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Journal of Plankton Research Vol.22 no.5 pp.987–995, 2000
SHORT COMMUNICATION
Relative abundance, rate of increase, and fungal infections of
freshwater phytoplankton
Harald Holfeld
Max-Planck-Institut für Limnologie, Abteilung Ökophysiologie, Postfach 165,
24302 Plön, Germany
Present address: Limnologische Flußstation des Max-Planck-Instituts für
Limnologie, Postfach 260, 36105 Schlitz, Germany
Abstract. Fungal infections of seven species of phytoplankton were examined in relation to the host
species’ exponential rate of net increase, and to their proportional contribution to the total phytoplankton biovolume. Infections were observed to increase at biovolume proportions of the host
species of as low as 1%. In most algal species, infected cells were always found at higher proportions,
with the exception of Stephanodiscus rotula and Fragilaria crotonensis. In these two species, high
proportions of biovolume were reached without any evidence of infected cells. The increase in
infected cells was usually associated with a growing host population, whereas peak and decreasing
densities of infected cells were usually observed when host populations were declining. The results
show that the fungal parasites can exist on their host population even if it comprises only a small
fraction of the total phytoplankton biovolume, and that the parasites become evident while the host
population is still increasing.
In addition to phagotrophic mortality from zooplankton grazing, phytoplankton
are subject to non-phagotrophic mortality from parasitic infections (Hutchinson,
1967; Reynolds, 1984; Lampert et al., 1997). Freshwater phytoplankton species
can be infected by oomycetes and chytridiomycetes [e.g. (Canter-Lund and Lund,
1995)]. These parasites are dispersed as flagellated zoospores. During dispersal,
the zoospores depend on internal energy storage. After contact with a suitable
host cell, they settle upon it and grow into a thallus that exploits the host cell
contents. The host cell is harmed or more usually killed by the parasites (CanterLund and Lund, 1995). Infection can occur over a wide range of environmental
conditions and at low densities of the host alga (Holfeld, 1998).
In general, parasites are adapted to exploit small discontinuous environments,
represent the extreme in specialized resource exploitation and exist in nonequilibrium conditions (Price, 1980). These criteria are fully applicable to fungal
parasites of phytoplankton: they completely rely on the host cell for nourishment,
one individual usually infects only one host cell or colony, they are host-species
or even host-race specific, and they depend on a resource whose density can
change over several orders of magnitude within a few weeks.
In terrestrial plant populations, the level of disease can be reduced if the susceptible individuals grow in mixed stands together with resistant plants, an effect
attributable to inoculum interception (Burdon, 1987). This concept applies to
pathogens with non-motile, passively dispersed propagules such as conidia,
ascospores or basidiospores. Zoosporic fungi, in contrast, are dispersed over short
© Oxford University Press 2000
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Table I. The host algae and their parasites
Host alga
Parasite
Reference of parasite description
Stephanodiscus alpinus
Stephanodiscus rotula
Asterionella formosa
Zygorhizidium sp. 1
Unknown operculate chytrid
Rhizophydium planktonicum
Rhizophydium tetragenum
Zygorhizidium affluens
Zygorhizidium planktonicum
Zygorhizidium sp. 2
Rhizophydium tetragenum
Zygorhizidium planktonicum
Hapalopera piriformis
Zygorhizidium parallelosede
–
–
(Canter, 1969)
(Pongratz, 1966)
(Canter, 1969)
(Canter and Lund, 1953)
–
(Pongratz, 1966)
(Canter and Lund, 1953)
(Fott, 1942)
(Canter, 1954)
Fragilaria crotonensis
Synedra acus
Ankyra judayi
Elakatothrix genevensis
distances by motile, actively swimming propagules. Encounter of host cell and
parasite zoospore is not simply determined by the surface area or by the geometric
size and shape (‘effective cross-section’) of the potential host cell which is hit by
the zoospore’s swimming path. As has been shown (Canter and Jaworski, 1981,
1982, 1983, 1986), there is an attraction mechanism involved which is triggered by
light supply to the host cell and which includes the release of chemicals by the host
cell (Roos, 1989). However, the attraction of parasite zoospores to algal cells
seems to be relatively unspecific. In laboratory experiments with zoospore suspensions of several diatom parasites, Canter and Jaworski recorded attraction to a
wide range of non-host algae, including pennate and centric diatoms, the green
alga Staurastrum and the blue-green Oscillatoria (Canter and Jaworski, 1981, 1982,
1983, 1986). Dead material and heat-killed algal cells caused no attraction (Canter
and Jaworski, 1981). Therefore, the possibility exists that the presence of living
non-host algae interferes with host detection by the parasite zoospores. In this
case, the proportion of the host algae within the total phytoplankton population
at which infection, especially the increase in infection, can be observed is a reasonable measure of the zoospores’ ability to detect their resource.
