Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate

Abstract

Climate change scenarios predict that rivers, lakes, and reservoirs will experience increased temperatures, more intense and longer periods of thermal stratification, modified hydrology, and altered nutrient loading. These environmental drivers will have substantial effects on freshwater phytoplankton species composition and biomass, potentially favouring cyanobacteria over other phytoplankton. In this Review, we examine how several cyanobacterial eco-physiological traits, specifically, the ability to grow in warmer temperatures; buoyancy; high affinity for, and ability to store, phosphorus; nitrogen-fixation; akinete production; and efficient light harvesting, vary amongst cyanobacteria genera and may enable them to dominate in future climate scenarios. We predict that spatial variation in climate change will interact with physiological variation in cyanobacteria to create differences in the dominant cyanobacterial taxa among regions. Finally, we suggest that physiological traits specific to different cyanobacterial taxa may favour certain taxa over others in different regions, but overall, cyanobacteria as a group are likely to increase in most regions in the future.

Introduction

Cyanobacterial blooms present major challenges for the management of rivers, lakes and reservoirs. Blooms have adverse impacts on aquatic ecosystems and human health, with wide-ranging economic and ecological consequences (Hallegraeff, 1993, Mur et al., 1999). The increased frequency and intensity of blooms have been attributed to anthropogenic changes, principally nutrient over-enrichment and river regulation (Anderson et al., 2002). More recently, it has been predicted that a changing climate associated with rising levels of atmospheric CO₂ will increase the occurrence of blooms (Beardall et al., 2009, Paerl and Huisman, 2009, Paul, 2008), or at least favour cyanobacterial dominance of phytoplankton communities (Mooij et al., 2005). Decision support trees for bloom formation (e.g., Oliver and Ganf, 2000), as well as numerical model predictions that allow testing of multiple stressors (e.g., Trolle et al., 2011), suggest that there may be synergistic interactions amongst an array of environmental drivers to promote cyanobacterial blooms.

Why would cyanobacteria, and not other phytoplankton, be favoured under future climatic conditions? It is possible that cyanobacteria have several physiological characteristics that may be acting in concert to allow them to dominate in a changed climate. Alternatively, there may be physiological attributes of different cyanobacterial taxa that may leave them vulnerable under some conditions expected with climate change. An improved understanding of the interactions amongst both the environmental drivers that are predicted to change in different regions and cyanobacterial physiology is crucial for developing management strategies to mitigate or avoid the potential of more frequent blooms under future climate scenarios (Brookes and Carey, 2011, Paerl et al., 2011).

Cyanobacterial blooms are not a new phenomenon and have been occurring for centuries in both marine and freshwater systems (Codd et al., 1994, Fogg et al., 1973, Hayman, 1992, Paerl, 2008). Since the 1960s, however, there has been a dramatic global increase in the number of publications and reports of cyanobacterial blooms (Anderson et al., 2002, Carmichael, 2008, Hallegraeff, 1993, Hamilton et al., 2009, Paerl and Huisman, 2008, Van Dolah, 2000), primarily in freshwater and estuarine environments (Paerl, 1988). While increased reports may to some extent be due to increased monitoring efforts (Sellner et al., 2003), there is substantial evidence that blooms are increasing not only in frequency, but also in biomass, duration and distribution (Anderson et al., 2002, Glibert et al., 2005, Hallegraeff, 1993, Smayda, 1990). Furthermore, it has been hypothesised that cyanobacteria may continue to increase in response to global climate change (Mooij et al., 2005, Paerl et al., 2011, Paerl and Huisman, 2009).

The proliferation of cyanobacteria can have numerous consequences. In addition to risks to human and animal health (Chorus and Bartram, 1999, Ibelings and Chorus, 2007), there may also be substantial economic costs for water treatment and losses in tourism, property values, and business (Dodds et al., 2009, Steffensen, 2008). With a global distribution, escalating bloom occurrence and worldwide concern (Lundholm and Moestrup, 2006), it is important to review the evidence for the likelihood of cyanobacterial increases with climate change and how this may be related to cyanobacterial eco-physiology. Cyanobacteria have an extensive evolutionary history, and fossil evidence indicates that they were abundant over 2.5 billion years ago (Summons et al., 1999), and may have emerged as early as 3.5 billion years ago (Schopf, 2000). They are the earliest-known oxygen-producing organisms, and have key roles in global primary production and nitrogen-fixation (Chorus and Bartram, 1999). The lengthy history and variable environmental conditions under which cyanobacteria evolved have resulted in the adaptation of some cyanobacterial taxa to extreme environments, and collectively they are widely dispersed across the globe (Badger et al., 2006). They exist across a multitude of hot, cold, alkaline, acidic and terrestrial environments, and can proliferate to be the dominant primary producers in freshwater, estuarine, and marine ecosystems (Chorus and Bartram, 1999, Mur et al., 1999). Our focus in this Review is on freshwater and estuarine cyanobacteria.