Chapter 31; Ecosystem Effects Work Group
Report
Workgroup Co-Chairs:
John W, Fournie, Elizabeth D, Hilborn
Workgroup Members':
Geoffrey A, Codd, Michael Coveney, Juli Dyble, Karl Havens, Bas W.
Ibelings, Jan Landsberg, Wayne Li taker
Authors:
Bas W, Ibelings, Karl Havens, Geoffrey A. Codd, Juli Dyble, Jan Lands-
berg, Michael Coveney, John W. Fournie, Elizabeth D. Hilborn
Introduction
Harmful cyanobaclerial blooms represent one of the most serious ecologi-
cal stressors in lakes, rivers, estuaries and marine environments. When
there are persistent or frequent blooms with high biomass of cyanobacle-
rial cells, colonies or filaments in the water, a wide range of impacts on the
ecosystem may occur. These are well established in the scientific literature
and are summarized in Paerl et al. (2001). Blooms may shade the water
and thereby inhibit growth of other primary producers including phyto-
plankton, benthic algae and vascular plants and may elevate pH, particu-
larly in poorly buffered waters. High population densities of large cyano-
bacleria interfere with food collection by filter-feeding zooplankton. The
senescence and subsequent microbial decomposition of blooms may im-
pact benthic macro-invertebrate community structure, as well as Fish and
other biota, due to increased organic loading and resulting anoxia of sedi-
ments, accumulation of NH4 in the water and accompanying increases in
pH. Blooms of toxic cyanobacteria have been implicated in mass mortali-
ties of birds and Fish (e.g., Matsunaga et al. 1999; Rodger et al. 1994), but
1 See workgroup member affiliations in Invited Participants section.
H. Kenneth Hudnell (Ed.): Proceedings of the Interagency, International
Symposium on Cyanobaclerial Harmful Algal Blooms
Advances in Experimental Medicine & Biology, [pgs.] (2006)
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2 Fournie J et al.
the importance of cyanotoxins relative to the other stressors thai accom-
pany blooms remains unknown. With persistent blooms, there are substan-
tial declines in biodiversity at all levels ranging from phytoplankton and
zooplankton to birds. Changes in nutrient cycling and disruptions of car-
bon and energy How in pelagic and benthic food webs are observed (Paerl
et al 1998). Where blooms become severe in shallow lakes, a positive
feedback loop develops through various biological mechanisms related to
the presence of cyanobacteria and fish that maintains a turbid water state
(Scheffer and Carpenter 2003).
A major uncertainty regarding the effects of cyanobacterial blooms is
the role that cyanotoxins play in contributing to the various biological re-
sponses listed above. There are three reasons for this uncertainty: (a) most
research to examine cyanobacterial bloom effects at the ecosystem level
has focused on factors not associated with toxins but with the mere pres-
ence of cyanobacteria; (b) no experimental studies have been done at the
whole community level to examine effects of blooms in the presence of vs.
absence of cyanotoxins; and (c) experimental studies dealing with
cyanotoxins have largely involved exposure of a single species to a single
toxin under ideal conditions in the laboratory. Studies have not examined
synergistic effects with other natural stressors, nor have they adequately
investigated how multiple toxins of natural and anthropogenic origin might
affect the biota. Thus, laboratory results are not readily transferable to the
field.
The objective of this report is to identify major knowledge gaps regard-
ing the impacts of cyanobacterial blooms on biota in lakes, rivers and estu-
aries from the individual to ecosystem level. The text is organized around
six charges given to the Ecologic Effects Working Group. All of the identi-
fied research components are considered by the Working Group to be a
high priority. Careful consideration was given to information already
available in the primary literature in determining research needs to avoid
duplicity of effort. A simple conceptual model illustrates the interrelation-
ship among the research and modeling work discussed in the subsequent
sections of this paper (Fig. 1).
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Chapter 31; Ecosystem Effects Work Group Report 3
( HAB )
Toxins
(Other Effects)
Individual and
Population Effects
Cyanotoxin
Exposure
Single vs. multiple or
sequential town
exposures
Presence of other
bioactive compounds
Effects of chronic vs.
acute and episodic
exposures
Exposure with other
stressors (low DO, NH4,
etc.)
Effects on physiology,
pathology, genotowcity,
v behavior, reproduction
Communify^^X
and Ecosystem \
Responses
Dependent on direct
and indirect effects of
toxins
Dependent on the
many othsr impacts of
blooms
Fig. 1. Conceptual model of the ecosystem effects of cyanobacteria and cyanoioxins
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4 Fournie J et al.
There is a logical order in which the research topics noted here might be
addressed, starting with the species level work and then scaling up to the
community level with environmentally-relevant experiments based on
findings from previous work. Development of community bioaccumulation
models may occur in concert with controlled and observational research,
so that at any given time, modeling tools may become available for appli-
cation with clearly identified levels of uncertainty and defined boundaries
of applicability.
Charge 1
Identify research needed to quantify effects of cyanotoxins un-
der environmentally relevant conditions.
