« Previous | Contents | Next »
Listen
12.0 CLIMATE CHANGE AND HARMFUL BLOOMS
Climate change is another mechanism potentially opening up Scottish coastal waters to altered phytoplankton dynamics and HAB behaviour, similar to the effects of advection and ballast water delivery of species discussed in Section 11.0. While climate is no less a factor in making Scottish coastal waters " open systems", it is more difficult to assess such "changing environment" effects associated with climate change because their time course of expression is longer, develops gradually and is cloaked within the inherent variability of phytoplankton dynamics that accompanies climate and weather-driven processes. There is also a practical problem: the appropriate time series of measurements needed to detect such change is usually not available. This makes it very difficult to distinguish between altered phytoplankton behaviour induced by aquaculture from that due to natural processes and climate change. HAB species blooms are very unpredictable, with at least 11 types of variability in species occurrence and bloom patterns known (see Table 1 in Smayda, 1998a). Habitat-plankton variability also occurs as a set of events, with the different types and impacts having both short- and long-term temporal scale effects and local and far-field spatial effects. These features lead to differing, rather than uniform HAB species responses, which increases the difficulty in distinguishing between anthropogenic stimulation of harmful blooms and natural behavior. Maddock et al. (1981) encountered such difficulties in analyzing a 24-year phytoplankton time series for Plymouth waters and in seeking to quantify causal connections with climate. While able to sub-group 107 species into eight clusters applying Lamb's weather classification, the patterns of species' changes were less erratic than weather conditions, and significant correlations were difficult to detect. Maddock et al. concluded that phytoplankton respond only to certain features of weather properties, or to those accompanying long-term changes. Establishing what the specific driving factors are is the difficult part.
Despite these complications, the potential effects of climate change on phytoplankton behavior in Scottish coastal waters must be considered, if only because climate and meteorological events are well known regulators of phytoplankton growth, i.e. seasonal wind regulation of the annual spring bloom, interannual variations in this event and in mini-blooms, and species successions. Given the openness of Scottish coastal waters to local and far-field advections of bloom species, the relevance of meteorological and climate forcing of phytoplankton to the aquacultural issues addressed in this report is even more evident. The following sections summarize the evidence from European waters, and elsewere, that climate through its disturbances, anomalies, regional patterns and long-term change can affect HAB events. Similar climatically induced impacts are expected to occur in Scottish coastal waters, and carry the potential danger of being falsely attributed to aquacultural stimulation. Since the specific mechanisms involved are poorly understood, the general evidence that climate change makes coastal waters " open systems" will be the focus.
12.1 Climate, weather and harmful blooms
Previous sections dealt with the well documented truism that coastal phytoplankton communities are "open" to disruption and bioinvasion through their responses to aquaculture, exposures to ballast water, and advective seedings of species. In each of these mechanisms, the altered physical and chemical habitat properties are secondary to the biological impacts. In the case of aquacultural impacts, the altered biology is either the result of altered nutrient-growth relationships and/or grazing. In the case of ballast water and advection, the primary feature ("stress") is in the introduction of species; neither the physical or chemical conditions are significantly altered. Whether the introduced species grow subsequently is determined by the local growth conditions and competition between the indigenous and introduced species (strains). In contrast, meteorological (wind- and weather-driven events) and climatological changes primarily cause physical and chemical changes that are imposed on the local plankton communities, i.e, the direct biological effects are secondary. There is also a much more diverse impact on the habitat and plankton growth conditions. Physical changes lead to variability in temperature, irradiance, precipitation, run-off, mixed-layer depth, etc. This variability is not only random; trends and cycles also occur, the wavelength of which varies with the parameter (Smayda, 1998a). For example, there are different hydrographic cycles, with periods of 3-4, 6-7, 10-11, 18-20 and 100 years (Gray and Christie, 1983). These cycles may be superimposed upon long-term trends (Reynolds, 1990), such as the cyclical occurrences of wet and dry years (Currie, 1984) and interannual shifts in wind stress patterns (Horne and Platt, 1984). Variance in the physical habitat leads to variance in plankton cycles, ecosystem structure and productivity. A 30-year decline in phytoplankton and zooplankton could be related to changes in mixed-layer depth associated with a long-term increase in northerly winds (Dickson et al., 1988). Two crisp peaks of warm-water phytoplankton abundance characterized a 24-year time series, with each pulse lasting two years (Maddock et al., 1989). Chemical (=nutrient) variability driven by physical changes also occurs, including nutrient loading via run-off (in coastal systems), seasonal mixing, watermass incursions, and altered nutrient ratios (Smayda, 1998a).
