Oceanogr., 35(Y), 1990, 1456-1468
0 1990, by the American Society of Limnology and Oceanography, Inc.
Limnol.
Eflects of fish chemical cues on vertical migration
behavior of Chaoborus
Sara F. Tjossem
Ecology and Systematics, Corson Hall, Cornell University, Ithaca, New York 14853-2701
Abstract
I quantified the diel vertical distributions of Chaoborus (phantom midge) larvae in water that
had been conditioned by fish or not exposed to fish, using flow-through laboratory columns and
reciprocal transfers of larvae between a pond with fish and another without fish. The larvae that
received fish-conditioned water underwent a significantly greater intensity of migration than did
those that received fish-free water. Results support the hypothesis that Chaoborus larvae alter their
vertical migration behavior in response to the presence of planktivorous fish, in particular, to
associated chemical cues. Their behavioral flexibility in migrating permits response to a patchy
environment that is variable both seasonally and between habitats.
Among the many hypotheses for the
adaptive significance of vertical migration
(see Kerfoot 1985; Bayly 1986), recent theoretical (Gabriel and Thomas 198 8) and field
studies (e.g. Stich and Lampert 198 1; Gliwicz 1986) favor predator evasion to explain why zooplankton avoid surface water
during the day. Predatory invertebrates are
likely to respond to the migration of their
zooplankton resources and to the risk encountered from their own predators (Gerritsen 1980). Populations of phantom midge
larvae show great variation in migratory behavior (Luecke 19 8 6). Field observations
show that only migratory larvae coexist with
fish, and within migrating populations individual larvae in the benthos may not take
part in a daily pattern (LaRow 1976). Highly visible species either are eliminated from
lakes by fish predation or they do not occur
when fish are present (Stenson 1978; von
Ende 1979). In lakes without fish, Chaoborus larvae tend to be larger species that undergo little or no migration, such as Chaoborus americanus (Fedorenko and Swift
1972), although Swift (1976) found a migrating population in the absence of fish.
The underlying mechanisms for this variability are just beginning to be understood.
Luecke ( 1986) studied the migration of
Chaoborusflavicans in Lake Lenore, Washington-a
lake known to have been fishless
until 1979 when cutthroat trout were introduced. In 1976 the larvae were nonmigratory, but by 1982 the population had begun
migration. He suggested two possible mechanisms underlying this change: natural selection and behavioral changes. He noted
that a subpopulation isolated from fish in a
nearby pool continued to migrate and concluded that selective predation by trout on
nonmigrating
individuals
was responsible
for the change in larval migration pattern.
It is likely that fish can exclude populations
that are unable to migrate (von Ende 1979),
but another possibility is that chaoborids
possess phenotypic plasticity by which they
can adjust migration behavior in response
to the presence or absence of predatory fish.
I have addressed this question of induced
behavioral response in both field and laboratory experiments with C. flavicans and
Chaoborus albatus. If migration behavior
can be altered, the larvae must be able to
detect the presence of fish. My experiments
Acknowledgments
indicate that Chaoborus can detect the presWork was partially supported by the American Muence of fish by some waterborne cue, reseum of Natural History Roosevelt Fund, USDA Hatch
Project NY (C)-l83424 to N. Hairston, the Society of sulting in migrating populations of chaoborSigma Xi, and a Mellon grant-in-aid of research. Access ids increasing their intensity of migration
to the Arnot Pond courtesy of the Arnot Teaching and when exposed to water conditioned by fish.
Research Forest.
Aquatic invertebrates have been shown
N. G. Hairston, Jr., C. D. Harvell, B. Peckarsky, G.
to
respond to chemicals exuded by their
T. Epp, K. D. Hambright, P. Dawidowicz, and M. L.
predators (Have1 1986; Harvell 1990). AlDini helped to revise this manuscript.
1456
Chemically induced migration
though much of the work has been on the
induction
of morphological
defenses, behavioral flexibility is also found in aquatic
organisms (Peckarsky 1980; Sih 1986; Dodson 1988). Many of these results are, however, responses to the proximity of predators, whereas the migration
response of
Chaoborus seems to be qualitatively different because the larval behavior changes
without the direct presence of predatory fish.
