North American Journal of Fisheries Management 27:369–386, 2007
Ó Copyright by the American Fisheries Society 2007
DOI: 10.1577/M05-212.1
[Article]
Changes in Algal Species Composition Affect Juvenile Sockeye
Salmon Production at Woss Lake, British Columbia: A Lake
Fertilization and Food Web Analysis
DONALD J. MCQUEEN*
125 Pirates Lane, Nanaimo, British Columbia V9R 6R1, Canada
KIM D. HYATT
D. PAUL RANKIN
AND
Fisheries and Oceans Canada, Pacific Region, Science Branch, Pacific Biological Station,
Nanaimo, British Columbia V9R 5K6, Canada
CHARLES J. RAMCHARAN
Department of Biology, Laurentian University, Ramsey Lake Road, Sudbury, Ontario P3E 2C6, Canada
Abstract.—In recent decades, the abundance of sockeye salmon Oncorhynchus nerka in the Nimpkish River
watershed (Vancouver Island) has declined by more than 80%. To improve sockeye salmon abundance, one of
three Nimpkish nursery lakes (Woss Lake, 13.6 km2) was fertilized; a second (Vernon Lake, 8.4 km2) was
maintained as an unmanipulated reference. For 3 years (2000–2002), we assessed changes in phytoplankton,
zooplankton, and juvenile sockeye salmon and then used food web analysis to model the fate of fertilizer
phosphorus (FP) as it moved up the food web to juvenile sockeye salmon. As the experiment progressed, we
found two distinctly different results. During the first 2 years (2000 and 2001), fertilization was associated with
higher concentrations of P, chlorophyll, and phytoplankton. However, because most of the algae were inedible
diatoms (principally Rhizosolenia eriensis), only 8% of the algal standing stock was available to zooplankton
and less than 0.1% of the FP was incorporated into sockeye salmon biomass via limnetic pathways. The result
was that juvenile sockeye salmon growth rates in the treated and control lakes were not significantly different.
During the third year (2002), a bloom of the diatom Leptocylindrus increased Woss Lake edible algal biomass
by a factor of 7; zooplankton production tripled, and juvenile sockeye salmon production increased by 19%.
Consequently, Woss Lake juvenile sockeye salmon grew twice as fast as they did in untreated Vernon Lake,
and juvenile sockeye salmon fall weights were 50% higher than those recorded before the lake was fertilized.
We conclude that for north Pacific coastal lakes, bottom-up effects resulting from changes in phytoplankton
species composition can profoundly alter rates of juvenile sockeye salmon production. Regulation of algal
species composition through manipulations of fertilizer composition and application timing might be used to
reduce blooms of nuisance algae and increase age-0 sockeye salmon yield.
Sockeye salmon Oncorhynchus nerka returning to
the Nimpkish River watershed on northern Vancouver
Island have historically been of great importance to
both the ‘Namgis First Nation and the commercial
fishery. The Canadian Department of Fisheries (1958)
stated that the Nimpkish River fishery was ‘‘second in
value only to that of the Fraser in the southern half of
the Province.’’ During recent years, the Nimpkish River
fishery has been in decline, and the lake fertilization
experiment described here is part of a larger Nimpkish
River watershed salmon restoration initiative coordinated by the Nimpkish Resource Management Board
and the ‘Namgis First Nation (ALBY Systems, Ltd.,
and Northwest Hydraulic Consultants, Ltd. 2000).
* Corresponding author: [email protected]
Received December 7, 2005; accepted July 24, 2006
Published online March 29, 2007
Nelson and Edmondson (1955) were the first to
propose a theoretical basis for the enhancement of
sockeye salmon production through nursery lake
fertilization. They suggested that carcasses deposited
from returning adults produce nutrients which stimulate
the growth of phytoplankton, thus supporting increased
production by zooplankton. The result is enhanced
food availability for juvenile sockeye salmon, yielding
higher in-lake fry growth rates and larger smolts that
survive better at sea. This bottom-up or donor control
theory is based on two assumptions: (1) larger sockeye
salmon smolts from fertilized lakes survive better at
sea, thus ensuring increased returns of adults, and (2)
in-lake growth rates for juvenile sockeye salmon can be
significantly influenced by increased P and N supply.
Evidence supporting the first assumption is reasonably strong. Some very early sockeye salmon literature
(Barnaby 1944; Foerster 1954; Ricker 1962) demonstrated a positive relationship between sockeye salmon
369
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MCQUEEN ET AL.
smolt length and marine survival, and all recent nursery
lake fertilization studies that included estimates of
marine survival (Leisure Lake: Kyle 1994 and Koenings and Kyle 1997; Packers Lake: Kyle 1994; Chilko
Lake: Bradford et al. 2000) have shown a positive
relationship between smolt weight and smolt-to-adult
survival.
Evidence supporting the second assumption (donor
control) is also reasonably strong. Over the past 30
years, the food web literature has verified the general
predictability of bottom-up relationships between
nutrients and algae, algae and zooplankton, and
zooplankton and planktivorous fish (reviewed in
McQueen et al. 1986; Koenings and Kyle 1997). A
recent review of the sockeye salmon nursery lake
fertilization literature (Hyatt et al. 2004b) found that in
all cases (23 studies), chlorophyll-a concentrations
were higher in fertilized lakes and that in most cases,
fertilization was associated with increased zooplankton
biomass (17 of 18 studies), smolt weight (17 of 19
studies), and smolt biomass (13 of 15 studies).
However, the pelagic food web literature has also
featured considerable disagreement about the relative
strength of these bottom-up relations in comparison to
top-down processes, which tend to reduce bottom-up
control (reviewed in Shapiro and Wright 1984; Mehner
et al. 2002; Jeppesen et al. 2003). For example,
although Hyatt et al. (2004b) found that most nursery
lake fertilizations produced larger smolts, unintended
and confounding outcomes were also common.
Fertilizers that were relatively rich in P (low N: P
ratio) promoted blooms of blue-green algae that could
not be consumed by zooplankton grazers (Stockner and
Hyatt 1984; Stockner and Shortreed 1988; Hardy et al.
1986; Perrin et al. 1986), and the result was minimal
increases in zooplankton and fish production. Also, in
some cases where zooplankton production was enhanced by fertilization, juvenile sockeye salmon were
out-competed for the increased food supply by very
large populations of threespine sticklebacks Gasterosteus aculeatus (Hyatt and Stockner 1985; O’Neill
1986; O’Neill and Hyatt 1987; Hyatt et al. 2000) or by
populations of the macroinvertebrate Neomysis mercedis, which could consume 5–10 times as much
zooplankton as the juvenile sockeye salmon population
(Cooper 1988; Cooper et al. 1992; Hyatt et al. 2005).
On balance, Hyatt et al. (2004b) suggested that
nursery lake fertilization is a technique that has good
potential for sockeye salmon population enhancement.
However, two questions related to the dynamics of
nutrient flow through aquatic ecosystems remain
unanswered: (1) what percentage of the P augmented
by the addition of fertilizers makes its way up through
pelagic food webs to be incorporated into juvenile
sockeye salmon, and (2) is this bottom-up transfer large
enough to justify the considerable expense involved in
fertilizer application and monitoring?
