Download harmful algal blooms, coastal eutrophication and climate

Biol. Mar. Mediterr. (2008), 15 (1): 6-15
G.M. Hallegraeff
School of Plant Science, University of Tasmania, Private Bag 55, Hobart, Tasmania, Australia.
[email protected]
HARMFUL ALGAL BLOOMS,
COASTAL EUTROPHICATION AND CLIMATE CHANGE
FIORITURE DI ALGHE POTENZIALMENTE TOSSICHE,
EUTROFIZZAZIONE COSTIERA E CAMBIAMENTI CLIMATICI
Abstract - Algal bloom phenomena range from harmless water discolorations (“red tides”), to species
that cause disastrous mortalities of finfish in intensive aquaculture operations, and most seriously species
that produce potent neurotoxins which in extreme cases can kill human consumers of seafood products
(causative organisms of various Shellfish Poisoning and Fish Poisoning syndromes). Since many algal
blooms are more or less monospecific, correctly assessing the precise taxonomic identity of the causative
organisms is crucial in deciding whether knowledge on toxicology, physiology and ecology from similar
blooms in other parts of the world can be applied to the local conditions. Molecular approaches (notably
sequencing of the large subunit rRNA) have been indispensable in redefining HAB species, or detecting and
monitoring previously cryptic taxa. Evidence for an alarming global increase in the past two decades in the
frequency, intensity and geographic distribution of HAB phenomena has been brought to the attention of
numerous international forums such as UNESCO, FAO and WHO and has been partly explained on the
basis of increased public awareness and increased utilisation of coastal waters for aquaculture. However,
ship ballast water discharges, coastal eutrophication, and also climate change are increasingly contributing
to the impacts of algal blooms on fisheries, aquaculture, human health, tourism, the marine environment
and thereby regional economies. Examples from the Mediterranean are discussed.
Key-words: climate change, HABs, ballast water, eutrophication.
Introduction - Harmful algal blooms (HABs) in a strict sense are completely
natural phenomena which have occurred throughout recorded history. Even non-toxic
algal blooms can have devastating impacts, however, when they lead to indiscriminate
kills of fish and invertebrates by generating anoxic conditions in sheltered bays (as
occurred off the Emilia-Romagna coast in September 1984; Vollenweider et al.,
1992). Other algal species, even though non-toxic to humans, can produce exudates
that can cause damage to the delicate gill tissues of fish (raphidophytes Chattonella,
Heterosigma, dinoflagellates Karenia, Karlodinium, haptophyte Prymnesium). Whereas
wild fish stocks are free to swim away from problem areas, caged fish in intensive
aquaculture operations are trapped and thus can suffer devastating mortalities. Of
greatest concern to human society are algal species that produce potent neurotoxins
that can find their way through shellfish and fish to human consumers where they
evoke a variety of gastrointestinal and neurological illnesses. One of the first recorded
fatal cases of food poisoning after eating contaminated shellfish happened in 1793,
when English surveyor Captain George Vancouver and his crew landed in British
Columbia (Canada) in an area now known as Poison Cove. He noted that, for local
Indian tribes, it was taboo to eat shellfish when the seawater became bioluminescent
due to algal blooms by the local dinoflagellate Alexandrium catenella/ tamarense, which
we now know to be a producer of Paralytic Shellfish Poisons (PSP). The increase in
shellfish farming worldwide is leading to more reports of Paralytic, Diarrhetic (first
documented in 1976 in Japan), Neurotoxic (reported from the Gulf of Mexico as
early as 1844) or Amnesic Shellfish Poisoning (first identified in 1987 in Canada). The
English explorer Captain James Cook already suffered from the tropical illness of
Ciguatera Fishfood Poisoning when visiting New Caledonia in 1774. Worldwide, close
to 2000 cases of food poisoning from consumption of contaminated fish or shellfish
are reported each year. Some 15% of these cases will prove fatal. If not controlled,
the economic damage through the slump in local consumption and exports of seafood
Harmful Algal Blooms, Coastal Eutrophication and Climate Change
7
products can be considerable. Whales and porpoises can also become victims when
they receive toxins through the food chain via contaminated zooplankton or fish.
