Limnol. Oceanogr., 56(4), 2011, 1545–1547
2011, by the American Society of Limnology and Oceanography, Inc.
doi:10.4319/lo.2011.56.4.1545
E
Comment: Lake 227 shows clearly that controlling inputs of nitrogen will not reduce or
prevent eutrophication of lakes
M. J. Paterson,a,* D. W. Schindler,b R. E. Hecky,c D. L. Findlay,a,1 and K. J. Rondeaub
a Freshwater
Institute, Fisheries and Oceans Canada, Winnipeg, Manitoba, Canada
of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada
c Department of Biology, University of Minnesota, Duluth, Minnesota
b Department
The conclusion from our earlier paper, that decreasing
nitrogen (N) inputs to lakes does not substantially reduce
symptoms of eutrophication (Schindler et al. 2008), was
recently challenged by Scott and McCarthy (2010). They
reanalyzed graphs from our paper showing data from Lake
227 at the Experimental Lakes Area (ELA) in Ontario,
which was artificially eutrophied with N and phosphorus
(P) from 1969 through 1989 and with P alone from 1990
until the present. They interpreted declining trends in total
nitrogen (TN), chlorophyll a (Chl a), and phytoplankton
biomass to mean that the lake became less eutrophic after
N inputs were terminated in 1990. They then concluded
that ‘‘the degree of eutrophication can be controlled by
managing N inputs concurrently with P.’’
We now have four more years of data for Lake 227, for a
total of 41 yr at a constant P loading rate. Schindler et al.
(2008) review the loading history of Lake 227, while
Findlay et al. (1994) give full N and P budgets from 1970 to
1992. All samples were collected and analyzed using
consistent methods (Stainton et al. 1977; Findlay et al.
1994; Schindler et al. 2008). Statistics reported below were
calculated using SYSTAT 12 (SYSTAT 2007). We have
used a threshold for significance of 0.05; and, to remain
consistent with Scott and McCarthy (2010), we have not
corrected probabilities for multiple comparisons.
Reanalysis of our results including the more recent data
clearly refutes the conclusion of Scott and McCarthy that
the lake has become less eutrophic as the result of decreased
inputs of N. There has been no significant declining trend
in either Chl a (r 5 20.26, p 5 0.27, n 5 20) or
phytoplankton biomass (r 5 20.22, p 5 0.36, n 5 20) since
we ceased adding N to the lake in 1990 (Fig. 1a,b).
Separate analyses of trends after 1996, which Scott and
McCarthy used to make many of their arguments, are not
different from those for 1990–2009 (Chl a: r 5 20.16, p 5
0.61; phytoplankton biomass: r 5 20.35, p 5 0.14; n 5 13).
In fact, there is no significant trend in the annual average
Chl a or biomass over the 41 yr since fertilization with P
began, regardless of the N : P ratio used in loading (Chl a: r
5 20.05, p 5 0.77; biomass: r 5 20.23, p 5 0.14). We note
that in fig. 1 of Schindler et al. (2008), the 1975 data point
for Chl a was repeated for 1976 and all subsequent points
were offset in error by 1 yr. This error does not affect the
* Corresponding author: [email protected]
1 Present address: Plankton R Us, Winnipeg, Manitoba,
Canada
major conclusions of Schindler et al. (2008) and only
marginally affects the correlations undertaken by Scott and
McCarthy (2010).
The biomass of Cyanobacteria (not shown) also showed
no significant trend over time (r 5 20.38, p 5 0.10, n 5 20
after 1990; r 5 0.08, p 5 0.60, n 5 41 for the entire data
set). However, the abundance of heterocysts has increased
significantly (r 5 0.59, p , 0.0005, n 5 36), particularly
after reduction of N loading in 1990 (Fig. 1c). Using the
regression equation of Finday et al. (1994), which is based
on studies of Lake 227 by Hendzel et al. (1994), this
increase in heterocyst abundance indicates that N fixation
has increased considerably since 1990 (Fig. 1d; r 5 0.61, p
5 0.005, n 5 20). The rate of increase in heterocysts
roughly doubled after 1997, indicating that N fixation is
still increasing. This observation reinforces our earlier
arguments (Schindler et al. 1977, 1987) that the responses
of lakes to changes in nutrient inputs result from slow
changes in species and biogeochemical processes, requiring
several years to fully play out. Successful strategies to
control eutrophication must account for these rates of
change.
