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Limnd.
Nitrogen-fixing cyanobacteria in the plankton of lakes and
estuaries: A reply to the comment by Smith
Smith (1990) has uncovered an interesting pattern between concentrations of total
P (TP) and aereal rates of N fixation in a
diverse set of aquatic ecosystems. However,
we disagree with his suggestion that this relationship generally holds true in estuaries,
Acknowledgments
We thank N. Hairston, Jr., and D. Rudnick for comments on our reply. We also thank V. H. Smith for
sharing earlier drafts of his comment.
and we believe he is premature in rejecting
the hypothesis that N : P loading ratios are
of importance in regulating N fixation in
lakes.
Smith’s pattern between TP and N fixation for estuaries (his figure 4) does indeed
resemble that for lakes (his figure 3), except
that for a given TP concentration, N fixation
rates appear higher for the estuarine data.
Unfortunately, the analysis includes data
only from the Baltic Sea and the Harvey
1860
Comment
estuary (Australia), and the apparent relationship between TP and N fixation rates is
driven entirely by data from the Harvey.
Although he cannot be faulted for including
only these two estuaries in his analysis since
published data on rates of planktonic N fixation are not available for any other estuaries (Howarth et al. 1988a), we cannot accept these two estuaries
as being
representative. For instance, unpublished
data indicate that rates of N fixation are
immeasurably low in Narragansett Bay (S.
Seitzinger pers. comm.; J. Cole pers. comm.)
even though the growing season mean TP
concentration
is -70 mg mm3 (Pilson
1985) -higher than for any of the Baltic stations used by Smith.
Not only is his relationship between TP
and N fixation in estuaries driven by data
from only one estuary (the Harvey), but
those data are not direct measures of N fixation and may significantly overestimate
rates. With the exception of the Harvey data,
all of the N fixation data used by Smith are
based on acetylene reduction assay. For the
Harvey, he used estimates based on watercolumn N budgets during the time of Nodularia blooms, roughly 2 months each year
(Lukatelich and McComb 1986). These indirect estimates of N fixation are 4-5 times
higher than rates measured by acetylene reduction assay in the Harvey (Huber 1986)
probably because the mass balances include
N fluxes from sediments to the water column. Such fluxes are high in these shallow
waters, in part due to resuspension of sediments (Lukatelich and McComb 1986). We
suspect that the relationship seen in Smith’s
figure 4 between P concentrations and “N
fixation” in the Harvey estuary may be a
result of a correlation between sediment P
and sediment N fluxes in various years.
Rates of N fixation are indeed high in this
estuary (1.2 g N m-* yr-‘; Huber 1986; Howarth et al. 1988a), but not as high as the
estimates used by Smith (up to 12 g N m-*
yr’, with a mean value of 5.3 g N mm2yr-I).
Rates of N fixation by plankton in most
estuaries in the world are probably low
(Nixon and Pilson 1983; Howarth 1988;
Howarth et al. 1988a), as indicated by the
virtual absence of species of heterocystic cyanobacteria in the plankton of most estu-
aries and coastal seas (Home 1977; Howarth et al. 1988b). In this regard, we believe
the Harvey estuary and the Baltic Sea should
be viewed as interesting exceptions rather
than as typical estuaries. Significant rates of
N fixation in the oxic water columns of lakes
have always been found to be associated
with heterocystic cyanobacteria (Stewart
1969; Granhall and Lundgren 197 1; Home
and Goldman 1972; Paerl et al. 198 1; Home
et al. 1972; Carr and Whitton 1982; Levine
and Lewis 1984, 1985; Home and Galat
1985). This is also true for the Harvey estuary (Huber 1986) and the Baltic Sea
(Brattberg 1977; Hiibel and Hi.ibel 1980;
Lindahl et al. 1980; Lindahl and Wallstrom
1985). Although many species of heterotrophic bacteria are capable of fixing N (Paerl
1990), N fixation by heterotrophic bacteria
in the water column of lakes has only been
reported as a significant process (i.e. measurable) in anoxic hypolimnetic
waters
(Brezonik and Harper 1969; Keim and Brezonik 197 1).
Since dissolved inorganic P (DIP) concentrations are higher in most temperate estuaries than in the Baltic Sea (Boynton et
al. 1982), we question whether the absence
of heterocystic cyanobacteria from most estuarine and coastal marine waters is a result
of low P concentrations. An experimental
addition of P to the MERL tanks at the
University of Rhode Island in summer 1988
increased DIP values to 300 mg mm3, yet
virtually no heterocystic cyanobacteria were
found in the plankton (Frithsen et al. unpubl. data).
We have extensively discussed potential
reasons why rates of N fixation by plankton
in most estuaries and coastal seas are not
higher (Howarth and Cole 1985; Howarth
1988; Howarth et al. 19888; Marino et al.
1990). We have hypothesized that low
availabilities of MO and Fe (either alone or
interactively) limit rates of N fixation in oxic
marine waters. Turbulence (Carpenter and
Price 1976; Doremus 1982; Paerl 1985) and/
or relatively low light levels resulting from
turbid waters and deep mixed layers in estuaries may also limit plankton N fixation.
These physical factors may interacct with
trace-metal limitations to make N fixation
Comment
particularly difficult in most estuaries (Howarth et al. 1988b; Marino et al. 1990).
