YOUNG, STEPHEN, AND PENELOPE WATT. Behavioral

Limnol. Oceanogr., 38(l),
0 1993, by the American
Behavioral
1993, 70-79
Society of Limnology
and Oceanography,
mechanisms controlling
Inc.
vertical migration
in Daphnia
Stephen Young and Penelope Watt
Department
of Biology,
Imperial
College, Silwood
Park, Ascot, Berks SL5 7DE, U.K.
Abstract
We used infrared video monitoring to study cladoceran vertical migration in laboratory tanks exposed
to natural and simulated daylight cycles. There are changes in the behavior patterns at different times of
the year, with both Daphnia magna and Daphnia longispina showing increased vertical migration and
greater average depth later in the year. This change in behavior pattern is due to temperature, not daylength,
changes. Our animals show a complex endogcnous migration pattern, with a strong downward excursion
in the middle of the night, another before dawn, and then a morning rise, of which only the last depends
on a visual stimulus. We propose that the morning rise acts as a correcting movement bringing animals
to a depth just safe from visual predators. The midnight sinking is unlikely to be due to a random
spreading-out process. Fish taste cues enhanced the dawn excursion, but not the midnight one. Responses
to fish cues were most pronounced for D. magna at low temperatures.
Much recent work on vertical migration has
concentrated on functional explanations, and,
in several cases, it has been clearly demonstrated that the behavior pattern is strongly
linked to fish predation (Lampert 1989; Stich
and Lampert 1981; Gliwicz
1986; Dodson
198 8, 1990). In this view plankton forsake
food-rich surface waters during daylight hours
and keep to a zone just too dim for fish to spot
them. Wright et al. (1980) suggested that small
daphnids ought to be safe from white crappie,
a planktivore in the midwestern lakes of the
U.S., at light intensities < 30 mW m-2, though
Janssen (198 1) observed herring foraging effectively at 13 mW m-2. Behavioral acuity
measurements for three species of teleost, reviewed by Douglas and Hawryshyn (1990),
provide strikingly consistent measurements,
suggesting that a 2-mm Daphnia will be safe
at ~20 mW m-2, while a 3-mm animal needs
to be at ~0.1 W m-2 to achieve the same level
of invisibility.
If this model is the sole explanation for vertical migration, we would expect
to see a single daily movement, with animals
moving to deeper, darker waters in the day,
reaching their maximum depth at midday, and
moving to surface waters after dusk and remaining there through the night.
Since the function of the response is to hide
prey in a dim light zone, it is natural to con-
elude that visual stimuli control the behavior,
and the consensus view is that the proximal
cause of vertical migration is a form of phototaxis (Wright et al. 1980; Dodson 1990). Animals are thought to track an optimum light
intensity zone as it daily descends and ascends
through the water. Ringelberg (1964) has shown
that Daphnia magna can manage a sort of stepwise approximation to tracking an optimal light
level by a series of ballistic leaps triggered by
changes in light levels. Although the behavioral responses are to the rate of change of
illumination
rather than to an absolute light
level, the effect is that animals tend to remain
within a band of optimal light levels, though
the accuracy of tracking depends on the turbidity of the water.
We set out to investigate two problems encountered by this theory of vertical migration.
First, observations of vertical migration in the
field and in the laboratory often show patterns
much more complicated than a single daily up
and down movement (Hutchinson
1967; Dumont and De Meester 1990; Vijverberg 199 1).
Downward
excursions have been reported
during the night, followed by upward movement after dawn while light levels are still rising (e.g. Bosch and Taylor 1973). This phenomenon is often referred to as “reverse
vertical migration” (Ohman et al. 1983). While
accepting that this term adequately describes
data sets in which animals are nearer the surface at midday than at midnight, we feel the
implication that there is no daytime downward
movement in these cases is probably unhelpful. Animals may well be showing a “normal”
Acknowledgments
We thank Jim Grover for comments and Thames Water
for collecting Daphnia magna from Wraysbury reservoir.
This work was supported by a grant from the Natural
Environment Research Council.
