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Climate change: Links to global expansion of harmful
cyanobacteria
Hans W. Paerl a,*, Valerie J. Paul b,1
a
b
Institute of Marine Sciences, University of North Carolina at Chapel Hill, 3431 Arendell Street, Morehead City, NC 28557, USA
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
Eutrophication
a formidable challenge to water quality, water supply and fisheries managers, because
Climate change
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
Cyanobacteria (blue-green algae) are the Earth’s oldest
known oxygen-producing organisms, with fossil remains
dating back w3.5 billion years (Schopf, 2000). Cyanobacterial
proliferation during the Precambrian period is largely
responsible for the modern-day, oxygen-enriched atmosphere, and subsequent evolution of higher plant and animal
life (Schopf, 2000; Whitton and Potts, 2000). This long evolutionary history has served cyanobacteria well, for it has
enabled them to develop diverse and highly effective
ecophysiological adaptations and strategies for ensuring
survival and dominance in aquatic environments undergoing
natural and human-induced environmental change (Hallock,
2005; Huisman et al., 2005; Paerl and Fulton, 2006; Paul, 2008).
Today, they enjoy a remarkably broad geographic distribution, ranging from polar to tropical regions in northern and
southern hemispheres, where they are capable of dominating planktonic and benthic primary production in diverse
habitats.
* 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
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As a “microalgal” group, the cyanobacteria exhibit highly
efficient nutrient (N, P, Fe and trace metal) uptake and storage
capabilities, and they are the only oxygenic phototrophs
capable of utilizing atmospheric dinitrogen (N2) as a nitrogen
source to support growth via N2 fixation (Fogg, 1969; Gallon,
1992). Furthermore, many planktonic genera are capable of
rapid vertical migration by altering their buoyancy, allowing
them to exploit deeper, nutrient-rich waters while also taking
advantage of radiant-rich conditions near the surface (Ibelings
et al., 1991; Walsby et al., 1997; Reynolds, 2006). Lastly, some
genera have formed symbioses (as endosymbionts) in diatoms, sponges, corals, lichens, ferns, and mutualistic associations with a variety of other organisms which provide
protection and enhance nutrient cycling and availability in
nutrient-deplete waters (Paerl and Pinckney, 1996; Carpenter,
2002; Rai et al., 2002).
Over the past several centuries, human nutrient overenrichment (particularly nitrogen and phosphorus) associated with urban, agricultural and industrial development, has
promoted accelerated rates of primary production, or eutrophication. Eutrophication favors periodic proliferation and
dominance of harmful blooms of cyanobacteria (CyanoHABs),
both in planktonic (Fogg, 1969; Steinberg and Hartmann, 1988;
Huisman et al., 2005; Paerl and Fulton, 2006) and benthic
(Baker et al., 2001; Dasey et al., 2005; Wood et al., 2006;
Izaguirre et al., 2007; Elmetri and Bell, 2004; Albert et al.,
2005; Ahern et al., 2007; Paerl et al., 2008) environments.
In freshwater ecosystems, P availability has traditionally
been viewed as a key factor limiting CyanoHAB proliferation
(Schindler, 1975; Schindler et al., 2008), and excess P (relative
to N) loading has been identified as favoring CyanoHABs
(Smith, 1983; Watson et al., 1997; Downing et al., 2001). The
emphasis on P controls is based on the N2 fixing capabilities of
some CyanoHAB genera, which help satisfy cellular Nrequirements under P-limited conditions (Paerl and Fulton,
2006). However, at the ecosystem level, only a fraction,
usually far less than 50%, of primary and secondary production demands are met by N2 fixation, even when P supplies are
sufficient (Howarth et al., 1988; Lewis and Wurtsbaugh, 2008;
Paerl and Scott, 2010). Hence, N2 fixation appears to be
controlled by factors in addition to P availability. Nutrient
loading dynamics have changed substantially over the past
several decades. While P reductions have been actively
pursued, human population growth in watersheds has been
paralleled by increased N loading, often at higher rates than P
(Vitousek et al., 1997; Paerl and Scott, 2010). Excessive N loads
are now as large a concern as P loads as stimulants of freshwater, estuarine and marine eutrophication and harmful algal
(including cyanobacterial) blooms (Conley et al., 2009; Paerl,
2009; Ahn et al., 2011).
Mass development of CyanoHABs, increases turbidity and
hence restricts light penetration in affected ecosystems (Figs.