Pelagic environments and plankton processes are inherently variable, largely because they are open to wind-, weather-, and climate-driven disturbances. These disturbances range in magnitude from micro-scale turbulence to storm events to large scale ocean-atmosphere interactions, such as the North Atlantic Oscillation ( NAO) and El Niño-Southern Oscillation ( ENSO) conditions. Arrayed along a continuum from short-term to long-term drivers of habitat and plankton change, the duration, magnitude and persistence of weather/climate effects increase as follows:
Short-term weather event ? Local anomalous event ? Regional event ( NAO, ENSO) ? Hydro-climate change ? Climate change ? Regime shift
The different intensities, scales and scope of meteorological and climatological impacts are outlined in the following sections.
12.1.1 The rainfall-runoff-high irradiance event and HABs
A characteristic, short-term, weather-driven event frequently reported to precede a red tide or harmful bloom is the rainfall-runoff-high irradiance event [see Sections 7.1.2b and 8.2]. In this sequence, the bloom is stimulated by the high irradiance levels that often follow after a period of high rainfall and runoff. This weather pattern can contribute to the bloom event in three ways: supply nutrients, increase watermass stability, and detoxify the recipient watermass. A large scale regional weather pattern of this type over north- and west-Scotland in late June-early July 1988 preceeded, if not triggered, several harmful blooms that affected fish farms, including in Loch Torridon and along the west coast of the Shetland Isles (Bruno et al., 1989). The fish loss was valued at several million pounds sterling. Bruno et al. stated that one of the prerequisites for blooms in Scottish waters is a period of bright, warm, calm weather following a period of disturbed wet conditions.
Other examples of apparent bloom stimulation of harmful species accompanying rain-runoff events include an ichthyotoxic bloom of the silicoflagellate, Dictyocha speculum, in Danish waters (Henriksen et al., 1993) preceded by very heavy rain during which " runoff of fertillizers from land probably triggered the bloom" (Moestrup, and Thomsen 1990). Blooms of toxic and benign Chrysochromulina spp. in southern Scandinavian waters runoff events that resulted in high N:P ratios (Sections 7.1.2, 7.1.4; Dahl et al., 1998; Lindahl and Dahl, 1990), and blooms of the harmful cyanophyte Schizothrix calcicola bloom in shrimp ponds were associated with strong rains (Alonzo-Rodriguez, R. and F. Páez-Osuna 2003). Blooms of the PSP toxic species Gymnodinium catenatum at Tasmanian aquacultural sites have become fairly predictable responses to rain-runoff events, with selenium delivered in the runoff thought to be the critical bloom trigger (Doblin et al., 1999; Hallegraeff et al., 1995). Blooms of K. mikimotoi in Omura Bay, Japan, have likewise been linked to the rain-runoff event. While changes in nutrient levels and their ratios induced by runoff are usually the most evident signals, the blooms are undoubtedly responses to the coupled effects of watermass stability, irradiance, and "water quality", modified by the runoff. The particular combination of factors changed by the hydro-climate modification, and essential to bloom stimulation, undoubtedly varies at a given site and for a given species, rather than is site- and species-specific. This feature contributes to the observed variability in whether, or not a bloom takes place following a rain-runoff event, and which species will bloom, should there be bloom.
Anomalous, weather-driven blooms are also known, as in Hiroshima Bay where blooms of the ichthyotoxic raphidophyte, Chattonella antiqua, followed typhoons (with accretion of nutrient-rich runoff) that inflicted high financial loss to fish farms (Kimura et al., 1973). Longer lasting runoff events also occur, such as the annual blooming of ichthyoxic H. akashiwo in the Strait of Georgia, British Columbia, where it appears to dependent upon Fraser River runoff (Taylor and Haigh, 1993).
