Review of Harmful Algal Blooms in Scottish coastal waters.

125 Pages·2002·0.3 MB·English

by  Paul Tett

Review of Harmful Algal Blooms in Scottish coastal
waters.
report to SEPA
by
Paul Tett & Vivien Edwards
School of Life Sciences,
Napier University, Edinburgh EH10 5DT.
June 2002
Summary
(by chapter)
1. The first chapter outlines the problem and the approach taken in this report, which deals
with the existence, causes, and effects, of harmful algal blooms and eutrophication in Scottish
coastal waters and estuaries.
2. Chapter 2 provides an introduction to phytoplankton in general, hydrography of Scottish
waters, and phytoplankton seasonal cycles.
3. Potentially harmful algae in Scottish waters are listed in this chapter, and the term
'Harmful Algal Bloom' (HAB) is defined to include effects of toxic organisms at low
concentrations as well as when abundant. The history of Scottish HABs in the latter part of the
20th century is reviewed. The greatest recent concern relates to 'shellfish-vectored toxins',
produced by algae and concentrated and stored especially in mussels or scallops. When
sufficiently intoxicated shellfish are eaten by humans, the toxins cause Amnesic Shellfish
Poisoning (ASP), Diarrhetic Shellfish Poisoning (DSP) or Paralytic Shellfish Poisoning (PSP).
The cause of ASP is domoic acid, produced by diatoms of the genus Pseudo-nitzschia.
Monitoring of shellfish for this toxin became regular in 1999 and soon detected domoic acid at
levels which resulted in widespread and long-lasting closure of scallop fisheries. The cause of
DSP is okadaic acid, produced mainly by dinoflagellates of the genus Dinophysis. Systematic
monitoring of shellfish for okadaic acid began in 1997 and has resulted in occasional local bans
on the harvesting of farmed and wild mussels and oysters. PSP is caused by saxitoxin, made
by dinoflagellates of the genus Alexandrium. Following an outbreak of PSP in 1968, regular
monitoring of Scottish east coast shellfish has detected potentially harmful levels of the toxin at
some sites in many years. Extension of the monitoring to the other coasts of the mainland, and
to the islands, following the detection of high levels of saxitoxin in west coast shellfish in 1990,
showed that the toxin was widespread in May and June, but regularly present in significant
amounts only in Orkney. Again, bans on harvesting has prevented any known human cases of
PSP. Circa 1980, the main concern was toxic Red Tides of Gyrodinium-like dinoflagellates,
and blooms of several toxic small flagellates. These may have become less common, but
remain a hazard to fish farms. Colonial flagellates, especially Phaeocystis sp., cause foam in
some estuaries and Forths.
4. Eutrophication is, according to the C.E.C., "the enrichment of water by nutrients
especially compounds of Nitrogen and Phosphorus, causing an accelerated growth of algae and
higher forms of plant life to produce an undesirable disturbance to the balance of organisms and
the quality of the water concerned." The Comprehensive Studies Task Team (CSTT) defined
hypernutrification as occurring when winter DAIN exceeds 12 m M in the presence of at least
0.2 m M DAIP, and eutrophication as occurring when chlorophyll exceeds 10 mg m-3 in
Harmful Algal Blooms page ii printed August 27, 2002
summer. Appendix 1 argues for the use of these standards to indicate the occurrence of
eutrophic conditions only, reserving the word eutrophication for cases of human-induced
change in trophic state with harmful consequences. Some Scottish coastal waters are clearly
hypernutrified, mainly by riverine nutrients. However, lack of light, or losses due to dilution,
sinking or grazing, prevents the occurrence of eutrophic conditions (and of eutrophication) in
many cases. The most effective controls are those exerted by protozoan and mesozooplankton
consumers of micro-algae. HABs may develop when these controls are absent or weak.
5. Prediction of the bulk effect of anthropogenic nutrients on phytoplankton in small
water-bodies - those of the size of a sea-loch basin - relies on calculating the equilibrium
concentration enhancement (ECE) of nutrients. The procedure used by Fisheries Research
Service (FRS) then compares this with concentrations of total nutrients at a reference site (Loch
Linnhe). The zone B procedure of the CSTT considers the potential for conversion of the ECE
plus background nutrients into phytoplankton. The reliability of this conversion is improved by
results from a recent SNIFFER-funded study (summarised in Appendix 2) . An unresolved
issue is how to take account of the dissolved organic nutrients naturally present in seawater.