Our analysis had two primary objectives. The first
was to model the amount of added fertilizer phosphorus
(FP) that successfully moved up through the Woss
Lake food web to stimulate additional juvenile sockeye
salmon production. The second objective was to
quantify the increase in sockeye salmon biomass
stimulated by known fertilizer additions. During 3
years (2000–2002), we fertilized Woss Lake and
maintained nearby Vernon Lake as an unmanipulated
reference. We then measured phytoplankton and
zooplankton community changes associated with
fertilizer addition. We used estimates of zooplankton
and sockeye salmon fry production and consumption
(along with diet analyses) to model the fate of FP that
was initially incorporated by algae and that moved up
through the food web to juvenile sockeye salmon. This
nutrient flow analysis allowed us to estimate the
additional sockeye salmon production that was attributable to fertilizer addition, and detailed speciesspecific data for biomass and density allowed us to
evaluate the effects of changing abundances of
‘‘edible’’ algae and zooplankton on annual changes in
sockeye salmon production.
Study Area
Woss and Vernon lakes lie within the Nimpkish
River watershed, which is located at the northern end
of Vancouver Island, southeast of Port Hardy. The
Nimpkish River watershed is the largest on Vancouver
Island, draining north into Broughton Strait approximately 10 km southeast of Port McNeill, British
Columbia. Woss Lake (Figure 1) has a surface area of
1,366 ha, a maximum depth of 150 m, and a watershed
area of 246 km2. The Woss River system produces
approximately 25% of the total Nimpkish River
sockeye salmon. Vernon Lake (Figure 2) has a surface
area of 837 ha, a maximum depth of 102 m, and a
watershed area of 306 km2. Vernon Lake and the
Sebalhal River produce approximately 20% of total
Nimpkish River sockeye salmon (ALBY Systems,
Ltd., and Northwest Hydraulic Consultants, Ltd. 2000).
Methods
Sampling and analysis.—From May to October of
each year (2000–2002), total P (TP), NO3 þ NO2, and
chlorophyll-a samples were collected from stations 1
and 3 in both Woss Lake (Figure 1) and Vernon Lake
(Figure 2). Samples were collected approximately once
every 3 weeks between May and October (n ¼ 8
sampling dates in 2000; n ¼ 9 in 2001; n ¼ 8 in 2002).
Epilimnetic samples were collected by combining van
ALGAE EFFECT ON SOCKEYE SALMON
371
FIGURE 2.—Left panel: Vernon Lake, British Columbia,
limnological sampling stations and transect lines. Sampling
stations are designated 1–4; fish acoustic transects are shown
as lines across the lake. Right panel: Vernon Lake (837 ha)
bathymetry contours (m) are presented.
FIGURE 1.—Left panel: Woss Lake, British Columbia,
limnological sampling stations and transect lines. Sampling
stations are designated 1–4; phosphorus test stations are
designated A–H. Fish acoustic transects are shown as lines
across the lake. Right panel: Woss Lake (1,366 ha)
bathymetry contours (m) are presented.
Dorn samples taken from depths of 1, 3, and 5 m.
Hypolimnetic samples were taken from a depth of 20
m. All sampling containers were rinsed three times
with water from the appropriate lake, station, and
depth. Each water sample destined for TP analysis was
poured through a 100-lm mesh into 50-mL screw cap
test tube that was stored in the dark until analysis.
Unfiltered water for NO3 þ NO2 analysis was drawn
into a syringe, passed through an acrodisk filter, and
injected into a screw cap plastic bottle that was
returned to the laboratory and frozen until analysis.
Unfiltered water for chlorophyll-a analysis was poured
into a 1-L plastic bottle, held in the dark on ice,
returned to the laboratory, and filtered (47-mm
millipore) at 0.3 atmospheres. The filters were frozen
and held in the dark until analysis. Samples were
analyzed at the Canadian Department of Fisheries and
Oceans (CDFO) Cultus Lake Laboratory using standardized methods described in Stephens and Brandstaetter (1983).
Phytoplankton samples were collected from each
lake from each of two stations approximately once
every 3 weeks between May and October (n ¼ 8
sampling dates in 2000; n ¼ 9 in 2001; n ¼ 8 in 2002)
using the epilimnetic sampling methods described for
water chemistry. Unfiltered water was placed in 500mL plastic jars and preserved with Lugol’s solution.
Laboratory methods are described in Tremel et al.
(2001). In brief, samples were counted using the
Utermöhl (1958) technique. Taxonomic (genus level)
determination followed Bourrelly (1966, 1968, 1970).
Individual cells were measured and their biovolume
was determined using formulae of basic geometric
shapes (Vollenweider 1969; Rott 1981; Hopkins and
Standke 1992). Biovolumes were recorded as cubic
microns per milliliter (lm3/mL) divided by 1,000,
which are equivalent to cubic millimeters per cubic
meter; assuming that 1 mm3 equals 1 mg, the units can
be expressed as 1 mg/mm3, or 1 lg/L. Qualitative
assessment of ‘‘edibility’’ was based on size and
digestibility. Single cells or colonies less than 30 lm
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MCQUEEN ET AL.
in width and length were considered edible (Cyr 1998;
Cottingham 1999) except for those that were ‘‘digestion
resistant.’’ Algae with thick gelatinous sheaths were
considered to be digestion resistant, independent of
size (Stutzman 1995).
Zooplankton samples were collected approximately
every 3 weeks (n ¼ 8 sampling dates in 2000; n ¼ 8 in
2001; n ¼ 10 in 2002), spring to fall, at each of four
stations in Woss Lake (Figure 1) and three stations in
Vernon Lake (Figure 2). A metered (Rigosha and Co.,
Ltd.; Model 5571), square-mouth (Filion 1991) vertical
haul net (30 3 30 cm; 100-lm mesh) was winched at 1
m/s between 25 and 0 m. Samples were preserved in a
4% solution of buffered and sugared formalin and were
returned to the laboratory. For each sample, the
Rigosha meter values were used to calculate net
filtration efficiency. For each date, a composite
zooplankton sample was created from the four (Woss
Lake) or three (Vernon Lake) zooplankton samples
taken from the lake. The composite comprised
zooplankton found in equal volumes of lake water
taken from each of the sampling stations. These
combined samples were identified to species for
cladocerans, copepod adults, and copepodids and to
suborder for copepod nauplii. Eggs were counted for
all individuals of all species. Lengths of all animals
were measured using a semiautomated counting and
measuring system (Allen et al. 1994). Corrections for
contraction due to preservative were applied to the
body lengths of Holopedium gibberum (Yan and
Mackie 1987) but not other species (Campbell and
Chow-Fraser 1995). Animal weights were estimated
using length–weight regressions summarized in Girard
et al. (2005). In cases when preserved animals were
used to develop these regressions, a correction for
weight loss in formalin was applied (Giguère et al.
1989).
Nighttime juvenile sockeye salmon densities were
estimated by using a Simrad EYM 70-KHz sounder
deployed over whole-lake transects (Figures 1, 2) and
several depth strata. Five surveys per year were
conducted in 2000 and 2001; eight surveys were
conducted in 2002. Detailed survey methods are
described by Hyatt et al. (1984, 2000, 2004a, 2005).
Echo counting is frequently confounded by fish
schooling behavior during short nights in May–July;
therefore, the best estimates were obtained between
August and the presmolting period in February.
Density estimates were used to determine total
numbers of juvenile sockeye salmon found in each
lake, and these data were used to estimate sockeye
salmon mortality throughout the late-summer, fall, and
winter periods. Details regarding transducer design and
counting methods are provided by Hyatt et al. (1984),
Hyatt and Stockner (1985), and Gjernes et al. (1986).