Methods
Chaoborus adults live <6 d, with females
laying up to 500 eggs in rafts on the water;
most eggs hatch in 2-4 d. They pass quickly
through the first two instars and can develop
to the 4th instar in 6-8 weeks. The fraction
of a population that migrates may depend
on the depth of the water column, the season, and the instar (Parma 1971). Juday
(192 1) estimated that an average of 33% of
the benthic larvae became planktonic each
night, but this average does not indicate an
individual’s activity pattern. LaRow (1976)
noted that, at least under laboratory conditions, some individuals may undergo frequent emergence and re-entry to the sediments at night. Temperate
species of
phantom midges generally have one generation per year, and the larvae can overwinter as 3rd or 4th instars (Borkent 198 1).
Pupation occurs the following spring and
takes from 1 d to 2 weeks. Migration appears to be of highest intensity in the 3rd
and 4th instars and pupae (Parma 1971).
Two chaoborids, C. Jlavicans and C. albatus, were used in experiments to compare
the vertical distribution
of larvae exposed
to treatments of water from ponds that had
fish or were fish-free. Each species was censused in the field with a 32-liter SchindlerPatalas trap to quantify both density and
extent of migration. For all censuses and
experiments the intensity of migration was
measured by the difference between midnight and noon values of the number of
larvae per liter. Because C. flavicans occurred both in a pond with fish and in a fishfree pond, it could be used in both laboratory and reciprocal transfer experiments.
The larvae were collected from the Cornell
University
Experimental
Pond Facility, a
group of 0.1 -ha ponds near Ithaca. The two
1457
ponds were virtually identical in morphometry (0.1 ha, 2.3 m deep), stratification (1.5
m), and oxygen (range over depth, 11.0-0.5
mg liter-l); both had an anoxic hypolimnion
and both were classified as eutrophic (Wetzel 1983).
Ii early June both ponds had similar
numbers of zooplankton (+ fish pond = 29 1
liter-l, -fish pond = 273 liter-l), while in
early August the pond with fish had more
(+fish = 1,068 liter- l, -fish = 380 liter-l)
(K. D. Hambright pers. comm.). Zooplankton were collected by vertical tows of a 64pm mesh net. The pond with fish contained
a mixed assemblage of fathead minnows
(Pimephales promelas) and pumpkinseed
sunfish (Lepomis gibbosus). Both fish species readily ate Chaoborus larvae (pairs of
fathead minnows each ate an average of 7.8
larvae in 5 min, SD = 4.4, n = 6). In June
1989 field trials, each pond held an essentially pure population of C. flavicans, although some C. americanus were found in
the fish-free pond. I attempted to exclude
these large C. americanus from all experimental populations. During the August 1989
trials, the pond with fish held 77% C. jZavicans and the fish-free pond held 94% C.
jlavicans; the balance of larvae was Cha-
oborus punctipennis.
Chaoborus albatus was found only in a
pond with fish and so it could be used only
for laboratory experiments, not for a reciprocal transfer experiment in the field. The
pond with fish (-0.3 ha, 2.5 m deep) was
in Arnot Forest, a Cornell Research forest
near Newfield, New York, and the larvae
were collected with a 300-pm plankton net.
Abundances of the larvae were documented
at three depths (0.5, 1.25, and 2.5 m) in the
water column at 1800 (before dusk), 2400,
and 0600 hours (after dawn) on four dates
in summer 1988 with a 32-liter SchindlerPatalas trap. The daytime census samples
from Arnot Forest were taken at 0600 hours,
and the Cornell Experimental Ponds were
sampled at noon.
Field experiments - Reciprocal transfer
experiments with C. jlavicans from the two
Cornell ponds were carried out once in early
summer ( 15-l 7 June 1989) and again in late
summer (7-9 August 1989). Six woodenframed enclosures (2.5 x 0.75 x 0.75 m),
1458
Tjossem
each with its bottom and two sides covered
with seamless, 6-mil, clear plastic sheeting
and the remaining two sides covered with
‘750-pm nylon mesh, were anchored in the
center of each pond. As the enclosures sank,
they slowly filled with pond water and small
zooplankton that passed through the mesh
sides. A preliminary
trial had shown that
this mesh size allowed access to some small
plankton but prevented the escape of Chaoborus larvae. Thus the larvae put into the
+ fish pond enclosures were exposed to the
chemical presence of fish without being fed
upon by the fish. The tops of all enclosures
were covered with 0.5-cm mesh to prevent
fish from jumping into them. The enclosures protruded from the water -0.3 m,
giving a volume of 1,2 10 liters per enclosure
in the -fish pond and 1,320 liters per enclosure in the + fish pond. Because the enclosures were left in the ponds between trials, I brushed the sides to free them of
attached algae and to encourage water exchange before the second field trial, pumped
out the previous larvae, and then added a
new batch of phantom midge larvae taken
from the ponds.