Poisoning of manatees in Florida via contaminated sea grasses and of pelicans and sea
lions via contaminated anchovies have also been reported (Hallegraeff et al., 2003).
In the past three decades, harmful algal blooms seem to have become more frequent,
more intense and more widespread. Four explanations for this apparent increase in algal
blooms have been proposed: a greater scientific awareness of toxic species; the growing
utilization of coastal waters for aquaculture; the stimulation of plankton blooms by
domestic, industrial and agricultural wastes and/or unusual climate conditions; and the
transportation of algal cysts either in ships’ ballast water or associated with moving
shellfish stocks from one area to another (Hallegraeff, 1993).
Increase of algal blooms by cultural eutrophication - While some organisms such
as the dinoflagellates Karenia brevis, Alexandrium, Dinophysis and Pyrodinium appear
to be unaffected by coastal nutrient enrichments, many other algal bloom species
appear to be stimulated by “cultural eutrophication” from domestic, industrial and
agricultural wastes. Fig. 1 illustrates an 8-fold increase in the number of red tides per
year in Hong Kong Harbour in the period 1976 to 1986 (Lam and Ho, 1989). This
increase (mainly Karenia mikimotoi, Gonyaulax polygramma, Noctiluca scintillans and
Prorocentrum minimum) shows a striking relationship with the 6-fold increase in human
population in Hong Kong and the concurrent 2.5–fold increase in nutrient loading,
mainly contributed by untreated domestic and industrial waste. Red tide events in
Hong Kong harbour were less frequent in 1989-97 until the major bloom year of 1998.
Fig. 1 - Correlation between the number of red-tide outbreaks per year in Tolo Harbour (continuous line) and the increase of human population in Hong Kong (bar diagram), in the
period 1976 to 1986 (from Lam and Ho, 1989).
Correlazione fra il numero di episodi di red-tide/anno registrati a Tolo Harbour (linea continua) e
l’aumento della popolazione umana a Hong Kong (diagramma a barre), nel periodo dal 1976 al 1986
(da Lam e Ho, 1989).
Fig. 2 - Long-term trend in the frequency of red-tide outbreaks in the Seto Inland Sea, Japan, in the
period 1965–1986 (from Okaichi, 1990).
Tendenza a lungo termine della frequenza di episodi di red-tide in Seto Inland Sea, Giappone, nel
periodo 1965-1986 (da Okaichi, 1990).
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G.M. Hallegraeff
A similar experience was noted in the Seto Inland Sea, one of the major fish
farm areas in Japan (Okaichi, 1989) (Fig. 2). Between 1965 and 1976 the number of
confirmed red tide outbreaks (mainly Chattonella antiqua, since 1964; and Karenia
mikimotoi, since 1965) progressively increased 7-fold, concurrent with a 2-fold increase
in the COD (chemical oxygen demand) loading, mainly from untreated sewage and
industrial waste from pulp and paper factories. During the most severe outbreak in
1972, a Chattonella red tide killed 14 million cultured yellow-tail fish. Effluent controls
were then initiated to reduce the chemical oxygen demand loading by about half,
to introduce secondary sewage treatment, and to remove phosphate from house-hold
detergents (as happened with the replacement of polyphosphate in detergents in Italy).
Following a time-lag of 4 years, the frequency of red tide events in the Seto Inland
Sea then decreased by about 2-fold to a more stationary level.
Fig. 3 - Long-term trend in the phosphate, nitrate and ammonia loading of the River Rhine (top)
and concurrent changes in the N:P and Si:P nutrient ratios (bottom) (from Smayda 1990,
using data by Van Bennekom & Salomons, 1981).