Fish biosamples were collected using a midwater
trawl net (2 3 2-m mouth opening, 7.5-m length). Haul
depths were based on echo-sounding results. Detailed
survey methods are described by Hyatt et al. (1984,
2000, 2004a, 2005). During 2000–2002, we captured
2,003 juvenile sockeye salmon from Woss Lake and
1,128 from Vernon Lake. Sampled fish were used to
estimate lengths, weights, and ages. The average
length–weight regression for Woss Lake sockeye
salmon fry was
Weight ðgÞ ¼ 0:00001822 3 ðlength in mmÞ2:85 ;
for Vernon Lake fry, the length–weight regression was
Weight ¼ 0:00000502 3 ðlengthÞ3:15 :
At both Woss and Vernon lakes, we checked for
possible size-biased sampling by the trawl net. Juvenile
sockeye salmon were trawled from Woss Lake during
March 2002 and March 2003 and from Vernon Lake
during March 2002. Lengths and weights from these
trawl-caught fish were compared with those of smolts
trapped during early April of the same years. This type
of comparison at other lakes (Hyatt et al. 2004a) has
shown that as juvenile sockeye salmon grow larger
than 40 mm, increased swimming speeds allow some
individuals to avoid capture by trawl nets. In the case
of Woss and Vernon lakes, the correction for fish larger
than 40 mm was
Corrected length ¼ 0:629 3ðlength in the trawlÞ1:125 :
Although this correction had a relatively minor effect
on mean length, it was applied to all data.
Immediately upon capture, juvenile fish destined for
stomach content analysis were placed into a 90%
solution of ethanol and were subsequently frozen. Prior
to analysis, stomachs were removed, contents were
washed into a petri dish, and all zooplankton were
counted. Stomach content data from 810 stomachs
collected over 3 years (2000–2002) were used to
estimate the numbers of each prey species consumed
by sockeye salmon, and these data were used to
parameterize the fish bioenergetics model (described
below). Because many of the prey had been damaged
during consumption, we estimated individual prey
weights from the average weights of each prey taxon
found in the zooplankton samples from each sampling
date. Individuals smaller than 0.4 mm were excluded
from the zooplankton samples used to estimate average
prey weights (Beauchamp et al. 2004; Hyatt et al.
2005).
ALGAE EFFECT ON SOCKEYE SALMON
Production and consumption analysis.—The goal of
production and consumption analysis was to calculate
consumption by the fish as a percentage of production
by each zooplankton prey species type. When
consumption exceeded production, we expected to
see the zooplankton population decline, at which point
we could assume that the sockeye salmon production
capacity of the lake had been reached or exceeded.
Species-specific zooplankton production rates were
calculated using the egg ratio methods of Borgmann et
al. (1984) as modified based on studies by Paloheimo
(1974) and Cooley et al. (1986). These methods are
described in Hyatt et al. (2005). For each species, we
used the production model to calculate the new
biomass b produced between sample times t and t þ
1; the new biomass was compared with btþ1 – bt
observed in the field. In most cases, calculated
production was larger, but occasionally our egg counts
were low and calculated production was less than the
minimum value derived from field data. In such cases,
we used the estimate based on field samples.
Calculated rates of zooplankton consumption by
age-0 sockeye salmon were based on the bioenergetics
model of Kitchell et al. (1974, 1977), as summarized in
Hanson et al. (1997). All simulations began on 15 June
(the approximate date of the first reliable acoustic
density estimates of fish) and ended on 31 October
(139 d). Model inputs included vertical fish distribution
within the water column, water column temperature,
fish length, weight, and diet. Energy densities for the
sockeye salmon and the various prey species were
entered as joules per gram wet weight. Because Levy
(1990) reported various diel migration patterns for
juvenile sockeye salmon, we investigated vertical
activity in both lakes on 26–27 June 2000, 6–7 August
2000, and 18–19 August 2002. We found that a
variable portion of the sockeye salmon population
entered the epilimnion at dark and returned to the
hypolimnion at dawn. However, on all dates, the
population median remained at or just below the
thermocline. We therefore assumed that individual fish
spent the night moving into and out of the epilimnion.
By alternating daily temperatures between epilimnetic
and hypolimnetic values, we adapted the Wisconsin
model to simulate two diel vertical migration patterns:
12 h day : 12 h night and 8 h day : 16 h night. We also
ran the model under the assumption that the fish did not
migrate but remained near the metalimnion. We found
that consumption rate estimates based on the 12 h : 12 h
pattern were about 10% higher than those based on the
8 h : 16 h pattern and that consumption rates based on
no migration were intermediate between the two.
Because individuals migrated for unknown durations,
we used output from the 12 h : 12 h pattern. This may
373
have slightly overestimated food consumption rates,
but because summer epilimnetic temperatures in both
lakes were low (13–178C) the error was much smaller
than that associated with our ability to assess
population density.
Fertilizer loading and dispersal.—Woss Lake was
fertilized for 3 years (2000–2002; Table 1). Vernon
Lake was not fertilized and remained the reference lake
throughout. The fertilizer had an N : P ratio of 30:1 by
atomic weight (13.5:1.0 by mass) and was made from a
mix of 28:0:0 (28% N, 0% P, 0% K) and 10:34:0 (10%
N, 14.85% P, 0% K). Details regarding fertilizer mix
and chemistry are described by Stockner and MacIsaac
(1996). With each succeeding year, the fertilizer was
applied earlier in the year and the total quantities added
were also increased (Table 1). The fertilizers were
added twice per week from a boat into the eastern and
western sections of the lake. To assess the extent of
fertilizer mixing during 2000, Gwa’ni Hatchery staff
collected P samples on five dates (26 July and 2, 16,
23, and 30 August) from eight stations in Woss Lake
(Figure 1, A–H). All samples were taken at a depth of 3
m at all stations. In addition, stations C and F were
sampled at 25-m depth. The P concentrations at the
center stations proved to be no higher than those at the
edge stations, suggesting that the P mixed completely.
Also, because the deep samples always contained less
than one-half the P measured in the surface samples,
we concluded that most of the fertilizer remained in the
epilimnion.
Statistics.—Throughout the experiment, data on
water chemistry, phytoplankton, and zooplankton were
collected from both lakes on the same dates. In all
cases, samples collected from different stations were
combined (see above) to generate single measures for
each variable from each lake on each sampling date.
Since there was only one treated lake (Woss Lake) and
one untreated reference lake (Vernon Lake), there
could be no treatment replication and repeatedmeasures statistics could not be applied. Therefore, to
test the null hypothesis that values (e.g., epilimnetic TP
concentration) in each lake were not different, we used
a modification of the control–impact pair analysis
described by Stewart-Oaten et al. (1986). We compared
the mean differences between measurements from
Woss Lake paired in time with measurements from
Vernon Lake. For each variable, the null hypothesis
was that the mean difference equaled zero. Throughout,
we used log10 transformed data to linearize relationships and reduce variance. We applied Tukey’s onedegree-of-freedom test and the von Neumann ratio test
and confirmed additivity (i.e., P . 0.05) and
independence (no serial correlation) for TP, chlorophyll a, edible algal biomass, zooplankton biomass,
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MCQUEEN ET AL.
TABLE 1.—Summary of fertilizer loading in Woss Lake, British Columbia, during 2000–2002.