To demonstrate this ability, the proportions of each of seven host species (five
diatoms and two green algae) were calculated (Table I) within the total biovolume of the phytoplankton. Naturally occurring epidemics in a lake could be
followed in these phytoplankton species in some detail. In the host–parasite
associations considered, the host cell dies during the infection, leaving empty frustules or cell walls following dehiscence of the parasite sporangium. For identification of the parasites, it was necessary to consult the original descriptions
(Table I). With some experience, it was possible to recognize infected algal cells
even if they were only infected by early stages of the parasites. These biovolumeproportional data for each host species were related to changes in the absolute
density of infected cells of that host species. The characteristics of the parasites
involved, and the seasonality of the host species as well as the prevalence of infection, have been reported by Holfeld (Holfeld, 1998).
This study was carried out at Schöhsee, a stratified hardwater lake near Plön,
North Germany (54°N), which has no permanent surface directional flow.
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Fungal infections of freshwater phytoplankton
Phytoplankton are by far the dominant fraction of the seston in this lake (H.Rai,
personal communication) and are, therefore, likely to play the principal role in
the interaction between particles and parasite zoospores.
Samples were taken from the upper, mixed layer of the lake. A subsample
was fixed with several drops of Lugol’s solution and examined using an inverted
microscope. Where possible, 400 individuals of each phytoplankton species,
infected and uninfected by fungi, were counted to give a counting precision of
±10% within 95% confidence limits, assuming the cells are randomly distributed (Lund et al., 1958). Host cells bearing at least one dehisced parasite
sporangium were considered to be dead and were not counted. Samples were
taken weekly between 17 March 1987 and 2 May 1989, except for a 10 week
period from 14 December 1987 until 22 February 1988 when no samples were
taken.
The cell volumes used to estimate the biomass of individual phytoplankton
species were based on measurements by U.Sommer (personal communication),
on the list of Kümmerlin and Bürgi (Kümmerlin and Bürgi, 1989) and on direct
measurements. In the latter case, the cell shape of a given phytoplankton species
was approximated as that of the nearest corresponding geometric figures (Rott,
1981), and the relevant dimensions of ~30 cells from each species were measured.
The volume of each single cell was estimated and these individual volumes were
used to calculate the mean volume for a given species. The total phytoplankton
biovolume was calculated as the sum of the biovolumes of all phytoplankton
species co-occurring at a given sampling date. The proportion of the host species
is given as a percentage of the total phytoplankton biovolume.
The population density of phytoplankton species can change dramatically over
a short period of time. The challenge for a parasite is to take advantage of an
increasing host population so as to be able to increase its own numbers. Given
the dynamic nature of phytoplankton populations, a critical factor is the developmental phase of the host population at which the absolute numbers of infected
cells can increase. Thus, the exponential rate of net increase of the host species,
kn, was calculated according to the formula:
kn = (ln N1 – ln N0)/(t1 – t0)
where N0 is the cell concentration of the host species at the start of the time interval being considered (t0) and N1 is the cell concentration at the end of the time
interval (t1) (Reynolds, 1984). In this study, the length of the time interval is 1
week according to the sampling schedule. Here, the exponential rate of net
increase is calculated per day (day–1).
For each host alga, samples without and with infected cells were distinguished.
In the latter case, a further distinction was made between ‘increasing’ (preceded
by a lower value and followed by a higher value), ‘peak’ (preceded by a lower
value and followed by a lower value) and ‘decreasing’ (preceded by a higher value
and followed by a lower value) absolute density (cells ml–1) of the infected cells
of the host alga.
On some occasions, the diatoms were dominant components of the phytoplankton (Figure 1). In contrast, the two green algae were never prominent in
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H.Holfeld
(a)
(b)
Fig. 1. Occurrence of chytrid infections in seven phytoplankton species in relation to the proportion
of phytoplankton biovolume and exponential rate of net increase of the host species.