Why are rates of N fixation high in the
Harvey estuary and in portions of the Baltic
Sea? This is an interesting and still unanswered question. The Baltic Sea has very
low salinities (generally < 6%~as opposed to
35o/oofor full-strength seawater), but this is
not true of the Harvey estuary. However,
we note that the Baltic Sea has very high
levels of dissolved organic matter (Wulff and
Stigebrandt 1989) which may interact with
Fe and MO to make these metals more available in the water column (Howarth et al.
1988b). The Harvey estuary has anoxic and
hypoxic events associated with its cyanobacterial blooms (Lukatelich and McComb
1986); reducing conditions also may increase trace metal availabilities (Howarth et
al. 1988b). Potential reasons for the relatively high rates of N fixation in the Baltic
Sea and Harvey estuary were discussed further by Howarth et al. (19886).
Salt lakes provide another test of the generality of Smith’s hypothesis that TP controls rates of N fixation in both saline and
freshwaters. We recently published a study
on the controls on abundance of N-fixing
cyanobacteria in a set of saline lakes in Alberta (Marino et al. 1990). Although TP is
a good predictor of the relative abundance
of cyanobacteria in the plankton of freshwater lakes in Alberta (Trimbee and Prepas
1987), it is not true for Alberta salt lakes.
In fact, the relative abundances of N-fixing
cyanobacteria are inversely correlated with
TP concentrations in these lakes (Marino et
al. 1990). MO availability, as indicated by
the ratio of SO, : MO, proved to be the best
predictor of the relative abundance of Nfixing cyanobacteria in these saline lakes
(Marino et al. 1990). Our preliminary data
on MO concentrations in Pyramid Lake, a
salt lake with significant rates of N fixation
and included in the data set used by Smith,
indicate a low SO, : MO ratio, suggesting that
Pyramid Lake fits the pattern we found in
the Alberta salt lakes and that its relatively
high rates of N fixation should be expected
(Marino et al. 1990).
With regard to N fixation in freshwater
lakes, Smith rejects the hypothesis that the
N : P ratio of nutrient inputs is an important
1861
regulator (Schindler 1977; Howarth et al.
19886). We believe such a rejection is premature. We agree that N fixation rates by
plankton are related to P concentrations
(Home and Goldman 1972; Vanderhoef et
al. 1974; Howarth et al. 19888) but N concentrations also play a major role (Horne
and Goldman 1972; Car-r and Whitton 1982;
Howarth et al. 19886). The process of N
fixation is energetically expensive, and cyanobacteria gain a competitive advantage
by fixing N only when the ratio of available
N to available P is low (Tilman et al. 1982).
Thus, significant rates of N fixation by
plankton in lakes should only be expected
when the ratio of available N to available
P is low (Howarth et al. 19886).
Unfortunately, N and P availabilities are
not necessarily the same as concentrations,
and one generally is forced to use some imperfect measure to approximate the relative
availabilities of N and P in lakes. Ratios of
N: P concentrations in the water column,
either total (TN: TP) or inorganic (DIN:
SRP), are possible surrogate measures of
the ratio of N : P availabilities. The TN : TP
ratio will overestimate the ratio of available
N to available P because organic P is more
available than organic N (Howarth 1988).
The DIN : SRP ratio will underestimate the
ratio of available N to available P because
SRP includes some organic phosphate esters. Also, both TN : TP and DIN : SRP ratios can vary greatly in time. The annual
N : P loading ratio is just another surrogate
measure of the ratio of available N to available P; it also is an imperfect measure because biogeochemical processes in a lake will
alter the relative availabilities of N and P
compared to the loading inputs.
Nonetheless, from experiments at the Experimental Lakes Area (Schindler 1977; Flett
et al. 1980) and from our review of the literature (Howarth et al. 1988b), the N : P
loading ratio appeared to be a reasonable
predictor of whether N fixation by plankton
would occur in lakes. Most of the lakes included in Smith’s analysis (his figure 1) also
fit this pattern. Only two lakes with N : P
loading ratios above 15 (mass ratio: equivalent to a molar N : P ratio of 34) have significant rates of N fixation. Both lakes (Sodra Bergundasjon and Shagawa) are shallow,
Comment
with significant sediment-water exchanges
that can have a large influence on the ratio
of available N to available P in the water
column (Toetz and McFarland 1987). One
must also remember that loading estimates
are often subject to great error. The data
supporting the estimates for loading to Shagawa are unpublished, and the loading estimates to both Shagawa and SGdra Bergundasjon may well be in error because they
do not include subsurface inputs (Toetz and
McFarland 1987).
In conclusion, P is one important control
on planktonic N fixation, but we do not
believe it is the only important control. N
fixation rates in many saline waters are
probably low even at relatively high P concentrations. Other controls such as N availability, trace metal availabilities,
turbulence, and light are probably significant
(Howarth et al. 19 8 8b). Our conclusion must
be tempered: given the sparcity of actual N
fixation data in many saline waters, we have
been forced to draw inferences from abundances of N-fixing cyanobacteria. Future
work should measure rates of N fixation
directly in a variety of estuarine ecosystems
and saline lakes (Howarth et al. 1988b).
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