213–220. https://doi.org/10.1127/fal/2017/0989 (2017).

    Article 

    Google Scholar 

  • 25.

    Reichwaldt, E. S., Wolf, I. D. & Stibor, H. Effects of a fluctuating temperature regime experienced by Daphnia during diel vertical migration on Daphnia life history parameters. Hydrobiologia 543, 199–205. https://doi.org/10.1007/s10750-004-7451-x (2005).

    Article 

    Google Scholar 

  • 26.

    Orcutt, J. D. & Porter, K. G. Diel vertical migration in zooplankton. Constant and fluctuating temperature effects on life history parameters of Daphnia. Limnol. Oceanogr. 28, 720–730 (1983).

    ADS 
    Article 

    Google Scholar 

  • 27.

    Stich, H. B. & Lampert, W. Growth and reproduction of migrating and non-migrating Daphnia species under simulated food and temperature conditions of diurnal vertical migration. Oecologia 61, 192–196. https://doi.org/10.1007/BF00396759 (1984).

    ADS 
    Article 
    PubMed 

    Google Scholar 

  • 28.

    Fischer, J. M. et al. Diel vertical migration of copepods in mountain lakes: The changing role of ultraviolet radiation across a transparency gradient. Limnol. Oceanogr. 60, 252–262. https://doi.org/10.1002/lno.10019 (2015).

    ADS 
    Article 

    Google Scholar 

  • 29.

    Kessler, K., Lockwood, R. S., Williamson, C. E. & Saros, J. E. Vertical distribution of zooplankton in subalpine and alpine lakes: Ultraviolet radiation, fish predation, and the transparency-gradient hypothesis. Limnol. Oceanogr. 53, 2374–2382 (2008).

    ADS 
    Article 

    Google Scholar 

  • 30.

    Bergström, A.-K., Karlsson, J., Karlsson, D. & Vrede, T. Contrasting plankton stoichiometry and nutrient regeneration in northern arctic and boreal lakes. Aquat. Sci. https://doi.org/10.1007/s00027-018-0575-2 (2018).

    Article 

    Google Scholar 

  • 31.

    Sterner, R. W. On the phosphorus limitation paradigm for lakes. Int. Rev. Hydrobiol. 93, 433–445. https://doi.org/10.1002/iroh.200811068 (2008).

    CAS 
    Article 

    Google Scholar 

  • 32.

    Sterner, R. W. C: N: P stoichiometry in Lake superior: Freshwater sea as end member. Inland Waters 1, 29–46 (2011).

    CAS 
    Article 

    Google Scholar 

  • 33.

    Modenutti, B. E. et al. Environmental changes affecting light climate in oligotrophic mountain lakes: The deep chlorophyll maxima as a sensitive variable. Aquat. Sci. 75, 361–371. https://doi.org/10.1007/s00027-012-0282-3 (2013).

    CAS 
    Article 

    Google Scholar 

  • 34.

    Longhi, M. L. & Beisner, B. E. Environmental factors controlling the vertical distribution of phytoplankton in lakes. J. Plankton Res. 31, 1195–1207. https://doi.org/10.1093/plankt/fbp065 (2009).

    CAS 
    Article 

    Google Scholar 

  • 35.

    Leach, T. H. et al. Patterns and drivers of deep chlorophyll maxima structure in 100 lakes: The relative importance of light and thermal stratification. Limnol. Oceanogr. 63, 628–646. https://doi.org/10.1002/lno.10656 (2018).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 36.

    Laspoumaderes, C. et al. Glacier melting and stoichiometric implications for lake community structure: Zooplankton species distributions across a natural light gradient. Glob. Change Biol. 19, 316–326. https://doi.org/10.1111/gcb.12040 (2013).

    ADS 
    Article 

    Google Scholar 

  • 37.

    Jacobs, A. F. G., Jetten, T. H., Lucassen, D., Heusinkveld, B. G. & Joost, P. N. Diurnal temperature fluctuations in a natural shallow water body. Agric. For. Meteorol. 88, 269–277. https://doi.org/10.1016/S0168-1923(97)00039-7 (1997).

    ADS 
    Article 

    Google Scholar 

  • 38.

    Vilas, M. P., Marti, C. L., Adams, M. P., Oldham, C. E. & Hipsey, M. R. Invasive macrophytes control the spatial and temporal patterns of temperature and dissolved oxygen in a shallow lake: A proposed feedback mechanism of macrophyte loss. Front. Plant Sci. 8, 2097. https://doi.org/10.3389/fpls.2017.02097 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 39.

    Burks, R. L., Lodge, D. M., Jeppesen, E. & Lauridsen, T. L. Diel horizontal migration of zooplankton: Costs and benefits of inhabiting the littoral. Freshwat. Biol. 47, 343–365 (2002).

    Article 

    Google Scholar 

  • 40.

    Morris, D. P. et al. The attenuation of solar UV radiation in lakes and the role of dissolved organic carbon. Limnol. Oceanogr. 40, 1381–1391 (1995).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 41.

    Balseiro, E. G., Modenutti, B. E., Queimaliños, C. & Reissig, M. Daphnia distribution in Andean Patagonian lakes: Effect of low food quality and fish predation. Aquat. Ecol. 41, 599–609 (2007).

    CAS 
    Article 

    Google Scholar 

  • 42.

    Modenutti, B. E., Wolinski, L., Souza, M. S. & Balseiro, E. G. When eating a prey is risky: Implications for predator diel vertical migration. Limnol. Oceanogr. 63, 939–950. https://doi.org/10.1002/lno.10681 (2018).

