Table Of ContentScottish Executive Environment Group
Harmful Algal Bloom Communities in
Scottish Coastal Waters:
Relationship to Fish Farming and Regional
Comparisons – A Review
February 2006
Paper 2006/3
Final Report
HARMFUL ALGAL BLOOM COMMUNITIES IN SCOTTISH COASTAL
WATERS: RELATIONSHIP TO FISH FARMING AND REGIONAL
COMPARISONS - A REVIEW
Theodore J. Smayda
Graduate School of Oceanography
University of Rhode Island
Kingston,
RI 02881
November, 2004
TABLE OF CONTENTS
EXECUTIVE SUMMARY AND RECOMMENDATIONS............................................. 1
1.0 INTRODUCTION................................................................................................17
2.0 AMNESIC SHELLFISH POISONING AND PSEUDO-NITZSCHIA BLOOMS ... 19
2.1 Nature of Amnesic Shellfish Poisoning (ASP)................................................. 20
2.2 Scottish coastal waters and ASP....................................................................21
2.3 Domoic acid, the cause of ASP: its source and vectoring............................... 22
2.4 What is Pseudo-nitzschia? ............................................................................. 24
2.5 Domoic acid (DA) production by Pseudo-nitzschia species and strains ......... 26
2.5.1 Influence of cell size.................................................................................27
2.5.2 Influence of growth phase, cell division and bacteria ............................... 28
2.5.3 Influence of irradiance, phosphorus, silica, nitrogen ................................ 30
2.5.4 Iron metabolism and DA synthesis...........................................................33
2.5.5 Summary.................................................................................................. 34
2.6 Secretion of domoic acid: importance and trophic vectoring........................... 35
2.7 Pseudo-nitzschia blooms and ASP in Scottish coastal waters........................ 36
2.8 Distribution of Pseudo-nitzschia and DA in European waters.........................37
2.9 Vulnerability of scallops to DA intoxication relative to other shellfish .............. 38
2.10 Pseudo-nitzschia, ASP and fish farms in Scotland ....................................... 39
3.0 DINOPHYSIS BLOOMS AND DIARRHETIC SHELLFISH POISONING...........40
3.1 Nature of Diarrhetic Shellfish Poisoning (DSP)...............................................40
3.2 Dinophysis species: DSP toxicity, taxonomic problems, autecology............... 41
3.3 Dinophysis blooms.......................................................................................... 43
3.4 Dinophysis and DSP in European coastal waters...........................................45
3.5 Dinophysis blooms and DSP in Scottish coastal waters ................................. 47
4.0 ALEXANDRIUM BLOOMS AND PARALYTIC SHELLFISH POISONING ....... 49
4.1 Nature of Paralytic Shellfish Poisoning (PSP)................................................. 49
4.2 Toxic Alexandrium species and PSP in Scottish coastal waters.....................51
4.2.1 Alexandrium tamarense ........................................................................... 51
4.2.2 Alexandrium minutum............................................................................... 54
4.2.3 Alexandrium ostenfeldii and the toxin spirolide ........................................ 55
5.0 BLOOMS OF OTHER HARMFUL DINOFLAGELLATES IN SCOTTISH
COASTAL WATERS ............................................................................................... 57
5.1 Karenia mikimotoi (Gyrodinium aureolum)...................................................... 57
5.2 Lingulodinium polyedrum................................................................................59
6.0 PHYTOFLAGELLATE SLOOMS IN SCOTTISH COASTAL WATERS............. 61
6.1 Introduction.....................................................................................................61
6.2 Flagellate X - what is it?.................................................................................. 61
6.3 Ubiquity and abundance of phytoflagellates ................................................... 63
6.4 Raphidophyte blooms ..................................................................................... 65
6.4.1 Heterosigma akashiwo............................................................................. 66
6.4.1a Taxonomic status ................................................................................... 66
6.4.1b Blooms and fish farm mortality...............................................................66
6.4.1c Toxic mechanisms.................................................................................. 67
6.4.2 Heterosigma akashiwo blooms and fish kills in European waters ............ 68
6.4.3 Is Heterosigma akashiwo indigenous in European coastal waters?.........70
6.4.4 Heterosigma akashiwo in Scottish and Irish coastal waters.....................70
6.4.5 Rarity of Heterosigma akashiwo blooms at fish farm sites in European
waters: an enigma.............................................................................................71
6.4.5a Influence of temperature ........................................................................ 72
6.4.5b Role of nutrients ..................................................................................... 73
6.4.5c Summary................................................................................................74
6.5 Chattonella spp. and Fibrocapsa japonica blooms ......................................... 75
7.0 HAPTOPHYTE BLOOMS: CHRYSOCHROMULINA, PRYMNESIUM,
PHAEOCYSTIS........................................................................................................ 77
7.1. Chrysochromulina blooms in Scandinavian waters........................................ 77
