Lirnnd.
Oceanogr.,
23(6), 1978, 1114-1125
@I 1978, by the American
Society of Limnology
Limnetic feeding
Lake Washington
Douglas
Fisheries
and Oceanography,
Inc.
behavior of juvenile sockeye salmon in
and predator avoidance1
M. Eggers2
Research
Institute,
College
of Fisheries,
University
of Washington,
Seattle 98195
Abstract
Patterns of limnetic feeding behavior (vertical movement, schooling, diel feeding chronology, zooplankton prey selectivity)
of Lake Washington juvenile sockeye salmon are described.
A general hypothesis
to explain the relative fitness of alternative
behaviorial
decisions is
presented. The limnetic feeding behavior of the salmon appears to minimize their vulnerability to predation by the visual piscivore,
northern squawfish. Seasonal variation indicates
that sockeye feeding behavior is a short term optimization
process involving foraging success
and encounters with northern squawfish.
Lake Washington
sockeye salmon can afford to
spend a large amount of their time engaged in antipredator
behavior at the expense of foraging
success because Lake Washington is comparatively
zooplankton-rich
and the energy demands
of the fish can be met in short foraging periods. Sockeye in other less productive
systems
show a more aggressive exploitation
of the zooplankton.
Lake Washington anadromous sockeye
salmon (Oncorhynchus
nerka) spawn in
the Cedar River, spend 1 year in the lake,
and then 2 years in the ocean before maturing (Woodey 1972). To survive this
period of freshwater residence and have
reserves of energy sufficient
for migration to oceanic feeding grounds, the limnetic-feeding
juvenile
sockeye must
make behavioral decisions on timing and
duration of feeding, location of feeding in
the water column, prey organisms to pursue upon encounter, and mode to adopt
when not feeding. The Lake Washington
environment
provides seasonal and vertical gradients of prey abundance, prey
species composition,
light intensity, and
temperature.
In addition, the visual piscivorous predator, northern
squawfish
(Ptychocheilus
oregonensis), causes considcrable mortality of juvenile sockeye in
Lake Washington (Fig. 1). This environmental heterogeneity
implies
a wide
variation in fitness over the set of altcr’ Contribution
313 from the Coniferous
Forest
Biome and 479 from the College of Fisheries, University of Washington, Seattle. This study was supported by National
Science
Foundation
grant
DEB74-20744 AO2 to the Coniferous Forest Biome,
Ecosystems
Analysis Studies. Additional
support
was provided
by the Washington
Sea Grant Program (NOAA).
2 I thank C. IIarris, T. Zarct, ancl W. Odum for
reading the manuscript.
native behavioral decisions. These juvenile sockeye exhibit complicated seasonal and diel patterns of feeding behavior
(Woodey 1972; Eggers 1975; Doble and
Eggers 1978).
Here I present a generalized hypothesis regarding the relative fitness of alternative behaviors in the planktivore
feeddescribe
the known
ing repertoire,
feeding
behavior
of juvenile
sockeye
salmon in Lake Washington
and assess
this in terms of the hypothesis, and then
contrast the feeding habits of Lake Washington sockeye with those of juvenile
sockeye in other lakes with different environmental
characteristics.
Planktivore feeding
predator avoidance
behavior
and
In order to interpret patterns of feeding
behavior,
one must consider the costs
and benefits of alternative feeding behaviors. Juvenile sockeye salmon are visual
predators and require light to see their
zooplankton prey (Brett and Groot 1963;
Ware 1973; Eggers 1977; Vinyard
and
O’Brien 1976). However, when sockeye
are feeding they are themselves vulnerable to the visual piscivore,
northern
squawfish.
Planktivorous
fish must move through
the water column to feed as prey in their
vicinity
are consumed. This movement
1114
Juvenile
sockeye feeding
has two consequences
regarding
their
own vulnerability
to predators.
