water research 46 (2012) 1349e1363

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Climate change: Links to global expansion of harmful

Hans W. Paerl a,*, Valerie J. Paul b,1 a Institute of Marine Sciences, University of North Carolina at Chapel Hill, 3431 Arendell Street, Morehead City, NC 28557, USA b Smithsonian Marine Station, Ft. Pierce, FL 34949, USA article info abstract

Article history: Cyanobacteria are the Earth’s oldest (w3.5 bya) oxygen evolving organisms, and they have Received 20 May 2011 had major impacts on shaping our modern-day biosphere. Conversely, biospheric envi- Received in revised form ronmental perturbations, including nutrient enrichment and climatic changes (e.g. global 11 July 2011 warming, hydrologic changes, increased frequencies and intensities of tropical cyclones, Accepted 2 August 2011 more intense and persistent droughts), strongly affect cyanobacterial growth and bloom Available online 18 August 2011 potentials in freshwater and marine ecosystems. We examined human and climatic controls on harmful (toxic, hypoxia-generating, food web disrupting) bloom-forming cya- Keywords: nobacteria (CyanoHABs) along the freshwater to marine continuum. These changes may Cyanobacteria act synergistically to promote cyanobacterial dominance and persistence. This synergy is a formidable challenge to water quality, water supply and fisheries managers, because bloom potentials and controls may be altered in response to contemporaneous changes in Hydrology thermal and hydrologic regimes. In inland waters, hydrologic modifications, including Nutrients enhanced vertical mixing and, if water supplies permit, increased flushing (reducing Freshwater residence time) will likely be needed in systems where nutrient input reductions are Marine neither feasible nor possible. Successful control of CyanoHABs by grazers is unlikely except Water quality management in specific cases. Overall, stricter nutrient management will likely be the most feasible and practical approach to long-term CyanoHAB control in a warmer, stormier and more extreme world. ª 2011 Elsevier Ltd. All rights reserved.

1. Introduction enabled them to develop diverse and highly effective ecophysiological adaptations and strategies for ensuring Cyanobacteria (blue-green ) are the Earth’s oldest survival and dominance in aquatic environments undergoing known oxygen-producing organisms, with fossil remains natural and human-induced environmental change (Hallock, dating back w3.5 billion years (Schopf, 2000). Cyanobacterial 2005; Huisman et al., 2005; Paerl and Fulton, 2006; Paul, 2008). proliferation during the Precambrian period is largely Today, they enjoy a remarkably broad geographic distribu- responsible for the modern-day, oxygen-enriched atmo- tion, ranging from polar to tropical regions in northern and sphere, and subsequent evolution of higher plant and animal southern hemispheres, where they are capable of domi- life (Schopf, 2000; Whitton and Potts, 2000). This long evolu- nating planktonic and benthic primary production in diverse tionary history has served cyanobacteria well, for it has .

* Corresponding author. Tel.: þ1 252 726 6841x133; fax: þ1 252 726 2426. E-mail addresses: [email protected] (H.W. Paerl), [email protected] (V.J. Paul). 1 Tel.: þ1 772 462 0982. 0043-1354/$ e see front matter ª 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.watres.2011.08.002 1350 water research 46 (2012) 1349e1363

As a “microalgal” group, the cyanobacteria exhibit highly In freshwater ecosystems, P availability has traditionally efficient nutrient (N, P, Fe and trace metal) uptake and storage been viewed as a key factor limiting CyanoHAB proliferation capabilities, and they are the only oxygenic phototrophs (Schindler, 1975; Schindler et al., 2008), and excess P (relative capable of utilizing atmospheric dinitrogen (N2) as a nitrogen to N) loading has been identified as favoring CyanoHABs source to support growth via N2 fixation (Fogg, 1969; Gallon, (Smith, 1983; Watson et al., 1997; Downing et al., 2001). The

1992). Furthermore, many planktonic genera are capable of emphasis on P controls is based on the N2 fixing capabilities of rapid vertical migration by altering their buoyancy, allowing some CyanoHAB genera, which help satisfy cellular N- them to exploit deeper, nutrient-rich waters while also taking requirements under P-limited conditions (Paerl and Fulton, advantage of radiant-rich conditions near the surface (Ibelings 2006). However, at the ecosystem level, only a fraction, et al., 1991; Walsby et al., 1997; Reynolds, 2006). Lastly, some usually far less than 50%, of primary and secondary produc- genera have formed symbioses (as endosymbionts) in dia- tion demands are met by N2 fixation, even when P supplies are toms, sponges, corals, lichens, ferns, and mutualistic associ- sufficient (Howarth et al., 1988; Lewis and Wurtsbaugh, 2008; ations with a variety of other organisms which provide Paerl and Scott, 2010). Hence, N2 fixation appears to be protection and enhance nutrient cycling and availability in controlled by factors in addition to P availability. Nutrient nutrient-deplete waters (Paerl and Pinckney, 1996; Carpenter, loading dynamics have changed substantially over the past 2002; Rai et al., 2002). several decades. While P reductions have been actively Over the past several centuries, human nutrient over- pursued, human population growth in watersheds has been enrichment (particularly nitrogen and phosphorus) associ- paralleled by increased N loading, often at higher rates than P ated with urban, agricultural and industrial development, has (Vitousek et al., 1997; Paerl and Scott, 2010). Excessive N loads promoted accelerated rates of primary production, or eutro- are now as large a concern as P loads as stimulants of fresh- phication. Eutrophication favors periodic proliferation and water, estuarine and marine eutrophication and harmful algal dominance of harmful blooms of cyanobacteria (CyanoHABs), (including cyanobacterial) blooms (Conley et al., 2009; Paerl, both in planktonic (Fogg, 1969; Steinberg and Hartmann, 1988; 2009; Ahn et al., 2011). Huisman et al., 2005; Paerl and Fulton, 2006) and benthic Mass development of CyanoHABs, increases turbidity and (Baker et al., 2001; Dasey et al., 2005; Wood et al., 2006; hence restricts light penetration in affected ecosystems (Figs. Izaguirre et al., 2007; Elmetri and Bell, 2004; Albert et al., 1 and 2). This, in turn, suppresses the establishment and 2005; Ahern et al., 2007; Paerl et al., 2008) environments. growth of aquatic macrophytes and benthic microalgae and