Tendenza a lungo termine del carico di fosfati, nitrati e ammoniaca del fiume Reno (in alto) e dei conseguenti cambiamenti nel rapporto dei nutrienti N:P e Si:P (in basso) (da Smayda 1990, utilizzando i
dati di Van Bennekom & Salomons, 1981). A similar pattern of a long-term increase in nutrient loading of coastal waters is
evident for the North Sea in Europe (Smayda, 1990) (Fig. 3). Since 1955 the phosphate
Harmful Algal Blooms, Coastal Eutrophication and Climate Change
9
loading of the River Rhine has increased 7.5-fold, while nitrate levels have increased
3-fold. This has resulted in a significant 6-fold decline in the Si:P ratio, because longterm reactive silicate concentrations (a nutrient derived from natural land weathering)
have remained constant. More recently, improved wastewater treatment has been
causing increases in the ammonia:nitrate ratio of River Rhine discharge (Riegman
et al., 1992). The nutrient composition of treated wastewater is never the same as
that of the coastal waters in which it is being discharged. Furthermore, atmospheric
deposition of N needs also be included in budgets of anthropogenic nutrient input.
There is considerable concern (Officer and Ryther, 1980; Ryther and Dunstan, 1971;
Smayda, 1990) that such altered nutrient ratios in coastal waters may favour blooms
of nuisance flagellate species which replace the normal spring and autumn blooms of
siliceous diatoms. The remarkable increase of foam-producing blooms of the haptophyte
Phaeocystis pouchetii, which first appeared in Dutch coastal waters in 1978, is probably
the best-studied example of this phenomenon (Lancelot et al., 1987). The comparable
“Mare Sporco” mucus phenomenon in the Adriatic Sea, even though reported as
early as 1729, undoubtedly reflects a highly eutrophic ecosystem driven by nutrients
from the River Po catchment (Stachowitsch et al., 1990, Vollenweider et al., 1992).
The 1988 bloom in the Kattegat of the haptophyte Chrysochromulina polylepis, not
unusual in terms of biomass but unusual in terms of its species composition and toxicity,
has been related to a change in the nutrient-status from nitrogen- to phosphoruslimitation (Maestrini and Graneli, 1991). As in Hong Kong and Japan, several North
European countries have now agreed to reduce phosphate and nitrate discharges by 50%
in the next several years, but their efforts will almost certainly be in vain if neighbours
continue polluting. Furthermore, such indiscriminate reductions in nutrient discharges
are not addressing the problem of changing nutrient ratios of coastal waters. Changed
patterns of land use, such as deforestation, can also cause shifts in phytoplankton
species composition by increasing the concentrations of humic substances in land
run-off. Experimental evidence from Sweden indicates that river water draining from
agricultural soils (rich in N and P) stimulates diatom blooms but that river water draining
from forest areas (rich in humic and fulvic acids) can stimulate dinoflagellate blooms
of species such as Prorocentrum minimum (Graneli and Moreira, 1990). Agricultural
run-off of phosphorus can also stimulate cyanobacterial blooms, for example of
Nodularia spumigena in the Baltic Sea and in the Peel-Harvey Estuary, Australia.
A more complex “cultural eutrophication” scenario has emerged in coastal waters of
New Jersey, New York and Rhode Island, USA, where an unusual “brown tide” by the
chrysophyte picoplankton Aureococcus anophagefferens has been circumstantially linked
to the discharge of chelators (such as citric acid) in detergents and lawn treatments,
together with a suppression of zooplankton grazing by pesticides (Cosper et al., 1991).
This “Ecosystem Disruptive Algal Bloom” (Sunda et al., 2006) was responsible for a
reduction in the extent and biomass of eelgrass beds and caused starvation and recruitment
failure in commercial scallop populations. Overexploitation of top predator fish can
increase populations of small planktivorous fish and jellyfish removing herbivorous
zooplankton thus releasing HAB species from grazing pressure (Fig. 4; Boero et
al., 2008). Eutrophication problems like this cannot be readily diagnosed by routine
monitoring programmes that focus on macronutrients or algal chlorophyll biomass alone.