First,
prey movement increases the contrast of
the prey as well as the size of the retinal
image; hence, movement increases the
visibility
of prey (Ware 1973; Zaret in
press; Eggers 1977). Second, two objects
that are moving relative to each other are
more likely to come into contact than if
one of these objects is stationary. This result has been established in the theories
of line transects (Skellam 1958), of search
(Koopman 1956; Cushing and IIardenJones 1968), and of prey encounter by
tactile invertebrate
predators (Gerritsen
and Strickler
1977). The net effect of
these consequences
is to increase the
probability
that sockeye will be encountered by a visual piscivore while foraging.
If light is not required for feeding and
the organism is vulnerable
to predation
by a visual predator, then the optimal behavior would be to feed in the dark. If
the food is in the upper strata and the
organism must migrate into those strata
to feed, it should do so during darkness,
as do filter-feeding
herbivorous
and
grasping carnivorous
zooplankton.
Recent papers have argued convincingly
that the nocturnal
type (Hutchinson
1967) of vertical migration of zooplankton
is an antipredator adaptation (Swift 1975;
Zaret and Suffern
1976; Vinyard
and
O’Brien
1976). If light is required
for
feeding, the situation is more complicated. The organism must necessarily
expose itself to predation to feed.
Visual acuity is determined
by the
brightness contrast threshold of the retina-if the contrast of the retinal image of
the object is above the contrast threshold,
the object will be recognized
(Hester
1968). At low light intensity the contrast
threshold of the fish eye is an increasing
function
of light intensity
(Ware 1973;
Confer and Blades 1975; Vinyard
and
O’Brien 1976; Eggers 1977); hence, prey
sighting distances increase with light intensity. At high light intensity the determinant of prey sighting distances is the
minimum area that can be discriminated
by the retina, so that prey sighting dis-
0’
1115
I
I
I
I
1
I
I
I
I
I
I
I
JJASONDJFMAM
Month
estimated
number
of Lake
Fig. 1. UpperWashington juvenile sockeye salmon consumed per
month, June 1972 to May 1973, based on squawfish
abundance
and production
(Eggers et al. 1978)
and total respiration
computed from relations
in
Winberg (1956). Lower-estimated
abundance
of
sockeye (dashed line) back-calculated
from February abundance assuming squawfish predation
accounted for all sockeye mortality. Plotted points are
juvenile
sockeye abundance estimated by simultaneous acoustic and midwater trawl sampling (Traynor 1973).
tances are determined
by prey size and
motion and do not vary with further increase in light intensity. Zooplankton
are
more abundant in the upper strata of the
water column and the time necessary to
ingest plankton supplying
a given level
of energy can be expected to decrease as
the planktivore
moves from darker to
lighter
regions of the water column.
However,
if light intensity
is high and
zooplankton have a fairly uniform density
in the epilimnion,
the marginal benefit
from moving higher in the water column
vanishes as the near-surface strata are approached because of the asymptotic relation between light intensity
and prey
sighting distances.
By a similar argument, the probability
of encountering
a piscivorous
predator
increases as the planktivore
moves into
more lighted regions of the water column. Brief feeding high in the water column with high vulnerability
to predation
1116
Eggers
and extended feeding lower in the water
therefore be many strategies of feeding
column with a lower vulnerability
to prebehavior
of comparable
fitness for a
dation are possible alternate behaviors.
planktivore
such as juvenile
sockeye
The costs to the sockeye of being in
salmon. Similarly,
mcsopelagic
commumore lighted regions of the water column
nities in marine pelagic ecosystems typmay be mitigated
by schooling,
since
ically have many fish species that show
schooling reduces the chance of being
a wide variety in patterns of diel vertical
preyed upon (Brock and Riffenburgh
migration
and partitioning
of the water
1960; Olson 1964). By aggregating
in
column (Pearcy et al. 1977; Pearcy and
schools fish reduce the chance of being
Laurs 1966; Roe 1974; Maynard et al.
encountered
by a sight-oriented
preda1975).
tor, and even if encountered,
their
chance of being eaten is reduced because
Feeding behavior of Lake Washington
an individual
predator can consume only
juvenile sockeye salmon
a small part of the school. Because of visual field overlap and competition
for
The lacustrine growth of juvenile Lake
Washington
sockeye has three stages: a
zooplankton
among members
of the
period of near-exponential
growth, from
school, the rate of zooplankton ingestion
for a schooled feeder is lower than for a the time of entry to the lake until midausolitary feeder under identical conditions
tumn; a period of low or negative growth
in late fall and winter; a period of high
(Eggers
1976). Therefore,
schooling
planktivores
would
spend a greater
growth rate in spring before smoltificaamount of time foraging than a solitary
tion and seaward migration.