7.1.1 Chrysochromulina taxonomy and autecology........................................... 77
7.1.2 The 1988 Chrysochromulina polylepis bloom in southern Scandinavian
waters ............................................................................................................... 79
7.1.2a Scale of mortality.................................................................................... 79
7.1.2b Bloom pattern, dynamics and causation ................................................ 80
7.1.2c Phosphorus limitation and toxicity .......................................................... 82
7.1.3 The 1991 Chrysochromulina leadbeateri bloom in Northern Norway ....... 83
7.1.4 The 1992 Chrysochromulina spp. bloom in Danish waters ...................... 85
7.2 Prymnesium blooms and fish kills...................................................................86
7.3 Phaeocystis blooms........................................................................................90
7.4 Relevance of Haptophyte blooms to Scottish aquaculture.............................. 91
8.0 SILICOFLAGELLATE BLOOMS AND FISH MORTALITY ............................... 92
8.1 Autecology of Silicoflagellates ........................................................................ 92
8.2 Silicoflagellate bloom regulation and ichthyotoxicity ....................................... 94
9.0 DIATOM BLOOMS AND FISH MORTALITY.....................................................97
10.0 FISH FARMS, SHELLFISH CULTIVATION AND HARMFUL BLOOMS....... 100
10.1 Aquacultural wastes: composition and habitat impacts............................... 100
10.2 Fish farms, nutrient wastes and blooms in Scotland...................................104
10.3Fish farm wastes and phytoplankton growth...............................................107
10.4Fish farm mortality, polyamines and blooms...............................................110
10.5 Shellfish cultivation and blooms..................................................................113
10.5.1 Shellfish cultivation in Scotland ............................................................ 113
10.5.2 Extensive nature of shellfish cultivation: impacts on natural phytoplankton
community....................................................................................................... 114
10.5.3 Vulnerability of cultured bivalves to indigenous, harmful phytoplankton
species............................................................................................................ 115
10.5.4 Shellfish cultivation, wastes and blooms .............................................. 117
10.6 Summary and recommendations................................................................119
11.0 SCOTTISH COASTAL WATERS AS OPEN SYSTEMS ............................... 120
11.1 Contrasting behavior of HAB species in Scottish coastal waters and
elsewhere in Europe...........................................................................................120
11.2 Ballast water introductions of HAB species into Scottish waters................. 122
11.3 Advection of HAB species in coastal currents............................................. 127
11.4 Scottish waters as advective sources of HAB species................................ 128
11.5 Scottish waters as advective recipients of HAB species.............................129
11.5.1 Offshore advections ............................................................................. 129
11.5.2 Onshore - offshore advections ............................................................. 131
11.6 Advections of HAB species in Irish coastal waters: an analogue of Scottish
coastal waters..................................................................................................... 133
11.7 Ecophysiological capacity of HAB species for advective seedings ............. 134
11.8 Summary .................................................................................................... 135
12.0 CLIMATE CHANGE AND HARMFUL BLOOMS...........................................136
12.1 Climate, weather and harmful blooms ........................................................ 137
12.1.1 The rainfall-runoff-high irradiance event and HABs.............................. 138
12.1.2 Regional scale climatological events and HABs................................... 139
12.2 Climate, regime changes and harmful blooms in the North Sea.................140
12.2.1 Climate warming and harmful blooms .................................................. 140
12.2.2 Climate and ecosystem regime changes.............................................. 142
12.2.2a Induced versus reflected events......................................................... 142
12.2.2b Effects of North Sea hydro-climate changes on the phytoplankton ... 143
12.2.2c Ecosystem regime shifts and climate ................................................. 144
12.3 Climate change, aquaculture and harmful blooms in Scottish coastal waters
............................................................................................................................ 145
12.4 ASP in Scottish waters and climate change................................................ 146
13.0 ACRONYMS USED IN THIS REPORT..........................................................148
14.0 FIGURES ....................................................................................................... 150
15.0 REFERENCES...............................................................................................168
EXECUTIVE SUMMARY AND RECOMMENDATIONS
1. The phytoplankton species composition, succession, spring bloom dynamics
and environmental regulation in Scottish coastal waters have a Boreal
character similar to Scandinavian coastal waters and the North Sea.
