CHRYSOPHYTE BLOOMS
IN THE
PLANKTON AND NEUSTON
OF
MARINE AND FRESHWATER
SYSTEMS
AUGUST 1992
yr Environment
Environnement
Ontario
ISBN 0-7729-9997-X
CHRYSOPHYTE BLOOMS IN THE PLANKTON AND NEUSTON
OF MARINE AND FRESHWATER SYSTEMS
Report prepared by:
K.H. Nicholls
Limnology Section
Water Resources Branch
Ontario Ministry of the Environment
AUGUST 1992
©
Cette publication technique
n’est disponible qu’ en anglais.
Copyright: Queen’s Printer for Ontario, 1992
This publication may be reproduced for non-commercial purposes
with appropriate attribution.
PIBS 2082
Log 92-2345-107
ABSTRACT
This report reviews the major developments in recent understanding of bloom-causing
chrysophytes in both marine and freshwater environments. It also points out information
deficiencies and suggests lines of future research.
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Freshwater Chrysophyte Blooms - Phytoplankton ....................... 8
Characterization of Chrysophyte Volatilities .......................... 11
Bloom Development - Ecological Considerations ...................... 12
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LIST OF TABLES
Table 1 Common odours in the influents of three drinking water utilities expressed as
percentage occurrence of all odours.
Table 2 Densities or organisms associated with odours in drinking water from Lake
Lyseren, Norway.
Table 3 Occurrence of Uroglena blooms in Ontario lakes during 1987-1990.
Table 4 Volatile excretory products of three algal species, including the chrysophyte
Synura uvella.
Table 5 Summary of chrysophyte responses to experimental nutrient additions.
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Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
LIST OF FIGURES
An hypothesis relating precipitation and associated physical-chemical changes
to development of Aureococcus blooms in Long Island embayments (after
Cosper et al. 1990).
Hypothetical population density changes over time for two phytoplankton
species, "A” and "B", of which, only species "A" is an odour producer. If
sampling and identification are done at the peak of odour production but
after the population has peaked (arrow), species "B” may be erroneously
implicated as the cause of the problem.
The effects of temperature on the growth rate of cultured Synura sphagnicola
at eight different light intensities ranging from 11 - 110 E/ m?/s (from Healey
1983).
The interactions of a number of factors originating from human influences
and their stimulatory effect on phytoplankton in a hypothetical softwater lake.
a) Annual average biovolume of Chrysochromulina breviturrita and Synura
spp. in the phytoplankton of Dickie Lake, Ontario, 1976-1990; b) Seasonal
distributions of C. breviturrita and Synura spp., 1976 - 1979 (Nicholls unpubl).
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INTRODUCTION
Excessive accumulations of algae in freshwater lakes and coastal marine environments
have been observed for centuries. Homer's //liad mentions discolouration of the sea and
the Bible contains a reference to "the bloodied waters of the Nile”. Charles Darwin
apparently observed a "red tide” off the coast of Chile, and North American Indians
wouldn't eat shellfish from "shining waters” based on previous experiences with algal
bloom related shellfish poisonings (Red Tide Newsletter 3(2), April 1990). Among the
causes most often cited are enrichment of aquatic systems with nutrients from human
activities (Vallentyne, 1974; Smayda and White, 1990). While there is strong evidence
that excessive supply of nitrogen and phosphorus and other nutrients is often the
underlying cause of algal blooms, it is also clear that bloom development depends upon
the coming together, in appropriate combination, of a number of critical biotic, physical
and chemical environmental factors (Paerl 1988).
The implication of the early historical evidence of algal blooms is that the consequences
of accelerated human population growth and contemporary urbanization and
industrialization activities cannot be the only causative factors for algal blooms. For
example, there were especially intense blooms of the dinoflagellate Alexandrium
cantenella off the Norwegian coast in 1988, which may have been in response to
abnormally high water temperatures. Paleo-oceanographic evidence (B. Dale, University
of Oslo, unpublished) suggests that similar blooms developed as far back as 2000 years
ago when human induced influences were undoubtedly negligible.
During the past 5-10 years, however, there is good evidence that the frequency, intensity
and geographic extent of algal blooms, in both freshwater (Skulberg et al. 1984) and
marine environments (Smayda 1990), have increased dramatically in response to human
influences related mainly to active transport of bloom-causing organisms (e.g., ship
ballast, aquaculture stocking) and stimulation of bloom development by nutrient
enrichment. Until recently, the algal bloom phenomenon was generally believed to be
monopolized by blue-green algae in lakes and dinoflagellates in the sea, although less
significant blooms caused by other algal groups have been recognized (Pearl 1988). The
International Conference on Toxic Dinoflagellates (1974, 1978, 1985) changed its name
for the June 1989 meetings in Sweden to "The Fourth International Conference on Toxic
Marine Phytoplankton” in order to better reflect the recent catastrophic non-
dinoflagellate blooms of the mid- to late 1980s. These blooms resulted in human death
and sickness, severe economic losses and inestimable ecological damage and were caused
by the prymnesiophytes Chrysochromulina polylepis and Prymnesium parvum in
Scandinavian coastal waters in 1988 and 1989 (Underdal et al. 1989; Kaartvedt et al.
1991), the chrysophyte Aureococcus anophagefferens in New England in 1985-1988
(Nuzzi and Waters 1989; Cosper et al. 1990), and the diatom Nitzschia pungens f.
multiseries on Canada's east coast in 1987 (Subba Rao et al. 1988). In freshwater, algal
blooms of non blue-green origin with economic and/or nuisance/aesthetic implications,
have included the dinoflagellates Ceratium hirundinella (Nicholls et al. 1980) and
Glenodinium sanguineum (Dodge et al. 1987), the prymnesiophyte Chrysochromulina
breviturrita (Nicholls et al. 1982) and the chrysophytes Synura petersenii (Nicholls and
Gerrath 1985), Synura uvella (Clasen and Bernhardt 1982) and Uroglena americana
(Kurata 1989). These species are only the tip of the iceberg however; a recently
published guide to the taxonomy of organisms causing "red tides” in Japan (Fukuyo et al.
1990) includes 200 species representing ten algal classes. Interestingly, this
comprehensive listing includes only one chrysophyte species (Uroglena americana).