1 and 2). This, in turn, suppresses the establishment and
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).
w a t e r r e s e a r c h 4 6 ( 2 0 1 2 ) 1 3 4 9 e1 3 6 3
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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
Trichodesmium 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 habitat for benthic
flora and fauna (Jeppesen et al., 2007; Scheffer et al., 1997,
Scheffer, 2004). CyanoHABs also cause nighttime oxygen
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
and Johnstone, 2006; Paerl and Fulton, 2006). Persistence of
CyanoHABs can lead to long-term loss of benthic habitat (c.f.,
Karlson et al., 2002). Lastly, numerous planktonic and benthic
cyanobacterial bloom genera produce toxic peptides and
alkaloids (Berry et al., 2008; Humpage, 2008; Liu and Rein,
2010). Ingestion of these cyanotoxins has been linked to
liver, digestive and skin diseases, neurological impairment
and even death (Chorus and Bartram, 1999; Carmichael, 2001;
Humpage, 2008). Hence, toxic CyanoHABs are a major threat
to the use of freshwater ecosystems and reservoirs for
drinking water, irrigation, and freshwater and marine fishing
and recreational purposes (Chorus and Bartram, 1999;
Carmichael, 2001; Osborne et al., 2001, 2007).
Widely-distributed toxin-producing CyanoHABs include
the planktonic N2 fixing genera Anabaena, Aphanizomenon,
Cylindrospermopsis, Nodularia, the non-N2 fixing genera
Microcystis and Planktothrix, and the benthic N2 fixing genera
Lyngbya, Hormothamnion and (some species of) Oscillatoria, and
non-N2 fixing genera Phormidium, Symploca, and Oscillatoria.
2.
Influence of a changing climate on
CyanoHAB proliferation
While the connection between eutrophication and CyanoHABs expansion is well-established (Fogg, 1969; Paerl, 1988;
Reynolds, 2006; Paerl and Fulton, 2006), climatic changes
have also been implicated (Briand et al., 2004; Elliott et al.,
2005, 2006; Paerl and Huisman, 2008; Paul, 2008; Paerl et al.,
2011a,b). In particular, global warming and associated hydrologic changes, both of which are well-documented (IPCC,
2007), strongly affect the physicalechemical environment
and biological processes, most notably metabolism, growth
rates and bloom formation (Fig. 3).
Warming can selectively promote cyanobacterial growth
because as prokaryotes, their growth rates are optimized at
relatively high temperatures (Robarts and Zohary, 1987;
Butterwick et al., 2005; Watkinson et al., 2005). This provides
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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, water column transparency, mixing conditions, water residence times, temperature
and grazing are shown.
CyanoHABs a distinct advantage under nutrient-enriched
conditions, when competition with eukaryotic primary
producers, including diatoms, chlorophytes, cryptophytes and
dinoflagellates can be intense (Paerl et al., 2011a,b). Fig. 4 shows
that as growth rates of these eukaryotic taxa level off or decline,
cyanobacterial growth rates reach their optima and continue to
remain high, even when temperatures exceed 25 C.
Warming of surface waters intensifies vertical stratification
in both freshwater and marine systems. Seasonal warming
Fig. 4 e Effects of temperature on species-specific growth
rates of a representative CyanoHAB species (Microcystis
aeruginosa) vs. commonly encountered eukaryotic algal
bloom species, including the chlorophyte Golenkinia
radiata, the diatom Skeletonema costatum, and the
dinoflagellate Prorocentrum minimum. Growth rate data are
from Reynolds (2006), Grzebyk and Berland (1995), and
Yamamoto and Nakahara (2005).
also lengthens the period of stratification. In freshwater
systems, stratification tends to take place earlier in spring, the
stratification is maintained throughout summer, and destratification is postponed to later in autumn (De Stasio et al., 1996;
Peeters et al., 2007; Elliott et al., 2005; Elliott, 2010). Many CyanoHAB species are able to uniquely exploit stratified conditions. Most bloom-forming cyanobacteria contain gas vesicles
which provide buoyancy (Walsby et al., 1997), enabling them to
form dense surface blooms in stratified waters (Figs. 1 and 2),
where they can take advantage of high levels of irradiance to
optimize photosynthesis (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 IJsselmeer, Netherlands, were higher than the surrounding surface
waters. This represents a positive feedback mechanism,
whereby buoyant cyanobacteria enhance surface temperatures, which promotes their competitive dominance over
eukaryotic phytoplankton.
Surface-dwelling CyanoHAB taxa contain photoprotective
accessory pigments (e.g. carotenoids) and UV-absorbing
compounds (mycosporine-like amino acids (MAAs), scytonemin) that ensure long-term survival under extremely high
irradiance conditions (Paerl et al., 1983; Castenholz and GarciaPichel, 2000; Paul, 2008; Carreto and Carignan, 2011), while
suppressing non-buoyant species through competition for light.