The ECE procedure can also be applied to larger water bodies, such as the Minch,
corresponding to CSTT's zone C, and allows apportioning of observed nutrient concentrations
against known sources. However, better estimates of water flows are needed for this application,
and the box-model approach is too simple for the complex hydrography of zone C regions.
Three-dimensional, coupled physical-biological models are needed.
6. "Undesirable disturbance to the balance of organisms" is most simply understood as a
shift from diatom to flagellate-dominated phytoplankton caused by an increase in the availability
of Nitrogen relative to Silicon. We review theory and observations of nutrient ratios, and
propose that N:Si molar ratios less than 2.5:1 should be considered acceptable in Scottish
waters. An acceptable range of N:P ratios from 7:1 to 30:1 is also proposed, although the
evidence for unacceptable effects outside this range is weak. A preliminary analysis suggests
that no Scottish salt waters are outside the N:P limits, whereas the N:Si limit may be exceeded in
some of the most nutrient-enriched sea-lochs, especially in the waters of the Northern isles
where nitrate is naturally abundant. However, many other factors contribute to maintaining the
balance of species. These include physical conditions, grazing, and the success and survival
strategies of individual species. These factors are reviewed, and some of their effects are
demonstrated with field data and model results. It is tentatively concluded that those algae
associated with eutrophic conditions, Red Tides, and substantial blooms (Gyrodinium,
Phaeocystis, and toxic flagellates) may be stimulated by nutrients, but that suitable physical
conditions and lack of grazing must also be invoked to explain their blooms. In contrast,
explanations for the occurrence of the organisms (Alexandrium, Dinophysis and Pseudo-
nitzschia) causing the shellfish-vectored poisonings, remain speculative.
Harmful Algal Blooms page iii printed August 27, 2002
7. Apparent fluctuations in the toxicity of harmful algae might result from mis-
identification or trivial taxonomic confusion. Real fluctuations might arise from changes in the
mixture of strains occurring in a given algal population as a result of genetic re-assortment
during sexual reproduction at intervals of several years. Additionally, there is laboratory
evidence that physiological stress, in particular severe depletion of one nutrient relative to others,
increases cellular toxin content. Fish-farm perturbation of N:P ratios in Scottish waters is
insufficient to cause such stress, but disturbances to N:Si ratios might play a part. Correlations
should be sought amongst data on algal abundance and shellfish toxicity obtained during the
FRS monitoring programme.
8. In order to examine the impact of nutrient enrichment on the balance of phytoplankton
in Scottish waters, we compare a pristine site, Loch Creran between 1972 and 1982, with Loch
Striven circa 1980 and subsequently. Striven was and remains enriched with nutrients
associated with freshwater from the Clyde and other rivers. Creran, although productive and
containing populations of Alexandrium, Dinophysis and Pseudo-nitzschia species, was not
eutrophic and did not experience HABs. Striven is eutrophic as defined in Appendix 1, and has
had several harmful blooms. In addition, Striven in 1980 contained small to medium-sized
populations of Dinophysis and Pseudo-nitzschia species. Although okadaic acid was
subsequently found during a Dinophysis bloom in an adjacent loch, only low levels of domoic
acid and saxitoxin have been recorded from the Firth of Clyde, into which Striven drains. The
comparison between Creran and Striven suggests that increased nutrient inputs increase the size
of algal blooms and the probability of harmful effects from algae such as Gyrodinium
aureolum and 'flagellate X'. It also shows that hydrographic and other factors are important in
controlling the balance of organisms. Taking account of Firth of Clyde as well as Striven data,
suggests that nutrient enrichment does not automatically lead to greater shellfish intoxication.
There should be (a) further studies of phytoplankton in some lochs originally studied before
1984 and now the site of major fish-farms, and (b) a few key sites chosen to bring together
long-term programmes of monitoring of nutrients, phytoplankton and algal toxins.
Appendix 1. The CEC definition of 'eutrophication' in the Urban Waste Water Treatment
Directive is best understood as 'the process of anthropogenic nutrient enrichment leading to
enhanced biomass and production and consequentially to undesirable effects'. 'Eutrophic'
should be kept as a value-free label for a state that might be natural and can be objectively
defined by measurements of nutrients, biomass or production. The word is so used in this
document, without necessary implication of undesirable effects.
Appendix 2. This summarises SNIFFER-funded work on the value of the yield of
phytoplankton chlorophyll from nutrient-nitrogen.