It is clear, therefore, that with so many different taxa now implicated in algal blooms,
bloom phenomena present special challenges to both the scientist and the user of aquatic
resources concerned about understanding and predicting the potential for bloom
development and toxin production. This paper reviews the major developments in recent
understanding, as well as the major information deficiencies relating to bloom-causing
chrysophytes in both marine and freshwater environments.
Bloom Definition
Phytoplankton blooms have been defined in different ways (Pearl 1988; Richardson 1989;
Legendre 1990). For the purposes of this paper, I define a chrysophyte bloom as an
accumulation of organisms of the classes Chrysophyceae and/or Synurophyceae to a level
of intensity which results in one or more of the following:
1) a visible colouration of the water,
2) an effect on aesthetic value and/or human use of the water (e.g., taste and
odour problems in water supplies),
3) major direct effects on other aquatic biota (toxin production, physical
damage, e.g., clogging of gill lamellae), and
4) major indirect effects on other biota (e.g., food web disruption leading to
starvation, dissolved oxygen depletion resulting from bloom
decomposition).
Marine Chrysophyte Blooms
The most important species of marine chrysophyte causing blooms (and the only species
discussed in this paper) is Aureococcus anophagefferens, a picoplanktonic alga, first
described by Sieburth et al. (1988). This species, which may be synonymous with the
open ocean taxon Pelagococcus subviridis (Cosper et al. 1990), developed dense blooms
in embayments of Long Island, New York in 1985-1988 and quickly gained notoriety as .
"brown tide” throughout the region including parts of New Jersey and Rhode Island
Sound where it was also observed (Nuzzi 1988; Nuzzi and Waters 1989; Smayda and
Villareal 1989). After the initial invasion in 1985, the brown tide did not return to
Naragansett Bay in 1986, but did to Barnegat Bay and to the Long Island bays during
three subsequent years, but at lower densities. Densities during the peak of the 1985
bloom approached 3 x 10° cells/L.
The effects of the Aureococcus blooms were disastrous. Anecdotal evidence suggested
that thousands of acres of eelgrass (Zostera marina) beds, plants which are important as
settling sites for larval shellfish, were essentially eliminated through light exclusion
effects (Nuzzi 1988); however, quantitative data on distribution and density immediately
before and after the bloom years apparently does not exist (Dennison et al. 1989).
Because the critical life history of the bay scallop (Argopecten irradians) through larval,
immature and sexually mature adult stages covers less than a two year period, the bay
scallop fishery was virtually wiped out (Bricelj and Kuenstner 1989) where the
Aureococcus bloom developed during two consecutive years. The effect was one of
physical interference in filter feeding so that the scallops apparently starved to death; no
toxicity has been implicated (Gallager et al. 1989; Ward and Targett 1989). The
combined value of the annual bay scallop, blue mussel and cultured oyster (Crassostrea
virginica) harvest from this region, lost to the effects of the brown tide, was over $2.5
Million (Nuzzi 1988). Other damage was not easily quantified. For example, terns and
other fish-eating birds left the region apparently because they couldn't see their prey
(Nuzzi 1988).
The critical questions at the time of the Aureococcus bloom were obviously related to
the cause. Why did it happen? First of all, it is unfortunate that it seemed to take a
catastrophic event like this to focus attention on a chrysophyte. One major consequence
of this bloom was that there followed a flurry of research activity at laboratories in the
region. _Aureococcus was brought into laboratory culture from isolations made in 1986
and effects on growth rates of several environmental factors were determined. Field
studies to determine the water quality /productivity relationships in Long Island Sound
area were also initiated (Nuzzi and Waters 1989; Cosper et al. 1989). Cosper et al.
(1987) showed that Aureococcus grew much better in enriched coastal bay water than in
enriched synthetic ocean media. Dzurica et al. (1989) achieved improved growth of
Aureococcus in media containing organic phosphate compounds auch as
glycerophosphate and chelating agents such as nitrilotriacetic acid (NTA) and citric acid.
This species also demonstrated strong heterotrophic growth capabilities with rapid
uptake of glutamic acid and glucose. Still, the culture studies alone were not able to link
these special characteristics of laboratory growth to bloom development..."How these
factors are involved in the dominance of A. anophagefferens over other phytoplankton
species in nature remains to be further investigated...” (Dzurica at al. 1989).
One of the most convincing explanations for the cause of the bloom was developed by
Cosper et al. (1990). I have summarized it here, because it appears to represent a
particularly good example of the fortuitous interaction of a number of environmental
factors with the particular physiological adaptations and requirements of Aureococcus. It
is an attempt to communicate more widely the Cosper et al. hypothesis in the hope that
it might serve as a model for Salhancone o other algal bloom phenomena, possibly
involving multiple environmental factors.
The first important point to realize is that the brown tide occurrence in 1985 was over a
wide geographic area, and because the bloom did not appear to spread from one coastal
bay system to the next, but rather developed more or less simultaneously at all locations,
factors initiating the bloom appear to be regional (e.g., weather) rather than localized
(e.g., the effects of a single point-source of nutrients). In this regard, the precipitation
data are most revealing. Rainfall on Long Island during 1985 was the third lowest since
1949 and was again well below the annual average in 1986 and 1987. This low
precipitation resulted in salinity levels that were 20% higher than normal. The
laboratory studies had shown a severe reduction in growth rate of Aureococcus below 28
ppt, compared with 30 ppt, but growth at the lower salinities could be enhanced by
addition of organic rather than inorganic nutrients. This is where the seasonal pattern of
annual precipitation is apparently of some importance in bloom development.
Aureococcus blooms developed during the summers of 1985, 1986 and 1987, but were
most intense in 1985 and least intense in 1987. During 1985 and 1986, low winter
rainfall was followed by high precipitation in spring. In 1987, spring precipitation was
low and the bloom was not nearly as well developed. The implication is that rainfall was
important for nutrient supply, but only enhanced bloom development if it followed a
period of low rainfall which set up the optimum salinity levels. In addition, the low
winter rainfall resulted in generally longer water residence times in the Long Island
Sound embayments thereby helping to ensure that an adequate overwintering "seed"
population was present for the summer season (Fig. 1).
The Cosper et al. explanation for the Aureococcus bloom might be expanded after
further investigation to include some additional facts and suggestions put forward by
Sieburth (1989) and Minei (1989) relating to the possible stimulatory effects of
agricultural and lawn fertilizers on Aureococcus and toxic effects of pesticides on
zooplankton in the Long Island area.