Other mechanisms surface-dwelling cyanobacteria have
for dealing with UV stress include production of antioxidant
enzymes, such as superoxide dismutase, catalase, and glutathione peroxidase, and antioxidant molecules, including
w a t e r r e s e a r c h 4 6 ( 2 0 1 2 ) 1 3 4 9 e1 3 6 3
ascorbate, carotenoids, and tocopherols (Paerl et al., 1985; He
and Häder, 2002; Xue et al., 2005). Cyanobacteria have been
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,
induction of UVR (100e400 nm) resistant proteins and lipids,
and upregulation of peptides and proteins (Castenholz and
Garcia-Pichel, 2000). Carotenoids can help protect cyanobacterial surface blooms from UVR (Paerl et al., 1983). The
beneficial effects of carotenoids may be indirect since they do
not optimally absorb UVR, and they may primarily serve as
antioxidants and inhibitors of free radical reactions
(Castenholz and Garcia-Pichel, 2000). Planktonic cyanobacteria and motile species that occur in microbial mats can
migrate vertically in the water column or within benthic mats
to move away from UVR. Increasing temperatures, stronger
stratification and longer bloom-susceptible periods will affect
both the composition and successional patterns of cyanobacterial and eukaryotic algae in aquatic ecosystems. Longer
bloom periods provide a wider “window” for the establishment and succession of CyanoHABs. For example, it has
recently been shown that competition among toxic vs. nontoxic strains of the often-dominant CyanoHAB Microcystis is
strongly affected by the length of the springesummer period
and light availability needed for supporting various strains
(Kardinaal et al., 2007).
3.
The link to carbon dioxide dynamics
A key driver of global warming is the rising level of the
atmospheric greenhouse gas carbon dioxide (CO2), which is
emitted from accelerating rates of fossil fuel combustion and
biomass burning (IPCC, 2007). In nutrient-enriched freshwater
systems, dense CyanoHAB blooms exhibit high photosynthetic demands for CO2; to the extent that ambient waters
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;
Ibelings and Maberly, 1998; Huisman et al., 2005). When this
occurs, buoyant CyanoHABs have a distinct advantage over
sub-surface phytoplankton populations, since surfacedwelling taxa can directly intercept CO2 from the atmosphere, thereby minimizing dissolved inorganic carbon (DIC)
limitation of photosynthetic growth and taking advantage of
rising atmospheric CO2 levels (Paerl and Ustach, 1982). Rising
levels of atmospheric CO2 may lead to acidification of both
freshwater and marine surface waters, a subject of current
research (Doney, 2006; Keller, 2009). However, in CyanoHABimpacted eutrophic systems, this effect is likely to be negated
by the increased bloom activity, which enhances CO2
consumption and elevates pH levels. In addition, some nonsurface dwelling CyanoHABs are capable of sustained
growth under the high pH conditions resulting from active
photosynthesis and CO2 withdrawal during blooms, by being
able to directly use bicarbonate (HCO3) as a DIC source
(Shapiro, 1990; Kaplan et al., 1991; Badger and Price, 2003).
Elevated CO2 was shown experimentally to enhance growth,
C:N ratios and N2 fixation in the open ocean bloom-forming
cyanobacterium Trichodesmium erythraeum (Levitan et al.,
1353
2007) and may similarly affect other N2 fixing planktonic and
benthic cyanobacteria.
4.
Hydrologic changes associated with
climatic change
Global warming and associated changes in climatic oscillations affect patterns, intensities and duration of precipitation
and droughts, with ramifications for CyanoHAB dominance.
For example, larger and more intense precipitation events
mobilize nutrients on land and increase nutrient enrichment
of receiving waters (Paerl et al., 2006; King et al., 2007).
Freshwater discharge to downstream waters would also
increase, which in the short-term may prevent blooms by
flushing. However, as the discharge subsides and water residence time increases, its nutrient load will be captured and
cycled by receiving water bodies, eventually promoting bloom
potentials. This scenario will most likely occur if elevated
winterespring rainfall and flushing events are followed by
protracted periods of drought. Examples include the Swan
River and its estuary in Australia, Hartbeespoort dam reservoir, South Africa, the Neuse River Estuary, North Carolina,
and the Potomac Estuary, Maryland, USA (Sellner et al., 1988;
Robson and Hamilton, 2003; Huisman et al., 2005; Paerl,
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
Taihu and other large lakes in China, Lake Erie, US Great
Lakes, Lake Victoria and Lake George, Africa) (Huisman et al.,
2005; Qin et al., 2010; Paerl et al., 2011a,b), and regions of the
Baltic Sea (Kahru et al., 1993: Suikkanen et al., 2007). Attempts
to control discharge of rivers and lakes by dams and sluices
may increase the residence time, thereby further aggravating
ecological and health problems associated with CyanoHABs
(Burch et al., 1994; Rahman et al., 2005; Mitrovic et al., 2006).
5.