    ADS 
    Article 

    Google Scholar 

  • 43.

    Gillooly, J. F., Charnov, E. L., West, G. B., Savage, V. M. & Brown, J. H. Effects of size and temperature on developmental time. Nature 417, 70–73. https://doi.org/10.1038/417070a (2002).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 44.

    Acharya, K., Kyle, M. & Elser, J. J. Biological stoichiometry of Daphnia growth: An ecophysiological test of the growth rate hypothesis. Limnol. Oceanogr. 49, 656–665 (2004).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 45.

    Souza, M. S., Hansson, L.-A., Hylander, S., Modenutti, B. E. & Balseiro, E. G. Rapid enzymatic response to compensate UV radiation in copepods. PLoS ONE 7, e32046. https://doi.org/10.1371/journal.pone.0032046 (2012).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 46.

    Wolinski, L., Modenutti, B., Souza, M. S. & Balseiro, E. Interactive effects of temperature, ultraviolet radiation and food quality on zooplankton alkaline phosphatase activity. Environ. Pollut. 213, 135–142. https://doi.org/10.1016/j.envpol.2016.02.016 (2016).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 47.

    Xie, J. et al. Physiological effects of compensatory growth during the larval stage of the ladybird Cryptolaemus montrouzieri. J. Insect Physiol. 83, 37–42. https://doi.org/10.1016/j.jinsphys.2015.11.001 (2015).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 48.

    Dmitriew, C. & Rowe, L. Resource limitation, predation risk and compensatory growth in a damselfly. Oecologia 142, 150–154. https://doi.org/10.1007/s00442-004-1712-2 (2005).

    ADS 
    Article 
    PubMed 

    Google Scholar 

  • 49.

    Malzahn, A. M. & Boersma, M. Effects of poor food quality on copepod growth are dose dependent and non-reversible. Oikos 121, 1408–1416. https://doi.org/10.1111/j.1600-0706.2011.20186.x (2012).

    Article 

    Google Scholar 

  • 50.

    Droop, M. R. Some thoughts on nutrient limitation in algae. J. PhycoI. 9, 264–272 (1973).

    CAS 
    Article 

    Google Scholar 

  • 51.

    Boersma, M. The nutritional quality of P-limited algae for Daphnia. Limnol. Oceanogr. 45, 1157–1161 (2000).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 52.

    Plath, K. & Boersma, M. Mineral limitation of zooplankton: Stoichiometric constraints and optimal foraging. Ecology 82, 1260–1269 (2001).

    Article 

    Google Scholar 

  • 53.

    Barbiero, R. P. & Tuchman, M. L. Results from the US EPA’s biological open water surveillance program of the Laurentian Great Lakes: II. Deep chlorophyll maxima. J. Great Lakes Res. 27, 155–166 (2001).

    CAS 
    Article 

    Google Scholar 

  • 54.

    Camacho, A. On the occurrence and ecological features of deep chlorophyll maxima (DCM) in Spanish stratified lakes. Limnetica 25, 453–478 (2006).

    Google Scholar 

  • 55.

    Pérez, G. L., Queimaliños, C. P. & Modenutti, B. E. Light climate and plankton in the deep chlorophyll maxima in North Patagonian Andean lakes. J. Plankton Res. 24, 591–599 (2002).

    Article 

    Google Scholar 

  • 56.

    Magee, M. R. & Wu, C. H. Response of water temperatures and stratification to changing climate in three lakes with different morphometry. Hydrol. Earth Syst. Sci. 21, 6253–6274. https://doi.org/10.5194/hess-21-6253-2017 (2017).

    ADS 
    Article 

    Google Scholar 

  • 57.

    Niedrist, G. H., Psenner, R. & Sommaruga, R. Climate warming increases vertical and seasonal water temperature differences and inter-annual variability in a mountain lake. Clim. Change 151, 473–490. https://doi.org/10.1007/s10584-018-2328-6 (2018).

    ADS 
    Article 

    Google Scholar 

  • 58.

    Kilham, S. S., Kreeger, D. A., Lynn, S. G., Goulden, C. E. & Herrera, L. COMBO – A defined freshwater culture medium for algae and zooplankton. Hydrobiologia 377, 147–159 (1998).

    CAS 
    Article 

    Google Scholar 

  • 59.

    Guillard, R. R. L. & Lorenzen, C. J. Yellow-green algae with chlorophyllide c. J. Phycol. 8, 10–14 (1972).

    CAS 

    Google Scholar 

  • 60.

    Balseiro, E. G., Souza, M. S., Modenutti, B. E. & Reissig, M. Living in transparent lakes: Low food P: C ratio decreases antioxidant response to ultraviolet radiation in Daphnia. Limnol. Oceanogr. 53, 2383–2390 (2008).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 61.

    Laspoumaderes, C., Souza, M. S., Modenutti, B. E. & Balseiro, E. Glacier melting and response of Daphnia oxidative stress. J. Plankton Res. 39, 675–686. https://doi.org/10.1093/plankt/fbx028 (2017).

    CAS 
    Article 

    Google Scholar 

  • 62.

    APHA. Standard methods for the examination of water and wastewater. (American Public Health Association, AWWA, 2005).

  • 63.

    Gorokhova, E. & Kyle, M. Analysis of nucleic acids in Daphnia: development of methods and ontogenetic variations in RNA-DNA content. J. Plankton Res. 24, 511–522 (2002).

    CAS 
    Article 

    Google Scholar 


  • Source: Ecology - nature.com

    Southward decrease in the protection of persistent giant kelp forests in the northeast Pacific