2. Annual primary production rates in Scottish coastal waters generally are
similar to rates in pristine Norwegian fjords, but lower than in nutrient enriched
Kattegat and Dutch Wadden Sea. Phytoplankton abundance and primary
production in sea lochs are projected to increase with modest nutrient
enrichment without changes in baseline phytoplankton structure and
dynamics. Irradiance may be more limiting than nutrients In some sea lochs.
3. An indigenous harmful algal flora occurs in Scottish coastal waters comprising
species that cause shellfish-borne illnesses in humans and other animals,
including Paralytic Shellfish Poisoning (PSP), Diarrhetic Shellfish Poisoning
(DSP) and Amnesic Shellfish Poisoning (ASP); ichthyotoxic species also
occur. This flora, also widely distributed in European coastal waters, includes
species from the dinoflagellate genera Alexandrium (PSP) and Dinophysis
(DSP), and the diatom genus Pseudo-nitzschia (ASP). Harmful algal species
occurrences and blooms (HABs) are not new phenomena in European waters
induced by initiation of aquaculture. A PSP outbreak was recorded in 1827
after ingestion of mussels harvested from the Firth of Forth; DSP illnesses
following shellfish consumption were reported from Norway in the early 1900s.
4. PSP, DSP and ASP outbreaks in Scottish waters parallel similar occurrences
elsewhere in European and global coastal waters. There is no reliable
evidence that novel HAB species have newly expanded into Scottish coastal
waters, nor that blooms of the indigenous HAB flora have increased in
frequency.
5. The HAB flora and their toxic events in Scottish and other European coastal
waters are generally similar, with some notable differences. Arrayed along a
continuum from high to low intensity, regional European and UK coastal
waters exhibit a north-south gradient in ASP intensity and an east - west
gradient in harmful blooms of haptophytes and raphidophytes.
6. Scottish coastal waters are unique relative to other European and global
coastal waters in the widespread persistence in ASP toxicity of the scallop
Pecten maximus. This distinction is not because of species differences. ASP
toxicity results from the toxin domoic acid (DA) produced by diatom species in
the genus Pseudo-nitzschia. The nine Pseudo-nitzschia species found in
Scottish waters are indigenous, cosmopolitan and commonly bloom in
European and global coastal waters.
7. Bloom behavior of Pseudo-nitzschia in Scottish waters is similar to that in
other geographical waters, rather than locally unique. Pseudo-nitzschia
blooms are common, generally multispecific, probably polyclonal, attain great
abundance, can be prolonged (weeks to months), and occur in diverse
habitats ranging from relatively pristine (i.e free of anthropogenic modification)
offshore waters to nutrient enriched nearshore waters. In the habitats where
1
Pseudo-nitzschia species normally bloom, fish farms are not a factor, and
therefore Pseudo-nitzschia blooms are not dependent on nutrient wastes
excreted at fish farms.
8. A complex combination of habitat-cellular-population events and conditions
regulates the synthesis of DA and its flux to filter feeding bivalves. This
negates efforts to link the Scottish ASP "epidemic" to a specific habitat
stimulus. Synthesis of DA is the most complex of the phycotoxins produced by
harmful algae; it is under multifactorial environmental control. Four essential
conditions are required for DA production: irradiance, a supply of NO and Fe,
3
and nutritional stress from phosphorus or silica limitation. DA synthesis
usually begins when the population becomes senescent; nutrient limitation,
not enrichment triggers DA production. Most of the DA produced is secreted
rather than retained by Pseudo-nitzschia cells which influences DA vectoring
pathways to shellfish. Bivalve ingestion and accumulation of extracellular DA
requires its prior assimilation by bacteria which are then grazed by
heterotrophic flagellates for vectoring to the shellfish. It is unknown how, and
if, this vectoring occurs vs. direct filtration of bacteria. The relative importance
of direct ingestion of DA present in Pseudo-nitzschia cells vs. the extracellular
pool in contributing to shellfish ASP toxicity is also unknown. Notwithstanding
uncertainty over the pelagic to benthic vectoring pathways of DA, ASP
contamination of the Scottish shellfish grounds most likely results from a
combination of direct transfer of DA from Pseudo-nitzschia to the shellfish,
and indirectly via microbial loop processes.