Harmful Algal Blooms page iv printed August 27, 2002
Table of contents
1. Introduction........................................................................................................1
1.1. General................................................................................................1
1.2. Sources and use of evidence................................................................2
1.3. This report...........................................................................................4
2. Phytoplankton (in general) and hydrography.....................................................6
2.1. Phytoplankton.....................................................................................6
2.2.Hydrography relevant to HABs in Scottish coastal waters....................8
2.3. Phytoplankton abundance and seasonality.........................................10
3. Harmful Algae and 'Harmful Algal Blooms' in Scotland..................................13
3.1. Harmful phytoplankters and harmful blooms....................................13
3.2. Before 1985.......................................................................................16
3.3. From 1990.........................................................................................21
3.4. Discussion and conclusions..............................................................27
4. Eutrophication..................................................................................................31
4.1. Introduction.......................................................................................31
4.2. Nutrients............................................................................................33
4.3 Hypernutrification and eutrophication................................................38
5. Predicting the bulk effect of nutrients on phytoplankton..................................42
5.1. Introduction.......................................................................................42
5.2. Equilibrium nutrient enhancement and hypernutrification..................46
5.3. Eutrophication in zone B...................................................................48
5.4. Zone C...............................................................................................49
5.5. Discussion and conclusions..............................................................52
6. The balance of organisms.................................................................................54
6.1. Introduction.......................................................................................54
6.2. Population growth rate.......................................................................55
6.3. Models for the balance of organisms.................................................57
6.4. Nutrient ratios and the balance of organisms.....................................60
6.5. Nutrient ratios in Scottish waters.......................................................62
6.6. The life styles of harmful algae..........................................................66
7. The toxicity of a given organism......................................................................70
7.1. Introduction.......................................................................................70
7.2. Toxicity and Taxonomy.....................................................................72
7.3. Toxicity, strains, and sexual reproduction..........................................76
7.4. Toxicity and physiology....................................................................78
7.5. Discussion and conclusions..............................................................80
8. Reference sites, eutrophication and HABs........................................................82
8.1. Introduction.......................................................................................82
8.2. Loch Creran and the Firth of Lorne...................................................82
8.3. Loch Striven and the Firth of Clyde...................................................87
8.4. Discussion and conclusion................................................................92
References............................................................................................................94
Appendix 1: The definition of eutrophication.....................................................108
Appendix 2 : The yield of chlorophyll from DAIN............................................116
Harmful Algal Blooms page v printed August 27, 2002
1. Introduction
1.1. General
Harmful marine micro-organisms have been a concern in United Kingdom waters since the first
reliable record of paralytic shellfish poisoning (PSP) in 1828 (Ayres, 1975). PSP is now
known to be caused by substances made by a planktonic micro-organism, the dinoflagellate
Alexandrium tamarense. The poisons are concentrated within plankton-feeding shellfish, such
as mussels or oysters. Humans who eat intoxicated shellfish suffer headaches, nausea,
diarrhoea, and, in extreme cases, respiratory paralysis and death. An outbreak of PSP in 1968
hospitalised scores of people in north-east England and south-east Scotland (Ingham et al.,
1968) and killed many sea-birds (Coulson et al., 1968). Thereafter, the monitoring of shellfish
toxicity by the public authorities, and the closure of shellfisheries when poison levels were
potentially harmful, has prevented further harm to human health, although the toxin-producing
dinoflagellate remains endemic in Scottish waters.
Other types of marine planktonic micro-organism also do harm. For example,
Gyrodinium mikimotoi, called here Gyrodinium aureolum, is a poisonous dinoflagellate that can
become so abundant as to make the sea look reddish-brown, a phenomenon known as a
red tide. Such a red tide killed farmed salmon in Argyll in 1980 (Jones et al., 1982). Problems
such as those due to Alexandrium tamarense and Gyrodinium aureolum seemed to be
becoming more common during the second half of the twentieth century, and thus the
International Commission for the Exploration of the Seas (ICES ) convened a meeting in 1984
to consider increasing reports of 'exceptional blooms' (Parker, 1987). These phenomena
included incidents of PSP, red tides, fish kills, and nuisances such as algal-generated foam
washed onto bathing beaches. Two questions were discussed then, and since: has there been an
increase in 'exceptional blooms', and, if so, what are the causes?