Salinization
Increasing frequency and severity of droughts is causing more
saline conditions in lake, reservoir, riverine and estuarine
environments worldwide. In addition, rising sea levels, and
ever-increasing demands on freshwater for drinking water
and irrigation purposes have promoted increased levels of
salinity. From a hydrologic perspective, this trend represents
a positive feedback loop, since increased water withdrawal for
human use threatens the freshwater supply because it is
getting saltier as a result of those withdrawals. Many CyanoHAB taxa can counter such extremeness by surviving for long
periods (up to many years) as dormant cysts in sediments,
soils, or desiccated mats in arid regions (Potts, 1994).
Increasing salinity levels also have major impacts on
planktonic and benthic microalgal community structure and
function. One impact of salinization is increased vertical
density stratification, which would benefit buoyant CyanoHABs that can take advantage of such stratification (Visser
et al., 1995; Walsby et al., 2006). In addition, some species of
common CyanoHAB genera such as Anabaena, Anabaenopsis,
Microcystis and Nodularia are quite salt tolerant, sometimes
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more so than counterpart eukaryotic freshwater phytoplankton species (Fig. 5). For instance, the growth rate of toxic
strains of Microcystis aeruginosa remains unaffected by salinities ranging from 0 g L1 up to 10 g L1, or 30% of seawater
salinity (Tonk et al., 2007). Intermittent salinity fluctuations of
up to 15e20 g L1 may still allow survival of Microcystis populations, but cause salt stress, leading to leakage of cells and
excretion of the toxin microcystin (Ross et al., 2006). Likewise,
Anabaena aphanizominoides can withstand salt levels up to
15 g L1, while Anabaenopsis and toxic Nodularia spumigena
even tolerate salinities ranging from 0 g L1 to more than
20 g L1 (Moisander et al., 2002; Tonk et al., 2007) (Fig. 5.
Laboratory experiments indicate that the nodularin content of
Nodularia correlates positively with salinity (Mazur-Marzec
et al., 2005). The high salt tolerance of these CyanoHABs is
reflected by increasing reports of blooms in brackish waters,
for example in the Baltic Sea (Northern Europe), Caspian Sea
(west Asia), Patos Lagoon Estuary (Brazil), the Oued Mellah
reservoir (Morocco), the Swan River Estuary (Australia), San
Francisco Bay (California, USA), Lake Ponchartrain (Louisiana,
USA), and the Kucukcekmece Lagoon (Turkey) (Paerl and
Huisman, 2009; Akcaalan et al., 2009). The increased expansion of CyanoHABs into brackish and full-salinity waters
potentially exposes other aquatic organisms and human users
(recreational, fishing) of these waters to elevated concentrations of cyanobacterial toxins.
6.
Grazer interactions
Cyanobacteria are generally considered to be relatively low
preference foods for marine herbivores because of chemical
and structural defenses and poor nutritional quality; however,
there is considerable variability in the ability of different
Fig. 5 e 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).
w a t e r r e s e a r c h 4 6 ( 2 0 1 2 ) 1 3 4 9 e1 3 6 3
grazers to consume and grow on cyanobacteria (Paerl et al.,
2001; Paul et al., 2001; Landsberg, 2002; Sarnelle and Wilson,
2005; Camacho and Thacker, 2006; Berry et al., 2008; Wilson
et al., 2006; Tillmanns et al., 2008). There is evidence that the
natural products from cyanobacteria, which are mainly lipopeptides, peptides, depsipeptides and alkaloids, can serve as
chemical defenses or may be toxic to grazers and competitors
(Christoffersen, 1996; Paul et al. 2001, 2007; Landsberg, 2002;
Berry et al., 2008). The chemical defenses of cyanobacteria
may play a critical role in bloom formation and persistence by
limiting the grazing activity of some potential consumers.
Hallock (2005) suggested that benthic marine cyanobacteria, which are resistant to strong solar radiation, warm
temperatures, abundant nutrients, and many generalist
grazers, may be useful indicators of stress conditions in reef
ecosystems. Benthic cyanobacteria can be early colonizers of
dead coral and disturbed substrates and are becoming
increasingly well-established on coral reefs. Tsuda and Kami
(1973) observed that low light penetration and selective
browsing by herbivorous fishes on macroalgae removed
potential competitors and favored the establishment of
unpalatable benthic cyanobacteria in tropical lagoonal environments. Crude extracts and isolated secondary metabolites
of several benthic marine cyanobacteria such as Lyngbya spp.
have been shown to deter grazing by generalist herbivores such
as fishes and sea urchins (reviewed by Paul et al. 2001, 2007).