70
Daphnia
vertical migration
vertical migration pattern, with a large downward movement around dawn and an upward
movement at dusk, complicated by an extra
nighttime
excursion
and a morning
rise
(Hutchinson
1967). This pattern could be detected only by frequent monitoring; single daytime and nighttime readings would give the
impression of reverse vertical migration.
Nocturnal descents were first observed by
Ruttner (1905) and were called twilight migrations
(Dammerungswanderung).
The
morning rise phase is in the wrong direction
for any simple negative feedback depth control
system using either absolute light levels or rates
of change in light intensity: in both cases a light
increase will result in downswimming.
Second, the “just safe” optimum light level
sweeps downward through the water of a clear
lake at dawn at a rate of 70 cm min-l, faster
than the maximum downward swimming speed
of Daphnia. Hutchinson (1967) reviewed studies of Daphnia downward movements and suggested a maximum speed of 20 cm min- I. Because there is some doubt about whether the
animals in these studies were actively swimming and not sinking, we have checked the
animals from our cultures, inducing active
downswimming
by a sudden large increase in
light intensity. We found D. magna capable of
swimming at a maximum rate of 45 cm min- 1
(avg speed = 29.3k3.5 cm min-l, n = 8). High
mortality during a brief period of visibility at
dawn could act as a strong selective force for
downward movement before dawn, beginning
well before any visual stimulus is availableHutchinson
(1967) reported observations of
predawn excursions.
The detectability of vertical migration patterns in short water columns in laboratory tanks
is a surprising but well-established phenomenon. In several cases field and laboratory data
are available for the same population and are
apparently identical apart from a hundredfold
change in vertical scale (Harris 1953; Schrijder
1959). A likely explanation is that the water
in laboratory tanks is completely undisturbed,
and lakes have considerable vertical stirring,
Thus a movement pattern which shows up as
a constant drift in a strongly stochastic population will only be detectable in the field if
data are available from a very long column of
water. We exploited the fact that plankton will
perform in this way to study twilight migration
71
and the morning rise phenomenon under controlled conditions in two species of Daphnia:
magna and longispina. Animals were exposed
to natural diurnal
light and temperature
rhythms and to carefully
simulated
light
rhythms at constant temperature. Infrared video techniques enable us to keep track of all the
individuals in the group through both light and
dark phases of the cycle. We made observations throughout the year to investigate the
summer inhibition
of vertical migration reported in field studies (e.g. Stich and Lampert
198 l), and, following a suggestion by W. Lampert, we have contrasted fish-tasting and nonfish-tasting water. Cyclomorphosis has not been
noted in any of the clones under study. Furthermore, there is no evidence that morphological and behavioral mechanisms of predator
avoidance are related (Ramcharan et al. 1992).
Methods
Experiments were conducted between April
1990 and May 199 1. We collected D. longispina from the Japanese Garden Pond at Silwood Park (which had never had a fish population)
and D. magna from Wraysbury
Reservoir, near Datchet (which has a small
population of fish, mainly ruffe, perch, and
roach, Duncan and dos Santos 1989). Clones
were raised parthenogenetically
from individual females isolated in pots containing 200 ml
of pond water. The water had been filtered
without pressure through a single sheet of filter
paper (Whatman type 1) to remove debris and
copepods but not algae. They were fed with
Scenedesmus acutus, cultured in a modified
Chu 10 algal culture medium. One source of
pond water was the Silwood Stores Pond, which
contains a substantial population
of rudd,
roach, and perch.
Figure 1 shows the vertical migration tank
and video system. Illumination
was supplied
through a rectangular aperture above the top
of the tank by either natural daylight viewed
through an open roof-light or a quartz-halogen
lamp with an integral dichroic reflector. Light
intensity was measured inside the experimental chamber (Fig. 2A shows typical readings).