The negative trend in TN concentrations after 1990
identified by Scott and McCarthy continues to be
significant with our longer data set (1990–2009: r 5
20.74, p , 0.0005, n 5 20) (Fig. 2a). Over the same time
period, there is no significant change in total phosphorus
(TP) (r 5 20.18, p 5 0.26, n 5 20) or TN : TP (r 5 20.32, p
5 0.16, n 5 20) (Fig. 2c,d). Most of the decrease in TN is in
total dissolved nitrogen (TDN) (r 5 20.70, p , 0.0005, n 5
20; Fig. 2b) and there are also significant declines in the
ratios of dissolved inorganic nitrogen : total dissolved
phosphorus (DIN : TDP; r 5 20.50, p 5 0.02, n 5 20)
and TDN : TDP (r 5 20.45; p 5 0.05, n 5 20) (not shown).
Clearly, reduction in artificial N loading has resulted in
lower N concentrations in Lake 227. N limitation for many
species of phytoplankton may also have increased because
of declines in DIN, which includes the forms of N that are
most available to many phytoplankton species. However,
N-fixing cyanobacteria increased after the cessation of
artificial N loading (Schindler et al. 2008), clearly
demonstrating their ability to offset declines in DIN, and
overall algal abundance has remained proportional to
annual P loading, which has been constant since 1969. To
be effective, eutrophication management must reduce
excessive phytoplankton abundance. The Lake 227 data
show that reductions of N in the absence of reductions in P
will shift the competitive advantage to N-fixing cyanobac-
1545
1546
Paterson et al.
Fig. 1. Annual average measures of phytoplankton abundance in Lake 227. (a) Chl a; (b) phytoplankton biomass. The
vertical dashed lines indicate when N fertilizer was reduced in
1975 and then eliminated in 1990. Annual P additions remained
constant throughout the 41-yr period. The strong decrease in
chlorophyll and phytoplankton biomass in 1996 resulted from a
large, but temporary increase in Daphnia following the introduction of predatory fish (Schindler et al. 2008). (c) Increases in
heterocysts from 1975 to 2009. N-fixing cyanobacteria were
absent before 1975, when inputs of N fertilizer were decreased. (d)
Changes in N fixation calculated from heterocyst counts using the
regression equation of Findlay et al. (1994).
teria and allow them to increase their dominance. In Lake
227, competitively favored N-fixing cyanobacteria increased their biomass until ultimately limited by P so that
the overall yield of phytoplankton was not affected after N
reduction or the elimination of artificial N inputs.
Changes in food web structure also do not appear to
have affected long-term phytoplankton dynamics in Lake
227. The extirpation of dense cyprinid populations
following the addition and removal of pike (Esox lucius)
in 1993–1994 and 1996, respectively, resulted in a 1-yr
increase in Daphnia pulicaria in 1996 (Elser et al. 2000).
Afterwards, zooplankton and phytoplankton community
structure rapidly returned to pre-pike conditions (Fig. 2e).
The inclusion of four more years of data from Lake 227
provides no support for the contention of Scott and
McCarthy (2010) the lake ‘‘has become increasingly Nlimited since N fertilization was halted and indicate that N
Fig. 2. Annual average trends in the ice-free season in Lake
227. (a) TN, (b) TDN, (c) TP, (d) TN : TP, and (e) zooplankton
biomass.
fixation by cyanobacteria was not sufficient to offset the
decrease in external N inputs.’’ Instead, the data indicate
that reducing inputs of inorganic N caused phytoplankton
to increasingly rely on fixation of atmospheric N to meet
their demands for biomass production, a conclusion
reached earlier by Hendzel et al. (1994). Even after 20 yr
without fertilization with N, and despite a 30% reduction in
TN concentrations in Lake 227 since 1990, there has been
no decrease in either chlorophyll or phytoplankton
biomass. Biomass remains 20 times higher than in similar
natural lakes in the ELA (D. Findlay unpubl. data).
Although our data set was collected from only a single
experimental lake, the additional data continue to strengthen our earlier conclusion (Schindler et al. 2008): the most
effective way to reduce eutrophication of lakes is to focus
on controlling inputs of P. The Lake 227 data provide no
evidence that controlling N adds additional benefits. While
the possibility exists that Lake 227 is somehow unique, we
have no reason to believe this is the case because the
Comments
processes invoked to explain the lake’s response over time
can occur in most lakes. Reductions of P alone have
resulted in large, comparatively rapid declines of phytoplankton biomass in many systems (Jeppesen et al. 2005),
but we are unaware of successful programs to limit
eutrophication by restricting inputs of N, either alone or
in combination with P (Schindler and Vallentyne 2008;
Schindler and Hecky 2009).
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Associate editor: Roland Psenner
Received: 02 June 2010
Accepted: 28 September 2010
Amended: 08 October 2010