To understand the effects of cyanotoxins on aquatic biota and ecosystems,
it is critical that environmentally-relevant exposure conditions be identi-
fied and evaluated. Almost all experimental studies of exposure have been
of single species exposed to individual cyanotoxins under optimal condi-
tions (see Ibelings and Havens, this issue for an overview). In addition,
there are a limited number of studies that have assessed the distribution of
cyanotoxins in lake food webs (Kotak el al. 1996; Ibelings et al. 2005).
These studies have furthered our understanding of potential ecological ef-
fects, but field studies alone are insufficient to identify associations be-
tween exposures and ecological effects during periods when cyanobacterial
blooms predominate in aquatic communities.
It is well established in the lexicological literature that stressors may
have antagonistic, additive or synergistic effects (Taylor et al. 2005).
Hence there is a need for studies that determine how exposure to cyanotox-
ins alone or in combination with other physiologically stressful conditions
(e.g., low dissolved oxygen, high ammonia (NH,t), high pH, poor food
quality, high and low temperature, salinity, etc.) affect the fitness of
aquatic biota. Often these sub-optimal or stressful environmental condi-
tions coincide with the presence of cyanotoxins in the water, and the rela-
tive contribution of each exposure is poorly understood. Bury et al. (1995)
demonstrated that NH4, like dissolved microcystin-LR, impeded fish
growth. Additionally, interactions may occur between different classes of
the cyanotoxins themselves. Indeed, lipopolysaccharide endotoxins can
inhibit glutathione 5-transferases in vivo, thereby reducing the capacity of
glutathione S-transferases to detoxify microcystins (Best et al. 2002).
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Chapter 31: Ecosystem Effects Work Group Report 5
Most controlled experiments have examined the biotic effects of micro-
cystin-LR, and to a lesser extent nodularin, with relatively few studies
looking at the effects of other cyanotoxins (Table 1). Although some
cyanobacteria produce saxiloxins, the ecological effects of these toxins
have been studied primarily in marine systems where they are produced by
dinoflagellates (Landsberg 2002), Toxins that have been less frequently
studied are cylindrospermopsin and its derivatives, and lyngbyatoxins.
Given the likelihood that these toxins are present in US waters (Carmi-
chael et al. 1997; Burgess 2001), their effects must be quantified if we are
to make predictions about the ecological effects of toxic cyanobactedal
blooms with a reasonable level of certainty.
Table 1. Number of peer reviewed papers on ecological effects of cyanotoxins by
class of toxins and group of aquatic organisms. Results from October 2005 search
(key words: toxin plus organism as listed in the column head) of ISl Web of
Knowledge (Thomson Scientific and Healthcare, Stamford, Connecticut).
Class of toxins
Znoplankton
Bivalves
Fish
Waterfowl
Microcystin
73
38
87
13
Nodularin
17
17
16
2
Anatoxin-a and a(s)
11
0
7
6
Cylindrospermopsin
5
2
7
0
Lyngbyatoxin
5
1
9
0
Microviridin
4
0
0
0
Saxitoxin (freshwater)
2
2
6
0
It is becoming increasingly clear that the numerous studies of micro-
cystin-LR may not be representative of the complexities of the interactions
between other cyanotoxins, cyanobacterial blooms, and other biota. Com-
plexity arises because: (a) other microcystin variants can be abundant and
may be ecologically more relevant, such as the less toxic microcystin-RR
which may be taken up preferentially into biota (Xie et al. 2005); (b)
cyanotoxins other than microcystins occur widely and have documented
adverse ecological effects, such as the association between anatoxin-a(s),
anatoxin-a and mass avian mortality events (Henriksen et al. 1997;
Krienitz et al. 2003); (c) there is an array of potentially harmful bioactive
compounds produced by cyanobacteria which have not been well-studied.
For example, microviridin-J has detrimental effects on molting in Daph-
nia, but its effects on other biota are not well understood (Rohrlack et aJ.
2004). There have been some examples of the toxicity of crude cell-
extracts exceeding the expected toxicity of the component cyanotoxins,
suggesting that unidentified compounds or synergistic effects are associ-
ated with observed toxicity (Ltirling 2003).
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6 Fournie J et al.
It also is critical that exposure studies use relevant organisms where
possible. For example, there is considerable variation in intraspecies sus-
ceptibility to cyanotoxins among Fish and birds, but only a relatively small
number of species have been studied (Carmichael and Biggs 1978; Fischer
and Dietrich 2000). Few experimental studies have been done using water-
fowl (Carmichael and Biggs 1978). This has largely necessitated the use of
oral toxicity data obtained from the study of other animal groups to esti-
mate the risk of avian toxicity (Krienitz et al. 2003).
Charge 1: Identify research needed to quantify effects of
cyanotoxins under environmentally relevant conditions
Near Term Research Priorities
• Laboratory studies exposing key aquatic biota to cyanotoxins under
simulated natural conditions, including low dissolved oxygen, elevated
pH, elevated ammonia, and other stressors associated with
cyanobacteria growth and senescence,
• Field and/or mcsocosm studies of the ecologic effects of cyanotoxins
under varying environmental conditions.
Charge 2
Identify research needed to quantify the physiological, patho-
logical and behavioral effects of acute, chronic, and episodic ex-
posures to cyanotoxins.