There was no gradient in light intensity detected between the bottom and the top of the
tank. In the natural daylight condition the tank
remained at the prevailing ambient air tem-
72
Young and Watt
Fig. 1. View of the apparatus with the tank chamber
lid removed. The tank (12 x 4 x 35 cm) is illuminated
during both the light and dark phase of the day by two
vertical arrays of nine wide-angle GaAIAS infrared emitters (RS components, type 585236; average power of 20
mW at 880 nm). The video camera (Cohu, type 4722),
direction of view indicated by arrowhead, is sensitive to
IR light. The baflles provide a dark background against
which Daphnia can be seen.
perature in the room (ranging from 23°C in
summer to 5°C in winter), while for the artificial light treatment the temperature was kept
constant at 15°C (comparable to spring air
temperatures in the field). At no stage did a
measurable temperature difference occur between the top and bottom of the tank.
The oxygen concentration
of water in the
experimental tank was checked five times during the course of the experiments and did not
differ appreciably between the top and bottom
of the tank.
To produce an artificial dawn-dusk light cycle we modeled the local daylight intensity cycle with a simple sinusoidal function. A computer control system evaluated this function
at 30-s intervals throughout the day and adjusted the dc voltage supplied to the lamp so
its output tracked the function curve. Peak
midday light level at the tank surface for the
artificial light treatment was set to 52 W m-2,
the mean value for the natural daylight treatment. The night period in the artificial light
cycle was completely dark.
For each run, between 15 and 20 animals
were transferred from their stock culture into
12
16
20
24
4
8
Time(houf-9
Fig. 2. A. Typical vertical migration pattern (0) for
three clones of Daphnia longispina from the Japanese Garden Pond at Silwood Park in a natural daylight run, expressed as three-point running averages of mean depths.
Average natural light intensity (0) over the 19-h period
when the runs were conducted (April 1990) is also shown.
B. Overall average depths for Daphnia in our study at the
five key points extracted from the video records. Vertical
bars show SEs of depths; horizontal bars are SEs of the
times at which the key points occurred: a-dusk; b-night
maximum; c-night minimum; d-dawn; e-brightest light
(N = 33). C. Similar data for animals in continuous darkness (N = 9).
the experimental tank and filmed over a 19or 24-h period. There is no evidence from our
observations that the number of animals per
liter has an effect on the vertical migration
pattern. The water in the experimental tank
was either the fish-taste treatment-water
collected from the Stores Pond on the same day
of the experiment and gravity filtered (Whatman type 1) to remove debris and copepods
without adversely affecting the chemical composition of the water or the concentration of
mixalgae - or the nonfish-taste treatment-a
ture of 200 ml of algal culture medium and
1,500 ml of distilled water. Daphnia clones
were successfully raised in this medium with
no adverse effects on their behavior. There were
differences in absorbance between water treat-
Daphnia
vertical migration
ments over a range of light intensities (Table
1). Trials were made with natural light over a
12-month period, with artificial light at differing daylengths (carried out in November 1990
and May 199 1 at daylengths of 15 h for 1 May
and 10 h for 1 November at 5 1.5”N and 0.5OW)
and in constant darkness by covering the rectangular aperture with light-proof paper.
The video tapes were analyzed by digitizing
the vertical positions of each animal in the
group at intervals of 10 min. The average depth
(vertical position) was then calculated each
hour of an experimental run for each group
(Fig. 2A). Forty-two experimental runs were
conducted: of these 30 were in the fish-taste
treatment, 12 in the nonfish-taste; 8 in artificial
light (34 natural), and 9 in continuous dark (33
light). In order to compare cycles of differing
photoperiod, we extracted mean depths from
the records for each replicate at dawn (d) and
dusk (a), light intensity = 2 mW mp2; at the
nighttime maximum (b) and minimum depths
(c); and at the daytime peak light intensity (e)
(Fig. 2B). Two summary statistics were calculated- the overall average depth,
(a + b + c + d + e)/5,
and the total vertical distance swum between
the five mean depths extracted from each record,
la - bl+lb - cl+Ic - dl
+Idel+leal.