Freshwater Chrysophyte Blooms
Phytoplankton
A number of chrysophyte taxa are known to produce substantial populations in
freshwater lakes and ponds. These include Mallomonas acaroides, M. caudata and M.
crassisquama (Kristiansen 1971; Thomasson 1970), Chrysosphaerella longispina (Pick et
al. 1984), several Dinobryon species (Eloranta 1989), Uroglena americana (Kurata 1989),
Synura spp (Nicholls and Gerrath 1985; Clasen and Bernhardt 1982). In this review, I
will restrict my summary to those genera known for their production of odour and
associated problems in domestic water supplies, recreational lakes and reservoirs.
Odours from blooms of Dinobryon, Synura, and Uroglena have most often been
described as fishy, but other descriptors include "cod liver oil” and "muskmelon” or
"cucumber", especially for the early bloom stages of Synura (Whipple et al. 1948; Lackey
1950; Palmer 1962; Taft 1965).
Where surface waters provide the raw water source for municipalities, some level of
treatment is usually provided before distribution to consumers. This treatment can range
from simple disinfection to complex filtration/sedimentation procedures. Excessive
densities of algae in the influents to these water treatment plants disrupt their normal
functioning and usually require modifications to routine operations including more
frequent filter backwashing, installation of microstrainers, adjustments to chemical
flocculation routines, or more expensive activated carbon filtration (Hutson et al. 1987).
At locations where only limited treatment is provided, as for example in regions of
chronic economic depression or where the source water supply has historically been of
good quality, occasional algal blooms may impart off-flavours which get through the
system to the consumer. At such times, complaints from consumers to water treatment
operators and waterworks officials are usually described by reference to common
naturally occurring odours, such as musty, earthy, fishy, oily, geranium, septic, etc. The
general practice of water treatment personnel is at least to record any complaints from
consumers and charactize the type of odour (Table 1). There is of course a danger in
assuming that all “fishy” odours in water supplies arise from chrysophyte blooms because
fish-like odours can originate from the decomposition of certain protein complexes. Only
rarely have chemical analyses been undertaken to characterize precisely the odour
causing compounds (Mallevialle and Suffet 1987).
A more ideal situation results from microscopic identification of organisms in the raw
(untreated) water source at the first sign of an odour problem (e.g., Table 2). One
difficulty with this scenario is that the odour from an algal population may not arise until
near the end of its period of healthy growth. So, by the time it is recognized as a
problem and investigated, some other species may have assumed dominance in the
phytoplankton. The result is that some “innocent” species may be mistakenly identified
as the problem organism (Fig. 2). Clearly, quick reaction times between odour detection
and identification of the cause are necessary to avoid erroneous explanations.
At some water treatment plants, the need for timely and accurate diagnosis has led to
the establishment of regular phytoplankton monitoring and routine measurements of
threshold odour concentrations (APHA 1985; Persson 1983; Persson and Jüttner 1983).
The data thus obtained permit the judicial application of remedial measures such as
activated carbon filtration in a cost effective, short-term, proactive manner.
Because chrysophytes tend to dominate the phytoplankton of north-temperate,
oligotrophic lakes (Janus and Duthie 1979; Eloranta 1986, this volume; Earle et al. 1986;
Willén et al. 1990; Pinel-Alloul et al. 1990; Nicholls et al. 1992), the major human use of
such lakes is for recreational purposes, rather than for drinking water supplies.
However, as was the case with drinking water supplies, the best source of information
about chrysophyte related odour problems may originate from user complaints.
In Ontario during the past four years, we have been made aware (through user
complaints) of nine episodes of fish-like odour production by Uroglena blooms. These
10
nine lakes (Table 3) included a wide range of lake type, from shallow, dystrophic lakes
such as Black Lake, to deep, clear water lakes such as Kawagama Lake. It is clear,
therefore, that circumstances other than nutrient supply alone are responsible for such
blooms. The species of Uroglena causing blooms in Ontario lakes have not been
determined, but in the case of perhaps the best known Uroglena lake in the world, Lake
Biwa in Japan, considerable research has been undertaken to determine the factors
stimulating growth and causing of recurrent blooms of U. americana since the early
1970s (Yoshida et al. 1983a, 1983b, 1983c; Kimura and Ishida 1986; Kimura et al. 1986;
Kurata 1986, 1989).
Taste and odour problems in Ontario lakes that originate from Synura have been more
widespread than those induced by Uroglena. Some of these episodes were reviewed by
Nicholls and Gerrath (1985) and it was concluded that in every case, in both hardwater
and softwater lakes, only one of the 20 known species of Synura (S. petersenii) was the
cause.
Characterization of Chrysophyte Volatilities
There have been only two or three significant studies of the volatile excretory products
of chrysophytes. Collins and Kalnins (1965) reproduced typical Synura odours in the
laboratory in bacteria-free cultures. By applying their solvent extraction and thin layer
chromatographic methods to culture filtrate as well as directly to cell concentrates, they
11
showed that the odour causing compounds were aldehydes and ketones (mainly n-
hapanal), which were excreted by living cells into the growth medium.
Some further work on a Synura bloom occurring in the Wahnbach Reservoir in Germany
was reported by Jiittner (1981, 1983), and based on similar findings from cultures of two
Ochromonas species, it was concluded that the Chrysophyceae, like higher terrestrial
plants, produce a wide spectrum of volatile organic compounds including a number of
dienals, alkenols, alkenones, alcohols and ketones (Table 4), of which oct-1-en-3-ol,
pentanone-3 and octanone-3 were the most important. Yano et al. (1988) identified the
related compounds (E,E)-2,4-heptadienal and (E,Z)-2,4-heptadienal as the causes of the
fishy odour in a Uroglena bloom in the Ninobiki Reservoir in Japan.
Bloom Development - Ecological Considerations
Aside from the explanation offered for the Aureococcus bloom, I have not to this point
discussed chrysophyte bloom ecology. The risk in delving into this topic is that I would
be repeating much of the information presented by other contributors to this volume
under the related topics of chrysophyte distribution, ecology and paleoecology. This is
because many of the strategies that permit chrysophytes to survive and flourish in lakes
are undoubtedly related to similar factors involved in bloom development (see also
review by Sandgren 1988). Therefore, this section on chrysophyte bloom initiation will
include only the essential highlights of the ecology of bloom-forming species, so that
12
more space can be devoted to detailing what I consider to be the major deficiencies in
our understanding of the chrysophyte bloom phenomenon. Hopefully, this approach will
provide some direction for future research and management.