Fig. 1 e Examples of freshwater systems impacted by proliferating CyanoHABs Upper left, MODIS satellite image of surface cyanobacterial blooms in Lake Erie (US-Canadian Great Lakes) during July, 2007. (Courtesy of NASA and Coastwatch-Great Lakes). Upper right, Cyanobacterial (Aphanizomenon flos aquae) bloom on Lake Dianchi, Yunan Provice, China, July 2006 (Courtesy of http://4.bp.blogspot.com/_KbJGi-TtEtQ/SVGUNroO4aI/AAAAAAAAAyE/iGR9zvvSrPg/s400/DianchiD Lake_China_BlueDGreenDAlgaeDBloom). Lower left, Cyanobacterial (Microcystis spp.) bloom in Lake Taihu, Jiangsu Province, China, photographed by author H. Paerl during a lake-wide bloom in July, 2007. Lower right, a CyanoHAB bloom (Microcystis and Anabaena spp.) on the lower St. Johns River, Florida during summer, 2005 (Courtesy of Bill Yates/CYPIX). water research 46 (2012) 1349e1363 1351

Fig. 2 e Examples of Marine CyanoHABs. Upper left, Lyngbya confervoides covering a nearshore reef off Fort Lauderdale, FL (photo credit K. Lane). Middle, mixed cyanobacterial community smothering corals in Papua New Guinea (photo credit R. Ritson-Williams). Upper right, blooms of Lyngbya sp. smothering seagrass beds near Sanibel Island, coastal Gulf of Mexico, Florida (Photo credit H. Paerl), in May 2007. Lower left, a bloom of the colony-forming filamentous cyanobacterium thiebautii, near Sanibel Island, coastal Gulf of Mexico, in May 2007 (Photo credit H. Paerl). Lower right, a massive cyanobacterial (Nodularia, Anabaena, Microcystis) surface bloom in the Baltic Sea-Gulf of Finland captured as a SeaWiFS image (June 2005) (Photo courtesy of NASA).

thereby negatively affects the underwater for benthic Microcystis and Planktothrix, and the benthic N2 fixing genera flora and fauna (Jeppesen et al., 2007; Scheffer et al., 1997, Lyngbya, Hormothamnion and (some species of) Oscillatoria, and

Scheffer, 2004). CyanoHABs also cause nighttime oxygen non-N2 fixing genera Phormidium, Symploca, and Oscillatoria. depletion through respiration and bacterial decomposition of dense blooms, which can result in fish kills and loss of benthic infauna and flora (Paerl, 2004; Watkinson et al., 2005; Garcia 2. Influence of a changing climate on and Johnstone, 2006; Paerl and Fulton, 2006). Persistence of CyanoHAB proliferation CyanoHABs can lead to long-term loss of benthic habitat (c.f., Karlson et al., 2002). Lastly, numerous planktonic and benthic While the connection between eutrophication and Cyano- cyanobacterial bloom genera produce toxic peptides and HABs expansion is well-established (Fogg, 1969; Paerl, 1988; alkaloids (Berry et al., 2008; Humpage, 2008; Liu and Rein, Reynolds, 2006; Paerl and Fulton, 2006), climatic changes 2010). Ingestion of these cyanotoxins has been linked to have also been implicated (Briand et al., 2004; Elliott et al., liver, digestive and skin diseases, neurological impairment 2005, 2006; Paerl and Huisman, 2008; Paul, 2008; Paerl et al., and even death (Chorus and Bartram, 1999; Carmichael, 2001; 2011a,b). In particular, global warming and associated hydro- Humpage, 2008). Hence, toxic CyanoHABs are a major threat logic changes, both of which are well-documented (IPCC, to the use of freshwater ecosystems and reservoirs for 2007), strongly affect the physicalechemical environment drinking water, irrigation, and freshwater and marine fishing and biological processes, most notably metabolism, growth and recreational purposes (Chorus and Bartram, 1999; rates and bloom formation (Fig. 3). Carmichael, 2001; Osborne et al., 2001, 2007). Warming can selectively promote cyanobacterial growth Widely-distributed toxin-producing CyanoHABs include because as prokaryotes, their growth rates are optimized at the planktonic N2 fixing genera Anabaena, Aphanizomenon, relatively high temperatures (Robarts and Zohary, 1987;

Cylindrospermopsis, Nodularia, the non-N2 fixing genera Butterwick et al., 2005; Watkinson et al., 2005). This provides 1352 water research 46 (2012) 1349e1363

Fig. 3 e Conceptual diagram, illustrating the multiple interacting environmental variables controlling CyanoHAB formation and proliferation along the freshwateremarine continuum. Key factors controlling cyanobacterial growth and dominance, including nutrient inputs/availability, transparency, mixing conditions, water residence times, temperature and grazing are shown.