Sockeye
feeding planktivore
to ingest the same feeding behaviors differ greatly during
amount of material. Since the magnitude
these growth stages.
of the advantage against predation
inJuvenile
sockeye are visual plankticreases while the foraging efficiency de- vorcs and feed only in the light (Eggers
creases with increasing size of the school,
1975). During the summer-fall
growing
school size is an important component of season, sockeye feed intensely
in the
the planktivore
behavioral repertoire.
afternoon and are nearly satiated right
The alternative behaviors of brief feedafter dusk. There is a low incidence
of
ing high in the water column and then
empty stomachs in the population
at this
migrating to dark areas, more extended
time (Doble and Eggers 1978). Intense
feeding in regions of intermediate
light
feeding begins 2 h before nightfall in Auintensity,
or more extended feeding in gust and around noon in October (Doble
schools in regions of high light intensity,
and Eggers 1978). It is evident that durmay have comparable fitness. Thus, the ing the summer-fall
growth stage, sockcriterion for optimal feeding behavior of eye are effective in capturing prey because stomach contents increase rapidly
a planktivorous
fish cannot be expressed
in a few hours.
simply
as minimized
foraging
time
In the winter growth stage a consider(Schoener 1971) or simple diel vertical
able part of the population
has empty
migration.
For visual-feeding
planktivorous fish, a given strategy of feeding be- stomachs (60-80% in December, 20-50%
in February). The rate of prey ingestion
havior can be expressed as a partitioning
for actively feeding fish (i.e. those fish
of the available daylight into the following behavior modes: Schooled and ac- with food in the stomach) is much lower
in winter than in the summer-fall
growtively feeding, schooled and not feeding,
ing season. The high incidence of empty
solitary and actively feeding, and solitary
and not feeding;. Each of these must be stomachs indicates that a portion of the
sockeye population is not feeding. At this
further characterized by the activity level
time, the sockeye occur in two layers
of the planktivore-its
location in the
with the lower layer consisting
of fish
water column-and
for schooling behavwith empty stomachs (Woodey 1972). As
ior, the size of the school. There may
Juvenile
Il.17
sockeye feeding
1.0
1 El El B
December
0
_.,.............*.
:
6’ . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . (3
-1.0
.. .. .
El
q
El
El
8
1
In
0
10
El
0
a
I
q
a
1 =
B
y
G&Q,=
1 Be=
1
nl
’
cyc lops
z
G
1
A
A
-1.0 -II
Diaphanosoma
*+ + f
P
$
4 +
++
+
+
+ +
-1.01
1
I
1
I
,
I
0
I
,
PF
+Y
1
u
I
I
1
MAMJJASONDJFMA
Eplschura
Time
of day
(hours)
Fig. 2. Diel patterns in mean dry weight of
stomach contents (mg) of fish with food in their
stomachs (solid line) and percentage of empty stomachs (dashed line) for juvenile sockeye captured on
each sampling date. Vertical lines represent 22 SE
of mean. SS-Sunset;
SR-sunrise.
Samples taken
18 and 19 December
1976, 26 and 27 February
1977, and 28 and 29 April 1977. (Details of methods
in Doble and Eggers 1978.)
dusk approaches, the two layers merge
and the interchange
between layers indicates that sockeye may undergo a fasting-feeding cycle with a period of several
days (Eggers 1975). In February,
the
sockeye exploit the zooplankton more actively than in December;
although the
rate of prey intake is comparable, the incidence of empty stomachs is lower. The
diel feeding pattern during the presmolt
growth period is similar to that of the
summer-fall
growth period. The level of
food in the stomach following
dusk is an
order of magnitude higher than the winter level, with low incidence
of empty
stomachs in the population
(Fig. 2).