12.1.2 Regional scale climatological events and HABs
Regional and basin-scale climatic impacts on habitat and plankton communities associated with the North Atlantic Oscillation ( NAO) and El Niño Southern Oscillation ( ENSO) are increasingly being reported. In the north Atlantic, sea surface temperature ( SST), precipitation, and wind/weather patterns are strongly influenced by atmospheric circulation patterns indexed as the North Atlantic Oscillation ( NAO). The NAO index is used as an indicator of climate change based on the difference in sea level atmospheric pressure between subpolar Iceland and subtropical Azores (Hurrell, 1985). Years with high (positive) winter (December to February) NAO indices tend to have strong westerly winds, increased storm activity, and milder winters; years with a low (negative) NAO are characterized by colder winters. Changes in NAO state are analogous to shifts in "ocean climate". The NAO has been identified as the climatic mechanism driving observed shifts in North Sea phytoplankton (Reid et al., 1998) and zooplankton (Fromentin and Planque, 1996) populations, and has been considered an accurate predictor of North Sea zooplankton abundance (Planque and Reid, 1998). Irigoien et al. (2000) concluded that diatom abundance in the English Channel was related to the NAO, although the data are limited. While there is solid evidence that large scale regional shifts in the plankton communities in Northern European waters are climate driven, and that these can be related to NAO patterns, there is little information on whether harmful bloom species and events are also affected, an issue that has not attracted much investigator attention. Belgrano et al. (1999) reported that Dinophysis blooms and DSP occurrences in Swedish coastal waters may have a NAO linkage.
There is much greater evidence from the Pacific that HAB events are influenced by "El Niño - Southern Oscillation" ( ENSO) events, the Pacific equivalent of the NAO. El Niño is a generic term describing anomalous warm events in the eastern boundary current regions of the global ocean (Norton et al., 1985). Historically, it has been applied to the ocean surface warming that occurs during winter off the coasts of Peru and Ecuador, usually during the Christmas season. [The Spanish words El Niño refer to the Christ Child.] The notoriety of El Niño lies in the large regional anoxic events and mortalities that accompany the red tides that develop then in lieu of upwelling induced diatom blooms. Mass mortality of piscivorous guano depositing birds along the Peruvian coast has been documented during El Niño events since 1828 (Rojas de Mendiola, 1979). The El Niño is one aspect of the global ocean-atmosphere perturbation termed the "El Niño - Southern Oscillation", or ENSO. The Southern Oscillation is the atmospheric pressure difference between the Pacific and Indian Oceans indexed as the Southern Oscillation Index ( SOI), and which is the sea level pressure difference between Tahiti and Darwin, Australia. Similar to the NAO, pronounced changes and anomalies in basin-wide ocean climate occur during the aperiodic ENSO years, including in wind stress, water column mixing, watermass warming and intrusions, precipitation and irradiance.
El Niño-Southern Oscillation ( ENSO) events as climatic drivers of harmful algal blooms have attracted attention after Erickson and Nishitani (1985) suggested there was a correlation between PSP outbreaks in the Pacific Northwest and this climatology. Exceptional PSP episodes occurred during seven of the nine ENSO events recorded there between 1941-1984. El Niño events are large-scale meteorological and oceanographic disturbances caused by an imbalance in atmospheric pressure and sea surface temperature between the eastern and western Pacific Ocean. Maclean (1989) showed that six major blooms of PSP toxigenic Pyrodinium bahamense var. compressum in the western Pacific between 1972-1988 coincided with ENSO events. A remarkable spreading of PSP and this species in the Indo-Pacific region was also observed during this period. El Niño events have been associated with multiple, novel blooms in New Zealand coastal waters. In 1992, prolonged, novel blooms of the raphidophytes Fibrocapsa japonica and Heterosigma akashiwo, and the silicoflagellate, Dictyocha speculum, all of which are toxic, bloomed during the low temperature phase of an El Niño event (Rhodes et al., 1993). Novel toxic blooms of Gymnodinium cf. breve [probably Gymnodinium brevisulcatum (see Chang, 1999)] and Alexandrium minutum developed after a prolonged period of anomalous weather/climate accompanying an El Niño event (Chang et al., 1995). The anomalous weather/climate was characterized by sub-normal temperatures, calmer conditions, increased rainfall and increased runoff, a combination of factors thought to have triggered the A. minutum bloom. In contrast, the concurrent bloom of Gymnodinium was thought to have been initiated by an El Niño induced onshore intrusion of offshore waters, within which Karenia cf. breve was entrained.