If there has been an increase, the most obvious cause is eutrophication, the harmful
result of over-fertilisation of waters. Other possible causes include climate change, the effects
of fisheries, toxic pollution, manipulation of river flows, and global transfers of harmful species
(Tett & Mills, 1991; Cloern, 1996). Alternatively, it may be that the real increase is not in the
frequency of the exceptional blooms themselves, but merely in reports of them. The sea and
marine products are more intensively monitored now than they were several decades ago. For
example, the programme of routine sampling of U.K. shellfish, begun after the 1968 PSP
outbreak, only began to include regular and extensive measurements of domoic acid, the cause
of Amnesic Shellfish Poisoning (ASP), in the late 1990s. Within two years, the discovery of
potential harmful levels of domoic acid in scallops from many sites between Islay and Orkney,
led to widespread closure of the scallop fishery (Gallacher et al., in press).
Harmful Algal Blooms page 1 printed August 27, 2002
Domoic acid originates in diatoms of the genus Pseudo-nitzschia, and these micro-
organisms, like dinoflagellates of the genera Alexandrium and Gyrodinium, are members of the
phytoplankton, the community of tiny drifting light-harvesting creatures sometimes called
algae but also including photosynthetic bacteria. As well as light, phytoplankton growth
requires compounds of nitrogen and phosphorus, called nutrients, and the addition of these
nutrients to the sea may stimulate excessive growth: the process of eutrophication. Fin-fish
farms are sources of these nutrients, a typical farm producing waste equivalent to a town the size
of Oban. There is thus concern, exemplified by a public petition to the Scottish Parliament
(Berry, 2000), and a report by the World Wildlife Fund, Scotland (MacGarvin, 2000), that the
growth of fish farming in the waters of northern and western Scotland is leading to widespread
eutrophication and thus increasing frequency and size of blooms which may include toxic
organisms. In addition, changes in the balance of nutrient elements, may have led to changes in
the balance of species in the phytoplankton (Justic et al., 1995; Riegman, 1998), tilting it
towards poisonous forms or causing greater toxicity in existing, potentially toxic, species
(Maestrini & Granéli, 1991).
Nutrients are naturally present in sea-water. Thus, in order to deal with this concern
about the effects of fish-farm waste, it is necessary to consider the extent to which its nutrients
add to the natural concentrations. In addition, there are other human-influenced sources of
nutrients, including 'urban waste water' (or sewage), acid rain, and the leaching of nitrates and
phosphates from forests and farms. Even if it turns out that increases in fish-farm, or other
human-made, nutrients, are not the main cause of shellfish poisoning, eutrophication caused by
these nutrients remains a matter for concern in some Scottish coastal waters. Its potential
consequences also include water foaming, red tides, fish kills, and excessive consumption of
oxygen in the deep waters of sea-lochs.
The aim of this report is to review evidence concerning the existence, causes, and effects,
of harmful algal blooms and eutrophication in Scottish estuaries, sea-lochs, Firths, and coastal
waters. Although SEPA's writ is restricted to near-shore waters, there are no watertight
compartments in the sea, and the scope of this review will therefore extend in some cases to the
edge of the Scottish continental shelf north and west of the Hebrides.
1.2. Sources and use of evidence
Scottish coastal waters are geographically and hydrographically complex. Populations of
planktonic algae undergo large seasonal changes in abundance, and in this complex environment
the seasonal patterns themselves vary according to location and from year to year. In addition,
climate change or anthropogenic impact may produce long-term trends, such as the alleged
increase in toxic blooms due to nutrients from salmon farms. Extracting these trends, and
dealing with spatial and inter-annual variability is difficult, because until recently observations
Harmful Algal Blooms page 2 printed August 27, 2002
were made intermittently, at different sites in different years, using methods that changed during
the years under consideration, and in programmes that had a variety of aims.
These and similar difficulties raise the question of the best way to arrive at conclusions
about patterns and causes of algal blooms. Reaching a verdict during a legal trial involves
interpreting human-made laws in relation to evaluated evidence about specific actions and
consequences. It might be thought that a similar process should be used to determine the true
causes of harmful algal blooms, by interpreting local events in terms of universally-applicable
natural laws. However, as the philosopher, Karl Popper, has demonstrated, refutation of
incorrect explanations is a more reliable strategy than that of searching directly for the truth -
which is often elusive. Modern scientific method uses this strategy of 'conjecture and refutation'
to approximate natural laws by sets of as-yet-unrefuted hypotheses. The scientific literature
contains accounts of these hypotheses and their tests, published after validation of methodology
by peer-review - i.e. after checking by other scientists. Such peer-reviewed articles are called
'papers' and represent a scientific gold-standard.