The duration of exposure to cyanobacterial blooms and toxins can range
from days to years, yet most studies have investigated the effects of short-
term exposures. Research is needed on the effects of long-term exposure
and adaptive responses of populations that may employ both existing phe-
nolypic plasticity and adaptive evolution. Although mortality has been ex-
amined as a common endpoint, sub-lethal effects require further study.
With the exception of Daphnia, few studies have examined behavioral re-
sponses and their significance to the affected species. A small number of
studies have demonstrated that fish behavior is affected by exposure to
cyanotoxins in water (Best et al. 2003; Baganz et al. 1998), Further re-
search needs include controlled experiments to examine effects of
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Chapter 31: Ecosystem Effects Work Group Report 7
eyanotoxins and toxin mixtures on: (a) behavior, especially as it relates to
escape from predators and ability to acquire resources; (b) reproduction;
(c) neurologic function, and (d) genotoxieity. Some work has been per-
formed to evaluate the role of enzyme inhibition and oxidative stress on
genotoxieity, however, the relevance of oxidative stress under field condi-
tions is unknown. Inhibition of protein phosphatases is the classic mode of
action of microcystins and nodularins, resulting in hyper-phosphorylation
of cytoskeletai proteins and the disruption of numerous other phosphoryla-
tion-regulated cell processes. Oxidative stress occurs during the detoxifi-
cation process. Detoxification produces glutathione-microcystin conju-
gates, a depletion of the cellular glutathione pool and an imbalance in
reactive oxygen species (Pflugmacher 2004).
The effects of chronic exposure to eyanotoxins are rarely investigated in
aquatic animals, despite their widespread geographic distribution and po-
tential lifelong exposure to toxic cyanobacterial blooms. Some eyanotoxins
have been reported to be tumor promoters, and the risk of tumorigenesis
increases with chronic exposure. Microcystins, nodularins, cylindrosper-
mopsins, aplysiatoxins, debromoaplysiatoxin, and lyngbyatoxin-a have all
been demonstrated to be lumurigenie, but these properties have only been
experimentally demonstrated in small mammals or cell assays (Fujiki et al.
1984; Falconer and Humpage 1996). Recent studies have investigated the
association between tumor-promoting eyanotoxins and an increased preva-
lence of fibropapillomas in seaturtles (Landsberg 2002; Arthur et al. 2005).
It is important to consider individual susceptibility as influenced by fac-
tors including age, disease, nutrition, and gender. Species-specific suscep-
tibilities include those related to differences in detoxification and metabo-
lism of eyanotoxins. More detailed knowledge is needed, both in the field
of toxicodynamics and toxicokinetics among species. There have been a
few sub-chronic exposure studies on the accumulation and depuration of
eyanotoxins in a limited number of animals. This type of research seems to
have focused on bivalves and, to a lesser extent, fish. The bivalve studies
showed a biphasic depuration of rnicrocystin. Fluctuating microcystin con-
centrations during depuration were speculated to be the result of an ongo-
ing process of covalenL binding and release of microcystins (Amorim and
Vasconcelos 1999). Overall much is unknown about the late of cyanobac-
terial cells and eyanotoxins after ingestion, Reports suggest that only a
small percentage of the toxins that are ingested with the food end up in the
blood and organs of the organisms: 2.7 % in Daphnia, and 1.7 % in rain-
bow trout (Rohrlack et at. 2005; Tencalla and Dietrich 1997). There are
barriers to microcystin uptake at various levels. Even if taken up, aquatic
organisms have the capacity for detoxification, which in fish is followed
by rapid excretion via the biliary excretion system. Studies that examine
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8 Foumie J et al.
chronic exposure of biota over ecologically relevant time scales of months
- years have, to our knowledge, not been conducted. In addition, very little
is known about patterns in the accumulation and depuration of cyanotoxins
other than microcystis Ultimately, good quantitative data is required for a
number of well defined endpoints for a range of toxin classes and aquatic
biota (Table 2).
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Chapter 31: Ecosystem Effects Work Group Report 9
Table 2. List of Definitions
Term Definition
Bioaccumulalion:
Bioeoncentration:
Biomagnification;
Biodilution:
Endpoint:
Exposure
Acute;
Chronic:
Subcitronic:
No-Observed-Adverse-
Effect Level (NOAEL):
Lowest Observable Ef-
fect Level (LOEL):
Toxicodynamics:
Toxicokinetics:
The process which causes an increased chemical con-
centration in an aquatic organism compared to the wa-
ter, due to uptake by all exposure routes (Gray 2002).
Uptake directly from the water, and results in the
chemical concentration being greater in an aquatic or-
ganism than in the water (Gray 2002).
Transfer of a chemical from food to an organism, result-
ing in a higher concentration in the organism than in its
diet. The result may be a concentration of the chemical
as it moves up the food chain (Gray 2002).
Decreased toxin levels are observed at each increase in
trophic level in the food web.
An observable or measurable biological event or chemi-
cal concentration (e.g., metabolite concentration in a
target tissue) used as an index of an effect of a chemical
exposure.