Figure 2B shows the average clocktimes at
which these key points occurred. The first statistic is referred to as “average depth AVD,”
and the second as the “minimum
vertical migration distance” MVMD. Data were analyzed
with the GLIM statistical package (Aitkin et
al. 1990). All our quoted standard errors are
based on samples of average depths from N
replicated runs rather than on the depths of
individual Daphnia within each run.
A subsidiary experiment tested the effect of
differing light stimulus regimes on the midmorning rise. The tank used in this experiment
had a movable septum which, when closed,
divided the tank vertically into halves so that
the animals in each half could be counted. The
tank was surrounded with light-proof paper so
that light, supplied artificially
by a quartzhalogen lamp with variable control, entered
through the top of the tank only. For each run
73
Table 1. Absorbance cm ’ readings over a range ol
wavelengths (nm) for fish-tasting and nonfish-tasting water
treatments used in experimental runs.
Wavelength
420
520
720
Fish
tasting
0.0222
0.0089
0.0032
Nonfi\h
tasting
0.00 1 1
0.0006
0.0004
25 animals (D. longispina) were added to the
tank that contained filtered (Whatman type 1)
water from Stores Pond (as above). At the start
of each run the tank was illuminated at a light
intensity corresponding to that which initiated
the midmorning
rise in D. longispina clones.
Animals were left for a period of 10 min to
acclimatize, the septum was then closed, the
number of animals in each half of the tank
counted by hand, and the percentage of animals in the top half of the tank calculated. At
lo-min intervals the light intensity was either
increased or decreased by a factor of two or
kept at the initial light level. For any one run
four readings were taken: one at the initial light
intensity and three under increasing, decreasing, or constant light conditions.
Results
The two species have broadly similar behavior patterns with no significant difference
in average depth (196 + 9 mm, N = 23, for D.
longispina; 199 -t 14 mm, N = 10, for D. magna), but the larger D. magna has a lower
MVMD (10 l* 22 mm compared with 167 + 14
mm for D. longispina, P < 0.05, F-test).
Figure 2B shows the overall average migration pattern for all treatments with a light cycle
and 2C for animals kept in continuous darkness. The twilight migration pattern is clearly
present in both cases, with two downward excursions during the hours of darkness that are
not significantly different from each other (P
> 0.05, t-test). The morning rise, however,
occurred only if a light stimulus was present.
Figure 3 shows the predawn excursion in more
detail for D. longispina for illuminated
and
continuous
dark groups. The downward
movement followed the same pattern for both
groups until the beginning of the light cycle.
when the animals in continuous darkness continued moving downward; those exposed to a
visual stimulus began their morning rise. The
subsidiary experiment testing the effect of dif-
74
Young and Watt
;
II
160r
Y
Time
6
8
Time
(min)
I
10
(h)
Fig. 3. Effects of continuing darkness on the dawn sinking response in Daphnia longispina. Controls-O,
whose
light regime is shown in the lower box; D. longispina kept in constant darkness-0
(N = 9 in each case-bars show
SEs derived from analysis of deviance residual). Data were derived from the video analysis of nine clones of D.
longispina filmed under natural daylight and continuous dark. Inset shows the results of the subsidiary experiment
which involved interfering with the light regime at the point indicated by the star. Data are the percentage of the
population in the top half of the tank at IO-min intervals after intervention
began. The three treatments were rising
light intensity (0), steady light intensity (V), and decreasing light intensity (0). Bars on the inset are binomial SEs based
on totals for each group averaging 23.
ferent light regimes on the midmorning
rise
confirmed that it depended on an increasing
* light intensity at this phase of the cycle (Fig.
3).
The extent of midnight
excursion,
[(a
+ c)/2] - b, is not significantly different for
animals exposed to a night sky (32 15 mm, N
= 25) and those in a simulated light cycle which
has a totally dark “night” (27 4 10 mm, N =
0
Figure 4 shows how the variation in vertical
scatter of the population (as measured by the
SD of the mean depth) varies with its mean
depth by night and day. Scatter is significantly
greater in the middle of the tank than at either
the top or bottom (P < 0.001, F-test) and is
significantly greater at night (P < 0.00 1, F-test).