Year
Start date
End date
Atomic
N : P ratio
P (kg/year)
Mean areal P load
(mgm2wk1)
N (kg/year)
Kilograms of
10:34:0
Kilograms of
28:0:0
2000
2001
2002
7 Jul
7 May
15 Apr
28 Aug
3 Sep
26 Aug
30:1
30:1
30:1
595
730
975
1.9
2.4
3.2
8,055
9,890
13,210
4,003
4,916
6,566
27,336
33,567
44,833
cladoceran eggs per female, copepod eggs per female,
and zooplankton production. In these cases, we tested
the null hypothesis for mean differences between the
two lakes. Data for total algal biomass were not
independent, and data for NO2 þ NO3 were neither
additive nor independent. In these two cases, we used
graphical or tabular presentation. When time series data
were not involved (i.e., sockeye salmon lengths and
weights restricted to specific time periods), we used
one-way analysis of variance (ANOVA). In all cases,
we report two-tail probability values.
Fertilizer effects on sockeye salmon production.—
One of the study objectives was to estimate the
quantity of FP that moved up the food web from algae
to zooplankton and into newly produced age-0 sockeye
salmon. For each year, we calculated FP uptake and
loss over a 139-d period between 15 June and 31
October. We based our calculations on field measurements of FP loading (g/ha per summer), total algal
biomass (mm3/m3 or lg wet weight [WW]/L), edible
algal biomass (lg WW/L), total zooplankton biomass
(lg dry weight [DW]/L), edible zooplankton biomass
(lg DW/L), total and edible zooplankton production
(lg DWL1d1), and average age-0 sockeye salmon
density (number/ha), weight (g WW), and production
(g WWha1d1).
Based on the assumption that all FP loaded into
Woss Lake was taken up by algae and based on the
known ratio of edible to total algal biomass, we were
able to estimate the percentage of FP that was
incorporated into edible algae. Similarly, based on
the known ratio of edible to total zooplankton biomass
and based on an assumed 15% FP transfer efficiency
from edible algae to zooplankton (Sommer 1998), we
estimated the quantity and percentage of FP that was
incorporated into edible zooplankton.
We estimated zooplankton production (g
DWha1139 d1 ) using the egg ratio method
described above, and we assumed that the P content
for zooplankton (based on DW biomass) averaged 1%
(Andersen and Hessen 1991; DeMott 1998; Elser et al.
2000). From this, we calculated the quantity of TP (g
DWha1139 d1) consumed during production by
both total zooplankton and edible zooplankton. This
allowed us to estimate the percentage of TP made up of
FP that was incorporated by edible zooplankton.
From the fish bioenergetics model, we estimated the
biomass of edible zooplankton (g DWha1139 d1)
consumed by juvenile sockeye salmon, which allowed
us to calculate the quantities of TP and FP (g
DWha1139 d1) and the percentage FP consumed.
Assuming that the P content of sockeye salmon
averaged 0.35% based on WW biomass (Larkin and
Slaney 1997), we calculated the quantities of TP and
FP (g WWha1139 d1) that were incorporated into
new sockeye salmon tissue and the quantity of new
sockeye salmon production (g WWha1139 d1) that
was stimulated by the addition of FP.
Error analysis.—The preceding calculations included two error types: those associated with parameter
estimation and those associated with measurement.
Parameter estimates included ecological efficiency,
percentage P in zooplankton, and percentage P in
juvenile sockeye salmon. Measurement error involved
the estimation of fish density.
Ecological efficiency for zooplankton consuming
algae is known to vary depending on cell type and on
the percentage of algae making up the diets of
omnivorous zooplankton species. Published values
range from 10% to 30% (i.e., Sommer 1998); we used
15%. Had we chosen the most extreme value (30%),
there would have been no change in our estimates of
total fish production based on field data, but the
amount of FP incorporated into fish would have
doubled and the percentage FP incorporated into fish
would have changed marginally from 0.14% to 0.27%.
Data from several sources (Andersen and Hessen 1991;
DeMott 1998; Elser et al. 2000) demonstrate that the
percentage P for Daphnia ranges from 0.8% to 1.5%.
For diaptomids, the range is 0.45–1.07%; for cyclopoid
copepods, it is 0.65–1.35%. Also, variation within the
same species ranges from 0.65% to 1.16%; we used
1%. Use of an extreme value, such as 1.5%, would not
have changed overall fish production, but the amount
of FP incorporated into fish would have declined by
32% and the percentage FP incorporated into fish
would have decreased marginally from 0.14% to
0.09%. Based on a study by Larkin and Slaney
(1997), the percentage P in juvenile sockeye salmon
was assumed to be 0.35% (WW basis). Increasing
percentage P in sockeye salmon to the unlikely value of
0.5% would have had no effect on total sockeye
ALGAE EFFECT ON SOCKEYE SALMON
salmon production, but the percentage FP incorporated
into fish would have increased marginally from 0.14%
to 0.19%. In summary, errors associated with parameter estimation had no effect on total fish biomass or
production, and minor effects on the percentage of FP
incorporated into sockeye salmon. However, errors in
parameter estimation could change the contribution of
FP to fish growth relative to the contribution made by
naturally occurring P. In the most extreme case for
2002, doubling ecological efficiency increased the
contribution of FP from 17% to 34%. It should be
noted, however, that the effect was symmetrical and
that a 50% reduction in ecological efficiency would
halve the contribution of FP to fish growth. From this,
we concluded that our use of mean parameter values
was justified and that resulting errors were probably
small and symmetrical.
Results
Oxygen, Temperature, and Water Chemistry
During all 3 years (2000–2002) in both lakes,
epilimnetic and hypolimnetic oxygen concentrations
gradually declined from spring highs of approximately
12 mg/L to late-summer lows of approximately 9 mg/
L. In both lakes, thermal stratification was established
by mid-June and lasted until mid-October. Thermoclines were broad (extending from approximately 15 to
20 m), and temperature changes were small (0.1–0.78C
per m). Epilimnetic temperatures were consistently
lower in Vernon Lake (maximum ¼ 13–148C) than in
Woss Lake (maximum ¼ 15–178C). This difference
was probably attributable to a substantial snow field in
the mountains surrounding the headwaters of Vernon
Lake.
On average, TP concentrations were higher in Woss
Lake than in Vernon Lake (paired t: df ¼ 21, P , 0.01;
Figure 3). Nitrogen concentrations (NO2 þ NO3) were
neither additive nor independent and could not be
analyzed statistically, but Woss Lake May–October N
concentrations averaged 18 lg/L in 2000, 20 lg/L in
2001, and 6 lg/L in 2002 and were always lower than
comparable measures from Vernon Lake, which
averaged 31 lg/L in 2000, 32 lg/L in 2001, and 25
lg/L in 2002. This was especially true during the third
year of the experiment, when loading rates were
increased and when Woss Lake N declined rapidly to
about 4 lg/L by the end of summer.
Chlorophyll a and Phytoplankton Biovolume
Chlorophyll-a concentration varied substantially
from year to year (Figure 3). In Woss Lake, there
was a fall bloom during 2000 and a spring bloom
during 2002. Vernon Lake chlorophyll-a concentra-
375
tions were relatively stable. Woss Lake chlorophyll-a
concentrations averaged 0.9 lg/L, which was significantly higher than the Vernon Lake average (0.4 lg/L;
paired t: df ¼ 21, P , 0.01).
Phytoplankton biovolume showed almost exactly the
same patterns as chlorophyll a (Figure 3; Table 2). At
Woss Lake during 2000, much of the total algal
biomass was made up of the diatom Rhizosolenia
eriensis (Bacillariophyceae; Figure 4). This diatom is a
large, inedible, flattened, cylindrical species measuring
approximately 75 3 6 3 4 lm and possessing a long
spine at each end. At Woss Lake during 2001, algal
abundances were relatively low and a variety of
Bacillariophyceae (Tabellaria, Cyclotella, and Asterionella) predominated. At Woss Lake during the spring
of 2002, there was a large spring bacillariophyte bloom
of Leptocylindrus, a small, edible, extremely fragile,
coiled, and flattened cylinder measuring approximately
20 3 8 3 3 lm. At Vernon Lake during 2000–2001,
Cyanophyceae were common, whereas Rhizosolenia
and Leptocylindrus accounted for no more than 2% of
the algal biovolume. At Vernon Lake during 2002,
biovolumes were very low (,200 mm3/m3) and
blooms were not observed. Overall, Woss Lake had
higher algal biovolumes than did Vernon Lake, and
much of that extra biomass comprised bacillariophytes
(Table 2).