Resulting in adverse effects from a single dose or expo-
sure to a substance
Continuous or repeated exposure to a substance over a
long period of time, typically the greater part of the total
life-span in animals or plants
Exposure for period typically involving a time period in
between acute and chronic
¦ The highest dose at which there are no biologically sig-
nificant increases in the frequency or severity of ad-
verse effects between the exposed population and its
appropriate control; some effects may be produced at
this level, but they are not considered adverse or precur-
sors of adverse effects. In comparison, see LOEL.
The lowest dose which produces an observable effect.
The determination and quantification of the sequence of
events at the cellular and molecular levels leading to a
toxic response to an environmental agent.
The determination and quantification of the time course
of absorption, distribution, biotransformation, and ex-
cretion of chemicals.
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10 Fournie J et al.
Charge 2: Identify research needed to quantify the
physiological, pathological and behavioral effects of acute,
chronic, and episodic exposures to cyanotoxins
Near Term Research Priorities
• Investigate the behavioral effects of cyanotoxin exposures
• Investigate sub-lethal effects of chronic exposures of key taxa of
aquatic biota including invertebrates, fish, bivalves and others.
Charge 3
Identify research needed to quantify biological effects of expo-
sure to multiple toxicants
An increasing number of reports describe the co-occurrence of different
cyanotoxins in aquatic systems, and there is an emerging catalogue of bio-
active materials associated with cyanobacteriai blooms. For example, co-
occurrence has been observed for microcystin and anatoxin-a, microcystin
and cyiindrospermopsin, and there is an assumed universal co-occurrence
of lipopolysaccharides with all other known cyanotoxins (Codd et al.
2005). Research on the death of lesser flamingos in Kenya's Rift Valley
lakes demonstrated that both microcystin and anatoxin-a were present in
the cyanobaeteria on which the birds were feeding (Krienitz et al. 2003).
The relative contribution of these cyanotoxins, which differ greatly in their
mode of action, to the mass bird mortalities remains unclear, as is the role
of co-occurring anthropogenic pollutants like heavy metals and organic
pesticides. Thus, research is needed to examine effects of simultaneous and
sequential exposure to multiple toxins (Codd et al. 2005). The Working
Group considers the highest priority for multiple-exposure studies of ef-
fects in US lakes to be the evaluation of the combination of microcystin
and cyiindrospermopsin. Research also is needed to examine effects of
other bio-active compounds, including non-microcystin cyclic peptides
and lipopeptides.
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Chapter 31: Ecosystem Effects Work Group Report 11
Charge 3; Identify research needed to quantify biological
effects of exposure to multiple toxicants
Near Term Research Priorities
• Investigate the effects of simultaneous and sequential exposure to
multiple toxins, particularly the combination of microcystins and
eylinclrospermopsin, and microcystins and anatoxins
Charge 4
Identify research needed to quantify effects of cyanotoxins at
whole community level
Community level effects are a function of: (a) the direct effects of
cyanotoxins; (b) the direct effects of cyanobacteria blooms; (c) the indirect
effects associated with altered competitive and predatory interactions; and
(d) changes in nutrient cycling. Effects may occur in all biota from bacteria
to birds and mammals and are integrally linked with a loss of biodiversity
in aquatic systems. Key research needs include studies involving complete
natural communities and studies with simple food chains to examine the
effects of exposure to toxic vs. non-toxic strains of cyanobacteria.
At this time we do not adequately understand the relative importance of
different uptake routes of toxins from the environment. Exposure to
cyanotoxins can be through direct ingestion of cells, uptake of toxins that
are present in the environment, or by the transfer of toxins through the
food web. Vectorial transport of cyanotoxins has been demonstrated in a
few experiments involving dissolved toxins. Fish may be negatively af-
fected by dissolved toxin uptake through the gills, but other biota are not
very sensitive to the toxins once they are extracellular (Liirling & Van der
Grinten 2003; Zurawell et al 1999). There is little information about the
relative importance of this exposure route vs. exposure by direct ingestion
of toxic cells. In one experiment, pike larvae were exposed to zooplankton
that had accumulated dissolved nodularin. There was a strong inhibition of
larval feeding rate despite the fact that only 0.03 % of the toxin that was
present in the zooplankton was actually taken up by the larvae (Karjalainen
et al. 2005). The remainder of the toxin was either metabolized or ex-
creted. If this is a representative result, vectorial transport of only a small
amount of the cyanotoxin that is produced at the base of the food web may
have significant ecological effects at higher trophic levels. Substantiation
of the relevance of vectorial transport and the effects of different classes of
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12 Fournic J et al.
cyanoloxins throughout the food web is of prime importance to understand
ecological effects of these toxins.