The distribution
of the depths of individual
Daphnia in a group was often strongly asymmetrical, but this analysis used the standard
deviation of each sample of depths as a dispersal measure and, since the distribution
of
the standard deviation data was symmetrical
and bell-shaped, we used a model with nor-
Daphnia
vertical migration
75
Table 2. Average depths (mm) and minimum vertical
migration distances (mm) for 25 runs in natural daylight
divided into groups by time of year. There arc significant
differences between the spring-summer and autumn-winter groups in MVMD
(P < 0.05, F-test) and AVD
(P < 0.01, F-test).
McanfSE
Spring-summer
Autumn-winter
24C
-
30
40
1
I
I
50
60
70
I
80
90
Standard deviation (mm)
Fig. 4. Variation in the vertical population scatter (as
measured by the SD of the mean depth) plotted against
mean depth for day (0) and night (0) data for Daphnia
magna. Bars give SEs for the scatter measures based on
17 1 samples from eight separate runs. For the graph, mean
depths were grouped into successive 30-mm intervals;
numbers on the graph show the sample sizes for each
group.
mal-distribution
errors to test for the effects of
light and of depth on the extent of dispersion.
The data were grouped into two extended
periods of experimental runs which had a gap
of >2 months between them, from 25 April
to 2 August (avg date, 1 June) and from 22
October to 12 March (avg date, 5 December).
Dates were selected within these periods on
the basis of equipment availability.
We called
the first group spring-summer and the second
group autumn-winter.
Table 2 shows that, for
animals exposed to natural daylight and ambient temperatures, the behavior pattern differs at different times of year, both in terms of
MVMD (P < 0.05, F-test) and AVD (P < 0.0 1,
F-test). Animals remain closer to the surface
and migrate over a shorter distance each day
in spring-summer
as compared to autumnwinter.
AVD
MVMD
AVD
MVMD
All
175+13
108224
225k9
178-1: 18
N
9
16
To test the hypothesis that seasonal effects
were due to changes in daylength, we simulated
long and short days with an artificial light
source in a constant temperature room at 15°C
(see methods). This simulation failed to produce the expected results. Figure 5A shows no
effect of daylength on the vertical migration
patterns for the eight runs in simulated daylight, and Table 3 compares this data with the
25 natural daylight runs also grouped by daylength. In the latter case there are statistically
significant differences between the long- and
short-day groups both for AVD (P < 0.01,
t-test) and MVMD (P < 0.001, t-test). Animals in the simulated daylight studies, whatever their daylength, behaved as if they were
experiencing natural daylight on a spring-summer day.
Because our natural daylight groups were exposed to ambient temperature conditions, there
were systematic ambient temperature differences between the long-day (12.6 f l°C) and
the short-day (average 9.5 * l°C) groups (P <
0.05, F-test). We found that a model based on
temperature differences, dividing the same data
set into high- (15-23.3”C) and low- (4.3-12.3”C)
temperature groups had a substantially lower
residual deviance than the daylength model
and produced a more consistent account. Figure 5B shows that vertical migration for these
two groups corresponds to the patterns observed at different times of the year, with reduced movements and shallower positioning
at high temperatures. In fact the simulated
daylight data for both long and short days are
close to high-temperature natural daylight data
(Table 4).
There was no evidence of a temperature gradient between the top and the bottom of the
tank in any of these studies and thus no pos-
76
Young and Watt
Table 3. Average depths (mm) and minimum vertical
migration distances (mm) for 25 runs in natural daylight
and 8 runs in simulated daylight, both sets divided into
long- and short-day groups.
Mean+SE
Long day
Short day
Q
I
I
0
o-
1
‘0
I
I
O\O
I
I/&l
I
I
I?
0
I
I
w
A
0
-1
a
b
c
d
Vertical
e
migration
abed
e
key points
Fig. 5. A. Vertical migration patterns for Daphnia
longispina and Daphnia magna exposed to simulated daylight patterns at a constant 15°C. The short-day group (0)
have 10-h daylengths; the long-day group (0) have 15 h.
