The interaction between climate warming and eutrophication to promote cyanobacteria is dependent on trophic state and varies among taxa

Cyanobacteria are predicted to increase due to climate and land use change. However, the relative importance and interaction of warming temperatures and increased nutrient availability in determining cyanobacterial blooms are unknown. We investigated the contribution of these two factors in promoting phytoplankton and cyanobacterial biovolume in freshwater lakes. Specifically, we asked: (1) Which of these two drivers, temperature or nutrients, is a better predictor of cyanobacterial biovolume? (2) Do nutrients and temperature significantly interact to affect phytoplankton and cyanobacteria, and if so, is the interaction synergistic? and (3) Does the interaction between these factors explain more of the variance in cyanobacterial biovolume than each factor alone? We analyzed data from . 1000 U.S. lakes and demonstrate that in most cases, the interaction of temperature and nutrients was not synergistic; rather, nutrients predominantly controlled cyanobacterial biovolume. Interestingly, the relative importance of these two factors and their interaction was dependent on lake trophic state and cyanobacterial taxon. Nutrients played a larger role in oligotrophic lakes, while temperature was more important in mesotrophic lakes: Only eutrophic and hyper-eutrophic lakes exhibited a significant interaction between nutrients and temperature. Likewise, some taxa, such as Anabaena, were more sensitive to nutrients, while others, such as Microcystis, were more sensitive to temperature. We compared our results with an extensive literature review and found that they were generally supported by previous studies. As lakes become more eutrophic, cyanobacteria will be more sensitive to the interaction of nutrients and temperature, but ultimately nutrients are the more important predictor of cyanobacterial biovolume. There is a growing concern that interactions between climate warming and eutrophication are enhancing the frequency and magnitude of cyanobacterial blooms globally (Hallegraeff 1993; Jöhnk et al. 2008; Huber et al. 2012) and expanding the geographic range of some cyanobacterial taxa (Ryan et al. 2003; Briand et al. 2004; Sinha et al. 2012). The toxins produced by a number of the dominant bloom-forming cyanobacteria present a considerable risk to drinking water (Codd et al. 2005) and pose a substantial economic cost (Ho et al. 2002; Steffensen 2008; Dodds et al. 2009). In addition, cyanobacterial blooms have considerable negative effects on aquatic food webs and ecosystem functioning (Bartram and Chorus 1999; Havens 2007; Paerl et al. 2011). As a result of these public health, ecological, and economic effects, there has been a considerable effort to understand the underlying processes leading to bloom formation (Falconer 2005; Huisman et al. 2005; Hudnell 2008). Increased nutrients and temperature are believed to be two of the most important factors driving the increase in cyanobacteria (Paerl and Huisman 2008; Conley et al. 2009). Cyanobacteria have several ecophysiological adaptations that may allow them to dominate aquatic systems under warmer and more nutrient-rich conditions (Carey et al. 2012). For example, some cyanobacteria produce gas vesicles that allow them to regulate their buoyancy (Ganf and Oliver 1982; Huisman et al. 2005; Hudnell 2008). Cyanobacteria may take advantage of warming both directly, from temperature increases, and indirectly, from enhanced stratification of the water column (Carey et al. 2012). Under increased thermally stratified conditions, which are anticipated with global warming, these cyanobacterial taxa might be able to migrate between wellilluminated surface layers and nutrient-rich hypolimnetic waters (Ganf and Oliver 1982; Walsby 1994; Bouterfas et al. 2002), escaping the increasingly nutrient-depleted epilimnion of lakes during extended stratification periods (Livingstone 2003). Cyanobacteria may also take direct advantage of warming because their growth rate will increase with temperature, while the growth rates of many other phytoplankton taxa decline over 20uC (Reynolds 2006; Litchman et al. 2010); however, see Lürling et al. (2013). The ability to fix nitrogen (Oliver and Ganf 2000; Reynolds 2006) and the ability to produce dormant cells to survive unfavorable conditions (Bartram and Chorus 1999; Kaplan-Levy et al. 2010) are other physiological adaptations that may provide cyanobacteria a competitive advantage over other phytoplankton (Litchman et al. 2010; Carey et al. 2012), especially under increasingly unpredictable future climate conditions (IPCC 2007). Although cyanobacteria as a group have many traits that make them highly adaptable to environmental changes, they are comprised of taxa with very different physiological characteristics. For example, the size range of a cyanobacterial phycosphere spans nearly eight orders of magnitude, from the smallest single-celled cyanobacterial picoplankton * Corresponding author: [email protected] Limnol. Oceanogr., 59(1), 2014, 99–114 E 2014, by the Association for the Sciences of Limnology and Oceanography, Inc. doi:10.4319/lo.2014.59.01.0099