Much research is needed to understand the degree of bioaccumuiation
that occurs in communities. Bioaccumuiation may vary considerably be-
tween species, but this has been studied only with a small number of or-
ganisms. Most bioaccumuiation studies have focused on microcystin. In
future research and modeling, it is critical that we distinguish between bio-
accumuiation, bioconcentration and biomagnification (Table 2). In most
studies, the term bioaccumuiation is used in a loose way, simply meaning
that toxins are present in biota, Ibelings et al. (2005) have argued that bio-
magnification is the most relevant process to study in food webs since
most of the transfer and uptake of cyanotoxins appears to be via food. An
increase in microcystin concentration, as it moves up the food chain was
not found by these authors, and was not expected due to the low octanol-
to-water partition coefficient of microcysiin-LR (De Maagd et al, 1999),
However it is known that the octanol-to-water coefficient varies widely
according to the microcystin variant and correlates with in vivo toxicity to
Tetrahymena (Ward and Codd 1999). Cyanobacterial toxins other than
microcystin may behave very differently, as indicated by the distribution
of the neurotoxin p-N-methylamino-L-alanine (BMAA) in the terrestrial
food web on the island of Guam. Biomagnification of this toxin may have
accounted for the exposure of the indigenous Chamorro people to high
concentrations of BMAA via their consumption of flying foxes (Cox et al.
2003). More knowledge is required on the potential for bioaccumuiation,
bioconcentration and biomagnification of different cyanotoxins and other
cyanobacterial bioactive compounds in the food web.
An important shortcoming of all but a few studies is the absence of data
on covalently-bound microcystin in biota. Microcystins are routinely ex-
tracted using aqueous methanol, but this does not extract quantities of the
methyldehydroalanine-conlaining microcystins which are covalently
bound to protein phosphatases in the cell, Lemieux oxidation does extract
these covalently bound forms. Studies that have compared standard aque-
ous methanol extraction to extraction after Lemieux oxidation have dem-
onstrated that a large part of the total microcystin pool in biota is indeed
covalently bound (Table 3), Most of the literature therefore severely un-
derestimates the concentration of total microcystin (free and bound forms).
Covalent binding of microcystins may reduce the transfer of free, unbound
microcystin along the food chains, and potentially contribute to biodilution
of microcystin (Karjalaincn et al. 2005). A relevant, but as yet unanswered
question, concerns the toxicity and bioavailability of the covalently-bound
microcystins {Ibelings et al. 2005).
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Chapter 31: Ecosystem Effects Work Group Report 13
Table 3. Comparison of standard aqueous methanol extraction and Lemieux oxi-
dation among organisms
Charge 4: Identify research needed to quantify effects of
cyanotoxins at whole community level
Near Term Research Priorities
• Investigate the effects of exposure lo toxic vs. non-toxic strains of
cyanobacteria in natural communities and simple food chains.
• Examine the potential for bioaccumulation, bioconcentration and
biomagnifications of different cyanotoxins and other cyanobacteria!
bioactive compounds in the food web.
• Determine the toxicity and bioavailability of covalently-bound
microcystes.
Charge 5
Identify research needed to determine the relative importance of
the effects of cyanotoxins vs. the effects of cyanobacteria at the
ecosystem level
Cyanobacterial bloom development, maturation and senescence can all re-
sult in adverse environmental conditions that affect biota independent of
the effects of cyanotoxins. Key research questions at the ecosystem level
of inquiry include: (a) how important are the effects of cyanotoxins vs. the
effects of cyanobacteria; (b) does the presence of high concentrations of
cyanotoxins, for instance through interference with zooplankton grazing,
contribute to the stability of the turbid water state in shallow eutrophic
lakes; (c) does the increasing occurrence of cyanotoxins in shallow lakes
Organism
MeOH extraction as
% of Lemieux oxida-
tion
Reference
Dungeness Crab (larvae)
Salmon (liver)
Blue mussel
Zebra mussel
0.01 Williams et al., 1997a
24 Williams el al., 1997a
0.1 Williams et al., 1997b
62 Dionisio Pires et al., 2004
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14 Fournie J et al.
undergoing eutrophication contribute to the shift from the clear to turbid
state? Effects of toxins on benthic communities and benthic processes are
not well understood, yet those processes play a key role in aquatic food
webs and nutrient cycling (Palmer et al. 2000), The relevance of these
processes is demonstrated by the consequences of the invasion by zebra
mussels (Dreissena polymorpha) in the Laurentian Great Lakes of North
America. It has been hypothesized that selective filler feeding by these
mussels has been instrumental in the return of Microcystis blooms to Lake
Erie (Vanderploeg et al. 2001). However, in the Netherlands, Microcystis
is efficiently grazed by Dreissena, resulting in a low concentration of
cyanobacteria in areas where the mussels are abundant (Dionisio-Pires et
al. 2004). This paradox is not fully understood, although emerging expla-
nations include variation in cyanotoxin concentrations of the Microcystis
strains involved and the relevance of nutrient recycling in lakes of widely
varying trophic status (Raikow et al. 2004). The pseudofcces of Dreissena
are rich in cyanobacteria and they may transfer toxins to the benthic food
web, where benthic feeders are potentially exposed to the toxins (Bab-
cock-Jackson et al. 2002), To further address these issues and gain a
deeper understanding of interactions between toxins, cyanobacteria and
other biota at the ecosystem level, we propose research at a high level of
integration, including the use of static and flowing mesocosms under con-
trolled conditions.