CyanoHABs a distinct advantage under nutrient-enriched also lengthens the period of stratification. In freshwater conditions, when competition with eukaryotic primary systems, stratification tends to take place earlier in spring, the producers, including , chlorophytes, cryptophytes and stratification is maintained throughout summer, and destra- dinoflagellates can be intense (Paerl et al., 2011a,b). Fig. 4 shows tification is postponed to later in autumn (De Stasio et al., 1996; that as growth rates of these eukaryotic taxa level off or decline, Peeters et al., 2007; Elliott et al., 2005; Elliott, 2010). Many Cya- cyanobacterial growth rates reach their optima and continue to noHAB species are able to uniquely exploit stratified condi- remain high, even when temperatures exceed 25 C. tions. Most bloom-forming cyanobacteria contain gas vesicles Warming of surface waters intensifies vertical stratification which provide buoyancy (Walsby et al., 1997), enabling them to in both freshwater and marine systems. Seasonal warming form dense surface blooms in stratified waters (Figs. 1 and 2), where they can take advantage of high levels of irradiance to optimize (Huisman et al., 2005). CyanoHABs themselves may locally increase water temperatures, through the intense absorption of light by their photosynthetic and photoprotective pigments. Using remote sensing, Kahru et al. (1993) found temperatures of surface blooms in the Baltic Sea to be at least 1.5 C above ambient waters, and Ibelings et al. (2003) noted that the surface temperatures within cyanobacterial blooms in Lake IJssel- meer, Netherlands, were higher than the surrounding surface waters. This represents a positive feedback mechanism, whereby buoyant cyanobacteria enhance surface tempera- tures, which promotes their competitive dominance over eukaryotic . Surface-dwelling CyanoHAB taxa contain photoprotective accessory pigments (e.g. carotenoids) and UV-absorbing compounds (mycosporine-like amino acids (MAAs), scytone- Fig. 4 e Effects of temperature on species-specific growth min) that ensure long-term survival under extremely high rates of a representative CyanoHAB species (Microcystis irradiance conditions (Paerl et al., 1983; Castenholz and Garcia- aeruginosa) vs. commonly encountered eukaryotic algal Pichel, 2000; Paul, 2008; Carreto and Carignan, 2011), while bloom species, including the chlorophyte Golenkinia suppressing non-buoyant species through competition for light. radiata, the Skeletonema costatum, and the Other mechanisms surface-dwelling cyanobacteria have dinoflagellate Prorocentrum minimum. Growth rate data are for dealing with UV stress include production of antioxidant from Reynolds (2006), Grzebyk and Berland (1995), and enzymes, such as superoxide dismutase, catalase, and gluta- Yamamoto and Nakahara (2005). thione peroxidase, and antioxidant molecules, including water research 46 (2012) 1349e1363 1353