9. The complex regulation of DA synthesis, and the ecophysiology and bloom
behaviour of Pseudo-nitzschia species do not support the view that fish farm
nutrient wastes have stimulated their blooms leading to ASP toxicity of
shellfish in Scottish waters. DA synthesis is a stress response; fish do not
excrete NO , the form of inorganic nitrogen required for DA synthesis. Fish
3
excrete NH , whereas the NO ("new N") required for synthesis of DA is
4 3
supplied by physical oceanographic processes. Pseudo-nitzschia species
appear to be more sensitive to elevated NH concentrations than other
4
diatoms. Experiments suggest that Pseudo-nitzschia species are vulnerable
to, and can be inhibited by the elevated NH concentrations found at fish farm
4
sites. The nitrogenous nutrition of Pseudo-nitzschia species does not conform
therefore to the type of nitrogenous wastes discharged at fish farms.
10. The most compelling conclusion is that the ASP outbreak on the Scottish
commercial scallop grounds is the result of natural causes, rather than due to
anthropogenic enhancement of Pseudo-nitzschia species, or coupled to
nutrients and waste products excreted by fish farms. Slow DA depuration
rates characterize scallops, and help to explain the high levels, prolonged
retention and persistence of DA far after termination of causative Pseudo-
nitzschia blooms. Prolonged blooms of Pseudo-nitzschia are neither required,
nor are the only source of DA. Chronic exposure of scallops to low Pseudo-
nitzschia population densities, coupled with low depuration rates, also can
lead to the accumulation and prolonged retention of DA.
11. The following studies on Pseudo-nitzschia and ASP are recommended:
2
A. Carry out a quantitative field investigation of Pseudo-
nitzschiapopulation dynamics at selected offshore sites.
Measurements should include species composition, abundance,
vertical distribution, cellular and extracellular DA concentrations,
and relevant physical and chemical variables. There is no
evidence that Pseudo-nitzschia blooms have occurred in the
scallop ground region. The field study recommended should
help to clarify this and the issues raised in Summary Statement
8.
B. Establish the locally occurring Pseudo-nitzschia spp. into
culture; analyze their DA activity, and carry out experiments on
their growth during exposure to different concentrations of fish
farm conditioned water and elutriates of unutilized food pellets.
These experiments will establish the degree of reactivity that the
local pseudo-nitzschioids have to salmonid exudates, to
processed food pellets, and their DA production capacity.
C. Investigate the DA accumulation, retention times and depuration
rates in king scallop, Pecten maximus, in feeding experiments
using local Pseudo-nitzschia species.
D. Investigate whether extracellular DA released by local Pseudo-
nitzschia species is vectored to Pecten maximus.
12. Reports of diarrhetic shellfish poisoning (DSP) in Scottish coastal waters are
rare, unlike in ten other European countries. This regional difference is the
converse of that for ASP. Since the Dinophysis species that produce okadaic
acid, the causative toxin of DSP, are ubiquitous in Scottish waters, local rarity
of DSP is not explained by Dinophysis absence.
13. DSP toxicity is a normal, latent feature of shellfish usually revealed only after
human consumption. The global increase in shellfish cultivation and
consumption, particularly of edible mussels, has heightened reports of DSP
occurrences and awareness of this malady. Thus, the increase in human DSP
illness has a dietary explanation; it is not the result of an altered ecology
favoring Dinophysis blooms and inducing their toxicity.
14. Blooms of Dinophysis differ significantly from other HAB species. Their
4 -1
blooms, which rarely exceed 10 cells L or discolor seawater, are usually
accumulations of slow growing cells physically aggregated by current
movements and transported long distances. DSP intoxication of shellfish is
usually not in response to a locally stimulated bloom, but results from
ingestion of cells produced elsewhere and advected to the growth site.
Shellfish can become toxic when feeding on the persistently low populations
3 -1
(<10 cells L ) that characterize Dinophysis.
15. Nutrient excretion and chemical conditioning of coastal waters at Scottish fish
farm sites are not expected to enhance Dinophysis blooms or DSP outbreaks,
even with further development of that industry, since neither is usually a
habitat stimulated event. Nonetheless, the proposed expansion of shellfish
culture in Scotland most likely will heighten future problems with DSP, and
3
affect the harvesting and marketing of cultured shellfish. This projection is
based on the evidence from elsewhere in Europe, particularly Ireland, and
given the characteristics of Dinophysis and DSP provided in Summary
Statements 13 and 14.
16. The Dinophysis species and oceanographic conditions contributing to the
significant DSP threat and impairment of the Irish shellfish industry occur also
in Scottish waters. The new and unique DSP toxins being reported from Irish
shellfish cultivation sites relative to those in France and Spain, despite the
common harmful Dinophysis species assemblage in European waters, is
further cause for concern.
• It is recommended that Scottish agencies and shellfish culturists
should evaluate the sources, bloom behaviour and impact of
Dinophysis and DSP on shellfish cultivation in Ireland and its
coastal waters for use as a model of potential impacts in Scottish
waters, and to develop proactive management strategies.