Charge 5: Identify research needed to determine the relative
importance of the effects of cyanotoxins vs. the effects of
cyanobacteria at the ecosystem level
Near Term Research Priorities
• Investigate the importance of the effects of cyanotoxins vs.
cyanobacteria at the community level.
• Determine if the presence of high concentrations of cyanotoxins
contributes to the stability of the turbid water state in shallow cutrophic
lakes.
• Determine if the increasing occurrence of cyanotoxins in shallow lakes
undergoing eutrophication contributes to the shift from the clear to
turbid state.
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Chapter 31: Ecosystem Effects Work Group Report 15
Charge 6
Identify how modeling can contribute to a predictive under-
standing of HAB bloom and eyanotoxin effects.
Basic models relating cyanobacterial growth to nutrient inputs and other
environmental conditions are readily available, and their development is
not a priority research area. Various factors including phosphorous, nitro-
gen, iron and light have been studied in the laboratory and are known to
have an effect on eyanotoxin concentrations (Wiedner et al. 2003).
However, there is a need for models that relate environmental conditions
to eyanotoxin types, concentrations and compartmentation (soluble vs. par-
ticulate pools) in blooms and water bodies containing benthic cyanoloxins.
Evidence is emerging that eyanotoxin concentrations increase in direct re-
sponse to exposure to grazers like zooplankton and fish (Jang et al. 2003,
Jang et al. 2004). This would strengthen the idea that cyanobacteria pro-
duce these energetically cosily toxins as a grazer-deterrent, but whether
this is the sole or primary purpose for toxin production is an important
question that demands further research. While many of these factors im-
pacting toxin production have been studied individually, modeling the in-
teractive effects of both the bottom-up and top-down factors could pro-
vide further insight into the potential toxicity of a bloom given a set of
environmental conditions.
Models are needed to describe the fate of cyanoloxins in water, sedi-
ment and food webs. This is not a trivial undertaking since toxins at every
level in the food web are potentially subject to covalent binding, metabo-
lism (detoxification) and excretion, and thus the amount of bioavailable
eyanotoxin that is transferred to the next trophic level is a complex issue.
As noted, modeling can be an ongoing activity, with predictive certainty
and general applicability increasing as ongoing research at the population,
community and ecosystem levels provides additional information for
model parameterization, calibration and verification.
Conclusions
The authors of this report have identified near term priorities for research
on ecological and ecosystem effects of harmful cyanobacterial blooms. Al-
though the negative impact of cyanobacterial blooms on many ecosystems
is well known, the specific contribution of cyanobacterial toxins to the
harmful effects is hard to distinguish. Most research has involved exposure
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16 FoumieJetal.
of a single species to a single toxin under controlled laboratory conditions.
More research is needed at the whole community level. The research pri-
orities ordered from the species level and scaling up to the community and
ecosystem level that have been identified are:
• To study the effects of cyanotoxins under environmentally relevant
conditions, including other environmental stressors; additive or
synergistic effects of combinations of cyanobacterial toxins or bioactive
compounds produced by cyanobacteria.
• To use relevant, naturally co-occurring organisms in exposure studies;
more knowledge is needed on species-specific toxicokinetics and
toxicodynamics.
• To obtain good quantitative data for a number of well-defined endpoints
for a range of toxin classes and biota.
• To study the effects of long term exposures and adaptive responses of
aquatic organisms.
• To identify community level effects of cyanotoxins. Key research needs
include studies of simple food chains and natural communities exposed
to toxic cyanobacteria.
• To identify the relative importance of different uptake routes from the
environment and the extent to which vectorial transport of toxins in the
food web takes place.
• To understand the potential for bioaccumulation, bioconeentration and
biomagnification of cyanobacterial toxins in aquatic food webs.
• To distinguish between the ecosystem effects of cyanobacterial toxins
and the harmful effects of cyanobacterial blooms in general (toxie vs.
non toxic blooms).
• To build and test models that relate environmental conditions to
cyanotoxin types, concentrations and compartmentalizati on and models
that describe the fate of cyanotoxins in water, sediment and food webs.
References
Amorim A, Vasconcelos V (1999) Dynamics of microcystis in the mussel Myti-
Ius galloprovincialis. Toxicon 37:1041-1052
-------
Chapter 31; Ecosystem Effects Work Group Report 17
Babcock-Jackson L, Carmichael WW, Culver DA (2002) Dreissenid mussclsin-
crease exposure of benthic and pelagic organisms to toxic microcystis. Verh
Internal Verein Limnol 28:1082-1085
Baganz D, Staaks G, Steinberg C (1998) Impact of the cyanobacterial toxin mi-
crocystin-LR on behaviour of zebrafish, Danio rerio. Water Res 32:948-952
Best JH, Pflugmacher S, Wiegand C, Eddy FB, Metcalf JS, Codd GA (2002). Ef-
fects of enteric bacterial and cyanobacterial lipopolysaccharides , and of mi-
crocystin-LR on glutathione S-tranfersase activities in zebra fish (Danio re-
rio). Aquatic Toxicology 60: 223-231.