ascorbate, carotenoids, and tocopherols (Paerl et al., 1985; He 2007) and may similarly affect other N2 fixing planktonic and and Ha¨der, 2002; Xue et al., 2005). Cyanobacteria have been benthic cyanobacteria. shown to adapt to UVB radiation (280e315 nm) hours to days after exposure, even without the productions of MAAs. Protective mechanisms include enhanced DNA repair, 4. Hydrologic changes associated with induction of UVR (100e400 nm) resistant proteins and lipids, climatic change and upregulation of peptides and proteins (Castenholz and Garcia-Pichel, 2000). Carotenoids can help protect cyano- Global warming and associated changes in climatic oscilla- bacterial surface blooms from UVR (Paerl et al., 1983). The tions affect patterns, intensities and duration of precipitation beneficial effects of carotenoids may be indirect since they do and droughts, with ramifications for CyanoHAB dominance. not optimally absorb UVR, and they may primarily serve as For example, larger and more intense precipitation events antioxidants and inhibitors of free radical reactions mobilize nutrients on land and increase nutrient enrichment (Castenholz and Garcia-Pichel, 2000). Planktonic cyanobac- of receiving waters (Paerl et al., 2006; King et al., 2007). teria and motile species that occur in microbial mats can Freshwater discharge to downstream waters would also migrate vertically in the water column or within benthic mats increase, which in the short-term may prevent blooms by to move away from UVR. Increasing temperatures, stronger flushing. However, as the discharge subsides and water resi- stratification and longer bloom-susceptible periods will affect dence time increases, its nutrient load will be captured and both the composition and successional patterns of cyano- cycled by receiving water bodies, eventually promoting bloom bacterial and eukaryotic algae in aquatic ecosystems. Longer potentials. This scenario will most likely occur if elevated bloom periods provide a wider “window” for the establish- winterespring rainfall and flushing events are followed by ment and succession of CyanoHABs. For example, it has protracted periods of drought. Examples include the Swan recently been shown that competition among toxic vs. non- River and its estuary in Australia, Hartbeespoort dam reser- toxic strains of the often-dominant CyanoHAB Microcystis is voir, South Africa, the Neuse River Estuary, North Carolina, strongly affected by the length of the springesummer period and the Potomac Estuary, Maryland, USA (Sellner et al., 1988; and light availability needed for supporting various strains Robson and Hamilton, 2003; Huisman et al., 2005; Paerl, (Kardinaal et al., 2007). 2008). This sequence of events has also been responsible for massive CyanoHABs in large lake ecosystems serving key drinking water, fisheries and recreational needs (e.g. Lake 3. The link to carbon dioxide dynamics Taihu and other large lakes in China, Lake Erie, US Great Lakes, Lake Victoria and Lake George, Africa) (Huisman et al., A key driver of global warming is the rising level of the 2005; Qin et al., 2010; Paerl et al., 2011a,b), and regions of the atmospheric greenhouse gas carbon dioxide (CO2), which is Baltic Sea (Kahru et al., 1993: Suikkanen et al., 2007). Attempts emitted from accelerating rates of fossil fuel combustion and to control discharge of rivers and lakes by dams and sluices burning (IPCC, 2007). In nutrient-enriched freshwater may increase the residence time, thereby further aggravating systems, dense CyanoHAB blooms exhibit high photosyn- ecological and health problems associated with CyanoHABs thetic demands for CO2; to the extent that ambient waters (Burch et al., 1994; Rahman et al., 2005; Mitrovic et al., 2006). contain virtually no free CO2, driving the pH up to 10 or higher; to the extent that the rate of CO2 supply can at times control the rate of algal biomass production (Paerl and Ustach, 1982; 5. Salinization Ibelings and Maberly, 1998; Huisman et al., 2005). When this occurs, buoyant CyanoHABs have a distinct advantage over Increasing frequency and severity of droughts is causing more sub-surface phytoplankton populations, since surface- saline conditions in lake, reservoir, riverine and estuarine dwelling taxa can directly intercept CO2 from the atmo- environments worldwide. In addition, rising sea levels, and sphere, thereby minimizing dissolved inorganic carbon (DIC) ever-increasing demands on freshwater for drinking water limitation of photosynthetic growth and taking advantage of and irrigation purposes have promoted increased levels of rising atmospheric CO2 levels (Paerl and Ustach, 1982). Rising salinity. From a hydrologic perspective, this trend represents levels of atmospheric CO2 may lead to acidification of both a positive feedback loop, since increased water withdrawal for freshwater and marine surface waters, a subject of current human use threatens the freshwater supply because it is research (Doney, 2006; Keller, 2009). However, in CyanoHAB- getting saltier as a result of those withdrawals. Many Cyano- impacted eutrophic systems, this effect is likely to be negated HAB taxa can counter such extremeness by surviving for long by the increased bloom activity, which enhances CO2 periods (up to many years) as dormant cysts in sediments, consumption and elevates pH levels. In addition, some non- soils, or desiccated mats in arid regions (Potts, 1994). surface dwelling CyanoHABs are capable of sustained Increasing salinity levels also have major impacts on growth under the high pH conditions resulting from active planktonic and benthic microalgal community structure and photosynthesis and CO2 withdrawal during blooms, by being function. One impact of salinization is increased vertical able to directly use bicarbonate (HCO3) as a DIC source density stratification, which would benefit buoyant Cyano- (Shapiro, 1990; Kaplan et al., 1991; Badger and Price, 2003). HABs that can take advantage of such stratification (Visser

Elevated CO2 was shown experimentally to enhance growth, et al., 1995; Walsby et al., 2006). In addition, some species of

C:N ratios and N2 fixation in the open ocean bloom-forming common CyanoHAB genera such as Anabaena, Anabaenopsis, cyanobacterium (Levitan et al., Microcystis and Nodularia are quite salt tolerant, sometimes 1354 water research 46 (2012) 1349e1363

more so than counterpart eukaryotic freshwater phyto- (west Asia), Patos Lagoon Estuary (Brazil), the Oued Mellah species (Fig. 5). For instance, the growth rate of toxic reservoir (Morocco), the Swan River Estuary (Australia), San strains of Microcystis aeruginosa remains unaffected by salin- Francisco Bay (California, USA), Lake Ponchartrain (Louisiana, ities ranging from 0 g L 1 up to 10 g L 1, or 30% of seawater USA), and the Kucukcekmece Lagoon (Turkey) (Paerl and salinity (Tonk et al., 2007). Intermittent salinity fluctuations of Huisman, 2009; Akcaalan et al., 2009). The increased expan- up to 15e20 g L 1 may still allow survival of Microcystis pop- sion of CyanoHABs into brackish and full-salinity waters ulations, but cause salt stress, leading to leakage of cells and potentially exposes other aquatic organisms and human users excretion of the toxin microcystin (Ross et al., 2006). Likewise, (recreational, fishing) of these waters to elevated concentra- Anabaena aphanizominoides can withstand salt levels up to tions of cyanobacterial toxins. 15 g L 1, while Anabaenopsis and toxic Nodularia spumigena even tolerate salinities ranging from 0 g L 1 to more than 20 g L 1 (Moisander et al., 2002; Tonk et al., 2007)(Fig. 5. 6. Grazer interactions Laboratory experiments indicate that the nodularin content of Nodularia correlates positively with salinity (Mazur-Marzec Cyanobacteria are generally considered to be relatively low et al., 2005). The high salt tolerance of these CyanoHABs is preference foods for marine herbivores because of chemical reflected by increasing reports of blooms in brackish waters, and structural defenses and poor nutritional quality; however, for example in the Baltic Sea (Northern Europe), Caspian Sea there is considerable variability in the ability of different