Bars show SEs of means for two runs in each case derived
from analysis of deviance residual. The vertical migration
key points on the x-axis are as defined for Fig. 1. Daylength
does not have a statistically significant effect on the vertical
migration patterns. B. Data for both natural and simulated
light conditions grouped by temperature. High-tempcrature group (0), > 15°C; low-temperature
group (O), < 15°C.
Sample sizes: D. longispina warm 8, cold 15; D. magna
warm 4, cold 6. The difference between low- and hightemperature groups is statistically significant, P < 0.00 1,
F-test). The 33 runs of data include 25 runs in natural
daylight and 8 in simulated daylight.
sibility of migration being restricted to a preferred temperature zone within the tank.
Overall, the presence or absence of fish taste
in the experimental water had a significant effect on the extent to which animals of both
species migrated below their average depth before dawn and at midnight. The groups in fishtasting water have predawn excursions that
carry them significantly below their AVD (Ta-
Avg day (h)
AVD
MVMD
Avg day (h)
AVD
MVMD
Natural
daylight
15.1 kO.3
184*9
104+ 17
10.7kO.3
232+10
205+ 18
N
13
12
Simulated
daylight
15
168f17
135+31
10
163+17
123&31
N
4
4
ble 5). The midnight excursions show no similar response -if anything they are deeper in
the nonfish-tasting water treatment (the waterexcursion interaction term in the analysis of
deviance is statistically significant, P -K 0.01,
on an F-test). If these data are divided, as before, into high- (> 15°C) and low- (< 15°C)
temperature runs then the vertical migration
pattern appears to be enhanced in fish-tasting
water in the case of D. magna at low temperatures (Fig. 6). Paradoxically, there is an accompanying decrease in average depth.
Discussion
Our results support the view that the main
vertical migration mechanism is independent
of visual tracking of a preferred light intensity
band. The midnight excursion and the downward phase of the predawn excursion are consistently present in all our records, both for
animals exposed to the night sky and for those
in total darkness. Tt thus seems unlikely that
field observations of the same phenomenon
are artefactual (Hutchinson
1967) or that this
part of the behavior pattern needs a moonlight
cue. Only the morning rise- the upward phase
of the predawn excursion-needs
a visual
stimulus. Our interpretation
of this phase of
the behavior is that animals need to correct
any overshoot during the predawn descent period, when there is no way of estimating the
minimum safe depth in the dark, and return
toward the surface, once visual information is
available, until they reach the upper limits of
a “safety zone” - above which they will be visually detected.
We observed a modulation in the behavior
pattern at different times of year with reduced
excursions in summer, which has also been
observed in the field (Stich and Lampert 198 1).
Daphnia
Table 4. Average depths (mm) and minimum
divided into high- and low-temperature
groups.
AVD
MVMD
AVD
MVMD
Low temp. (8.5kO.5”C)
vertical
Table 5. Extent to which the predawn and the midnight
excursions extend below AVD, showing the effects of a
fish-tasting water treatment.
Predawn
Midnight
Measure
AVD d
AVD b
+ Fish
N
-Fish
N
12.5k4.2
19.Ok4.2
21
21
4.61k5.5
29.3k5.5
12
12
77
distances (mm) for all 33 runs with a light period,
Simulated
daylight
N
4
168, i8
79*35
215f8
167+ 15
Once again visual cues do not seem to be responsible - ambient temperature appears to be
a better candidate for the controlling stimulus
than daylength.
Thus our overall view of Daphnia vertical
migration is that the main components are endogenous rather than phototactic. Circadian
rhythms have been observed in Daphnia for
vertical migration (Harris 1963) and for photopositive responses (Ringelberg and Servaas
197 l), so this suggestion is plausible. It does
not necessarily conflict with the theory that
avoiding fish predation is the ultimate cause
of vertical migration. Animals need to start
descending well before dawn to avoid dangerous regions and the predawn downward movement was most marked in water that had
contained fish-both
suggesting that its role is
fish-avoidance. Daphnia is known to be able
to detect fish-taste cues for at least 7 h in the
laboratory (Dodson 1988). In this series of experiments it is likely that such cues were present and detected for a longer period because
the predawn downward movement occurred
at least 11 h after the start of an experimental
run. The apparent “enhanced” migration of D.
magna at low temperatures may, in fact, be
due to bacterial degradation of the fish-taste
cues at high temperatures (C. Loose pers.
comm.) coupled with a difference in sensitivity
to fish taste between the two species (Dodson
1988).