Best JH, Eddy FB, Codd GA (2003). Effects of Microcystis cells, cell extracts and
lipopolysaccharide on drinking and liver function in rainbow trout Oncorhyn-
chus mykiss Walbaum. Aquatic Toxicology 64:419-426.
Burgess C (2001). A wave of momentum for toxic algae study. Environ Health
Perspect 109:160-1.
Bury NR, Eddy FB, Codd GA (1995) The effects of the cyanobacterium Micro-
cystis-aeruginosa, the cyanobacterial hepatotoxin microcystin-LR and am-
monia on growth-rate and ionic regulation of brown trout. J Fish Biol
46:1042-1054
Carmichael WW, Biggs D F (1978). Muscle sensitivity differences in two a vain
species to anatoxin-a produced by the freshwater cyanophyte Anabaena flos-
aquae, Canadian Journal of Zoology 56:510-512.
Carmichael WW, Evans WR, Yin QQ, Bell P, Moczydlowski E (1997). Evidence
for paralytic shellfish poisons in the freshwater cyanobacterium Lyngbya
wollei (Farlow ex Gomont) comb. nov. AppI Environ Microbiol 63:3104-
3110.
Codd GA, Lindsay J, Young FM, Morrison LF, Metcalf JS (2005). Harmful
cyanobacteria: From mass mortalities to management measures. In: Harmful
Cyanobacteria, Eds. J. Huisman, H.C.P. Matthijs and P.M. Visser, Springer,
Dordrecht, The Netherlands, pp. 1-23.
Cox PA, Banack SA, Murch SJ (2003). Biomagnification of cyanobacterial neuro-
toxins and neurodegenerative disease among the Chamorro people of Guam.
PNAS 100: 13380-13383
De Maagd PGJ, Hendriks AJ, Seinen W, Sijm D (1999) pH-dependent hydropho-
bicity of the cyanobacterial toxin microcystin-LR. Water Res 33:677-680
Dionisio Pires LM, Karlsson KM, Meriluoto JAO, Visser PM, Siewertsen K, Van
Donk E, Ibelings BW Assimilation and depuration of microcystin-LR by the
zebra mussel, Dreissena polymorpha. Aquat Toxicol. 2004;69:385-396.
Falconer IR, Humpage AR. 1996. Tumor promotion by cyanobacterial toxins.
Phycologia 35:74-79.
Fischer WJ, Dietrich DR (2000). Pathological and biochemical characterization of
microcystin-induced hepatopancreas and kidney damage in carp (Cyprinus
carpio), Toxicol AppI Pharmacol 164:73-81
Fujiki H, Suganuma M, Hakii H, Bartolini G, Moore RE, Takegama S, Sugimura
T. (1984). A two-stage mouse skin carcinogenesis study of lyngbyatoxin A. J
Cancer Res Clin Oncol 108: 174-176.
-------
18 Fournie J et ul.
Gray JS (2002). Bioinagnificution in marine systems: the perspective of an ecolo-
gist. Mar Poll Bull 45:46-52
Henriksen P, Carmichuel WW, An IS, Moeslrop O (1997). Detection of an ana-
toxin-a(s)-like anticholinesterase in natural blooms and cultures of Cyano-
bacteria/blue-green algae from Danish lakes and in the stomach contents of
poisoned birds. Toxicon 35:901-913
Ibelings BW, Bruning K, de Jonge J, Wolfstein K, Pires LMD, Postma J, Burger T
(2005). Distribution of microcystis in a lake food web: No evidence for bio-
magnification Microb Ecol 49:487-500
Jang MH, Ha K, Joo GJ, Takomura N (2003)Toxin production of cyanobacteria is
increased by exposure to zouplankton Freshw Biol 48:1540-1550
Jang MH, Ha K, Lucas MC, Joo GJ, Takamura N (2004). Changes in microcvstin
production by Microcystis aeruginosa exposed to phvtopianktivorous and om-
nivorous fish. Aquatic Toxicol 68: 51-59.
Liirling SVf (2003) Daphnia growth on microcystin-producing and microcystin-
free Microcystis aeruginosa in different mixtures with the green alga
Scenedesmus obliquus. Limnol Oceanogr 48:2214-2220.
Liirling M, van der Grinten E (2003) Life-history characteristics of Daphnia ex-
posed to dissolved microcystin-LR and to the cyanobacterium Microcystis
aeruginosa with and without microcystins. Environ Toxicol Chem 22:1281-
1287.
Kaijalainen M, Reinikainen M, Spoof L, Miriluoto JAO, Sivoncn K, Viitasalo M
(2005). Trophic transfer of cvanobacterial toxins from zooolankton to plank-
tivores: Consequences for pike larvae and mvsid shrimps. Environ Toxicol
20:354—362
Krienitz L, Ballot A, Kotut K, Wiegand C, Putz S, Metcalf JS, Codd GA, Pflug-
macher S (2003) Contribution of hot spring cyanobacteria to the mysterious
deaths of lesser flamingos at Lake Bogoria, Kenya. FEMS Microbiol Ecol
43:141-148
Kotak BG, Zurawell RW, Prepas EE, Holmes CFB (1996) Microcystin-LR con-
centration in aquatic food web compartments from lakes of varying trophic
status. Can J Fish Aquat Sci 53:1974-1985
Landsberg JH (2002) The effects of harmful algal blooms on aquatic organisms.