An understanding of the ecology of bloom forming chrysophytes must be based on a
solid physiological foundation. A classic example of this is the historical development
(spanning a period of nearly half a century) of the understanding of the relative roles of
phosphorus and potassium as factors controlling Dinobryon populations (see Shapiro
1988, p.11). Quantitative ecophysiological investigations of the bloom-forming
Chrysophyceae probably had their beginnings with the work of Gaidukov (1900) who
determined that Chromophyton rosanoffii Woronin emend. Couté (Gaidukov's
"Chromulina rosanoffii”) could be grown in a defined mineral medium. Subsequently,
Guseva (1935) was able to examine growth rates of Synura uvella and S. petersenii in
cultures based on isolations from the Moscow River Oxbow and from some peat pits in
the vicinity of Bolshero. She discovered that iron concentrations were critical for good
growth in both species. Optimum iron concentrations of 1.2-1.4 mg/L and nitrogen
concentrations of 1.0-2.0 mg NO,-N/L and 0.1-0.2 mg NH,*-N/L were determined for S.
petersenii. Today, we know that the relatively high iron requirement by Synura species
relates to their, use of iron-containing cytochrome-C as an electron donor in photosystem-
I (Raven, this issue). The tendency for certain Synura species to develop large
populations in dystrophic lakes and ponds may depend, in part, on the availability of
iron. Dokulil and Skolaut (1991) concluded that the summer populations of Dinobryon
13
species in the Mondsee in Austria were dependent on the supply of iron, the availability
of which was controlled through chelation by organic substances released by
decomposition of the spring diatom populations.
Light may also be a factor controlling bloom development in dystrophic waters, owing to
its rapid attenuation by dissolved organic matter (Jones and Arvola 1984). Little is
known, however, of the light quality and quantity preferences and the physiological
adaptive responses by phytoplankton as a whole (Falkowski 1984), let alone chrysophytes
in particular. In experiments on the role of colour and light intensity on the distribution
of several phytoplankton species, Wall and Briand (1979) found that chrysophytes
represented by Dinobryon and Mallomonas species tended to be favoured more by blue
light than were other groups of algae. They suggested that this is consistent with the
known vertical distribution of these algae in lakes and that the deep water occurrence of
these species may indicate a competitive advantage over other algae better suited to use
the higher intensity red wavelengths in surface waters.
There is ample evidence of stratified subsurface chrysophyte populations in rakes (Fee
1976; Nygaard 1977; Pick et al. 1984; Croome and Tyler 1988) and diurnal migrations of
some taxa have been demonstrated (Ilmavirta 1974; Jones 1988). The most obvious
attribute that the presence of flagella has provided to each of the genera being discussed
here (Dinobryon, Synura, Uroglena and Mallomonas) is the ability to “swim”. Subsurface
populations of these organisms are clearly there by choice. The suggestion above was
14
that some relative advantage over other algae relating to light quality and intensity may
exist for these motile chrysophytes. The operative word is "relative” because laboratory
studies have shown that species achieving significant populations in the wild at low light
and temperature may grow equally well or better at higher light intensities and higher
temperatures in the laboratory. For example, Healey (1983) showed that growth rate of
Synura sphagnicola isolated from a submetalimnetic bloom (ambient light 1% of surface
irradiance and temperature = 7-8° C) was a saturable function of light intensity over a
temperature range of 5-20° C in the laboratory (Fig. 3).
If light and temperature are not optimal for these organisms at these depths, then they
must be actively seeking these strata out for other reasons. Nutrient concentrations are
usually higher within and below the metalimnion because of decomposition and
mineralization of materials sedimenting from the upper trophogenic zone combined with
the upward diffusion of dissolved matter released from the lake sediment and/or from
similar processes of decomposition in the hypolimnion. By virtue of its motility, a cell in
a homogeneous solution of dissolved nutrients is ensuring a constant and maximum
concentration gradient across the cell membrane (assuming constant uptake rate and
constant swimming speed). While it has been shown that the net energy gain to a motile
cell (compared to a non-motile cell) under these conditions is negligible (Sommer 1988),
there may be considerable advantage in expending energy to seek out and remain in
strata with higher concentrations of essential nutrients. Bloom-forming species of
Mallomonas, Dinobryon, Synura and Uroglena are all large and highly motile. One
15
advantage that taxa with the ability to move vertically in the water column may have
over those that do not is exposure to "pockets” with higher nutrient levels; they are thus
able to exploit heterogeneities in growth promoting substances in their environment
within the limits of their swimming capabilities and net energy expenditures.
Biotic and Anthropogenic Factors
In general, chrysophytes tend to comprise a significant proportion of the total
phytoplankton of oligotrophic to mesotrophic lakes. The role of nutrients, originating
from human activities, as triggers of chrysophyte blooms is not clear, although it is
evident that substantial populations may develop in lakes and ponds with significant
inputs of nutrients. In eutrophic lakes, the seasonal distribution of chrysophytes may be
restricted mainly to early spring (Kristiansen 1988). Munch (1972) and Roijackers (1985)
both reported occasional blooms of Synura or Mallomonas in productive dimictic lakes.
Generally, eutrophied lakes are poorly represented by chrysophytes, but when point-
source nutrient loading controls have been initiated, the relative importance of
chrysophytes has increased (Dillon et al. 1978; Nicholls et al. 1986; Willén 1987).
Conversely, fertilization of low-productivity lakes has sometimes been followed by
blooms of chrysophytes, but the results thus far have not been consistent (Table 5). For
example, Langford (1950) fertilized four lakes in Ontario with a 12-24-12 formulation of
a commercially available fertilizer and achieved epilimnetic concentrations of total P
ranging from 0.05 to 0.9 mg/L (as P). All lakes, except an unfertilized control lake,
16
responded to treatments 3-4 weeks later with increases in Tabellaria, Asterionella and
Dinobryon. One of the lakes produced much higher densities of Synura. In contrast,
Lake Langvatn in central Norway showed no response among Synura, Uroglena, or
Dinobryon at fertilizer application rates similar to those used by Langford (Reinertsen
1982). In northern Sweden, a Uroglena bloom resulted from fertilization with nitrogen
alone in one lake, but no bloom developed in another lake receiving a similar treatment
(Holmgren 1984).