In freshwater ecosystems, cyanobacterial blooms can have
negative effects on large cladocerans such as Daphnia spp.,
which may be more susceptible to cyanobacterial toxins than
some other grazers (Tillmanns et al., 2008). Negative physiological effects (DeMott et al., 1991; Rohrlack et al., 2001, 2005 )
and negative fitness consequences (Gustafsson et al., 2005) on
zooplankton grazers such as Daphnia spp. have been observed;
however, the physiological susceptibilities of different populations of zooplankton can vary considerably. Some populations of Daphnia galeata and Daphnia pulicaria exposed to
chronically high abundance of cyanobacteria can adapt to
being more tolerant of cyanobacteria in their diets (Hairston
et al., 1999, 2001; Sarnelle and Wilson, 2005). Cyanobacteria
and cyanotoxins can also inhibit feeding by other grazers,
such as copepods and rotifers, in fresh and estuarine waters
(Sellner et al., 1993; Paerl et al., 2001; Reinikainen et al., 2002).
Grazer interactions with cyanobacteria are highly speciesspecific; considerable intra- and interspecific variation in the
effects of cyanobacteria and cyanobacterial toxins on
consumers have been observed in experimental studies
(Wilson and Hay, 2007; Tillmanns et al., 2008).
Additional complexity in zooplanktonecyanobacterial
interactions can be observed when higher trophic levels, such
as fishes that are zooplankton grazers, are included in
observational and experimental studies. Zooplankton species
that can control cyanobacteria, such as Daphnia spp.
(Sarnelle, 1993; Tillmanns et al., 2008), are often the preferred
food of planktivorous fishes in freshwater systems. Studies
manipulating fish abundance often demonstrate a typical
trophic cascade where zooplanktivorous fishes reduce the
abundance of zooplankton and increase the biomass of
phytoplankton (Brett and Goldman, 1997; Vanni et al., 1997;
Carpenter et al., 2001). Fish and zooplankton abundance
also directly and indirectly affect nutrient dynamics in these
1355
lakes (Sarnelle, 1993; Vanni et al., 1997). Both consumers and
nutrient availability can have pronounced effects on food
webs, including phytoplankton biomass and community
structure (Brett and Goldman, 1997). These complex factors
coupled with climatic variation can drive successional
patterns, phytoplankton and zooplankton dynamics in lake
ecosystems (Blenckner et al., 2007).
Little is known about how temperature and other abiotic
factors may play a role in specific trophic interactions.
Temperature, light, and nutrients may have interactive effects
on cyanobacterial growth and toxin production, with consequent effects on aquatic food webs. One laboratory study
showed that increases in water temperature could increase
the susceptibility of rotifers to toxic effects of anatoxina produced by Anabaena flos-aquae (Gilbert, 1996). Two planktonic rotifers were acclimated for many generations to low
(12e14 C), intermediate (19 C), and high (25 C) water
temperatures, and reproductive rates of the rotifers were
inhibited by the cyanobacterium and anatoxin-a. The negative
effects of the cyanobacterium and the toxin increased with
increasing temperature.
Studies have also shown correlations between climate
variation, often related to the North Atlantic Oscillation (NAO),
and spring plankton dynamics and clear water phases in
shallow, polymictic European lakes (Gerten and Adrian, 2000;
Scheffer et al., 2001; Abrantes et al., 2006; Blenckner et al.,
2007). Clear water phases, caused by grazing of zooplankton
on microalgae, were studied in 71 shallow Dutch lakes and
were found to occur earlier when water temperatures were
higher (Scheffer et al., 2001, Scheffer, 2004). Water temperatures were strongly related to the North Atlantic Oscillation
(NAO) winter index. A simulation model of algaeezooplankton
dynamics seemed to confirm the primary role of temperature
in determining the probability and timing of the clear water
phase. In a 42-year study of the small subalpine Castle Lake in
northern California, increasing water temperatures were
accompanied by increasing mean summer cyanobacteria biovolume, whereas diatoms and other phytoplankton groups did
not show significant trends with summer water temperatures
(Park et al., 2004). Summer water temperature also had
a significant positive correlation with biomass of Daphnia rosea,
a relationship also reported for European lakes where warm
winter air temperatures caused by the NAO enhanced spring
Daphnia biomass and influenced the timing of the clear water
phase (Straile and Adrian, 2000; Blenckner et al., 2007).
7.
Evidence from aquatic ecosystems
undergoing climatically-induced ecological
change
Evidence from geographically-diverse aquatic ecosystems
varying in size, morphology, salinity and hydrologic conditions, indicates that climatic change can act synergistically
with anthropogenic nutrient enrichment to promote global
expansion of CyanoHABs.
Kosten et al. (2011) conducted a survey of 143 lakes of
varying trophic state situated along a latitudinal gradient from
Northern Europe to Southern South America. They found that
the percentage of total phytoplankton biomass attributable to
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cyanobacteria increased markedly with temperature. These
authors also noted that temperature increases may lower the
nutrient input thresholds at which blooms can be initiated
and sustained; that is, at elevated temperatures, bloomforming CyanoHABs can proceed at lower nutrient input rates
and concentrations than when temperatures were relatively
cooler. For example, in Northern Europe (N. Germany,
Sweden, Finland) lakes that exhibit symptoms of long-term
(decadal-scale) warming, including warmer surface water
temperatures, stronger and more persistent vertical stratification, earlier melting of their ice covers and overall extended
warm water conditions and longer growing seasons show
increases in cyanobacterial dominance, bloom frequencies
and persistence (Weyhenmeyer, 2001; Nõges et al., 2003;
Wagner and Adrian, 2009; Feuchtmayr et al., 2009; Elliott,
2010).