Once the enclosures were in place, I collected Chaoborus at night from each pond
with a 300~pm mesh plankton net, including
animals from all depths to minimize any
bias in migratory tendency while sampling
the population. I poured the larvae into a
large container filled with water from the
fish-free pond, mixed them by gentle aeration, and withdrew subsamples for a final
density of 1.O larva liter-l for all enclosures.
This density was chosen to approximate the
average density of larvae found during the
daytime census of the fish-free pond. About
75% of introduced larvae were 3rd and 4th
instars early in summer, but by late summer
the population was 90% 3rd and 4th instars.
Chaoborus larvae returned to the same pond
from which they came are called source larvae, those transferred to the other pond are
called treatment larvae. The six enclosures
in each pond were assigned animals randomly so that three enclosures held source
animals and three held treatment animals.
Three stations outside the enclosures were
also sampled.
After 2 d of acclimation, larvae were sam-
pled at noon and midnight for 3 d at three
depths (0.3 m, 1.2 m from the surface, and
0.25 m off the bottom) with a hand-operated bilge pump modified with extensions
to reach each depth from the side of a boat.
A valve prevented water from entering the
sampler until the desired depth was reached,
and the sampler was cleared after each sample. All enclosure samples were taken at the
center of each enclosure, and the maximum
sampling depth was 0.25 m above the bottom to avoid excessive depletion of animals
from the cages, because most larvae were
near the bottom during the day. Each sample of 3.5 liters of water was concentrated
with an 85-hrn collecting filter, rinsed into
a sample bottle, and preserved with 75%
ETOH. To safeguard against selective removal of animals with a particular migration behavior, I removed < 10% of all
stocked larvae in field enclosures during
sampling.
General laboratory procedure - Experiments in the laboratory were carried out in
June and August to test the effect of fish
chemical cues on the vertical distribution
of larvae. I made three separate tests: C.
albatus, C. jflavicans from a pond with fish,
and C. Jlavicans from a fish-free pond. A
peristaltic pump circulated treatments of
+ fish or -fish aquarium water through six
Plexiglas columns (110 X 9 x 9 cm). Three
columns were used for each treatment in a
trial. Although these three columns were not
completely independent because they were
attached to the same aquarium, each trial
was repeated three times over a week, giving
a total of nine columns per treatment and
three fully independent replicates. The water in the -t-fish aquarium was conditioned
by placing eight (- 5 cm long) pumpkinseed
sunfish in it a day before trials began; the
fish remained in the aquarium during the
trials to provide fresh chemical cue to the
columns. The larvae in the columns were
isolated from direct fish contact by the recirculating water system that was turned on
1 d before each set of observations began.
During this time the fish were fed mixed
zooplankton that had been collected from
and rinsed in fish-free pond water.
The water from each aquarium
was
pumped through the columns at a water re-
Chemically induced migration
placement rate of - 15 h. Outlfows at the
tops maintained 1.O m of water in each column to give a total volume of 9.2 liters per
column. The placement of columns was
randomized during each trial to prevent any
systematic bias in treatment. Inflow tubes
were at the bottom of each column and outflow tubes at the top ensured turnover of
water. Each column was marked in lo-cm
increments, with the bottom 10 cm wrapped
in black plastic to provide a light gradient
for the larvae. As a refuge from light, the
bottom of each column was covered with a
l.O-cm layer of washed, black aquarium
pebbles. The columns were placed in a walkin incubator with the photoperiod set to the
natural daylength (14L : 1OD) of early summer; the temperature was kept at 19°C. Three
banks of daylight fluorescent lamps ensured
even illumination
across all columns as
measured by a LiCor light meter submerged
at depths in the water columns. The laboratory lights were much less intense than
sunlight, but provided a gradient of intensity sufficient to maintain diel vertical migration.