Stimulation of algal blooms by unusual climatological conditions - The dinoflagellate
Pyrodinium bahamense is presently confined to tropical, mangrove-fringed coastal waters
of the Atlantic and Indo-West Pacific. A survey of cyst fossils (named Polysphaeridium
zoharyii) going back to the warmer Eocene 50 million years ago indicates a much
wider range of distribution in the past. For example, in the Australasian region at
present, the alga is not found farther south than Papua New Guinea but, some 100
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G.M. Hallegraeff
Fig. 4 - Possible pathways for HAB formation when the “top-down control” of the food chain is
disrupted as e.g. by overfishing (from Turner & Graneli, 2006). Differential impacts of climate change on zooplankton or fish grazers can produce similar stimulation of HABs.
Possibili percorsi di formazione di HAB quando il controllo “top-down” della catena alimentare è perturbato come ad esempio dalla pesca eccessiva (da Turner & Graneli, 2006). Impatti differenziali di
cambiamenti climatici sugli organismi che si nutrono di zooplancton o pesci possono produrre simili
stimolazioni di Habs.
Fig. 5 - Global distribution of Pyrodinium bahamense in Recent Plankton (top) and much wider
distribution in the fossil cyst record (bottom) (from Hallegraeff, 1993).
Distribuzione globale di Pyrodinium bahamense nel Plancton attuale (in alto) e distribuzione molto più
ampia nel ritrovamento delle cisti fossili (in basso) (da Hallegraeff, 1993).
Harmful Algal Blooms, Coastal Eutrophication and Climate Change
11
000 years ago, the alga ranged as far south as Sydney Harbour (McMinn, 1989).
There is genuine concern that, with an increased greenhouse effect and warming of the
oceans, this species may return to Australian waters (Fig. 5). In the tropical Atlantic,
in areas such as Bahia Fosforescente in Puerto Rico and Oyster Bay in Jamaica, the
glowing red-brown blooms of Pyrodinium are a major tourist attraction.
At first considered harmless, Pyrodinium blooms gained a more sinister reputation
in 1972 in Papua New Guinea after red-brown water discolorations coincided with
the fatal food poisoning of three children in a seaside village, diagnosed as PSP.
Since then, these toxic blooms have apparently spread to Brunei and Sabah (1976),
the central (1983) and northern Philippines (1987) and Indonesia (North Mollucas).
There is strong circumstantial evidence of a coincidence between Pyrodinium blooms
and the El Niño Southern Oscillation (ENSO). Pyrodinium is a serious public health
and economic problem for these tropical countries, all of which depend heavily on
seafood for protein. In the Philippines alone, Pyrodinium has now been responsible
for more than 2000 human illnesses and 100 deaths resulting from the consumption of
contaminated shellfish as well as sardines and anchovies (Hallegraeff & MacLean, 1989).
Fig. 6 - Impacts on the Mediterranean basin due to large and regional scale wind systems and the
Mediterranean Oscillation (MO). Regional wind systems as shown for the central region
(dark arrows) with Italian nomenclature exist under different names in other parts of the
Mediterranean area. From: Workshop on the assessment, assimilation, and validation of data
for Global Change related research in the Mediterranean area. Casablanca, Feb. 21-24, 2001.
Impatti sul bacino del Mediterraneo dovuti a sistemi di vento sia su ampia scala che su scala regionale
e oscillazioni del Mediterraneo (MO). I sistemi di vento regionali, come indicato per la regione centrale
(frecce scure) con nomenclatura italiana, esistono con nomi diversi anche in altre parti del Mediterraneo. Da: Workshop sulla valutazione, l’assimilazione, e la convalida di dati per il Cambiamento Globale
correlato alla ricerca nell’area del Mediterraneo. Casablanca, 21-24 febbraio, 2001.