Fish predation, however, is unlikely to cause
the midnight excursion. Hutchinson (1967) argued that midnight excursions are often the
Excursion
migration
Natural
daylight
MeanlSE
High temp. (19.7kO.8”C)
vertical migration
165+13
129+25
N
All
8
166k 10
112k20
215+8
167+15
21
result of the spreading out of the population
down the vertical axis-in effect an increase in
variance-possibly
due to the loss of the putative phototactic depth control system.
We show an increase of variance with increasing depth at night, but the same phenomenon also happens (to a somewhat lesser extent) during the day, and, in both cases, the
cold
warm
w
g
‘$ loo
‘2
7”
a ,so _
z
5 2oo 5
D
0
a
1
I
I
I
b
c
d
e
Vertical
migration
I
a
b
c
d
e
key points
Fig. 6. Similar data to those in Fig. 5 for both species
exposed to fish- (0) and to nonfish-tasting (0) water. Sampie sizes: Daphnia longispina cold + fish-1 6, ‘cold -fish 5,
warm +fish 6, warm -fish 2; Daphnia magna cold +fish
3, cold -fish 3, warm +fish 2, warm -fish 2.
78
Young and Watt
variance reduces again when the population
nears the bottom of the tank. This change in
variance suggests that there is a boundary effect
squashing one tail of the distribution.
Animals
in our study are plainly able to stay close to
the surface in total darkness at 0300, so depth
control is not necessarily lost at night.
There are some suggestive field reports
(Ruttner 1905; Kikuchi
1930; Worthington
193 1) for situations in which phytophagous
and predatory cladocerans coexist. In this situation the predators show a simple n-shaped
curve at night, while the prey species show
midnight excursions, bracketing the predators’
upward movement. These differences in distribution patterns may well be associated with
invertebrate predator avoidance. Ohman et al.
( 1983) have suggested that the reverse migration patterns in the marine copepod Pseudocalanus are related to avoidance of nocturnally
migrating invertebrate
predators and Neil1
(1990) has shown that it is possible to induce
reverse migration in a previously nonmigrating population
of the copepod, Diaptomus
kenai, by exposing it to Chaoborus.
Thus, in our experiments, fish-tasting water
enhances the predawn excursion, which is only
worthwhile if there are fish around, while nonfish-tasting water enhances the midnight excursion, possibly because the absence of the
fish top predators increases the risk from invertebrate predators (see Spitze 1992). These
animals came from sites with no (Japanese
Garden Pond) or few (Wraysbury Reservoir)
fish predators but some invertebrate predators
(Duncan and dos Santos 1989) and although
nothing is known of the vertical distribution
of these predators, their presence may explain
the distinctive behavior patterns we observed.
The occurrence of summer inhibition of vertical migration in our small tanks shows that
temperature gradients, oxygen concentration
gradients, and lake-mixing
phenomena (see
Gerritsen
1982; Calaban and Makarewicz
1982) are not necessary conditions for the phenomenon. Our conclusion that high ambient
temperature was the most likely cause of vertical migration inhibition
led us to reconsider
metabolic advantage theories of vertical migration. Lampert ( 1989) reviewed these and
effectively ruled out positive metabolic gains
from vertical migration, either directly to the
Daphnia or via enhanced algal productivity.
We would speculate, however, that the losses
from vertical migration might be less severe if
it is cold even at the surface, and hence more
likely to be exceeded by gains from predator
avoidance. Thus the metabolic effects of temperature could contribute to the seasonal pattern of the intensity of vertical migration.
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Submitted: 20 December 1991
Accepted: 6 August 1992
Revised: 1 September 1992