During 2000–2001, biovolumes of edible algae were
significantly higher in Woss Lake than in Vernon Lake
(paired t: df ¼ 22, P ¼ 0.04). Woss Lake seasonal
(May–October) averages were higher in all years
(Table 2), especially during 2002, when the average
edible fraction increased to 727 mm3/m3 (Figure 4) but
was only 146 mm3/m3 in Vernon Lake. This was
primarily due to the 2002 bloom of Woss Lake
Leptocylindrus, which was restricted to May and June,
when edible algal biomass equaled 733 mm3/m3 on 06
May, 2,110 mm3/m3 on 27 May, and 2,976 mm3/m3 on
19 June (Figure 4). In Vernon Lake on the same dates,
edible algal biovolume was much lower: 133, 177, and
68 mm3/m3, respectively.
Zooplankton Biomass, Density, and Egg Counts
The Woss Lake pelagic zooplankton community
(Figure 5) comprised four species of Daphnia.
Daphnia dentifera were common, and the other three
(D. ambigua, D. thorata, and D. longirimus) were rare
(,1% of biomass). The lake also had two bosminids:
Bosmina longirostris was the most common, and B.
longispina was rare (,1% of biomass). We found only
one cyclopoid copepod (Diacyclops bicuspidatus
thomasi) and two calanoid copepods (Skistodiaptomus
oregonensis and Epischura nevadensis). Whereas the
cladoceran Holopedium gibberum was relatively com-
376
MCQUEEN ET AL.
FIGURE 3.—Characteristics of a phosphorus-fertilized lake (Woss Lake, British Columbia) and an unfertilized reference lake
(Vernon Lake) during 2000–2002. Left panels show epilimnetic total phosphorus (TP) concentration (lg/L), center panels show
chlorophyll-a concentration (lg/L), and right panels show total algal biovolume (mm3/m3, or lg wet weight/L).
mon, Polyphemus pediculus was relatively rare. In
general, the overall between-year pattern at Woss Lake
was one of gradual replacement of Daphnia by
Bosmina. At Vernon Lake, the zooplankton assemblage was almost identical except that Epischura and
Skistodiaptomus were absent and Hesperodiaptomus
kenai was present (Figure 5). At Vernon Lake,
Diacyclops bicuspidatus thomasi and B. longirostris
were the most common species.
The 2000–2002 Woss and Vernon Lake total
zooplankton biomass averages were not different
(paired t: df ¼ 24, P ¼ 0.55). This reflected a reversal
in zooplankton biomasses in 2000–2002. During 2000,
Vernon Lake biomasses were consistently higher than
those in Woss Lake (Figure 5). During 2001,
biomasses in the two lakes were approximately equal;
during 2002, Woss Lake biomasses were twice as high
as those in Vernon Lake (Figure 5). This between-lake
TABLE 2.—Average (May–October) phytoplankton algal biovolumes (mm3/m3) for a phorphorus-fertilized lake (Woss Lake,
British Columbia) and an unfertilized reference lake (Vernon Lake). Column head abbreviations are as follows: Cyanophyceae
(Cyano), Dinophyceae (Dino), Cryptophyceae (Crytpo), Chrysophyceae (Chryso), Chlorophyceae (Chloro), Bacillariophyceae
(Bacillario).
Chloro
Bacillario
Average algal
biovolume (mm3/m3)
Average edible algal
biovolume (mm3/m3)
1,355
601
1,367
1,676
751
1,476
92
102
727
12
19
98
636
274
172
70
83
146
Year
Cyano
Dino
Crypto
Chryso
2000
2001
2002
171
17
1
13
24
30
12
14
16
56
41
54
Woss Lake
70
54
8
2000
2001
2002
540
115
1
7
25
21
12
9
6
34
40
37
Vernon Lake
32
66
3
ALGAE EFFECT ON SOCKEYE SALMON
377
rates averaged 0.4 lg DWL1d1 in 2000, 0.5 lg
DWL1d1 in 2001, and 1.4 lg DWL1d1 in 2002;
these values did not significantly differ from the
Vernon Lake rates of 0.7 lg DWL1d1 in 2000, 1.2
lg DWL1d1 in 2001, and 0.8 lg DWL1d1 in
2002 (paired t: df ¼ 21, P ¼ 0.83). During the first 2
years of the experiment, total zooplankton production
rates were higher in Vernon Lake than in Woss Lake,
but during the third year the trend was reversed. The
change was especially apparent during the spring of
2002, when Leptocylindrus bloomed in Woss Lake.
Total daily zooplankton production in Woss Lake
averaged 1.6 lg WWL1d1 on 27 May, 2.3 lg
WWL1d1 on 18 June, 4.9 lg WWL1d1 on 9
July, and 0.7 lg WWL1d1 on 30 July, whereas the
corresponding averages in Vernon Lake were 1.0, 1.4,
0.4, and 0.2 lg WWL1d1, respectively. During the
rest of 2002, total zooplankton production in the two
lakes was not different.
Sockeye Salmon Fry Density, Length, and Weight
FIGURE 4.—Biovolumes (mm3/m3) of edible algae, edible
diatoms, and the inedible diatom Rhizosolenia eriensis in
Woss Lake, British Columbia, to which fertilizer phosphorus
was added during 2000–2002. Note the log scale on the y-axes.
difference was especially obvious during the spring of
2002, when Woss Lake edible algal biovolume was
high. For example, during 2002, Woss Lake total
zooplankton biomass equaled 85 lg DW/L on 18 June,
116 lg/L on 9 July, and 81 lg/L on 30 July. On the
same dates, Vernon Lake total zooplankton biomass
was only 60, 15, and 14 lg/L, respectively.
During 2000–2002, the average number of eggs per
cladoceran was significantly higher in Woss Lake (0.9
eggs/female) than in Vernon Lake (0.6 eggs/female;
paired t: df ¼ 18, P ¼ 0.02). The difference was
particularly notable during the spring of 2002, when
the averages in Woss Lake were 1.8 eggs/female on 27
May and 2.0 eggs/female on 18 June. During the same
dates at Vernon Lake, the averages were much lower:
0.8 and 0.1 eggs/female, respectively. Egg counts for
copepods were not different between the lakes.
Total Zooplankton Production
Species-specific zooplankton production rates were
estimated for each sampling interval within each year
for Woss and Vernon lakes. Woss Lake production
During 2000, age-0 sockeye salmon in both lakes
grew at about equal rates (Figure 6; Table 3). During
2001, Woss Lake fry gained weight earlier in the year
and ended the year slightly larger than the Vernon fry.
In 2002, Woss Lake age-0 fry grew much more quickly
than Vernon Lake fry, and December fry weights were
almost twice as large in Woss Lake than in Vernon
Lake. Overall, average December weights for Woss
Lake age-0 fry increased with each succeeding year
(ANOVA: F ¼ 10.8, df ¼ 330, P , 0.001), and those of
Vernon Lake fry declined with each succeeding year
(ANOVA: F ¼ 16.7, df ¼ 84, P , 0.001).