Juvenile
sockeye
salmon
in Lake
Washington show cxtrcme size-selective
predation
similar to that described
by
Brooks (1968) and Brooks and Dodson
Fig. 3. Ivlcv electivity
indices (1966-1971) for
each of four major zooplankton
species used by juvenilc sockeye in Lake Washington.
(1965). To demonstrate this, I calculated
electivity
indices (Ivlev 1961) from data
on the composition
of sockeye diet (Doble and Eggers 1978; Woodey 1972) and
from zooplankton
prey densities (W. T.
Edmondson pers. comm .). In calculating
the electivity
indices, I modified the in
situ prey densities for differential
visibility due to prey size (Eggers 1977; Confer
and Blades 1975; Werner and Hall 1974).
(Details of the source of the data and the
method of calculation are given in Eggers
1975.)
The largest zooplankton,
Epischura
and Viaphanosoma,
were selected for
when present (Fig. 3). The third largest
form, Diaptomus, was generally selected
against, especially in summer and early
fall. Diaptomus increased in the diet during late fall and winter when the abundance of Epischura
and Diaphanosoma
declined.
In some winters, Diaptomus
was a major food item, constituting
5090% of the diet; in other years, it constituted ~10% of the winter diet. Cyclops,
the smallest of the zooplankton forms caten by sockeye, is generally heavily se-
E ggers
1118
3 50s
0
s
b8
IO
0
1
Month
1969 Year-class
t
1
Id3
3
t lo-4
.$
to2
.g
IO’
L
B
8
Month
1968 Year-class
i
IO0
I
10-l
lo-2
3
6
Q
lo-3
50
‘\
/
I1
I I I II .I. 11
I1
MAMJJASONDJFMA
Month
1967 Year - class
1 I 1 Id4
Fig. 4. Nighttime
mean depth of occurrence
(solid line) of juvenile sockeye in Lake Washington
together
with index of ambient
light intensity
(clashed line) at depth of occurrence.
lectecl against, except during the first
months following
entry of the sockeye
into the limnetic
zone. In some years,
Cyclops was selected over Diaptomus
by the underyearling
sockeye during the
spring.
These marked seasonal patterns
of
prey selection
by juvenile
sockeye in
Lake Washington
support the optimal
foraging hypothesis (Charnov 1973, 1976;
Werner and Hall 1974; Eggers 1977; Doble and Eggers 1978). By restricting pursuit to large forms if sufficiently
abundant
and ignoring smaller zooplankton
forms
upon encounter,
sockeye maximize the
ration ingested per unit time or, equivalently, minimize the time necessary to ingest a given level of ration (Schoener
1971).
Juvenile sockeye in Lake Washington
show consistent seasonal and diel patterns of vertical movement. Sockeye occur over a wide depth interval (~20 m)
and are generally
located below 20 m
(Woodey 1972). They are seldom found
near the surface, significant
numbers
venturing
above 20 m only during the
spring. T’he extent of diel vertical migration is much reduced as compared to
more northerly sockeye systems, and the
shift in depth of peak abundance is generally ~10 m. Sockeye ascend during the
dusk feeding period and descend to daytime depths after dusk. There is no reascent following
dawn. The magnitude of
diel vertical
migration
is greatest in
spring, when the shift in the depth of
peak abundance of both yearlings
and
underyearlings
approaches 13 m.
The underyearlings
are close to the
surface during the few months after they
enter the lake (Fig. 4); the mean depth of
the population
shifts progressively
deeper from June through February. As smoltification approaches, the sockeye again
move higher in the water column, assuming a mean depth of occurrence similar
to that of very young sockeye following
entry into the limnetic zone.
Sockeye form schools throughout
the
summer--fall
growing
season (Woodey
1972). Schools disperse
as dusk approaches and re-form with increasing
light intensity
after dawn. During the
day, the schools are also stratified
by
depth as evidenced
by the echogram
(Fig. 5) taken 8 October 1974 in the central basin of Lake Washington.