e Fig. 5 Effects of salinity, as NaCl, on photosynthetic activity (as CO2 fixation) and growth of representative CyanoHAB genera. Note the high degree of variability among these genera for tolerating saline conditions. Some genera can be designated as “freshwater” by their intolerance of salinity (e.g. Cylindrospermopsis), while others (Nodularia, Anabaenopsis) can grow well in near-seawater salinity. Salinity is in practical salinity units (psu). Cyanobacterial strains used in the assays were recently isolated from natural waters. Figure adapted from Moisander et al. (2002). water research 46 (2012) 1349e1363 1355

grazers to consume and grow on cyanobacteria (Paerl et al., lakes (Sarnelle, 1993; Vanni et al., 1997). Both consumers and 2001; Paul et al., 2001; Landsberg, 2002; Sarnelle and Wilson, nutrient availability can have pronounced effects on food 2005; Camacho and Thacker, 2006; Berry et al., 2008; Wilson webs, including phytoplankton biomass and community et al., 2006; Tillmanns et al., 2008). There is evidence that the structure (Brett and Goldman, 1997). These complex factors natural products from cyanobacteria, which are mainly lip- coupled with climatic variation can drive successional opeptides, peptides, depsipeptides and alkaloids, can serve as patterns, phytoplankton and dynamics in lake chemical defenses or may be toxic to grazers and competitors ecosystems (Blenckner et al., 2007). (Christoffersen, 1996; Paul et al. 2001, 2007; Landsberg, 2002; Little is known about how temperature and other abiotic Berry et al., 2008). The chemical defenses of cyanobacteria factors may play a role in specific trophic interactions. may play a critical role in bloom formation and persistence by Temperature, light, and nutrients may have interactive effects limiting the grazing activity of some potential consumers. on cyanobacterial growth and toxin production, with conse- Hallock (2005) suggested that benthic marine cyanobac- quent effects on aquatic food webs. One laboratory study teria, which are resistant to strong solar radiation, warm showed that increases in water temperature could increase temperatures, abundant nutrients, and many generalist the susceptibility of rotifers to toxic effects of anatoxin- grazers, may be useful indicators of stress conditions in reef a produced by Anabaena flos-aquae (Gilbert, 1996). Two plank- ecosystems. Benthic cyanobacteria can be early colonizers of tonic rotifers were acclimated for many generations to low dead coral and disturbed substrates and are becoming (12e14 C), intermediate (19 C), and high (25 C) water increasingly well-established on coral reefs. Tsuda and Kami temperatures, and reproductive rates of the rotifers were (1973) observed that low light penetration and selective inhibited by the cyanobacterium and anatoxin-a. The negative browsing by herbivorous fishes on macroalgae removed effects of the cyanobacterium and the toxin increased with potential competitors and favored the establishment of increasing temperature. unpalatable benthic cyanobacteria in tropical lagoonal envi- Studies have also shown correlations between climate ronments. Crude extracts and isolated secondary metabolites variation, often related to the North Atlantic Oscillation (NAO), of several benthic marine cyanobacteria such as Lyngbya spp. and spring plankton dynamics and clear water phases in have been shown to deter grazing by generalist herbivores such shallow, polymictic European lakes (Gerten and Adrian, 2000; as fishes and sea urchins (reviewed by Paul et al. 2001, 2007). Scheffer et al., 2001; Abrantes et al., 2006; Blenckner et al., In freshwater ecosystems, cyanobacterial blooms can have 2007). Clear water phases, caused by grazing of zooplankton negative effects on large cladocerans such as Daphnia spp., on microalgae, were studied in 71 shallow Dutch lakes and which may be more susceptible to cyanobacterial toxins than were found to occur earlier when water temperatures were some other grazers (Tillmanns et al., 2008). Negative physio- higher (Scheffer et al., 2001, Scheffer, 2004). Water tempera- logical effects (DeMott et al., 1991; Rohrlack et al., 2001, 2005 ) tures were strongly related to the North Atlantic Oscillation and negative fitness consequences (Gustafsson et al., 2005)on (NAO) winter index. A simulation model of algaeezooplankton zooplankton grazers such as Daphnia spp. have been observed; dynamics seemed to confirm the primary role of temperature however, the physiological susceptibilities of different pop- in determining the probability and timing of the clear water ulations of zooplankton can vary considerably. Some pop- phase. In a 42-year study of the small subalpine Castle Lake in ulations of Daphnia galeata and Daphnia pulicaria exposed to northern California, increasing water temperatures were chronically high abundance of cyanobacteria can adapt to accompanied by increasing mean summer cyanobacteria bio- being more tolerant of cyanobacteria in their diets (Hairston volume, whereas diatoms and other phytoplankton groups did et al., 1999, 2001; Sarnelle and Wilson, 2005). Cyanobacteria not show significant trends with summer water temperatures and cyanotoxins can also inhibit feeding by other grazers, (Park et al., 2004). Summer water temperature also had such as copepods and rotifers, in fresh and estuarine waters a significant positive correlation with biomass of Daphnia rosea, (Sellner et al., 1993; Paerl et al., 2001; Reinikainen et al., 2002). a relationship also reported for European lakes where warm Grazer interactions with cyanobacteria are highly species- winter air temperatures caused by the NAO enhanced spring specific; considerable intra- and interspecific variation in the Daphnia biomass and influenced the timing of the clear water effects of cyanobacteria and cyanobacterial toxins on phase (Straile and Adrian, 2000; Blenckner et al., 2007). consumers have been observed in experimental studies (Wilson and Hay, 2007; Tillmanns et al., 2008). Additional complexity in zooplanktonecyanobacterial 7. Evidence from aquatic ecosystems interactions can be observed when higher trophic levels, such undergoing climatically-induced ecological as fishes that are zooplankton grazers, are included in change observational and experimental studies. Zooplankton species that can control cyanobacteria, such as Daphnia spp. Evidence from geographically-diverse aquatic ecosystems (Sarnelle, 1993; Tillmanns et al., 2008), are often the preferred varying in size, morphology, salinity and hydrologic condi- food of planktivorous fishes in freshwater systems. Studies tions, indicates that climatic change can act synergistically manipulating fish abundance often demonstrate a typical with anthropogenic nutrient enrichment to promote global trophic cascade where zooplanktivorous fishes reduce the expansion of CyanoHABs. abundance of zooplankton and increase the biomass of Kosten et al. (2011) conducted a survey of 143 lakes of phytoplankton (Brett and Goldman, 1997; Vanni et al., 1997; varying trophic state situated along a latitudinal gradient from Carpenter et al., 2001). Fish and zooplankton abundance Northern Europe to Southern South America. They found that also directly and indirectly affect nutrient dynamics in these the percentage of total phytoplankton biomass attributable to 1356 water research 46 (2012) 1349e1363