The responses of Dinobyron to lake fertilization are interesting. The early belief that
phosphate was toxic to Dinobryon, even at relatively low concentrations, was challenged
by Lehman (1976), who showed that when phosphorus was supplied even at high
concentrations to Dinobryon cultures as K,HPO, or KH,PO,, potassium, not phosphorus,
was the toxic element. However Lehman's work showed inhibition of growth of D.
sociale var. americanum and D. cylindricum at K concentrations greater than 500 ug/L
and 7500 ug/L, respectively, and these results do not entirely explain the inhibition
observed by Rodhe (1948) at much lower concentrations of K (25 ug/L). More recently,
Wilcox and DeCosta (1984) also observed a rapid disappearance of Dinobryon in
experimental enclosures fertilized with KH,PO, (100 ug K/L). Holmgren (1984) found
an apparent inhibition of Dinobryon spp. in a lake fertilized with phosphate alone (as
H,PO,), but Dinobryon spp. were consistently among the dominants in Lake ELA 261
after fertilization with H,PO, (Table 5). Clearly, the role of nutrient supply in
chrysophyte bloom development is poorly understood, but it is possible that in
17
combination with other factors, small increases in nutrient supply are stimulatory to some
chrysophyte populations.
Factors contributing to chrysophyte blooms probably relate as much to strategies that
allow populations to avoid losses as to factors that contribute directly to optimum
growth. Another advantage of the capability for vertical movement in lakes may be that
it affords protection from zooplankton grazing. In laboratory studies, Sandgren (this
issue) has demonstrated that Synura and other large chrysophytes are utilized as food
items by large Daphnia species, presumably through consumption of individual cells
rather than whole colonies. In support of these findings, Sandgren (ibid) assembled data
from the literature which showed that the presence of populations of large Daphnia in
lakes was associated with depressed chrysophyte populations. This finding raises an
interesting "chicken and egg” question: Is the predominance of chrysophytes in softwater
lakes a direct physiological response to chemical characterists of low pH waters, or is it
in response to decreased Daphnia grazing, since Keller et al. (1990) have shown with
field data and laboratory bioassays that densities of Daphnia galeata mendotae decline in
lakes below pH 6.0? Sandgren concluded that there is no refuge from zooplankton
grazing by virtue of large size among chrysophytes. There may, however, be protection
afforded by the deeper portions of the vertical migratory route (metalimnion or upper
hypolimnion) where low water temperatures are associated with low metabolic rates of
the grazing animals at these depths.
18
In summary, large populations of chrysophyte species may develop in softwater lakes
because of their ability to grow well at low temperatures and low light intensities
(although these may not be optimal), combined with the minimization of zooplankton
grazing impacts and adequate nutrient supplies. The latter two factors may be
augmented by human influences. For example, removal of large piscivorous fish results
in enhanced zooplanktivore populations and increased predation on large zooplankton
species. Watershed deforestation, human wastewater seepage and agriculturalization all
result in increased nutrient inputs to lakes, and the effects of acid deposition may act as
a double edged sword: 1) by decreasing lakewater alkalinity and thereby putting
additional stress on Daphnia spp., and 2) by enhancing leaching of growth promoting
substances (including trace metals such as cobalt needed for subsequent synthesis of
vitamin B,,). The combined effects of eutrophication and acidification have been
blamed for the recent algal blooms in Scandinavian coastal waters (Sangfors 1988;
Granéli et al. 1989).
While these factors may explain the occurrence of large chrysophyte populations (Fig. 4),
they do not necessarily explain some aspects of the bloom phenomenon itself. For
example, Uroglena blooms are often manifested as sudden mass accumulations at the
lake surface, much like the blue-green algal bloom phenomenon. Unlike the blue-green
algal bloom, for which an ecophysiological explanation exists (Reynolds and Walsby
1975), no similar explanation for the sudden surface accumulation of Uroglena has been
suggested. Considerable laboratory study of the now common Lake Biwa Uroglena
19
blooms has contributed much to an understanding of phagotrophism, nutrient, trace
metal and vitamin requirements (Yoshida et al. 1983a, 1983b, 1983c; Kimura and Ishida
1986; Kimura et al. 1986; Kurata 1986, 1989). The apparently now common episodes of
Uroglena surface blooms in Ontario (Table 3), may afford additional opportunities to
determine the factors contributing to the surface accumulations.
Neuston
The term "neuston” was first used by Naumann (1917) to designate the community of
organisms associated with the surface microlayer of lakes and ponds. Its use in
freshwater and marine contexts has been reviewed by Banse (1975) with reference to
subdivisions of the neuston (e.g., epineuston, hyponeuston) and other “nearby” biotopes
in aquatic ecosystems. It is important to realize that organisms inhabiting the neuston
are there for reasons related to surface tension, not because of buoyancy adaptations; so,
by definition, the neuston excludes surface accumulations of gas vacuolate blue-green
algae.
The neuston communities of freshwaters may include a wide variety of taxa (Frélund
1977; Fuhs 1982a, 1982b; Pentecost 1984; Estep and Remsen 1984; Timpano and Pfiester
1985). The highly visible oily sheen produced on the water surface by several
chrysophytes qualifies this type of growth as a “bloom” under the definition used in this
paper. The most commonly reported neustonic chrysophyte is Chromophyton rosanoffii
20
Woronin emend. Couté (Couté 1983), which forms curious epineustic "pseudocysts”.
Some aspects of the life history and seasonal development of this species have been
presented by Petersen and Hansen (1958) and Frélund (1977) who found a maximum
density of about 2 X 10° cells /cm°?. Heynig (1972) has also included C. rosanoffii among
a listing of other freshwater bloom forming algae such Aphanizomenon, Microcystis,
Dinobryon, Ceratium and Botryococcus.
Other Chrysophyceae known to inhabit the neuston (but not necessarily excluded from
planktonic, benthic or epiphytic existences in other habitats) include Chromulina
neustophila Conrad (Conrad 1940), Paraphysomonas vestita (Stokes) de Saed. (Frélund
1977), Epipyxis minuta (Mack) Hilliard (Petersen and Hansen 1958 [as Hyalobryon
minutum Mack]), Hyalocylix stipitata Pet.& Han. (Petersen and Hansen 1958), and
Kremastochrysis minor Catalan (Catalan 1987). Two or three other Chromulina species
are probably synonymous with Chromophyton rosanoffii since cell habit and morphology
appear identical except for the likely omission of the second short flagellum (Couté
1983). Those neustonic chrysophytes forming visible blooms are likely restricted to C.
rosanoffii, C. neustophila and K. minor.