At that
time the Lake Washington
planktivore
population
in the central basin consisted
of 47.3% juvenile sockeye salmon, 25.5%
longfin smelt (Spirinchus
thaleichthys),
and 27.0% threespine
stickleback
(Gasterosteus nculeatus).
These population
estimates were made from simultaneous
acoustic sampling and midwater trawling
during the night (Thorne et al. 1975).
We have no direct evidence as to whether the fish shown in the echogram are
stratified
by species by depth, since
schooled fish effectively
avoid our sampling gear. However, Woodey (1972) ob-
Juvenile
1718
1119
sockeye feeding
i
I
11
1I
II
1I
II
1756
1803
1810
1815
1822
1826
I
1832
Fig. 5.
0.1715-1~~
I1
1838
Echogram
isolume
1
1844
taken in central
rletcrmincd
from
1I
11
1858
1852
Time of Day (PDT)
basin of Lake
sd&~
light
Washington, 8 October 1974, 1718 to 1909 PDT. The
intensity
served similar patterns of school dispersal with approaching
dusk where fish
below the schooled layer were individual
targets. At that time juvenile
sockeye
were ~80% of the planktivore
population.
Schools occur only in the upper, more
lighted strata of the water column. During October the 0.17-1~~ isolume separates schooling
and nonschooling
fish.
This observation
is consistent with the
hypothesis
that maintenance
of fish
II
I909
and vertical
extinction
coefficient
of 0.35. m-1.
schools rcquircs sufficient
light so that
visual orientation among members is possible (Shaw 1961; John 1964; Hunter
1966; Whitney 1969). However, it is also
possible that this is strictly a behavioral
as sockeye are able to
phenomenon,
maintain schools at light intensities about
lo-” lux (Ali 1959).
Sockeye do not school during the winter growth period but resume schooling
during the prcsmolt growth period before
smolt migration,
The diel and vertical
1120
Table
Eggers
1. Comparative
size data for age 1 sockeye
smolts from various
systems producing
sockeye.
NO.
Yr
t
(mm)
1949-1970
1953-1972
1955-1973
1956-1972
1955-1958
1913-1915, 1951
1969-1976
22
20
19
16
3
4
6
83.7
88.4
101.3
91.6
82.0
59.7
69.0
77-91
80-96
91-113
81-97
4.8
5.7
9.3
6.6
59:&
64-78
:
--
Chilko
Shuswap
1950-1970
-
20
7
81.7
74.0
73-101
-
4.6
4.0
3.1-8.4
-
Cultus
Dalnec
1925-1971
1933-1941
21
7
81.6
116.0
68-94
106-133
6.2
16.4
3.0-8.6
12.5-23.0
Washington
1965-1969
5
126.5
120-133
18.5
16.7-20.5
System
Wood River
Kvichak
Naknek
Ugashik
Babine
Owikeno
Great Central
of
Year-class
* Alaska Department
of Fish and Game
t International
Pacific Salmon Fisheries
Range
E
Range
3.5-5.8
4.2-7.4
6.9-13-l
5.0-7.7
1
-
Source
-
ADF&G*
ADF&G*
ADF&G*
ADF&G*
Ricker (1962)
Foskett‘( 1958)
R. J. LeBrasseur
(per,. comm.)
1PSFC”t
Goodlad et al. (1974)
IPSFCt
Krogius and Krokhin
(1948)
J. C. Woodey
(pers. comm.)
J. J. Traynor
(pers. comm.)
(Fishery
Leaflet Series).
Commission
(unpublished).
pattern of school formation is similar to
that of the summer-fall
growing season.
It appears that the feeding behavior
repertoire
of Lake Washington juvenile
sockeye is a set of strategies to minimize
vulnerability
to predators, or equivalently, to minimize the rate of encountering
northern squawfish, subject to the constraints of energy requirements.
The fact
that juvenile
sockeye in Lake Washington occur over a wide depth interval and
show complicated
temporal and spatial
patterns of school formation attests that
the optimal feeding behavior may not be
unique but rather a fairly large subset of
the total possible feeding behaviors. This
hypothesis is supported by the observation that sockeye feed briefly, show extreme zooplankton prey selectivity, school
when light intensity is high, and migrate
into the upper strata where zooplankton
are more abundant only during periods
of low light intensity.