cyanobacteria increased markedly with temperature. These Midwest reservoirs and lakes, especially those undergoing authors also noted that temperature increases may lower the eutrophication accompanied by a loss of water clarity nutrient input thresholds at which blooms can be initiated (Chapman and Schelske, 1997). The mechanisms of invasion and sustained; that is, at elevated temperatures, bloom- and proliferation are under examination. However, it is forming CyanoHABs can proceed at lower nutrient input rates known that C. raciborskii, which is typically dispersed and concentrations than when temperatures were relatively throughout the water column, is adapted to low light condi- cooler. For example, in Northern Europe (N. Germany, tions encountered in many turbid, eutrophic waters (Padisa´k, Sweden, Finland) lakes that exhibit symptoms of long-term 1997; Stu¨ ken et al., 2006). It also prefers water temperature (decadal-scale) warming, including warmer surface water conditions in excess of 20 C, and survives adverse conditions temperatures, stronger and more persistent vertical stratifi- using specialized resting cells, akinetes (Briand et al., 2004; cation, earlier melting of their ice covers and overall extended Wiedner et al., 2007). warm water conditions and longer growing seasons show The filamentous toxin-producing CyanoHAB Lyng- increases in cyanobacterial dominance, bloom frequencies bya has likewise exhibited remarkable invasive abilities in and persistence (Weyhenmeyer, 2001; No˜ ges et al., 2003; a range of aquatic ecosystems, including streams, rivers, Wagner and Adrian, 2009; Feuchtmayr et al., 2009; Elliott, lakes, reservoirs, estuarine and coastal waters. Nutrient 2010). enrichment has been implicated in its expansion (Paerl and These results expand on previous studies confined to lakes Fulton, 2006). Lyngbya species often form periphytic or in tropical and subtropical waters that show a tendency benthic mats, although some species, such as Lyngbya birgei, toward domination by cyanobacteria, even when trophic are planktonic. Lyngbya outbreaks have been associated with states varied (Ganf and Horne, 1975; Talling, 1986; Lewis, 1987; human health problems. The marine species Lyngbya majus- Phlips et al., 1997; Bouvy et al., 2000; Velzeboer et al., 2000; cula is commonly known as “fireweed” or “mermaid’s hair” Koma´rkova´ and Tavera, 2003; Havens et al., 2003; Abrantes (Fig. 2). It is widely associated with contact dermatitis, where et al., 2006). Relatively high rates of N2 fixation, a key indi- the initial burning symptoms give way to blister formation cator of cyanobacterial activity and an important biogeo- and peeling of the skin (Carmichael, 2001). L. majuscula chemical process, are observed in tropical freshwater and produces a large suite of bioactive compounds, including the marine systems as well (Horne and Viner, 1971; Capone, 1983; dermatoxic aplysiatoxins and lyngbyatoxin A (Osborne et al., Capone et al., 2005). Overall, these studies show a strong 2001), and hundreds of other natural products (Paul et al., positive relationship between mean annual temperature and 2007; Liu and Rein, 2010). In freshwater environments, Lyng- cyanobacterial dominance, a trend originally observed by bya wollei has been associated with the production of paralytic Robarts and Zohary (1987). There are exceptions to this, shellfish poisoning (PSP) toxins (Carmichael, 2001). including high elevation (although cyanobacteria are common Lyngbya blooms are increasingly common in nutrient- in some high altitude, low latitude lakes (e.g. Lake Titicaca, enriched waters, including those that have experienced Peru-Bolivia) (Wurtsbaugh et al., 1985), high humic acid human disturbance such as dredging, inputs of treated content and resultant acidic conditions (i.e. pH < 6), extremely municipal waste, and the discharge of nutrient laden fresh- oligotrophic (severe nutrient-limited), rapidly flushed (short water through coastal canals (Paerl et al., 2006, 2008). Both residence time), and poorly-stratified (polymictic) conditions Lyngbya majuscula (marine) and Lyngbya wollei (freshwater) are (Vincent, 1987). Interestingly, the proportion of cyanobacteria opportunistic invaders when favorable environmental condi- in both planktonic and benthic habitats of these systems tions exist (nutrient over-enrichment, poorly flushed condi- increases as nutrient loading increases, which suggests tions). Following large climatic and hydrologic perturbations synergism between elevated temperatures and nutrient such as hurricanes, L. wollei is an aggressive initial colonizer of enrichment. flushed systems (Paerl and Fulton, 2006). Lyngbya blooms can Some of the CyanoHAB taxa typically associated with proliferate as dense floating mats that shade other primary warmer water conditions, including the planktonic hetero- producers, enabling Lyngbya to dominate the system by cystous N2 fixer Cylindrospermopsis sp, and the benthic/ effectively competing for light (Fig. 2). As is the case with planktonic non-heterocystous filamentous genus Lyngbya Cylindrospermopsis and Microcystis, this CyanoHAB can take spp. (some species are known to fix N2) have expanded into advantage of both human and climate-induced environmental temperate regions (Stu¨ ken et al., 2006; Wiedner et al., 2007). change. Cylindrospermopsis was originally described as a tropical and Interestingly, expansion of some CyanoHAB genera has subtropical species. However, Cylindrospermopsis raciborskii occurred even in some lakes that have experienced no recent appeared in Europe during the 1930s, and showed a progres- increase in nutrient (N and P) loading, indicating that in sive colonization from Greece and Hungary toward higher certain cases increasing temperature may play an indepen- latitudes near the end of the 20th century (Padisa´k, 1997). It dent role in promoting geographic expansion of some Cya- was first described in France in 1994, in the Netherlands in noHABs (Padisa´k, 1997; Stu¨ ken et al., 2006; Kosten et al., 2011). 1999, and it is now also widespread in lakes in northern Most CyanoHAB-impacted lakes, rivers, estuaries and coastal Germany (Stu¨ ken et al., 2006). C. raciborskii was first identified waters, however, also have a recent history of increases in in the United States in 1955, in Wooster Lake, Kansas. C. raci- nutrient loading accompanying human population increases borskii may have arrived in Florida almost 35 years ago, after in their water- and airsheds (Huisman et al., 2005; Paerl et al., which it aggressively proliferated in lake and river systems 2011a,b). These systems have, in general, shown increases in throughout central Florida (Chapman and Schelske, 1997). cyanobacterial dominance and production. They are also This CyanoHAB has spread throughout US Southeast and sensitive to the effects of regional warming. In central Florida water research 46 (2012) 1349e1363 1357