These results expand on previous studies confined to lakes
in tropical and subtropical waters that show a tendency
toward domination by cyanobacteria, even when trophic
states varied (Ganf and Horne, 1975; Talling, 1986; Lewis, 1987;
Phlips et al., 1997; Bouvy et al., 2000; Velzeboer et al., 2000;
Komárková and Tavera, 2003; Havens et al., 2003; Abrantes
et al., 2006). Relatively high rates of N2 fixation, a key indicator of cyanobacterial activity and an important biogeochemical process, are observed in tropical freshwater and
marine systems as well (Horne and Viner, 1971; Capone, 1983;
Capone et al., 2005). Overall, these studies show a strong
positive relationship between mean annual temperature and
cyanobacterial dominance, a trend originally observed by
Robarts and Zohary (1987). There are exceptions to this,
including high elevation (although cyanobacteria are common
in some high altitude, low latitude lakes (e.g. Lake Titicaca,
Peru-Bolivia) (Wurtsbaugh et al., 1985), high humic acid
content and resultant acidic conditions (i.e. pH < 6), extremely
oligotrophic (severe nutrient-limited), rapidly flushed (short
residence time), and poorly-stratified (polymictic) conditions
(Vincent, 1987). Interestingly, the proportion of cyanobacteria
in both planktonic and benthic habitats of these systems
increases as nutrient loading increases, which suggests
synergism between elevated temperatures and nutrient
enrichment.
Some of the CyanoHAB taxa typically associated with
warmer water conditions, including the planktonic heterocystous N2 fixer Cylindrospermopsis sp, and the benthic/
planktonic non-heterocystous filamentous genus Lyngbya
spp. (some species are known to fix N2) have expanded into
temperate regions (Stüken et al., 2006; Wiedner et al., 2007).
Cylindrospermopsis was originally described as a tropical and
subtropical species. However, Cylindrospermopsis raciborskii
appeared in Europe during the 1930s, and showed a progressive colonization from Greece and Hungary toward higher
latitudes near the end of the 20th century (Padisák, 1997). It
was first described in France in 1994, in the Netherlands in
1999, and it is now also widespread in lakes in northern
Germany (Stüken et al., 2006). C. raciborskii was first identified
in the United States in 1955, in Wooster Lake, Kansas. C. raciborskii may have arrived in Florida almost 35 years ago, after
which it aggressively proliferated in lake and river systems
throughout central Florida (Chapman and Schelske, 1997).
This CyanoHAB has spread throughout US Southeast and
Midwest reservoirs and lakes, especially those undergoing
eutrophication accompanied by a loss of water clarity
(Chapman and Schelske, 1997). The mechanisms of invasion
and proliferation are under examination. However, it is
known that C. raciborskii, which is typically dispersed
throughout the water column, is adapted to low light conditions encountered in many turbid, eutrophic waters (Padisák,
1997; Stüken et al., 2006). It also prefers water temperature
conditions in excess of 20 C, and survives adverse conditions
using specialized resting cells, akinetes (Briand et al., 2004;
Wiedner et al., 2007).
The filamentous toxin-producing CyanoHAB genus Lyngbya has likewise exhibited remarkable invasive abilities in
a range of aquatic ecosystems, including streams, rivers,
lakes, reservoirs, estuarine and coastal waters. Nutrient
enrichment has been implicated in its expansion (Paerl and
Fulton, 2006). Lyngbya species often form periphytic or
benthic mats, although some species, such as Lyngbya birgei,
are planktonic. Lyngbya outbreaks have been associated with
human health problems. The marine species Lyngbya majuscula is commonly known as “fireweed” or “mermaid’s hair”
(Fig. 2). It is widely associated with contact dermatitis, where
the initial burning symptoms give way to blister formation
and peeling of the skin (Carmichael, 2001). L. majuscula
produces a large suite of bioactive compounds, including the
dermatoxic aplysiatoxins and lyngbyatoxin A (Osborne et al.,
2001), and hundreds of other natural products (Paul et al.,
2007; Liu and Rein, 2010). In freshwater environments, Lyngbya wollei has been associated with the production of paralytic
shellfish poisoning (PSP) toxins (Carmichael, 2001).