Sockeye reduce the probability
of
being seen by northern squawfish by limiting their foraging time and by keeping
to regions of the water column where
light intensity is low. The foraging sockeye ignore small prey items upon encounter if large prey arc abundant, fur-
ther reducing the time necessary to meet
energy requirements.
Interpretation
of seasonal variation of
Lake Washington
feeding behavior
involves consideration
of the distribution
of northern squawfish, zooplankton abundance, and sockeye energy requirements.
The Lake Washington zooplankton community remains mostly above 20 m except in late fall and winter. During 1974
the ratio of the density of all zooplankton
except rotifers and nauplii in the stratum
O-20 m to their density in the stratum 2058 m varied from 0.99 to 13.05, and the
monthly
average was 4.02 (W. T. Edmondson pers. comm.). Lake Washington
zooplankton
show little if any diel vertical migration.
Sockeye are found higher in the water
column in spring and early summer, both
as underyearlings
after entry to the lake
and as yearlings before seaward migration. As summer progresses, underyearling sockeye move deeper in the water
column. Late in fall, sockeye are at their
maximal depth (Fig. 4). They occur in
higher light intensity during spring and
early summer, and as they move deeper
they occur in lower ambient light intensity. Spring and early summer feeding
Juvenile
sockeye feeding
behavior indicates a more aggressive exploitation of the water column. This may
result from a number of factors. The size
of zooplankton individuals
is smaller during spring. The underyearling
sockeye
are less efficient
in utilizing
the zooplankton not only because the zooplankton are small but also because the fish are
much smaller and are much slower swimmers than during later periods of their
lake residence;
hence, they must feed
longer or in regions of the water column
where zooplankton are abundant.
In spring, northern
squawfish
move
from limnetic regions into littoral regions
to spawn. They move back into the limnetic zone during midsummer
(Bartoo
1972; Olney 1975). Thus, the costs to
sockeye of being in lighted areas of the
water column are lower during spring.
In winter, Lake Washington
sockeye
virtually
cease exploitation
of the zooplankton, presumably because of declining zooplankton abundance and because
the ambient light intensity for the fish increases as increasing water clarity compensates for the low incidence
of solar
radiation (Fig. 4). Because of high body
reserves of energy, it may be advantageous for sockeye to wait out the winter
rather than risk predation.
Sockeye resume a more active exploitation of the zooplankton
by February
even though water temperature and zooplankton
abundance are lower than in
December. This may be in response to
declining bodily reserves of energy-the
energy demands of smoltification.
Spring
feeding behavior before smoltification
is
similar to summer-fall
feeding behavior,
except that sockeye are higher in the
water column, presumably as a response
to lower squawfish abundance.
Discussion
Lake Washington produces some of the
world’s largest age 1. + (notation of Koo
1962) sockeye smelts (Table 1). Comparison of the seasonal growth curves of
sockeye
from Lake Aleknagik-the
southernmost lake in the Wood River system which produces very small age l.+
125.0
1121
1
-s‘OO.O
s$ I
75.0-
2
_
*
L$ 50.09
25.0 -
Fig. 6. Comparison of seasonal growth trajectories of length and weight for Lake Washington
(from Woodcy 1972) and Lake Aleknagik (from D. E.
Rogers pers. comm.) juvenile sockeye.
smelts-with
those from Lake Washington reveals that the large size achieved
by Lake Washington sockeye is due to a
long growing season as well as a high rate
of growth (Fig. 6).
Brocksen et al. (1970) compare sockeye
growth rate and biomass, and biomass of
zooplankton
prey for Owikeno,
BabineNilkitwa, and Dalnee sockeye-producing
systems. These lakes differ greatly in the
size of smolts produced (Table 1). Dalnee
has a much greater sockeye production,
growth rate, and biomass, and zooplankton biomass per unit lake area than either
Owikcno
or Babine-Nilkitwa.