Until recently, Neurotoxic Shellfish Poisoning (NSP) by the dinoflagellate Karenia
brevis was considered to be endemic to the Gulf of Mexico and the east coast of
Florida, where red tides had been reported as early as 1844. An unusual feature of
NSP is the formation by wave action of toxic aerosols which can lead to respiratory
asthma-like symptoms in humans (somewhat similar to the Ostreopsis ovata associated
aerosols in Liguria in 2005). In 1987, a major Florida bloom was dispersed by the Gulf
Stream northward into North Carolina waters, where it has since persisted (Tester et
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G.M. Hallegraeff
al., 1991). Unexpectedly, in early 1993, more than 180 human Neurotoxic Shellfish
Poisonings were reported from New Zealand. Most likely, this mixed bloom of Karenia
mikimotoi and related species was again triggered by the unusual weather conditions at
the time, including higher than usual rainfall and lower than usual temperature, which
coincided with El Niño (Chang et al., 1998). Predicted global change impacts on wind
patterns in the Mediterranean are summarised in Fig. 6. There are early signs that
some parts of the Mediterranean may become less productive in response to climatedriven increased sea surface temperatures and associated reduced nutrient availability
(Goffart et al., 2002).
Ciguatera caused by the benthic dinoflagellate Gambierdiscus toxicus is a tropical
fishfood poisoning syndrome well-known in coral reef areas in the Caribbean, Australia,
and especially French Polynesia. Whereas, in a strict sense, this is a completely natural
phenomenon, from being a rare disease two centuries ago, ciguatera has now reached
epidemic proportions in French Polynesia. From 1960 to 1984, more than 24,000
patients were reported from this area, which is more than six times the average for
the Pacific as a whole. Evidence is accumulating that reef disturbance by hurricanes,
military and tourist developments (Bagnis et al., 1985), as well as coral bleaching
(linked to global warming) and perhaps in future increasing coral damage due to
ocean acidification (Hoegh-Guldberg, 1999) are increasing the risk of ciguatera. In
the Australian region Gambierdiscus toxicus is well-known from the tropical Great
Barrier Reef and southwards down to just north of Brisbane but in the past 5 years
this species has undergone an apparent range extension into South-East Australian sea
grass beds as far south as Melbourne, aided by a strengthening of the East Australian
Current. A similar expansion of Gambierdiscus into the Mediterranean and Eastern
Atlantic has also been reported (Aligizaki et al., 2008). The red-tide dinoflagellate
Noctiluca scintillans (known from the Sydney region as early as 1860) since 1994 has
expanded its range into Southern Tasmanian waters where it has caused problems for
the salmonid fish farm industry (Hallegraeff, 2002). In the North Sea regional climate
warming has caused an analogous northward shift of warm-water phytoplankton
(Edwards & Richardson, 2004).
Range extensions by ship ballast water transport - Ballast water is seawater which
has been pumped into a ship’s hold or dedicated ballast tanks to steady it by making
it heavier and thus less likely to roll; the water is released when a ship enters port.
Ballast water on cargo vessels was first suggested as a means of dispersing marine
plankton 100 years ago (Hallegraeff, 1998). However, it was only in the 1980s that the
problem sparked considerable interest, after evidence was brought forward that nonindigenous toxic species such as the PSP dinoflagellate Gymnodinium catenatum had
been introduced into Southern Australian waters into sensitive aquaculture areas, with
disastrous consequences for commercial shellfish farms. Molecular tools increasingly
offer the potential to detect non-indigenous microalgal strains and in some cases
even track donor source populations (Scholin et al., 1995). An example is the recent
detection in the Mediterranean ports of Sete and Barcelona of Alexandrium catenella
with a temperate Asian ribotype not found anywhere else in Europe (Lilly et al., 2002,
Fig. 7). The creation of numerous artificial structures for the protection of beaches
and harbours has also been invoked as a mechanism for the apparent increase of
Alexandrium bloom events in the Mediterranean (Garcés et al., 2000).