17. The following initiatives are recommended given the expected expansion of
shellfish culture in Scotland:
• Upgrade the DSP monitoring program, including analyses of the
toxin profiles of contaminated shellfish.
• Since advection of Dinophysis from offshore frontal zone growth
sites into coastal shellfish cultivation sites is the primary source of
DSP contamination in Ireland, a similar program of oceanographic
investigation of Scottish offshore and coastal waters, including the
Minch, should be initiated to document the occurrences and
behavior of frontal systems in response to physical forcing (winds,
etc.), and to quantify the distribution, abundance and species
composition of the Dinophysis population and other phytoplankton
components within these watermasses [see also Summary
Statement 11C].
• The use of remote sensing surveillance in this investigation is
encouraged.
• Monitor the Dinophysis populations at selected, representative
shellfish cultivation sites, with particular attention given to their
vertical distribution and advective incursions into the growth area.
Such surveillance has proved to be important at Spanish shellfish
growth sites in predicting DSP events.
18. The incidence of paralytic shellfish poisoning (PSP) blooms in Scottish coastal
waters is relatively low, similar to European coastal waters generally.
Regionally intense blooms occurred in 1969 and 1990; otherwise, toxin levels
exceeding threshold safety levels and mandating closure of shellfish grounds
have been infrequent and brief in duration. The frequency of PSP events in
the Orkney Isles may have increased in recent decades, but the evidence is
equivocal and the causative species uncertain. This region is potentially a
PSP "hot spot".
4
19. Three of the ten species of the dinoflagellate genus Alexandrium known to
produce paralytic shellfish toxins have been recorded in Scottish coastal
waters. Alexandrium tamarense had been considered the only one present
until recent reports of isolated occurrences of Alexandrium minutum and
Alexandrium ostenfeldii in Orkney waters. The long-term, episodic bloom
patterns of Alexandrium tamarense, a species widely distributed in Scottish
waters, are consistent with its behavior elsewhere. Its occasional large scale,
regional blooms appear to be related more to climate - oceanographic
interactions than to anthropogenic stimulation; this includes fish farm
operations.
20. There appears to be a north-south gradient in PSP toxicity of Alexandrium
tamarense populations worthy of further examination: northern populations
(Scotland, Faroe Islands) are toxic; southern populations (England, Ireland)
are not. A large "seed bank" of Alexandrium tamarense occurs in the Firth of
Forth region, from which excysted cells are advected southwards along the
coast of England. It is unknown whether these seeded cells initially are toxic,
or non-toxic, and whether the population retains, loses or gains toxicity during
advection. To help establish this, and whether there are potentially "safe" PSP
sites for shellfish cultivation where the Alexandrium tamarense population is
benign, it is recommended that:
• the toxicity of Alexandrium tamarense should be determined for
strains isolated into culture from representative sites in Scottish
coastal waters, including the Orkneys and Shetlands, along the
apparent N - S toxicity gradient.
• the ichthyotoxic potential of local strains of Alexandrium tamarense
from along the N - S gradient should be evaluated experimentally
given the unusual dieoff of farmed salmon reported from the Faroe
Islands during an Alexandrium tamarense bloom.
• the PSP toxin profiles of Scottish strains of Alexandrium tamarense
should be determined given that these profiles are also unresolved
for Alexandrium tamarense populations in the coastal waters from
Norway to Portugal, and the debate over whether European
populations are toxic.
21. Gymnodinium catenatum, which replaces Alexandrium tamarense as the
primary PSP species in Iberian waters, has been reported from the ballast
water of ships calling at Scottish ports. The potential recruitment of this highly
toxic species into the indigenous HAB flora can not be excluded. Novel and
persistent blooms of this species in Tasmanian waters, attributed to ballast
water introductions, have adversely affected shellfish cultivation.
22. The recent report that Alexandrium minutum, a PSP producing and
ichthyotoxic species, occurs in Orkney Isle waters requires confirmation.
Alexandrium minutum appears to be spreading within European coastal
waters, with a predilection to bloom in nutrient enriched water. There is no
evidence that this species poses a threat, either to wild or farmed fish and
shellfish stocks in Scottish waters, but investigators are alerted to its potential
blooms. Invasive species often exhibit recurrent, intense blooms for an
5
Description:An indigenous harmful algal flora occurs in Scottish coastal waters .. ecology and impacts of the Chrysochromulina and Prymnesium blooms in .. queen scallop (Chlamys opercularis), but at much lower levels (maximum = 48 µg g.