Fish densities in the two lakes were similar (Figure
6), ranging from 600 to 800 juveniles/ha in December.
The exception was Woss Lake in 2001, when densities
were exceptionally low (200–400 juveniles/ha). Annual mortality between June and December (Table 3) was
generally lower in Woss Lake (0–20%) than in Vernon
Lake (7–46%).
Juvenile Sockeye Salmon Diets and Edible
Zooplankton
Diet analysis (2000–2002) suggested that age-0
sockeye salmon consumed many prey types, but only
four taxonomic groups accounted for more than 95% of
the total prey biomass. In Woss Lake (Figure 7),
Daphnia (primarily D. dentifera) and Bosmina (primarily B. longirostris) constituted more than 95% of
the prey consumed. Epischura nevadensis were also
consumed, but in smaller quantities. In Vernon Lake,
Daphnia, Bosmina, and Hesperodiaptomus kenai were
the main prey types. Comparison of these trends in
prey selection with prey availability (Figure 5)
378
MCQUEEN ET AL.
FIGURE 5.—Zooplankton biomass (lg dry weight/L) in a phosphorus-fertilized lake (Woss Lake, British Columbia; left panels)
and an unfertilized reference lake (Vernon Lake; right panels) during 2000–2002.
confirmed that the preferred prey (Daphnia and
Bosmina) were common in both lakes, especially Woss
Lake. However, Diacyclops bicuspidatus thomasi were
also very common in the zooplankton samples but
seldom appeared in the sockeye salmon diets. Similarly, S. oregonensis were almost never consumed from
Woss Lake, and both calanoid and cyclopoid nauplii
were common in both lakes but never appeared in the
sockeye salmon stomachs.
Based on these results, Woss Lake edible zooplankton was defined to include Daphnia, Bosmina, and
Epischura nevadensis. Vernon Lake edible zooplankton included Daphnia, Bosmina, and Hesperodiaptomus kenai (Table 4). During 2000–2001, edible
zooplankton biomass was higher in Vernon Lake than
in Woss Lake. During 2002, the situation was reversed.
This substantial between-lake difference was especially
obvious in July, immediately after the mid-June peak in
edible algae in Woss Lake. For example, during 2002,
Woss Lake edible zooplankton biomass totaled 26 lg
DW/L on 18 June, 90 lg DW/L on 9 July, and 81 lg
DW/L on 30 July. On the same dates, Vernon Lake
edible zooplankton biomasses were 22, 2, and 4 lg
DW/L, respectively. Edible zooplankton production
showed the same pattern.
Age-0 Sockeye Salmon Bioenergetics Simulation
Input data used in the fish bioenergetics simulation
included epilimnetic and hypolimnetic water temperatures, fish weight (Figure 6; Table 3), fish density
(Figure 6; Table 3), and sockeye salmon diets (Figure
7). In Woss Lake, average edible zooplankton biomass
and production (Table 4) increased with each succeeding year; in Vernon Lake, edible zooplankton biomass
and production decreased. The consumption rate
(Table 4) was positively associated with fish density
(Table 3) and age-0 sockeye salmon growth rate (i.e.,
December weight; Table 3). Average Woss Lake
379
ALGAE EFFECT ON SOCKEYE SALMON
FIGURE 6.—Seasonal changes in juvenile sockeye salmon weight (g 6 95% CI; left panels) and population density (fish/ha 6
95% CI; right panels) in a phosphorus-fertilized lake (Woss Lake, British Columbia) and an unfertilized reference lake (Vernon
Lake) during 2000–2002.
consumption rate expressed as a percentage of edible
zooplankton biomass declined as zooplankton biomass
increased. Vernon Lake consumption rates were stable
over time (Table 4).
Relation between Fertilizer Phosphorus and
Production in Woss Lake
In Woss Lake during 2002, a bloom of edible algae
was associated with higher uptake of FP, and this effect
TABLE 3.—Juvenile sockeye salmon fork length (FL), weight (net weight [WW]), and density in a phophorus-fertilized lake
(Woss Lake, British Columbia) and an unfertilized reference lake (Vernon Lake) during 2000–2002. Parenthetic values are
confidence intervals.
Year
Dec mean
FL (mm)
Dec mean
WW (g)
Jun mean
density (fish/ha)
2000
2001
2002
68.8
71.4
72.9
3.2 (0.17)
3.6 (0.11)
3.8 (0.14)
665 (418)
253 (111)
624a (316)
2000
2001
2002
72.8
66.6
55.2
3.8 (0.50)
2.8 (0.15)
1.6 (0.34)
902 (403)
640c (472)
1,069 (474)
a
b
c
Sample taken on 5 Mar 2003.
Sample taken on 10 Jul 2002.
Sample taken on 9 Jul 2001.
Dec mean
density (fish/ha)
Mean density 15 Jun–
31 Oct (fish/ha)
Mean WW gain
15 Jun–31 Oct (g)
Mortality 15 Jun–
10 Dec (%)
Woss Lake
535 (147)
202 (91)
843b (264)
589
331
667
2.02
1.92
2.42
19
20
0
Vernon Lake
485 (126)
597 (169)
747 (262)
599
571
965
2.48
0.79
0.91
46
7
30
380
MCQUEEN ET AL.
FIGURE 7.—Mean number (top panels) and mean biomass (lg dry weight [DW]; bottom panels) of zooplankton prey found in
stomachs of juvenile sockeye salmon collected from a phosphorus-fertilized lake (Woss Lake, British Columbia) and an
unfertilized reference lake (Vernon Lake) during 2000–2002.
cascaded upward through the entire food web (Table
5). During 2002, total and edible zooplankton biomass
values were higher and consumption of edible
zooplankton by age-0 sockeye salmon was higher.
For 2002, we estimated that the age-0 sockeye salmon
biomass stimulated by fertilizer additions was about
five times greater than that in 2001 and 10 times greater
than that in 2000 (Table 5).
These between-year differences were strongly regulated by the quantity of FP incorporated into edible
algae, then edible zooplankton, and eventually age-0
sockeye salmon. For example, FP taken up by edible
algae was 14.7 times higher during 2002 than during
2000 and that taken up by edible zooplankton was 21.9
times higher. Therefore, even though age-0 sockeye
salmon production was only 1.4 times higher during
2002 than during 2000, the proportion of production
associated with FP was about 10 times higher.
Fertilizer Losses in Woss Lake
Throughout the 3-year experiment, there were
substantial losses as FP moved through the food web
(Table 5). Over the 3 years, 22.8% of the FP added to
Woss Lake was incorporated into edible algae.
Fertilizer phosphorus incorporated into edible zooplankton averaged 2.6%, and FP incorporated into
juvenile sockeye salmon biomass averaged only
0.06%. Based on 2000–2002 averages, 561 g
Pha1year1 was added to Woss Lake, and only
381
ALGAE EFFECT ON SOCKEYE SALMON
TABLE 4.—Average (15 Jun–31 Oct) prey consumption (DW ¼ dry weight) by age-0 sockeye salmon as a percentage of edible
zooplankton standing stock and production in a phosphorus-fertilized lake (Woss Lake, British Columbia) and an unfertilized
reference lake (Vernon Lake). For the zooplankton taxa, large tick marks indicate mean annual consumption rates greater than
1.0% of mean annual daily production.