Our strategy for applying this knowledge to explain events in Scottish waters, is to
compare locally-specific predictions of general theory with generalisations made inductively
from local observations. This allows us to eliminate local explanations that are incompatible
with theory (Box 1.1*). The strategy does not prove the surviving explanations to be true, but
does at least focus attention on issues requiring further attention, and on cases in which it may
be necessary to invoke the precautionary principle.
The issues involved in reaching a verdict on the basis of scientific knowledge are thus: (i)
the adequacy of existing theory; (ii) the reliability of the deductions involved in an application;
and (iii) the quality and quantity of local data.
Deduction is a logical process, and should not be controversial. However, in some of the
instances discussed here, the application of theory requires (a) a choice amongst alternative,
incompatible, but as yet unrefuted hypotheses, (b) the use of calculation schemes that assume
numerical values for certain environmental or biological properties, and (c) local data, which may
be imprecise, for other environmental or biological properties. In such cases, loosely described
as the use of 'models', it is desirable to demonstrate the impact of alternative choices,
assumptions, and uncertainties, on the final deduction. We use an abridged version of such
'sensitivity analysis' in crucial parts of this report.
Only some of the relevant local data have been published in the scientific literature, a part
of the part that was collected during projects aimed at developing or testing generalising
hypotheses - i.e. during scientific research. Other data were got during monitoring, a process
aimed at measuring compliance with a standard rather than generating new knowledge as such.
* Box 1.1. Assessing evidence about harmful blooms in Scotland.
Harmful Algal Blooms page 3 printed August 27, 2002
Although none of the data are secret, many are difficult to find, and most need to be interpreted.
It would be a large work to do this adequately for all the sources of information on Scottish
phytoplankton. We have instead made a sampling of the 'grey literature', which consists of
publicly-available documents of limited distribution that have (typically) not been through the
peer-review process. We refer to them here as 'reports', in contrast to 'papers' in the referee'd
literature.
1.3. This report
This report aims to describe phytoplankton and hydrographic conditions in Scottish coastal
waters and to list the algae whose blooms can have harmful consequences here. We then review
the evidence concerning changes in the frequency and distribution of harmful algal blooms, and
go on to consider eutrophication, the process of enrichment of waters with excess nitrogen and
phosphorus that in some cases leads to excess production of organic matter, degradation of
water quality and changes in the balance of organisms. We consider whether harmful algal
blooms, and their toxicity, might be a consequence of nutrient enrichment - i.e. a part of
eutrophication. Finally, we make a comparison between phytoplankton ecology in two coastal
waters that have been intensively studied. One (the Firth of Lorne and its sea-lochs, especially
Creran) was in 1970-84 in a pristine state; the other (the Firth of Clyde and its sea-lochs,
especially Striven) is substantially nutrient-enriched by drainage from the cities and farmlands
of western central Scotland. An appendix deals with the definition of eutrophication, and
distinguishes between the terms eutrophic and eutrophication. The former is a simple label for
any ecosystem that is rich in plant nutrients and the production of organic matter, whether from
natural or artificial causes. The latter refers to a process, implicitly human-driven, that augments
the nutrient and productive status of an ecosystem with undesirable consequences.
Work on this report was begun in Autumn 2000, following a decision by SEPA in
March 2000 to seek a technical review of the processes of algal blooms in Scottish coastal
waters in response to nutrient inputs and to changed nutrient ratios. Our brief was (1) to offer a
perspective that could inform application of the precautionary principle in regulating discharges
to coastal waters; and (2) to view any specific instances of algal blooms within a structure of
general understanding and modelling.
The literature survey and compilation of information on harmful algal blooms and
related phenomena was completed by March 2001, leading to a complete draft of this report in
May 2001. We mentioned the importance of peer review for accounts of scientific
investigations. This report has not been formally reviewed in this way, but it has been read by a
number of academic colleagues in universities and research institutes as well as within SEPA.
The process of collecting comments and responding to them, as well as clarifying the
expression of a complex mass of information, has taken a year. We are grateful to all those who
Harmful Algal Blooms page 4 printed August 27, 2002
commented or provided us with information, while accepting responsibility ourselves for all that
is written here.
Harmful Algal Blooms page 5 printed August 27, 2002