Despite these provocative ENSO- HAB linkages, there is not a simple relationship between such climatologically driven phenomena. Bloom regulation by other factors is not contravened, and the New Zealand results reveal the considerable variability as to which species will bloom. The ENSO- HAB correlations reported for British Columbia and Puget Sound (U.S.) coastal waters by Erickson and Nishitani (1985) were not as apparent subsequently (Gaines and Taylor, 1985; Taylor, 1993), and El Niño events in New Zealand did not always stimulate blooms (Chang, 1994).
The regional scale climatology of NAO and ENSO and the accompanying atmospheric forcing of altered ocean climate are natural events which make all coastal waters "open systems". Unpredictable HAB events in Scottish coastal waters related to NAO dynamics are therefore expected, and efforts to link such episodes causally to aquacultural activities must exclude unusual or cyclical, regional scale climatology as the driving force. Another climatological effect of interest is the potential role of long-term climate change and global warming on HAB events.
12.2 Climate, regime changes and harmful blooms in the North Sea
12.2.1 Climate warming and harmful blooms
The apparent global spreading of HABs has led some investigators to seek a common global stimulus. Climate change, specifically global warming, has been invoked as this stimulus, but the evidence is not convincing. The lack of long-term data sets makes it difficult to distinguish between the periodic blooms of rarer, indigenous species and "hidden flora" components from those species that are expanding their geographical ranges and heightened bloom occurrences in response to a climatic factor. It is also difficult to distinguish between ballast water introductions of HAB species into waters outside of their range from incursions accompanying climate-altered circulation patterns. Cultural eutrophication of coastal waters is the other global signal that is sometimes invoked (Hallegraeff, 1993), but since fish farms in Scottish coastal waters are not located in such degraded waters, the influence of cultural eutrophication on HABs is not considered in this report. Section 10 dealt with the effect of nutrients wastes from fish farms and shellfish cultivation on HABs.
Nehring (1998, 1998a) has argued that climate change, specifically a rise in temperature, explains the introduction and persistence of ten of the 16 non-indigenous species of diatoms, dinoflagellates and raphidophytes that he suggests have invaded the North Sea, several of which are toxic. The evidence he presents is compromised by Elbrächter's (1999) demonstration that many of these species were previously reported from European waters under different names, i.e the result of taxonomic confusion. Elbrächter termed these species " pseudo-exotic" in distinction from " exotic" species that appear to be non-indigenous, such as the toxic raphidophyte Fibrocapsa japonica and harmful K. mikimotoi, but whose presence Elbrächter did not attribute to cllimate change. [Authors note: Species misidentifications of taxonomically difficult phytoplankton are a general problem, particularly since investigators carrying out field studies often have limited taxonomic experience and rely on species depictions in taxonomic monographs for identifications.] Nehring (1998a) presented limited evidence that warming of the North Sea symptomatic of a climate change has occurred. Nehring (1998a) defined thermophilic species based on their geographic distributions - being normally found in more southerly and warmer waters - rather than on their physiology. This also compromises his invocation of climate change. Ecophysiological inconsistencies are evident among the species that he has classified as thermophilic.
Although Nehring's evidence for a climate change (temperature) affect is not convincing, other investigators have implicated long-term temperature trends in affecting phytoplankton community structure and blooms. In the Baltic Sea, the increase in dinoflagellate blooms ( Peridiniella catenata) is thought to have been favored by the milder winters (Wasmund et al., 1998). A "greenhouse" effects scenario has been formulated by Fraga and Bakun (1993) linking blooms of PSP toxic Gymnodinium catenatum off the Galician coast ( NW Spain) to climate change based on decadal changes in wind patterns. The mechanism proposed involves long-term changes in wind stress and seasonal upwelling, downwelling and alongshore transport processes. Historically, sediment core analyses suggest that G. catenatum bloomed from ca. 2000 to 500 years B.P. in Kattegat-Skagerrak waters and then became locally "extinct" during the "Little Ice Age" about 300 years B.P. (Dale et al., 1993). This behavior and the apparent retraction of G. catenatum to Iberian waters have been suggested as evidence for a climate change effect (Dale and Nordberg, 1993).