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Fungal infections of freshwater phytoplankton
(c)
(d)
Fig. 1. continued
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H.Holfeld
(e)
(f)
Fig. 1. continued
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Fungal infections of freshwater phytoplankton
(g)
Fig. 1. continued
terms of biovolume. The proportion of Ankyra judayi never exceeded 3%. The
situation was even more extreme with Elakatothrix genevensis, which was
recorded frequently, but only once exceeded 1% of the phytoplankton biovolume. Despite their unimportance in terms of proportion of biovolume, these two
species each harboured a specific and morphologically highly characteristic parasite (Fott, 1942; Canter, 1954). In all host species, infections were observed at low
proportions. Increases in the number of infected cells also occurred at these low
proportions. The phytoplankton species at higher proportions usually contained
infected cells, with the notable exceptions of Stephanodiscus rotula and Fragilaria
crotonensis. In these species, no infected cells were found at high proportions.
One might expect that an increase in infection required especially favourable
conditions. However, the species proportion at increasing infection did not differ
significantly from the species proportions in the remaining observations of
infected cells in any of the host species (Mann–Whitney U-test, always P > 0.12).
With the exception of S.rotula and E.genevensis, infections were found more
often in decreasing host populations. In contrast, increases in the density of
infected cells were generally associated with positive rates of net increase
(Figure 1; Table II). There were only a few decreases in infected cells at times of
net increase in the host algae.
This observation raises the question as to how parasitism can function at such
dilute host populations. The poor specificity reported for zoospores at the phase
of attraction to host or non-host cells (Canter and Jaworski, 1981, 1982, 1983,
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H.Holfeld
Table II. Median values of the exponential rates of net increase in seven algal species. The number of
observations (n) are given in parentheses. The records are differentiated according to the presence
and the tendency of the number of infected cells. The data for algae with infection in general and with
increasing, peak and decreasing infections were each compared with the rest of all observations of
algae (Mann–Whitney U-test)
Host alga
All
Algae
observations infected
of algae
Algae with
increasing
infection
Algae with
peak
infection
Algae with
decreasing
infection
Stephanodiscus alpinus
Stephanodiscus rotula
Asterionella formosa
Fragilaria crotonensis
Synedra acus
Ankyra judayi
Elakatothrix genevensis
0.02 (49)
0.01 (66)
–0.03 (89)
–0.01 (72)
0.00 (59)
–0.02 (47)
0.02 (86)
0.06 (4)
0.13* (3)
0.09* (7)
0.06 (4)
0.06 (9)
0.07 (4)
0.09* (8)
–0.02* (5)
–0.07 (4)
0.01 (9)
0.01 (10)
–0.01 (8)
–0.03 (5)
0.06 (15)
–0.09* (6)
–0.07 (3)
–0.16* (12)
–0.10* (8)
–0.18* (9)
–0.06 (4)
–0.04* (18)
–0.01* (17)
0.01 (10)
–0.03 (32)
–0.04 (25)
–0.03* (27)
–0.03 (15)
0.03 (46)
*P < 0.05.
1986) should result in deleterious zoospore losses. However, the attraction to cells
is reversible. Canter and Jaworski found that zoospores of Rhizophydium planktonicum swam in tighter circles when approaching a host cell, eventually coming
into contact with it (Canter and Jaworski, 1981). After contact, the smooth swimming motion of the zoospores became jerky and they rubbed against the diatom
walls. Presumably, the disposition for encystment of the zoospore occurs during
this phase because this process seems to be much more specific than the attraction of the zoospores to algal cells. Several non-host diatom species tested by
Canter and Jaworski (Canter and Jaworski, 1978), including those reported to
cause attraction (Canter and Jaworski, 1981), bore zoospore cysts of R.planktonicum only rarely. Similar results have been reported for the zoospores of
Zygorhizidium planktonicum (Canter et al., 1992) and Rhizophydium fragilariae
(Canter and Jaworski, 1982).
In this study, the parasites were able to respond quickly to an increase in host
cell density. They were not dependent on declining and possibly ‘weakened’ host
populations, and they had the potential for fast growth. Bruning showed that the
maximum growth rate of R.planktonicum was always higher than the phosphorusand light-dependent growth rate of the host Asterionella formosa, except at low
temperatures (Bruning, 1991a,b). Thus, as observed in natural phytoplankton
(Holfeld, 1998), numbers of infected cells can increase disproportionately to a
greater extent in actively growing host populations.
Acknowledgements
This work was supported by a grant from the Max Planck Society. The director
of the Max Planck Institute of Limnology, Professor W.Lampert, provided
research facilities. Professor U.Sommer initiated this investigation and gave
helpful advice during the work. Dr Douglas M.Fiebig improved the English and
made helpful comments.
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Received on June 27, 1999; accepted on November 22, 1999
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