Lyngbya blooms are increasingly common in nutrientenriched waters, including those that have experienced
human disturbance such as dredging, inputs of treated
municipal waste, and the discharge of nutrient laden freshwater through coastal canals (Paerl et al., 2006, 2008). Both
Lyngbya majuscula (marine) and Lyngbya wollei (freshwater) are
opportunistic invaders when favorable environmental conditions exist (nutrient over-enrichment, poorly flushed conditions). Following large climatic and hydrologic perturbations
such as hurricanes, L. wollei is an aggressive initial colonizer of
flushed systems (Paerl and Fulton, 2006). Lyngbya blooms can
proliferate as dense floating mats that shade other primary
producers, enabling Lyngbya to dominate the system by
effectively competing for light (Fig. 2). As is the case with
Cylindrospermopsis and Microcystis, this CyanoHAB can take
advantage of both human and climate-induced environmental
change.
Interestingly, expansion of some CyanoHAB genera has
occurred even in some lakes that have experienced no recent
increase in nutrient (N and P) loading, indicating that in
certain cases increasing temperature may play an independent role in promoting geographic expansion of some CyanoHABs (Padisák, 1997; Stüken et al., 2006; Kosten et al., 2011).
Most CyanoHAB-impacted lakes, rivers, estuaries and coastal
waters, however, also have a recent history of increases in
nutrient loading accompanying human population increases
in their water- and airsheds (Huisman et al., 2005; Paerl et al.,
2011a,b). These systems have, in general, shown increases in
cyanobacterial dominance and production. They are also
sensitive to the effects of regional warming. In central Florida
w a t e r r e s e a r c h 4 6 ( 2 0 1 2 ) 1 3 4 9 e1 3 6 3
(USA), numerous lakes have experienced the co-occurring
effect of nutrient over-enrichment and climate change,
including larger oscillations between particularly active storm
periods and extreme droughts, as well as long-term increases
in mean seasonal and annual air temperatures (Phlips et al.,
1997; Havens et al., 2007).
China’s third largest lake, Taihu is situated in Jiangsu
Province, China’s most rapidly-growing economic region
(Fig. 1). Rapid increases in urbanization, agricultural production and industrial output have led to a significant increase in
both N and P loading (Qin et al., 2007; Hai et al., 2010; Paerl
et al., 2011a,b). This trend has led to a phytoplanktonic
“state change”, from a largely diatom-dominated community
in the 1960s and 1970s to what is now a CyanoHAB (Microcystis
spp.) dominated community for much of the year (May
through October) (Chen et al., 2003a,b; Qin et al., 2010).
Increases in N and P loading have continued steadily since the
1960s, reflecting population growth in the Taihu Basin (Qin
et al., 2007, 2010). Regional warming has also taken place, as
shown in records kept by the Chinese Meteorological Bureau
at nearby Shanghai and a recent rise in mean lake water
temperatures (Qin et al., 2010) (Fig. 6). The recent increase in
warming has occurred much faster than nutrient loading (Qin
et al., 2010). Interestingly, bloom intensity or biomass, as
measured by depth-integrated chlorophyll a concentrations,
have also rapidly increased in parallel with air and water
temperature increases (Fig. 6). Qin et al. (2010) concluded that
these trophic changes were attributed to the combined effects
of nutrient over-enrichment and a warming trend.
The shallow lakes of the Netherlands provide a long-term
record of phytoplankton community changes accompanied
by cultural eutrophication and climatic changes. Eutrophic
conditions have been present for several centuries, following
the reclaiming of land from the sea by the formation of sub
sea-level polders (17th and 18th century), accompanied by
1357
agricultural expansion (rowcrop, cattle grazing and dairy
operations), urbanization and industrialization. However,
over the past 100 þ years, this region has also experienced
a rise in mean annual air temperatures. This has caused
surface water warming, an increased potential for water
column stratification and increased frequencies and magnitudes of buoyant, surface-dwelling CyanoHAB genera, especially non-N2 fixing genera such as Microcystis (indicative of N
enrichment). Regional warming further promotes such
blooms (Jöhnk et al., 2008).
Similarly, the Baltic Sea region, which has been impacted
by anthropogenic nutrient enrichment and has exhibited
symptoms of eutrophication for several centuries (Elmgren
and Larsson, 2001), has also shown a recent warming trend,
which has translated into changes in phytoplankton
community composition favoring cyanobacterial dominance
(Suikkanen et al., 2007). Paleolimnological evidence,
including diagnostic pigment analyses of sediments (Bianchi
et al., 2000) has indicated that cyanobacteria formed
a significant fraction of phytoplankton biomass prior to the
20th century. However, the relative dominance and persistence of CyanoHABs may have increased in response to more
favorable climatic conditions, especially warming (Suikkanen
et al., 2007).