The surface microlayer may also be enriched with bacteria (Maki and Remsen 1989).
Because chrysophytes of the Ochromonas-type are known facultative phagotrophs, the
generally low light environment of woodland ponds might provide a competitive
advantage to such chrysophytes as Chromophyton over other algae which must depend
21
only on autotrophic nutrition under conditions of higher light than is generally available
in shaded forest pools, which seem to be the preferred habitat of Chromophyton. Once
established in the neuston with some dependence on bacteria for a portion of their
energy supplies, other variables might enhance the availability of nutrients and other
growth factors in this specialized environment. For example, precipitation can provide
nutrients in dissolved, bioavailable form at levels often far exceeding concentrations
available to phytoplankton of oligotrophic systems (Parker et al. 1981). Danos et al.
(1983) found significantly higher concentrations of dissolved inorganic nitrogen,
phosphorus, silica and pigments in the surface microlayers of experimental ponds. Also,
the surface microlayer of seawater is enriched with surface active substances such as fatty
- acids and proteinaceous materials (Duce et al. 1972; Hardy 1982; Barlocher et al. 1988)
which may act as chelators of trace elements required by neustonic species - elements
which might not be available to planktonic species. A similar enrichment of the surface
microlayer of freshwater forest pools might be expected given the usually high organic
content of their terrestrial surroundings and the associated opportunities for the supply
of vitamins and other growth factors.
The surface film algal community may be immune from grazing by micro-crustaceans
that are adapted for planktonic filter-feeding. This specialized habitat may therefore
provide a refuge and protection from one of the important loss mechanisms influencing
phytoplankton. However, protists with special adaptations for existence at the air-water
interface, such as hypotrichid ciliates (Ricci et al. 1991), may exert some influence on
22
phytoneuston communities. Also, because of the specialized habitats of neustonic
chrysophytes (mainly physically stable, small, shallow forest pools), neustonic
chrysophytes have not in the past created any special problems for human use of these
waters. These specialized communities do, however, offer their potential use as model
systems for investigation of a number of chrysophyte related phenomena, including
bacterial - flagellate interdependencies and the possible production of volatile
compounds which might inhibit the growth of other organisms.
Information Needs
"A more definite knowledge of the factors involved in the
development of blooms in fresh and salt water can certainly
be gained from physiological experiments with cultures and
simultaneous qualitative and ecological observations” (English
translation from German)
Kolkwitz (1914)
This review has, I hope, consolidated some of the known information about the mass
occurrences of chrysophytes. However, it has also probably served to point out a number
of deficiencies in our understanding of the phenomena. I hope that many of these
information gaps will have already become apparent to the reader, but at the risk of
stating the obvious, I would like to provide my own thoughts on required future
23
directions for chrysophyte bloom research.
(I)
There is a need to continue development of remote sensing technology, especially
as it relates to coastal marine areas. The absorption and fluorescence spectra of
Aureococcus, the marine "brown-tide” organism, are different from those of other
coastal marine phytoplankton species (Yentsch et al. 1989); this might be
exploited by remote sensing. Recent advances in multispectral scanning
technology are leading to real-time assessments of the extent and dynamics of
both marine and freshwater algal blooms (Balch et al. 1991; Millie et al. 1991).
Even if the extent and frequency of marine algal blooms do not increase in the
future, the impacts of the marine blooms of the future will undoubtedly be more
dramatic as coastal salmon culture intensifies. Net pen farming of both Atlantic
and Pacific salmon now accounts for 30% of the world's production of canned
salmon. It has been predicted that by the year 2000, farmed salmon will account
for 90% of the total (Van Dyk 1990). Penned salmon are vulnerable to algal
blooms. On the British Columbia (Canada) coast alone, fish farming losses
resulting from diatom blooms have averaged between $2-4 million annually over
the period 1986-1990 (Red Tide Newsletter, 3(2):11, April, 1990). The
Prymnesium parvum bloom on the Norwegian southwest coast in 1989 caused
losses of caged salmon valued at $5 million (Kaartvedt et al. 1991).
24
(iI)
In the path of an advancing algal bloom, the only reactions possible today are, 1)
harvest the fish prematurely, 2) tow the net pens out to sea beyond the influence
of the bloom or 3) take a chance on the severity of the effects of the bloom.
Early warning systems based in part on remote sensing technology would help in
selecting one of these options.
More biochemical and toxicological work needs to be done on the volatile
excretory products of chrysophyte bloomers, especially Synura and Uroglena
species. One striking feature of the big blooms is that they are essentially
unialgal. This begs the question "are other species excluded because of toxic
excretions”? Kamiya et al. (1979) have demonstrated the presence of fatty acid
ichthyotoxins in Uroglena volvox, and toxin production by axenic cultures of
Ochromonas has also been found (Spiegelstein 1969). This is important because
there is at the present time a debate in progress on the role of bacteria in the
production of toxins associated with some marine dinoflagellate blooms (Taylor
1990). If bacteria are not implicated in the production of chrysophyte toxins, as
the scant research data would suggest, then progress in determining factors
responsible for toxin production might be relatively rapid because the work would
be based on a simpler biotic system.
Some indirect evidence for toxin production by either (or both) of Synura or
Chrysochromulina breviturrita may exist in data from Dickie Lake in Ontario.
(M)
Over a 15 year period of observation, years with high biovolume of Synura were
also years with low biovolume of Chrysochromulina breviturrita and vice versa
(Fig. 5). The recent Chrysochromulina polylepis poisonings in the Baltic
(Underdal et al. 1989) provided the first evidence for toxin production by
members of the prymnesiophyte genus Chrysochromulina (but see Nicholls et al.
1982). It cannot be determined conclusively from the Dickie Lake data on hand
whether or not C, breviturrita and Synura have inhibited each other’s growth;
however, the within year data suggest that Synura may have inhibited
Chrysochromulina because the Synura populations typically developed before the
Chrysochromulina populations. Chrysochromulina didn’t develop until mid- to
late summer, and then apparently only in Synura’s absence (Fig. 5). At this point,
this is speculative, but suggestive, and some experimental work needs to be done
on species interactions that include Synura, Uroglena and other bloom formers.