Climate Change - Prediction of the impact of global climate change on harmful
algal blooms is fraught with uncertainties, but we can learn important lessons from
the dinoflagellate cyst fossil record and long-term monitoring programmes such as
the Continuous Plankton Recorder surveys. Increased temperature, enhanced surface
Harmful Algal Blooms, Coastal Eutrophication and Climate Change
13
stratification, nutrient upwelling, stimulation of photosynthesis by elevated CO2,
changes in land runoff and nutrient availability, altered ocean pH, may produce
contradictory species- or even strain-specific responses. We can expect: (1) Range
expansion of warm-water species at the expense of coldwater species which are
driven pole wards; (2) Changes in abundance of selected HAB species; (3) Earlier
timing of peak production of some phytoplankton; (4) Knock-on effects for marine
food webs, notably when zooplankton and fish grazers are differentially impacted
by climate change. Ecosystems disturbed by pollution or climate change tend to be
more prone to ballast water invasions (Stachowicz et al., 2002). Some harmful algal
bloom phenomena (e.g. toxic dinoflagellates benefiting from land runoff and/or water
column stratification, benthic dinoflagellates responding to coral reef disturbance) may
increase, while others may diminish in areas currently impacted.
Fig. 7 - Molecular biogeography of LSU ribotypes in the Alexandrium tamarense/catenella dinoflagellate species complex. Black arrows indicate natural dispersal, while clear arrows suggest human-assisted dispersal. The appearance of temperate Asian ribotype in 1983 in the
Mediterranean can only be explained by human-assisted introduction (after Scholin et al.,
1995).
Biogeografia molecolare di ribotipi LSU nella dinoflagellata Alexandrium tamarense/catenella complex. Le frecce scure indicano la dispersione naturale, mentre le frecce chiare indicano una dispersione
favorita dall’uomo. La comparsa del ribotipo Asiatico temperato nel 1983 nel Mediterraneo può essere
spiegata soltanto da un’introduzione favorita dall’uomo (da Scholin et al., 1995).
Conclusions - It is unfortunate that so few long-term records exist of algal blooms at
any single locality; ideally we need at least 30 consecutive years. Whether the apparent
global increase in harmful algal blooms represents a real increase or not therefore is a
question that we will probably not be able to answer conclusively for some time to come.
There is no doubt that our growing interest in using coastal waters for aquaculture is
leading to a greater awareness of toxic algal species. People responsible for deciding
quotas for pollutant loadings of coastal waters, or for managing agriculture and
deforestation, should be made aware that one probable outcome of allowing polluting
chemicals to seep into the environment will be an increase in harmful algal blooms.
In countries which pride themselves on having disease- and pollution-free aquaculture,
every effort should be made to quarantine sensitive aquaculture areas against the
unintentional introduction of non-indigenous harmful algal species (e.g. the 2004
14
G.M. Hallegraeff
International Maritime Organisation (IMO) Convention for Ballast Water). Nor can
any aquaculture industry afford not to monitor for an increasing number of harmful
algal species in water samples (Zingone et al., 2006) and for an increasing number of
algal toxins in seafood products using increasingly sophisticated analytical techniques
such as LC-MS (as routinely conducted by the National Reference Laboratory on
Marine Biotoxins in Cesenatico). Last but not least, global climate change is adding
a new level of uncertainty to many seafood safety monitoring programmes, as are
range extensions of HAB species by ship ballast water transport and increased sea
surface temperatures. The greatest problems for human society will be caused by
being unprepared for significant range extensions or the increase of algal biotoxin
problems in currently poorly monitored areas. Increased vigilance in seafood biotoxin
monitoring programmes is recommended.
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