Taxona
Mean daily consumption Mean daily consumption
Mean daily
Average edible Mean daily edible
as a percent of edible
zooplankton bio- zooplankton pro- consumption by as a percent of edible
zooplankton production 1 2 3 4 5 6 7 8 9
zooplankton biomass
Year mass (lg DW/L) duction (lg DW/L) fish (lg DW/L)
2000
2001
2002
9.0
22.4
39.7
0.2247
0.3130
0.6933
0.0380
0.0329
0.0634
Woss Lake
0.42
0.15
0.16
17
11
9
2000
2001
2002
25.4
22.0
15.1
0.6675
0.5591
0.5071
0.0501
0.0348
0.0389
Vernon Lake
0.20
0.16
0.26
8
6
8
a
x
x
x
x x
x x
x x
x x
x x
x x
x
x
x
Taxon codes are as follows: (1) Other, (2) Bosmina, (3) Hesperodiaptomus kenai, (4) Skistodiaptomus oregonensis, (5) Diacyclops bicuspidatus
thomasi, (6) Daphnia, (7) Epischura nevadensis, (8) Holopedium, (9) Polyphemus.
0.33 g P/ha found its way into new sockeye salmon
biomass. The loss was 99.94%.
Discussion
Throughout the experiment, mean summer (May–
October) epilimnetic TP concentration and edible algal
biovolume were significantly (P , 0.05) higher in
Woss Lake than in Vernon Lake (Figure 8). However,
Woss Lake zooplankton biomass and age-0 sockeye
salmon December biomass were higher only during
2002, when the diatom Leptocylindrus bloomed at
Woss Lake in May and June. During the first 2 years of
the experiment, fertilization was associated with
relatively minor increases in Woss Lake sockeye
salmon production (39 kg/lake in 2000 and 69 kg/lake
in 2001; Table 5). During the third year (2002), the
estimated amount of sockeye salmon production
stimulated by fertilization increased to 380 kg/lake.
Some of this year-to-year variability could have been
due to chance: the 95% confidence intervals (CIs)
TABLE 5.—Fate of fertilizer phosphorus (FP) added to Woss Lake, British Columbia, during 2000–2002. For each year, all
averages are calculated over a 139-d period (Jun 15–Oct 31). Symbols and abbreviations are as follows: i ¼ input data from field
samples, TP ¼ total phosphorus, WW ¼ wet weight, and DW ¼ dry weight.
Study year
Variable
Units
2000
2001
2002
P loading to Woss Lake (i)
Average total algal biomass (i)
Average edible algal biomass (i)
FP incorporated into edible algae
Percent of FP incorporated into edible algae
Average total zooplankton biomass (i)
Average edible zooplankton biomass (i)
FP incorporated into edible zooplankton
Percent FP in edible zooplankton biomass
Edible zooplankton production (i)
TP consumed by edible zooplankton during production
Percent P taken up by edible zooplankton that was FP
Biomass of edible zooplankton consumed by sockeye salmon (i)
TP consumed by sockeye salmon
FP consumed by sockeye salmon
Percent FP consumed by sockeye salmon
Average sockeye salmon density (i)
Average sockeye salmon weight (i)
Mean (695% CI) sockeye salmon produced (i)
TP incorporated by sockeye salmon
FP incorporated into sockeye salmon
% of incorporated sockeye salmon P that is FP
Percent of FP incorporated in sockeye salmon
Biomass stimulated by fertilizer
Biomass stimulated by fertilizer (lakewide)
g/ha per summer
lg WW/L
lg WW/L
gha1139 d1
%
g DW/ha (lg DW/L)
g DW/ha (lg DW/L)
gha1139 d1
%
g DWha1139 d1
g/ha per summer
%
g DWha1139 d1
gha1139 d1
gha1139 d1
%
fish/ha over 139 d
g WW/139 d
g WWha1139 d1
g/ha over 139 d
g/ha over 139 d
%
%
gha1139 d1
kglake1139 d1
436
1,676
92
24
5.5
4,325 (17.3)
2,250 (9.0)
1.9
0.43
7,808
78
2.4
1,321
13.2
0.32
0.1
589
2.02
1,190 6 499
4.2
0.10
2.4
0.02
28
39
534
751
102
73
13.6
7,075 (28.3)
5,600 (22.4)
8.6
1.61
10,877
109
7.9
1,143
11.4
0.91
0.2
331
1.92
636 6 324
2.2
0.18
7.9
0.03
50
69
714
1476
727
352
49.3
12,625 (50.5)
9,925 (39.7)
41.5
5.81
24,092
241
17.2
2,203
22.0
3.79
0.5
667
2.42
1,614 6 742
5.6
0.97
17.2
0.14
278
379
382
MCQUEEN ET AL.
FIGURE 8.—Chemical and biological characteristics of a phosphorus-fertilized lake (Woss Lake, British Columbia) and an
unfertilized reference lake (Vernon Lake) during 2000–2002: May–October averages for epilimnetic total phosphorus,
phosphorus loaded as fertilizer, total phytoplankton biovolume, edible phytoplankton biovolume, total zooplankton biomass, and
edible zooplankton biomass; and December averages (695% CI) for age-0 sockeye salmon weight and biomass.
around age-0 sockeye salmon density were relatively
high (Figure 6), and this was reflected in the 95% CIs
for age-0 production rates (Table 5). However, the
variable yields in Woss Lake age-0 sockeye salmon
were also regulated by at least three other factors: (1)
year-to-year changes in percent edible algae, (2)
zooplankton species composition in coastal sockeye
salmon nursery lakes, and (3) year-to-year changes in
the density of the age-0 sockeye salmon.
Changes in the percentage edible algae were strongly
determined by the presence or absence of the inedible
diatom R. eriensis and the edible diatom Leptocylind-
rus. During 2000, a bloom of R. eriensis reduced
percent edible algae to 5.5%, and this was associated
with the lowest estimated augmentation in sockeye
salmon production (38.8 kg/lake). In contrast, during
2002 when R. eriensis was almost absent, Leptocylindrus bloomed, percent edible algae increased to
49.3%, and estimated age-0 sockeye salmon yield was
enhanced by 379.4 kg/lake. The Rhizosolenia problem
was also noted during several other nursery lake
fertilizations in British Columbia. At Mohun Lake,
Rhizosolenia densities increased when fertilizer was
added (Perrin et al. 1986). At Hobiton Lake, Rhizoso-
ALGAE EFFECT ON SOCKEYE SALMON
lenia bloomed when mean summer N : P ratio
increased to 129:1 (Hardy et al. 1986). At Kennedy
Lake, fertilizers with high N : P ratios stimulated
blooms of Rhizosolenia (Stockner and Hyatt 1984;
Stockner and Shortreed 1988). At Nimpkish Lake,
additions of 15:1 fertilizer stimulated Rhizosolenia
blooms; when the fertilizer N : P ratio was reduced to
1:1, Rhizosolenia became less abundant (Stockner and
Hyatt 1984). The potential key to Rhizosolenia control
is to reduce fertilizer N : P ratios. The obvious
disadvantage is that too little N is widely associated
with the growth of blue-green algae.
The structure of food webs in coastal nursery lakes
can also influence the relative percentages of FP
incorporated into algae, zooplankton, and fish. Over
the 3-year experimental period, Woss Lake ecological
efficiency from zooplankton to sockeye salmon
averaged less than 1% (Table 5). This is substantially
lower than the expected value of approximately 10%
(Gulland 1971) and may be partially due to the
structure of pelagic food webs found in coastal sockeye
salmon nursery lakes. Many coastal Pacific nursery
lakes have simple zooplanktonic food webs dominated
by Diacyclops bicuspidatus thomasi and S. oregonensis, both of which are too small and fast to be optimum
prey for juvenile sockeye salmon. Coastal food webs
also frequently lack an abundance of large Daphnia
that are more typical of eutrophic interior nursery lakes.