Included under the general topic of species interactions might also be the role of
parasitic symbioses and predation by non-crustaceans such as Bodo and
Rhizoochromonas species (Nicholls 1987,1990) as potential regulators of
chrysophyte populations. What are the environmental factors that allow Bodo
crassus and Rhizoochromonas endoloricata to achieve high population densities?
Because their flagellar structure is different from that of phagotrophic
chrysophytes with the ochromonad flagellation type, Mallomonas and Synura are
unlikely to utilize bacteria directly as a food source in the same way that several
26
(IV)
(V)
ochromonadalean species do (including Dinobryon and Uroglena) (Bird and Kalff
1986; Kimura et al. 1986a, 1986b; Boraas, this volume). Still, the other roles of
aquatic bacteria in modifying the growth medium and helping to structure the
phytoplankton community (Newhook and Briand 1987) need to be investigated
with reference to chrysophyte blooms.
Although much is now known about the physical and biochemical properties of -
dissolved organic matter (Gjessing 1976; Steinberg and Muenster 1985), there are
still important information gaps relating to the effects of natural organic materials
on aquatic organisms (Serrano and Guisande 1990; Steinberg 1990). The role of
organic acids and iron in dystrophic systems, both as directly available essential
growth factors and as substances regulating the availability of essential trace
elements, needs further work with respect to chrysophytes. There is some
evidence that the humic contents of Scandinavian lakes is increasing at rates as
high as 3% per year (Forsberg and Petersen 1990). Graneli et al. (1989) have
demonstrated enhanced growth of dinoflagellates in response to experimental
additions of humic substances in coastal areas of the Baltic influenced by these
increased inputs of dissolved humic materials from adjacent watersheds. Similar
experiments need to be done in freshwater systems with potential bloom forming
chrysophytes.
Experimenta! use of "BIOTRON” type technology (e.g., Ostroff et al. 1980;
27
Graham et al. 1985) should be encouraged for multifactorial laboratory
investigation of light, temperature, nutrients and other variables influencing
chrysophyte growth rates, and in particular, to answer questions about surface
water accumulations of Uroglena. Some relevant questions are: 1) where does
the population producing the surface bloom develop? 2) what causes mass
movement to the surface and what is the relative importance of active motility
and passive buoyancy? 3) once at the lake surface, are cells viable? 4) what are
the time dependent effects on cell viability of potentially damaging high intensity :
solar irradiance at the lake surface? 5) what are the diurnal vertical movements
under thermally stratified conditions? and 6) what are the relative roles of the
water column light, temperature and nutrient gradients as regulators of vertical
movements in the population? These questions might be answered through a
combination of careful observations of wild populations and laboratory
experimentation .
SUMMARY
Although there are many unanswered questions relating to the causes of chrysophyte
blooms, an apparent pattern has emerged from the recent studies of algal blooms in
coastal marine environments and freshwater lakes. That is that human influences in the
form of increased nuire supply from human waste, drainage from agricultural
operations, and contaminated precipitation provide the basic chemical medium for
28
promoting blooms. While this is probably a valid conclusion for algal blooms in general,
the relevance of this conclusion to the Chrysophyceae in particular has not been well
defined, especially for freshwater populations. Although chrysophyte blooms have
resulted from experimental fertilizations, a number of whole-lake and in-lake enclosure
fertilization experiments have not produced chrysophyte blooms. The triggering of a
chrysophyte bloom likely depends on the achievement of fundamental growth conditions
which are species specific and which may be realized only when the “right” combination
of natural and anthropogenically derived variables comes together. These natural
environmental variables could include temperature, salinity, hydrologic flushing rate,
turbulence, light, grazing, and inter-species competitions and inhibitions. Because these
natural influences are multi-factorial and highly interactive, their combinations in ways
that could trigger algal blooms are not predictable, given our present level of
understanding of the ecology of the most important bloom-forming species. A number of
experimental approaches to specific questions about the role of volatile excretory
substances as inhibitors of other algae, the role of bacteria either directly as an energy
source for phagotrophic chrysophytes, or indirectly as facilitators of nutrient availability,
and the role of chrysophyte motility (vertical migration), zooplankton grazing and light
effects are among those topics suggested as fruitful lines of future research on the
chrysophyte bloom phenomenon.
29
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56
TABLE 1 Common odours in the influents of three drinking water utilities
expressed as percentage occurrence of all odours.
UTILITY ODOUR PERCENTAGE
CHARACTERIZATION OCCURRENCE
Philadelphia Suburban "sewage" 83
Water Co. "creeky” 20
"musty” 10
Philadelphia Water "decaying vegetation” 62
Ea. "septic (sewage)” 52
vegetation” 22
“earthy” 43
"musty” 17
“fishy” 13
Lyonnaise Des Eaux “muddy” at
"fishy” 71
“musty” 38
"septic” 29
From Bartels et al. (1989)
oy)
TABLE 2 Densities of organisms associated with odours in drinking water from Lake Lyseren,
Norway.
ORGANISM CONCENTRATION DATE
(cells/mL)
Chlamydobacteria 2000 July 27, 1976
Chlorococcales 193 July 27, 1976
Asterionella formosa Hass. 60 July 31, 1975
Tabellaria fenestrata (Lyngb.) Kitz. 145 July 31, 1975
Dinobryon divergens Imh. 560 August 1, 1975
D. sociale var. stipitatum (Stein) Lemm. 2000 July 31, 1975
Chrysomonads 12000 July 31, 1975
From Berglind et al. (1983)
6S
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TABLE 4 Volatile excretory products of three algal species, including the chrysophyte Synura uvella.
Location and Date Dominant Species Excretory Products
Lake Constance Anabaena sp. dimethyldisulfide
17 October, 1978
Lake Constance Asterionella formosa octadiene
19 July, 1979 octatriene
Wahnbach Reservoir Synura uvella penten-3-one
10 October, 1978 pentanone-3
octanone-3
octanol-1
octanol-3
oct-1-en-3-ol
2-pentylfuran
trans, cis-2,4-decadienal
B-cyclocitral
6-methylhept-5-en-2-one
B-ionone
From Juttner (1981)
TABLE 5 Summary of chrysophyte responses to experimental nutrient additions
REFERENCE LAKE TREATMENT RESPONSE
Langford (1950) Four lakes in Apgr. fertilizer All lakes responded 3-4 weeks after treatment
Algonquin (12-24-12); 0.05- with large increases in diatoms and
Park, Ontario 0.9 mg P/L Dinobryon (and Synura in one lake)
Smith (1969) Crecy Lake 210 ug N/L;390 Main response was in Anabaena and
ug P/L; 270 ug Spirogyra blooms, but Dinobryon bloomed in
K/L 1961, three years after the last fertilization.