The observed growth rates of Lake Washington
sockeye are comparable to those in Lake
Dalnee; however, the biomass of sockeye
in Lake Washington (Traynor 1973; Eggers et al. 1978) is comparable to that
of Owikeno.
Minimum
biomass of zooplankton in Lake Washington
in winter
is comparable
to that of Lake Dalnee,
whereas maximum biomass of zooplankton in Lake Washington during summer
1122
Eggers
is five times that of Lake Dalnee. Lake
Washington planktivores,
of which sockeye constitute the greatest biomass, crop
less than 2% of the annual zooplankton
production
in Lake Washington
(Eggers
et al. 1978). Th us, Lake Washington
represents an extreme case, compared to
other sockeye systems, where growth is
very good and zooplankton standing crop
is very high.
It is useful to compare the feeding behavior of Lake Washington juvenile sockeye salmon to that in less food-rich environments.
However,
there is little
information
concerning seasonal patterns
of diel feeding chronology,
schooling,
vertical movements, and prey selection
in other sockeye lakes because most of
them are ice-covered much of the year.
Some information
does exist regarding
the summer-fall
feeding behavior of juvenile sockeye in Babine Lake (Narver
1970; McDonald 1973) and in Great Central Lake (Barraclough
and Robinson
1972) *
In Babine Lake sockeye undergo a pronounced diel vertical migration (Narver
1970; McDonald
1973). Most feeding occurred during two 3-h periods bracketing
sunrise and sunset when they were within 3 m of the surface. During the day the
juvenile
sockeye were well below the
thermocline
(35-55 m) and at night were
dispersed
between
5 and 15 m, with
some of the population
below the thermocline. In October, after fall overturn,
vertical migration was less pronounced
than in summer. The sockeye at this time
were deeper in the water column, disperscd through somewhat wider layers,
and ascended and descended less rapidly. Narver (1970) reported that during
summer, juvenile
sockeye in Babine
Lake schooled during the day, dispersed
before dusk, and re-formed schools after
dawn. During the clay the sockeye wcrc
layered, with most of the population
in
the lower layer (27-37 m). Sockeye in the
upper layer (17-22 m) were feeding
whereas fish in the lower layer were not
or did so at a low rate. Early in the day
gut contents of fish in the lower layer
were greater than those of the feeding
fish in the upper layer; by late afternoon
there was no difference. Only two of the
six major zooplankton
species in Babine
Lake showed diel vertical
migration.
Bosmina coregoni rose during the day
and Heterocope
septentrionalis
during
the night. The daytime depth of Heterocope corresponded with the depth of the
upper layer of sockeye. Thcsc sockeye
fed almost exclusively
on Heterocope.
Narver fc:lt that this layering was caused
by the daytime feeding on these large copepods by a part of the sockeye population that had been less successful in feeding during
the previous
dusk (as
evidenced by lower gut contents).
In Great Central Lake, the patterns of
diel vertical migration of juvenile
sockeye were similar to those in Babine Lake,
but the fish tended to be much deeper
(55-79 m) during the day. Narver (1970)
attributed
this to the clearer water of
Great Central Lake. Sockeye were not
present in the near-surface water during
midsummer
when epilimnial
temperatures were >21”C. Barraclough and Robinson (1972) found that feeding was restricted to the twilight
period at dawn
and dusk. In Great Central Lake, zooplankton (except for rotifers that were not
eaten by juvenile sockeye) showed little
diel vertical migration (LeBrasseur
and
Kennedy 1972). During the day sockcyc
were well below (~20 m) the daytime
concentrations
of zooplankton.
Narver (1970) commented that the observed patterns of limnetic
feeding bchavior of juvenile
sockeye in Babine
Lake apparently reduce risk of piscivore
predation,
but discounted
this because
he observed a low density of piscivorous
fish (rainbow trout, Salmo gairdneri,
and
lake trout, Salvelinus namaycush) in the
limnetic zone of Babine Lake. However,
this distribution
may be the result of successful antipredator
behavior of juvenile
sockeye. Piscivorous
fish may exploit
several habitats. During
1972 northern
squawfish in Lake Washington fed more
heavily on prickly sculpin (Cottus asper)
than on planktivorous
fish (Olncy 1975).