(USA), numerous lakes have experienced the co-occurring agricultural expansion (rowcrop, cattle grazing and dairy effect of nutrient over-enrichment and climate change, operations), urbanization and industrialization. However, including larger oscillations between particularly active storm over the past 100 þ years, this region has also experienced periods and extreme droughts, as well as long-term increases a rise in mean annual air temperatures. This has caused in mean seasonal and annual air temperatures (Phlips et al., surface water warming, an increased potential for water 1997; Havens et al., 2007). column stratification and increased frequencies and magni- China’s third largest lake, Taihu is situated in Jiangsu tudes of buoyant, surface-dwelling CyanoHAB genera, espe-

Province, China’s most rapidly-growing economic region cially non-N2 fixing genera such as Microcystis (indicative of N (Fig. 1). Rapid increases in urbanization, agricultural produc- enrichment). Regional warming further promotes such tion and industrial output have led to a significant increase in blooms (Jo¨ hnk et al., 2008). both N and P loading (Qin et al., 2007; Hai et al., 2010; Paerl Similarly, the Baltic Sea region, which has been impacted et al., 2011a,b). This trend has led to a phytoplanktonic by anthropogenic nutrient enrichment and has exhibited “state change”, from a largely diatom-dominated community symptoms of eutrophication for several centuries (Elmgren in the 1960s and 1970s to what is now a CyanoHAB (Microcystis and Larsson, 2001), has also shown a recent warming trend, spp.) dominated community for much of the year (May which has translated into changes in phytoplankton through October) (Chen et al., 2003a,b; Qin et al., 2010). community composition favoring cyanobacterial dominance Increases in N and P loading have continued steadily since the (Suikkanen et al., 2007). Paleolimnological evidence, 1960s, reflecting population growth in the Taihu Basin (Qin including diagnostic pigment analyses of sediments (Bianchi et al., 2007, 2010). Regional warming has also taken place, as et al., 2000) has indicated that cyanobacteria formed shown in records kept by the Chinese Meteorological Bureau a significant fraction of phytoplankton biomass prior to the at nearby Shanghai and a recent rise in mean lake water 20th century. However, the relative dominance and persis- temperatures (Qin et al., 2010)(Fig. 6). The recent increase in tence of CyanoHABs may have increased in response to more warming has occurred much faster than nutrient loading (Qin favorable climatic conditions, especially warming (Suikkanen et al., 2010). Interestingly, bloom intensity or biomass, as et al., 2007). measured by depth-integrated chlorophyll a concentrations, In efforts to protect the world’s drinking and irrigation have also rapidly increased in parallel with air and water waters, fisheries and recreational resources represented by temperature increases (Fig. 6). Qin et al. (2010) concluded that these ecosystems, researchers and water quality/resource these trophic changes were attributed to the combined effects managers are faced with simultaneous, interactive “moving of nutrient over-enrichment and a warming trend. targets” that represent formidable challenges, including The shallow lakes of the Netherlands provide a long-term effects of 1) nutrient over-enrichment, 2) temperature record of phytoplankton community changes accompanied increases, including changes in thermal stratification and 3) by cultural eutrophication and climatic changes. Eutrophic changes in freshwater discharge, flow (flushing) regimes and conditions have been present for several centuries, following water residence time. Despite the diverse findings showing the reclaiming of land from the sea by the formation of sub general trends in expansion of cyanobacterial blooms along sea-level polders (17th and 18th century), accompanied by latitudinal climatic gradients, there is substantial individuality