Distinguishing between climate change and anthropogenic modification as factors in altering dinoflagellate behavior can be difficult (Dickson et al. (1992). One effect of warming would be to increase water mass stratification, an effect favorable to dinoflagellate blooms, but an increase in anthropogenic nutrient levels also stimulates their blooms. Thus, similar relative shifts in dinoflagellate (or other groups) community structure and blooms are expected to occur for both climatic and anthropogenic stimuli. When these two stimuli converge, i.e. the HAB event is driven by both influences, it is difficult to sort out the primary cause. Long-term studies at Marsdiep in the Dutch Wadden Sea suggest that climatic trends can be overridden by eutrophication effects (Cadée, 1992). A continuous increase in the abundance and bloom duration (from 50 to 150 days) of Phaeocystis and a 60% increase in primary production have accompanied increases in anthropogenic loadings of nitrogen and phosphorus. The debate over the role of cultural eutrophication and climate as factors in the devastating 1988 Chrysochromulina polylepis bloom in southern Scandinavian waters was discussed in Section 7.1.2.
12.2.2 Climate and ecosystem regime changes
12.2.2a Induced versus reflected events
Phytoplankton dynamics in Scottish coastal waters are a component of, and influenced by the complex hydrography and trophic dynamics of the North Sea. The North Sea and its adjacent waters are well known to be under strong climatic control and the cause of changes and anomalies occurring at various scales of intensity and persistence, both oceanographically and biotically. The occurrence of regime changes (=whole ecosystem changes) are of special interest given their regional extent, persistence and far-field impacts potentially extending into the "open" Scottish coastal waters. A brief description of the two main types of weather and climatic impacts on plankton, and the phytoplankton - hydrography mosaic in the North Sea will precede discussion of climate driven regime changes.
A variable interplay among physical, chemical and biological parameters controls phytoplankton blooms and community assembly. Much of this variability, including episodic HAB blooms, is trivial and transitory; other perturbations have major impacts symptomatic of major habitat and/or ecosystem transitions. Hence, variability and change in habitat properties and plankton processes and responses signal the status and trends of the interactive habitat-plankton relationship. The problem is to establish the causal links between the signals. This is imperative, for example, in addressing the hypothetical question of whether an apparent increase in HAB events occurring in a region of increasing aquaculture is attributable to stimulation by the latter or to one (or more) of the "open system" exposures of that coastal system.
The variability and change observed in habitat properties and plankton processes can be treated as " events" that fall into one of two major types: induced and reflected events (see Smayda, 1998). Induced events generally are direct biotic (plankton) responses to abiotic (i.e. physical, chemical) factors, and are usually the result of linear processes. These events are usually transitional, but may signal the occurrence of a more fundamental change. Red tide outbreaks which frequently follow excessive rainfall and runoff are well-documented examples of transitory events that are induced [Section 12.1.1]. The takeover of the phytoplankton community in the Dutch Wadden Sea by Phaeocystis cf. pouchetii apparently in response to increased anthropogenic phosphorus levels is an example of an induced event, but in this case it is more sustained (Riegman et al., 1992).
Reflected events are the outcome of a complex series of non-linear processes accompanied by parallel trends in several physical, chemical and trophic properties, analysis of which is very difficult. The biotic variability and change observed usually signal that a fundamental ecosystem change(s) has taken place. In this instance, the biotic response of interest can be either an indirect or direct consequence of the primary driving force(s). For example, reflected events can result when an induced event (i.e. the abiotic induction of a biotic change) leads to cascading biotic changes. An example: the inverse relationship found by Dickson et al. (1988) between westerly winds and phytoplankton abundance led to a long-term decline in zooplankton; i.e. this upper level biotic change reflected a lower level abiotic (=mixing) /biotic (=phytoplankton) interaction. Reflected events can also result from biotic/biotic interactions, including the effects of over-fishing. Examples of biotic/biotic interactions among phytoplankton, zooplankton, macrofauna, fishes and birds symptomatic of reflected events and fundamental ecosystem changes are provided by Aebischer et al. (1990) and Lindeboom et al. (1995) for the North Sea.