In efforts to protect the world’s drinking and irrigation
waters, fisheries and recreational resources represented by
these ecosystems, researchers and water quality/resource
managers are faced with simultaneous, interactive “moving
targets” that represent formidable challenges, including
effects of 1) nutrient over-enrichment, 2) temperature
increases, including changes in thermal stratification and 3)
changes in freshwater discharge, flow (flushing) regimes and
water residence time. Despite the diverse findings showing
general trends in expansion of cyanobacterial blooms along
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
w a t e r r e s e a r c h 4 6 ( 2 0 1 2 ) 1 3 4 9 e1 3 6 3
in susceptibility among aquatic ecosystems due to differences
in hydrography and geomorphology, hydraulic residence time,
variable nutrient inputs and grazing pressures and seasonal
and inter-annual rainfall. Therefore, there is good reason to
examine susceptibility and needed management actions on
a system-specific basis.
8.
Future research and management
ramifications and needs
Clearly, nutrient reduction strategies aimed at CyanoHAB
control must take co-occurring climatic changes favoring
CyanoHAB dominance into account. Specifically, nutrient
concentration and loading thresholds below which CyanoHABs can be controlled may need to be revised, because they
are changing due to the nutrient-climate change interactions
taking place (Paerl et al., 2011a,b; Kosten et al., 2011). Critical
nutrient loads above which CyanoHAB dominance is
promoted under favorable hydrologic (reduced flushing and
increased residence time) and temperature (increases)
conditions may need to be revised downward in order to
compensate for more favorable growth and competition (with
eukaryotes) conditions. In all likelihood, these nutrient
loading adjustments will be system-specific, because nutrient
loading characteristics are often a unique product of the size,
population density and development patterns/activities of
watershed/airsheds and the area/morphometry/volume,
hydrologic residence time, vertical mixing and optical properties of receiving waterways. Superimposed on this will be
changes in seasonal temperature, irradiance, precipitation
and wind conditions.
An additional set of factors that were not addressed in this
article, but will need to be factored into determining and
predicting changes in ecosystem-level sensitivity to CyanoHAB invasion, magnitudes and persistence, are changes in
“top down” consumption (zooplankton and benthic grazing).
These changes could at least in part be driven by climatic
changes, including impacts of temperature regimes on grazer
community structure and activity, as well as human activities,
including habitat disturbances and alterations, introductions
of exotic species, fishing pressure, and the construction of
barriers such as dams, locks, and submerged structures (piers,
jetties, artificial reefs, etc.).
The interactive nature of these complex and often nonlinear alterations in physical, chemical and biotic drivers/
perturbations of aquatic ecosystem function will require new
quantitative approaches to detecting, quantifying, synthesizing and modeling impacts and effects. Furthermore, the
synthesis and modeling product will help managers and
decision makers account for and adjust their strategies for
CyanoHAB control in response to future climate change and
human impact scenarios. Lastly, management actions will
need to be system-specific, due to the aforementioned
complex interactions of controlling variables, which vary in
individual water bodies. This is an unenviable but essential
task as we strive to formulate effective, verifiable and
accountable management strategies aimed at controlling
CyanoHABs and protecting our precious water resources well
into the 21st century.
9.
Conclusions
Recent research and models, laboratory studies and field
observations show that the combination of anthropogenic
nutrient loading, rising temperatures, enhanced vertical
stratification, and increased atmospheric CO2 supplies will
favor cyanobacterial dominance in a wide range of aquatic
ecosystems (Fig. 3). Cyanobacteria have efficient CO2 and
nutrient uptake mechanisms, are well protected from light and
UV radiation, and are highly adaptable, allowing them to take
advantage of changing environmental conditions in aquatic
environments. The expansion of CyanoHABs has serious
consequences for human drinking and irrigation water
supplies, fisheries and recreational resources. This has ramifications for water management. In addition to nutrient
reduction, water authorities combating CyanoHABs will have
to accommodate the hydrological and physicalechemical
effects of climatic change in their management strategies,
keeping in mind regional climatic and anthropogenicallydriven changes taking place. In all likelihood, quantitative
“fine tuning” of management strategies will need to be systemspecific. A key general control we can exert to reduce the rate
and extent of global warming however is curbing greenhouse
gas emissions. Without this essential step, it is likely that
future warming trends and resultant physicalechemical
changes in a broad spectrum of aquatic ecosystems will play
into the hands of this rapidly expanding group of nuisance
species.
Acknowledgments
We thank A. Joyner, N. Hall and T. Otten for technical assistance and J. Huisman, J. Dyble Bressie, and A. Wilson for
helpful discussions. This work was supported by the National
Science Foundation (OCE 07269989, 0812913, 0825466, and
CBET 0826819), the U.S. Dept. of Agriculture NRI Project 0035101-9981, U.S. EPA-STAR project R82867701, NOAA/EPAECOHAB Project NA05NOS4781194, and North Carolina Sea
Grant Program R/MER-47. This is contribution #853 of the
Smithsonian Marine Station at Fort Pierce.
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