Fig. 6 e Changes in mean daily spring surface air temperature from March 1 to May 31 since 1951 at Shanghai Meteorological Station, Meteorological Bureau of China, changes in mean daily surface water temperature from March 1 to May 31 in Lake Taihu since 1995, and changes in annual mean surface chlorophyll a concentrations over a similar time frame (lake monitoring data were first systematically collected in 1995 and are from Qin et al., 2010). Lake Taihu is located approximately 100 km west of Shanghai, China. 1358 water research 46 (2012) 1349e1363

in susceptibility among aquatic ecosystems due to differences in hydrography and geomorphology, hydraulic residence time, 9. Conclusions variable nutrient inputs and grazing pressures and seasonal and inter-annual rainfall. Therefore, there is good reason to Recent research and models, laboratory studies and field examine susceptibility and needed management actions on observations show that the combination of anthropogenic a system-specific basis. nutrient loading, rising temperatures, enhanced vertical stratification, and increased atmospheric CO2 supplies will favor cyanobacterial dominance in a wide range of aquatic 8. Future research and management ecosystems (Fig. 3). Cyanobacteria have efficient CO2 and ramifications and needs nutrient uptake mechanisms, are well protected from light and UV radiation, and are highly adaptable, allowing them to take Clearly, nutrient reduction strategies aimed at CyanoHAB advantage of changing environmental conditions in aquatic control must take co-occurring climatic changes favoring environments. The expansion of CyanoHABs has serious CyanoHAB dominance into account. Specifically, nutrient consequences for human drinking and irrigation water concentration and loading thresholds below which Cyano- supplies, fisheries and recreational resources. This has rami- HABs can be controlled may need to be revised, because they fications for water management. In addition to nutrient are changing due to the nutrient-climate change interactions reduction, water authorities combating CyanoHABs will have e taking place (Paerl et al., 2011a,b; Kosten et al., 2011). Critical to accommodate the hydrological and physical chemical nutrient loads above which CyanoHAB dominance is effects of climatic change in their management strategies, promoted under favorable hydrologic (reduced flushing and keeping in mind regional climatic and anthropogenically- increased residence time) and temperature (increases) driven changes taking place. In all likelihood, quantitative conditions may need to be revised downward in order to “fine tuning” of management strategies will need to be system- compensate for more favorable growth and competition (with specific. A key general control we can exert to reduce the rate eukaryotes) conditions. In all likelihood, these nutrient and extent of global warming however is curbing greenhouse loading adjustments will be system-specific, because nutrient gas emissions. Without this essential step, it is likely that e loading characteristics are often a unique product of the size, future warming trends and resultant physical chemical population density and development patterns/activities of changes in a broad spectrum of aquatic ecosystems will play watershed/airsheds and the area/morphometry/volume, into the hands of this rapidly expanding group of nuisance hydrologic residence time, vertical mixing and optical prop- species. erties of receiving waterways. Superimposed on this will be changes in seasonal temperature, irradiance, precipitation and wind conditions. Acknowledgments An additional set of factors that were not addressed in this article, but will need to be factored into determining and We thank A. Joyner, N. Hall and T. Otten for technical assis- predicting changes in ecosystem-level sensitivity to Cyano- tance and J. Huisman, J. Dyble Bressie, and A. Wilson for HAB invasion, magnitudes and persistence, are changes in helpful discussions. This work was supported by the National “top down” consumption (zooplankton and benthic grazing). Science Foundation (OCE 07269989, 0812913, 0825466, and These changes could at least in part be driven by climatic CBET 0826819), the U.S. Dept. of Agriculture NRI Project 00- changes, including impacts of temperature regimes on grazer 35101-9981, U.S. EPA-STAR project R82867701, NOAA/EPA- community structure and activity, as well as human activities, ECOHAB Project NA05NOS4781194, and North Carolina Sea including habitat disturbances and alterations, introductions Grant Program R/MER-47. 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