12.2.2b Effects of North Sea hydro-climate changes on the phytoplankton
Although a common phytoplankton flora characterizes the North Sea, marked regional differences occur in species assemblages and abundance. Braarud et al. (1953) carried out an extensive regional survey (100 stations) of the North Sea and adjacent waters between 53°N and 63°N when the spring bloom was either in progress or near termination depending on local conditions. A regional mosaic of phytoplankton communities was found rather than a uniform assemblage, with 16 distinct vegetation types (phytoplankton societies) recognized (Figure 18). In Scottish coastal waters, a similar community was present in the Shetland-Orkney area which graded southwards into four different types along the east coast of the UK in waters of different origin and character. Similarly, the phytoplankton communities in the Southern Bight, along the German and Danish coasts, northern North Sea, and Scandinavian coastal waters, etc. were vegetatively distinct even though the species selected were from the common pool of species that characterizes the North Sea and contiguous waters.
Braarud et al. demonstrated that the 16 vegetation types recognized matched up regionally with the distribution of different water masses and surface currents in the North Sea. Such regional phytoplankton heterogeneity is a persistent North Sea feature based on previous surveys, although the specific locations of the vegetation types vary with hydrographic conditions. The different communities within their hydrographic milieu and their geographical locations are subject to further modification because of "local climate". Dickson et al. (1992) describe an unprecedented increase in ceratian abundance ( Ceratium furca, C. fusus, C. tripos) in the north-central North Sea during 1987-1988. This unusual behavior was unique in the three decade time series of Continuous Plankton Recorder ( CPR) observations. This ceratian response accompanied the westward transport of freshened surface water outflowing from the Skagerrak and Norwegian coast under the stress of an anomalously strong easterly air stream. Thus, the intra-regional openness of North Sea phytoplankton communities, including those in Scottish coastal waters, is also subject to modification because of far-field influences.
In addition to "local climate" effects, the entire North Sea system is open to large-scale anomalies. Edwards et al. (2002) describe two such events based on CPR surveys: the "cold boreal event" of 1978-1982, and the "warm temperate event" of the late 1980s to early 1990s. Winters during this period were the coldest in a half-century, with reduced inflow of warm, nutrient-rich Atlantic water into the North Sea. These events were viewed as hydro-climate changes that occurred within the long-term climatic pattern then in progress, and signalled by the NAO index. Specifically, occasionally extreme climatic events that contain 'oceanographic elements' punctuate decadal trends in NAO, or enhance its effects and cause notable biological shifts, such as during the two North Sea events noted above. The decrease in temperature during the "cold boreal event" led to reduced abundance of diatoms and dinoflagellates, delayed and diminished the spring bloom, and was accompanied by the absence or scarcity of the usually dominant species. Ceratium macroceros disappeared, and by 1995 had yet to recover despite restoration of growth conditions. This reveals that changes in hydro-climate can influence niche structure, "knocking out" a species, or having its niche preempted by a more competitive species (Smayda, 2002). In contrast, abundance of the cold water species Ceratium longipes greatly exceeded its long-term mean. During this event, the northern North Sea was open to unusual, advected intrusions of sub-Arctic species, such as the diatom Navicula planamembranacea.
The opposite affects accompanied the "warm temperate event" of the late 1980s. The NAO index increased to its highest positive level observed in the 20th century, resulting in a strong westerly wind component and high air temperature around the British Isles. The warmer climate (mild winters), accompanied by an increased inflow of relatively warm Atlantic water into the North Sea, combined to produce an extremely warm hydro-climate. This resulted in a marked increase in phytoplankton biomass above the long-term mean, particularly during winter, and was accompanied by a series of short-lived, exceptional phytoplankton blooms, including the oceanic diatom Thalassiothrix longissima (Reid et al., 1992). Heterotrophic dinoflagellates, Protoperidinium spp., which prey on other dinoflagellates, appeared earlier and in greater abundance, and their annual cycle was altered relative to their long-term behavior. A 24-yr phytoplankton time series from the Plymouth area based on net tows showed two crisp peaks of abundance of warm-water species, each pulse lasting two years (Maddock et al., 1989).