Rev Fish Sci 10:113-390
Matsunaga H, Harada KI, Senma M, Ito Y, Yasuda N, Ushida S, Kimura Y
(1999). Possible cause of unnatural mass death of wild birds in a nond in Ni-
shinomiva, Japan: Sudden appearance of toxic cyanobacteria. Nat Toxins
7:81-88
Paerl HW, Pinckney JL, Fear JM and Peierls BM (1998). Ecosystem responses to
internal and watershed organic matter loading: consequences for hypoxia in
the eutrophying Neuse River Estuary, North Carolina, USA. Marine Ecology
Progress Series 166:17-25.
Paerl HW, Fulton III RS, Moisander PH and Dyble J (2001). Harmful algal
blooms with an emphasis on cyanobacteria. TheScienti lie World Journal 1:76-
113.
-------
Chapter 31: Ecosystem Effects Work Group Report 19
Palmer MA, Covich AP, Lake S, Biro P, Brooks, JJ, Cole J, Dahni C, Gibert J,
Goedkoop W, Martens K, Verhoeven J and van de Bund WJ (2000). Link-
ages between aquatic sediment biota and life above sediments as potential
drivers of biodiversity and ecological processes. Bioscience 50:1062-1075,
Pflugmacher S (2004), Promotion of oxidative stress in the aquatic maeronhvte
Ceraiophvllum demersum during biotransformation of the evanobacterial
toxin microevstin-LR. Aquat Toxicol 70:169-178
Raikow DF, Sarnelle O, Wilson, AE, Hamilton, SK (2004) Dominance of the nox-
ious cyanobacterium Microcystis aeruginosa in low-nutrient lakes is associ-
ated with exotic zebra mussels. Limnol Oceanogr 49:482-487
Rodger HD, Turnbul! T, Edwards C, Codd OA (1994) Cyanobacterial (blue-
green-algal) bloom associated pathology in brown trout, Salmo-trutta L, in
Loch Lcvcn, Scotland, J Fish Dis 17:177-181
Rohrlack T, Christoffersen K, Kaebernick M, Neilan BA (2004), Cyanobacterial
protease inhibitor mieroviridin J causes n lethal molting disruption in Daphnia
oulicaria. Appl Environ Microbiol 70:5047-5050
Rohrlack T, Christoffersen K, Dittmann E, Nogueira I, Vasconcelos V, Borner T
(2005). Ingestion of mieroevstins bv Daphnia: Intestinal uptake and toxic ef-
fects. Limnol Oceanogr 50: 440-448
Scheffer M, Carpenter SR (2003). Catastrophic regime shifts in ecosystems: link-
ing theory to observation TREE 18: 648-656
Taylor RL, Caldwell GS, Bentley MG (2005). Toxicity of algal-derived aldehydes
to two invertebrate species: Do heavy metal pollutants have a synergistic ef-
fect? Aquatic Toxicol 74: 20-31
Tencalla F, Dietrich D (1997), Biochemical characterization of mierocvstin toxic-
ity in rainbow trout (Oncorhvnchus mvkiss). Toxicon 35: 583-595 APR 1997
Vanderploeg HA, Liebig JR, Carmichael WW, Agy MA, Johengen TH, Fahnen-
stiel GL, Nalepa TF (2001) Zebra mussel (Dreissena polymorpha) selective
filtration promoted toxic Microcystis blooms in Saginaw Bay (Lake Huron)
and Lake Erie. Can J Fish Aquat Sci 58:1208-1221
Ward CI, Codd GA (1999). Comparative toxicity of four mieroevstins of different
hvdrophobicities to the protozoan. Tetrahvmena nvriformis. J Appl Microbiol
86:874-882
Wiedner C, Visser PMf Fastner J, (2003). Effects of light on the mierocvstin con-
tent of Microcystis strain PCC 7806. Appl Environm Microbiol 69:1475-148
Williams DE, Craig M, Dawe SC, Kent ML, Holmes CFB, Andersen RJ (1997)
Evidence for a eovalently bound form of microcystin-LR in salmon liver and
dungeness crab larvae. Chem Res Toxicol 10:463—169
Williams DE, Dawe SC, Kent ML. Andersen RJ, Craig M, Holmes CFB (1997)
Bioaccumulation and clearance of microcystins from salt water, mussels,
Mytilus edulis, and in vivo evidence for eovalently bound microcystins in
mussel tissues. Toxicon 35:1617-1625
Xie LQ, Xie P, Guo LG, Li L, Miyabara Y, Park HD (2005). Organ distribution
and bioaccumulation of mieroevstins in freshwater fish at different trophic
levels from the eutrophic Lake Chaohu. China. Environ Toxicol 20:293-300
-------
20 Fournie J et at.
Zurawell RW, Kotak BG, Pre pas EE {1999). Influence of lake trophic status on
the occurrence of microcvstin-LR in the tissue of pulmonale snails. Freshw
Bio! 42:707-718
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