Prickly
sculpin
are benthic
and extremely abundant in Lake Washington
Juvenile
sockeye feeding
(Rickard 1978). Th us, in Lake Washington, benthic-littoral
regions offer squawfish other prey than planktivorous
fish.
Piscivores may switch from one habitat
to another depending
on the respective
foraging success (MacArthur
and Pianka
1966). Foraging success is influenced
by
the abundance as well as the antipredator
behavior of the prey in the alternative
habitats. It is thus hard to establish cause
and effect when evaluating structural differences among open-water
communities. The limnetic feeding behavior of cohabiting zooplankton,
planktivorous
fish,
and piscivorous fish is highly interrelated
because of the reciprocal tradeoffs in behaviors that most efficiently
exploit resources or avoid predators.
If the nocturnal type of vertical migration in zooplankton
communities
is an
adaptive response to visual planktivore
predation
as Zaret and Suffern (1976)
suggest, then one would expect little or
no diel vertical migration where planktivores are controlled by piscivorous fish.
The general lack of nocturnal patterns of
zooplankton
vertical migration
in Lake
Washington, Great Central Lake, and Babine Lake supports this hypothesis. The
only zooplankter
that shows substantial
vertical migration is Heterocope
in Babine Lake. Heterocope, a large predatory
copepod, is the major dietary item of juvenile
sockeye salmon (Narver
1970;
McDonald
1973). Why does Ileterocope
migrate from a region of low sockeye
abundance to a region of high sockeye
abundance during the day? If darkness is
an effective refuge from visual planktivores, why is Heterocope
not found
deeper during the day? McDonald (1973)
found no upper layer of feeding sockeye
associated with Heterocope
in Babine
Lake, indicating
that sockeye may have
been responding to environmental
differences in the 2 years. The pattern of mutual diel vertical migration of zooplankton and planktivorous
fish is a complex
equilibrium
of the processes of resource
exploitation
and predator avoidance affecting four trophic levels.
The patterns of diel vertical migration
in Babinc and Great Central lakes differ
1123
from those in Lake Washington. In Lake
Washington
the extent of diel vertical
migration is ~13 m, and most of the year
sockeye are below 20 m even when epilimnial
temperatures
are within
their
tolerance ranges. There is no postdawn
feeding period in Lake Washington.
Because Lake Washington is a zooplanktonrich (both abundant and large) environment, sockeye can meet energy requircments by feeding relatively
deep in the
water column. When sockeye do show
diel vertical migration, they migrate only
to the lower edge of the region of high
zooplankton
abundance.
Furthermore,
their energy requirements
are met in a
single feeding period near dusk.
Brett (1971) suggested that the Babinetype diel vertical migration is an energyconserving
device as a consequence
of
lake stratification,
reasoning that the daily temperature regime under vertical migration optimized
the conversion
efficiency of ingested material. However, as
Swift (1975) showed for Chaoborus, the
increased respiratory
efficiency
cannot
compensate for the reduced food intake
following
migration into regions of low
prey abundance.
Also, Brett’s bioenergetic hypothesis is inconsistent
with the
observation
that diel vertical migration
can occur in a homothermous
water column, as it certainly does in the fall in
Babine Lake (McDonald
1973) and in the
spring in Lake Washington, On the other
hand, Brett’s hypothesis,
or McLaren’s
(1963) similar hypothesis, is not inconsistent with the hypothesis developed here,
because any energy bonus resulting from
minimizing
respiration costs at low temperatures
serves to reduce energy requirements,
hence reduces the foraging
time needed to ingest the needed energy,
and thus decreases vulnerability
to predators.
It would appear that juvenile
sockeye
in Lake Washington modify their location
in the water column, the timing and duration of their feeding, their pattern of
school formation and dispersal, and the
set of prey they pursue upon encounter
so as to minimize exposure to predators
while still achieving their minimum
ra-
Eggers
1124
tion requirements.
also commensurate
These quantities
with fitness.
are
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Submitted: 2 November
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1977
1978