12.2.2c Ecosystem regime shifts and climate
The "cold boreal" and "warm temperate" events in the North Sea attributable to extreme climatic events, while prolonged and characterized by altered plankton behavior, were followed by a return to more or less normal conditions. While the changes in biota were substantial, they were muted in comparison with more dramatic cases of ecosystem regime changes, in which the disturbance is much more prolonged, ecologically deeper and the result of strong coupling between climatology and physical oceanographic processes. During such periods, oceanic intrusions into the North Sea contribute significantly to the hydro-climate changes, as during the "cold boreal" and "warm temperate" events (Edwards et al., 2002). Both the northern and southern boundaries of the North Sea are open to oceanic intrusions from boreal and lusitanian (from southern Europe) systems. This contributes to changes in key phytoplankton species (Boalch, 1987; Edwards et al., 2001) and long-term changes in abundance, including in zooplankton populations. Dickson et al. (1988) associated a 30-yr decline in CPR collections of phytoplankton and zooplankton from around the British Isles to the long-term increase in the northerly wind component over the eastern North Atlantic and associated changes in depth of the mixed layer. The special feature of regime changes is they appear to represent a major change from a fairly stable assemblage of organisms making up the different trophic compartments in the ecosystem to another, quite different mix of species. That is, the ecosystem equilibrium shifts to another stable state. A major shift in biogeochemical processes may also occur, such as the shift from a nitrogen to phosphorus limited system that accompanied the El Niño driven shift in North Pacific phytoplankton communities to a Trichodesmium [a N-fixing cyanophyte] dominated system (Karl et al., 1995).
The best known regime shift - the Russell Cycle - has been reported from the English Channel (Cushing, 1982; Russell et al., 1971; Southward, 1980). Studies of the English Channel ecosystem carried out since the early 1900s have revealed the occurrence of long-term changes and patterns (the 60-yr Russell Cycle) in nutrients, plankton, benthos, fish stocks and trophodynamic shifts accompanying cooling and warming trends and oscillations in response to changes in westerly wind frequency. The Russell Cycle was initiated in the western part of the English Channel in 1925 by a decline in recruitment to the herring stock, followed in 1931 by the last recorded year-class entry into the fishery, and thereafter by the collapse of the Plymouth herring stock in 1936. The species composition of the macro-zooplankton communities indicative of different water mass types also changed during this period, and there was a significant decrease in zooplankton biomass. During the following decade, the abundance of demersal fish larvae decreased significantly, whereas pilchard fecundity increased. These biotic changes were accompanied by a decrease in winter phosphorus levels, an essential nutrient for phytoplankton growth. This ecosystem shift which persisted for ca. 25-years was characterized by low nutrient levels, different key species, lower plankton biomass, fewer fish larvae and a change in fish stocks dominated by herring, gadoids and flat-fish to dominance by pilchards and small zooplankton (Mann and Lazier, 1991). Equally dramatic, between 1965 and 1979 the system began to reverse itself and returned to pre-1930 levels. These regime shifts have been related to long-term patterns in the NAO index indicative of a flip-flop change from colder, more northerly weather to warmer, more westerly weather. The more recent contributions of Aebischer et al. (1990) and Lindeboom et al. (1995) provide additional data on regime shifts in North Sea habitats and the complex, climate-driven trophic interactions that determine and reflect the outcome of ecosystem regime change.
12.3 Climate change, aquaculture and harmful blooms in Scottish coastal waters
It is unknown to what extent the ecosystem regime change that occurred during the Russell Cycle, or the lesser ones during the North Sea "cold boreal event" of 1978-1982 and the "warm temperate event" of the late 1980s to early 1990s, extended into Scottish coastal waters. Given the regional scope and persistence of these climatically induced events, it seems likely that habitat conditions and biotic behaviour were altered. In addition to the ballast water and advective introductions of species into Scottish waters [Section 11.2], and the various types of weather- and climate-driven variability in these waters, climate and ecosystem regime changes are expected to increase the "openness" of Scottish waters to variable phytoplankton behavior, including harmful blooms.