Schindler et al. ELA Lake Two years of Dinobryon and Synura occasionally among
(1971, 1973), (Kling 304 each of the dominants in early summer of some years
and Holmgren following
(1972), Findlay and treatments: N, P
Kling (1975), and C; N and C;
Findlay (1978, 1981, N and P
1983)
See above ELA Lake Four years of Dinobryon, Mallomonas, and Synura
261 HPO, additions consistently among the dominants; Uroglena
important only in 1975
See above ELA Lake Inorganic P and Inconsistent response with occasional
227 N added weekly domination by Dinobryon and Mallomonas
for several years spp in some years.
Findlay and Kasian ELA Lake Basin divided by Dinobryon less important in 206NE;
(1987) 226NE and a curtain; 226NE _ occasional dominance by Synura in both
226SW fertilized with N, basins; Uroglena was a dominant in 226NE
P and C, and during all three post fertilization years.
226SW, with N
and C.
Ramberg (1976) Lakes Fertilization for Chrysophyte portion of total phytoplankton
Vitalampa one year with showed little change from pre-fertilization
and Botjarn, NH,NO, years
Sweden
Witt (1977) Vorderer Additions of P as Shift from dinoflagellates to chlorophytes; no
Finstertaler NaH,PO, response in chrysophytes
See, Austria
DeNoyelles and eight 0.1 ha N, P and K in Chrysophytes remained dominant in reference
O’Brien (1978) ponds, low, medium and ponds, but were replaced by chlorophytes and
Cornell Univ.
high dose rates
61
cyanophytes in treated ponds
Reinertsen (1982)
Yan and Lafrance
(1984)
Yan and Lafrance
(1984)
Wilcox and
DeCosta (1984)
Holmgren (1984)
Chow-Fraser and
Duthie (1987)
Olofsson et al. (1988)
Lake
Langvatn,
central
Norway
Mountain top
and Labelle
Lakes,
Sudbury, Ont.
Lakes,
Sudbury, Ont.
Cheat Lake,
W. Virginia
Four lakes in
the Kuokkel
area of N.
Sweden
An
embayment of
Sweden
N, P and K
supplied as
commercial
fertilizer in 1975
and 1976
P and N added as
20-40-0
commercial
fertilizer and as
H,PO, and
NH,NO,
P added as
HPO,
P added to
enclosures as
KH,PO,
N and P added as
NH,NO, and
HPO, in various
combinations
over several years
N and P added as
NH,H,PO,
Continuous low
dosage of N and
P in commercial
fertilizer
62
No major response among Synura, Uroglena
or Dinobryon (all three present
prefertilization)
Dinobryon and Mallomonas spp replaced by
other algae, mainly Cryptomonas spp
Low level fertilization resulted in continued
domination of chrysophytes; higher
fertilization rates led to replacement by other
groups
Dinobryon replaced by chlorophytes
Additions of N alone stimulated Uroglena; N
and P additions to the same lake the
following year led to dominance by Uroglena
and Dinobryon, but by cryptophytes in
another lake; additions of P alone inhibited
Dinobryon spp
Dinobryon crenulatum was one of 17 taxa
showing a significant increase
Chrysophytes dominated before and after
fertilization with only minor shifts in
community composition
REDUCED PRECIPITATION
lower but
adequate
supply of
nutrients
reduced flushing
elevated
salinity
Aureococcus
bloom
development
overwintering
inoculum
An hypothesis relating precipitation and associated physical-chemical changes to development of Aureococcus
Figure 1
blooms in Long Island embayments (after Cosper et al. 1990).
Figure 2
odour from species “A” ———\
TA
species “B’
cell density
species “A
time (days) Â
Hypothetical population density changes over time for two phytoplankton species, "A" and "B", of which, only
species "A" is an odour producer. If sampling and identification are done at the peak of odour production but
after the population has peaked (arrow), species "B" may be erroneously implicated as the cause of the problem.
Growth Rate (doublings-day')
(D,) eanyesodue |
Figure 3
The effects of temperature on the growth rate of cultured Synura sphagnicola at eight different light intensities
ranging from 11-110 HE/M°/s (from Healey 1983).
HUMAN INFLUENCES
ATMOSPHERIC
DEPOSITION
LAND AND
WATER USE
read nutrients
issolve
i leas bacteria
organic elements G
masi toxins nutrients
nutrients and me
trace elements Ht pesticides
(e.g. Co) ‘
alkalinity i. phytoplankton
loss "| stimulation
toxin
"neutralization"
zooplankton
toxicity
destruction
of fish
habitat
trace metal
chelation decreased
phytoplankton
grazing
overfishing
of large
piscivores
vitamin
synthesis
increased predation
on large zooplankters
by small fish
fe.
7
Figure 4 The interactions of a number of factors originating from human influences and their stimulatory effect on
phytoplankton in a hypothetical software lake.
1.0
N S
Biovolume N N N
3 N N N
mm*/L N Synura N gs A =
0.1 N N N A N
Q WN Sù \) NS NS NS NS
NE oN N N SN N Bs NS
N N N A N N A N
N N ON N NS RN 2 NN
NN NN BS N N RA NY RS N
N N NN & N N R NN A
N A NS NH N NAN N N À
MmINNay &N NN NANA N N À
cotN NNN SN NN NS Sn 2 S NN
0.02
0.1 C. breviturrita
1976 1978 1980 1982 1984 1986 1988 1990
Saar 1977 1978 1979
=
® 2
E Synura
S 1
‘2 0 Fes aa aoe ‘om 01 -
2 “
où
à ie
os 2 C. breviturrita
3
Figure 5 a) Annual average biovolume of Chrysochromulina reviturrit and Synura spp. in the phytoplankton of Dickie
Lake, 1976 - 1990; b) Seasonal distributions of C. and Synura spp., 1976 - 1979 (Nicholls unpubl).
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