Simply put, the zooplankton species composition
typically found in coastal nursery lake food webs
reduces efficient nutrient transfer from fertilizer up
through the food web to juvenile sockeye salmon.
The third factor causing year-to-year variability in
Woss Lake sockeye salmon production was the density
of age-0 fish. During the 1980s and 1990s, before
Woss Lake was fertilized, density (acoustic assessments) and length–weight surveys were conducted over
11 years. Densities varied from 500 to 4,000 juveniles/
ha, and fall weights varied inversely from 2.6 to 1.0 g
as density increased (Figure 9). During the prefertilization years 1978 and 1979, fall densities were
very low (mean ¼ 588 juveniles/ha) and were within
the range observed during 2000–2002; also, fall fry
weight averaged 2.3 g and estimated net fall fry
production approximated 1,291 g/ha. In comparison,
during 2000–2002, Woss Lake fall fry density
averaged 529 fry/ha, weight averaged 3.5 g, and net
production approximated 1,887 g/ha. This production
increase averages 31%.
At the outset, our stated objectives were to estimate
the amount of fertilizer incorporated into juvenile
sockeye salmon and the amount of extra juvenile
biomass stimulated by the addition of fertilizer and to
determine whether increased production was large
383
FIGURE 9.—Relation between sockeye salmon fall fry
weight and juvenile density in a phosphorus-fertilized lake
(Woss Lake, British Columbia) and an unfertilized reference
lake (Vernon Lake) (open circles ¼ Woss Lake during
unfertilized years, 1978–1996; closed circles ¼ Woss Lake
during whole-lake fertilization, 2000–2002; triangles ¼
Vernon Lake during 2000–2002).
enough to justify the expense of fertilizer application.
During the years in which fertilization occurred, an
average of 23% of FP was incorporated into edible
algae, 2.6% was incorporated into edible zooplankton,
and 0.06% was incorporated into juvenile sockeye
salmon (Table 5). Fertilizer loss was 99.94%. The
amount of extra juvenile sockeye salmon biomass
stimulated by FP can be estimated in three ways. First,
as noted above, within-lake comparisons of historical
(1978 and 1979), pre-fertilization data versus production data from 2000–2001 in Woss Lake resulted in an
estimated net production increase of 31% (596
gha1year1). Second, the estimated quantity of extra
juvenile sockeye salmon stimulated by FP was 29 g/ha
in 2000, 50 g/ha in 2001, and 278 g/ha in 2002. This is
our most direct production estimate and yields an
average increase of 12% (119 gha1139 d1). Third,
comparison of the 2000–2002 age-0 sockeye salmon
summer production average in Woss Lake (1,146
gha1139 d1) with that of Vernon Lake (937
gha1139 d1; Table 5) yields a between-lake,
treatment versus control production increase of 18%
(209 gha1139 d1). The average of all three
estimates is approximately 300 g/ha per growing
season, which represents an average annual lakewide
increase of approximately 400 kg of juvenile sockeye
salmon biomass stimulated by 40,000 kg fertilizer/year
(average loading ¼ 767 kg P/year). Third, during 2000–
2002, the average annual cost of fertilizer plus
application in Woss Lake was Can$40,000, which
384
MCQUEEN ET AL.
TABLE 6.—Summary of potential sockeye salmon production and net economic benefits associated with the addition of
fertilize phosphorus to Woss Lake, British Columbia. Smolt production scenarios are based on estimates reported over 13 years
(1978–1996; Hyatt et al. 2004a). Adult returns during prefertilization years (1978–1996) are based on a low average smolt-toadult survival rate of 2.5%. Adult returns during fertilization years (2000–2002) are augmented by 14%, as suggested by
Bradford et al. (2000). Net benefits were calculated as the landed value of incremental adult production minus fixed costs of lake
treatment, where landed value is assumed to be $10 per fish and fixed costs are estimated to be $40,000 per year.
Adult returns
Smolt production
scenario
Number of
smolts
Pre-fertilization
Fertilization
Net economic
benefit
Lowest recorded
Average recorded
Highest recorded
380,000
1,340,000
5,210,000
9,500
33,500
130,250
10,830
38,190
148,485
26,700
þ6,900
þ142,350
translates to approximately $100/kg of enhanced fry or
$3 per enhanced smolt.
Proof of whether this high cost is justified really
depends on whether larger smolt weights can be
associated with increased marine survival. At Woss
Lake during 1978–1979 (nonfertilized), fall fry weights
averaged 2.3 g; during 2000–2002, (fertilized) fall fry
averaged 3.5 g. At Vernon Lake during 2000–2002,
fall fry weights averaged 2.7 g. The question is whether
a 1.0-g increase in mean smolt weight can significantly
affect marine survival. Three published sockeye
salmon nursery lake fertilization studies have included
measurements of marine survival. At Leisure Lake
(Kyle 1994; Koenings and Kyle 1997), smolt weight
increased by 112% from 1.7 g during the unfertilized
period to 3.7 g during the fertilized period, and smoltto-adult survival increased by 25%. At Packers Lake
(Kyle 1994), smolt weight increased by 100% from 5.7
to 100.4 g, and marine survival increased by 43%. At
Chilko Lake (Bradford et al. 2000), each 1-g increase
in smolt weight was associated with a 14% increase in
the adult return rate.
Based on these observations, it is reasonable to
assume that treatment-induced size increases for Woss
Lake smolts are likely to increase the average smolt-toadult survival rate by at least 14%. Consequently,
observations of the overall mean and range of Woss
Lake smolt production may be used in combination
with typical marine survival rates and landed-value
estimates for coastal sockeye salmon to determine a
possible range of net economic benefits for Woss Lake
fertilization (Table 6). These calculations suggest that
lake fertilization would probably yield negative net
economic benefits (i.e., losses of $26,000) in years at
the bottom end of the range of smolt output (i.e.,
380,000 fall fry observed in 1978 and 1979), but that
the benefits would become positive (minimum benefits
of $6,900) if fall fry production remains at or above the
overall average of 1.34 million/year (Table 6).
Furthermore, 50 years of overfishing and logging-
related habitat destruction have apparently reduced
total sockeye salmon returns to the Nimpkish River
system by at least 80%. Therefore, even modest
production increases delivered by lake fertilization at
low stock sizes would potentially halt or reverse the
long-term stock declines that could provoke future
Species-at-Risk Act listings.
Acknowledgments
We thank Hank Nelson, Bert Svanvik, and their staff
at the Gwa’ni Hatchery on the Nimpkish River. We are
also grateful for the help we have received from
members of the Nimpkish Resource Management
Board, especially Mike Berry, Hank Nelson, and Bert
Svanvik. Our field crew was headed by Barry Hanslit,
and we thank summer staff, including Eric Demers and
Leila Sumi. Finally, we are grateful to Margot Stockwell for redrafting Figures 1–6 and to our zooplankton
and phytoplankton experts, Stanley Sutey and Elaine
Carey. This work was supported by a grant from the
Natural Sciences and Engineering Research Council of
Canada to D.J.M., various CDFO operating grants to
K. Hyatt, funds from the ‘Namgis First Nation, and a
grant from the Pacific Salmon Endowment Fund to the
Nimpkish Resource Management Board. We dedicate
this paper to Bertil Svanvik (Wagidis), who suddenly
and tragically passed away while leading his team on
the soccer field. Bert was a key member of our research
team, and he will be sorely missed.
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