Returning to the hypothetical question raised earlier of whether an apparent increase in HAB events in a region of increasing aquaculture is attributable to stimulation by the latter, or reflects one (or more) of the "open system" exposures of that coastal system. Applying this question to Scottish coastal waters, and specifically whether aquaculture has stimulated harmful blooms, as some have argued, what can be concluded? There is, first, no evidence of an increase in harmful algal blooms in Scottish waters. Second, while blooms at fish farm sites are known from other regions, and there is evidence that fish wastes can stimulate growth of harmful species, there is no evidence for such impacts in Scottish waters. Third, blooms of the harmful species present in Scottish waters are not dependent on aquacultural stimulation; all harmful species have bloomed in habitats not influenced by fish farm wastes or by shellfish cultivation. Forth, cultured shellfish are prone to DSP toxicity, but the toxin is usually not derived as a consequence of local bloom stimulation. but, rather, from ingestion of Dinophysis cells advected into the shellfish cultivation sites from pristine growth areas located offshore.
The above conclusions are based on careful scrutiny of the available data and from the known ecophysiology of the harmful species involved, and presented in this report. The basic conclusion to the question posed is that there is no evidence that aquaculture is contributory to the harmful bloom occurrences reported for Scottish coastal waters. Should an increase in harmful blooms occur, whether in frequency, by type, or in novel species, efforts to equate this to aquacultural stimulation must be tempered by the knowledge that Scottish coastal waters are " open systems" vulnerable to the incursions of bloom species and regional habitat perturbations associated with weather and climate. It is incumbent on proponents of the aquacultural stimulation hypothesis to rule out such local and far-field effects and, in reaching this conclusion, not to rely on qualitative and anecdotal observations at the expense of quantitative analysis.
12.4 ASP in Scottish waters and climate change
Gallacher et al. (2002) have suggested that the persistent amnesic shellfish toxicity of shellfish in Scottish waters (Figure 2) may be a consequence of climate change. They report that winter water temperatures have increased by 4°C the "past six years" [years unstated], accompanied by intensified wind speeds that have increased mixing, enhanced offshore circulation and the influx of southerly water masses, and also enhanced offshore nutrient fluxes. The required effect of this hydro-climate change leading to ASP toxicity of the scallop grounds [unmentioned by Gallacher et al.] would be the growth stimulation of Pseudo-nitzschia species and/or its production of domoic acid, the source of ASP. The temperature requirements and responses of Pseudo-nitzschia spp. are largely unknown . Should Pseudo-nitzschia pungens f. multiseries have been the species involved, then the imputed winter warming would not appear to account for the occurrence of ASP in the shellfish. Pseudo-nitzschia pungens f. multiseries blooms at very low temperatures (-1° to 3°C), occurs over a temperature range of 2° to 28°C (Lewis et al., 1993), and has an optimal temperature for growth and photosynthesis at 15° to 20°C (Pan et al., 1993). Pan et al. (1993) concluded that factors other than temperature trigger its blooms.
A clear distinction must be made between temperature stimulated growth of Pseudo-nitzschia spp. and the influence of temperature on DA production. Pseudo-nitzschia seriata produces higher amounts of DA at 4°C than P. pungens f. multiseries (Bates, 1998). Domoic acid production in the latter species is temperature sensitive; it is much lower at 0° to 5°C than at 13°C (Smith et al., 1993). Both P. seriata and P. pungens f. multiseries are capable of growth at very low temperatures, even under ice, as shown for Nova Scotian populations (Lewis et al., 1993; Smith et al., 1993). The high Q 10 for DA production in P. pungens f. multiseries led Lewis et al. to conclude that its production "can be greatly reduced" by small changes in temperature. These limited data suggest that if there is indeed a temperature effect contributory to ASP phycotoxin presence om the scallop grounds, this might primarily be the result of increased DA production rates and, secondarily, bloom stimulation of Pseudo-nitzschia spp. However, attribution of the ASP "epidemic to an increase in winter water temperature is very speculative and compromised by the multifactorial regulation of DA synthesis shown to occur experimentally and expected to occur in situ [see Section 2.5].
Gallacher and co-workers presented their temperature warming hypothesis as a preliminary assessment, which they state will be the subject of future research. In the interim, based on available evidence detailed in this report the most compelling conclusion is that the scallop ground ASP outbreak is the result of natural causes rather than attributable to anthropogenic stimulation, including fish farm activities, or to the putative winter warming effect.
« Previous | Contents | Next »