Larvae were collected at night from the
field and immediately brought back to the
laboratory and counted out in sets of 30
under dim illumination.
Sets of larvae (30
larvae per column) were randomly assigned
to treatments of either + fish or -fish water.
Chaoborus jlavicans larvae were collected
with a 300~pm plankton net at night from
a +fish and a -fish pond; the C. albatus
came only from a pond with fish during
census samples. A mix of 3rd and 4th instar
larvae was sorted from each population. The
larvae in the columns were fed a rinsed,
mixed assemblage of zooplankton (excluding Chaoborus larvae) from the fish-free
pond. I recorded the number of larvae observed in each 1O-cm increment of each column the following noon, then again at midnight and the next noon. Each time I
randomized the order of observing the columns. At the end of each trial I emptied and
rinsed the columns with deionized water and
began again with fresh water and newly
caught animals. Because Chaoborus larvae
show least light sensitivity at wavelengths
of 620 nm or longer (Swift and Forward
1980), I minimized
light disturbance by
1459
conducting night counts with a flashlight
whose dim beam was covered with a red
gelatin filter (Kodak No. 25 Wratten) to allow only wavelengths of 6 10 nm and longer
to pass. Under this dim light the larvae did
not show any noticeable change in behavior
while I counted them.
Because C. albatus came only from a pond
with fish, I had to remove fish chemical cues
from their home pond water to create a fishfree water treatment. I reasoned that if the
fish cue were proteinaceous, it would be denatured by high heat (Haschemeyer and
Haschemeyer 1973). I had also observed in
preliminary trials that the effect of fish-conditioned water was short-lived (1 d) if the
water was not continuously
renewed with
+ fish aquarium water. In 1988 I autoclaved
(45 min at 250°C) the Arnot +fish pond
water and then aerated it. In 1989 experiments on both C. jlavicans and C. albatus,
I used water from the fish-free Cornell pond
filtered through 75-pm mesh instead of autoclaved water.
The significance of differences in vertical
distributions between treatments was tested
with ANOVA and planned comparisons of
the means (Snedecor and Cochran 1980).
Results
Field experiments -The vertical distributions of both C. jlavicans and C. albatus
from field samples show that the larvae undergo a distinct pattern of diel vertical migration, since the greatest numbers of animals were in the water column at night (Fig.
1). Both populations of C. jlavicans underwent migration, but the larvae from the pond
with fish showed a much greater intensity
of migration than did those from the fishfree pond. The C. Jlavicans larvae in the
pond with fish were not up in the water
column during the day, whereas larvae from
the fish-free pond showed a lower intensity
of migration and some were found throughout the water column both day and night.
The intensity of migration was defined as
the difference between midnight and noon
values of the number of larvae per liter. The
C. albatus in the pond with fish showed a
marked pattern of vertical migration.
For maximal depth values, the sampling
pump collected animals 0.25 m above the
1460
Tjossem
ARNOT FOREST
c. aL?Jatus
With a stocking density of 1.O liter-l, 320
larvae were in the upper 1,069 liters of water, and the remaining 890 larvae were in
the bottom 141 liters of the enclosures (see
Figs. 2-3).
CORNELL PONDS
C. flavicarrs
Fig. 1. Field census data for Chaoborus albatus
(1988) and Chaoborusflavicans
(1989). Schindler-Patalas samples at three depths were pooled for a wholewater-column estimate. Chaoborus albatus densities
are k 1 SE (n = 2); C. flavicans samples are not replicated.
bottom of the enclosures, and missed those
larvae on the very bottom. The number of
larvae right on the bottom has been roughly
calculated by knowing that the initial stocking densities were 1.0 larva liter-’ and assuming that mortality was negligible over
the 3 d. If the samples at each depth are
representative of densities in the water column, one can take the average of the densities at the three depths and calculate the
density over all depths except for the very
bottom. The three depths are then considered to represent the water column. For example, in early summer the average number
of larvae over the surface, middle, and maximal depths was 0.3 liter-’ in 1,069 liters.
I then pooled the number of larvae in the
surface and middle of the water column from
the three sampling days and compared the
difference between mean numbers at midnight and noon to determine the intensity
of migration (Table 1). These depths were
chosen because the light levels at both were
determined to be high enough for fish to
locate larvae (Vinyard and O’Brien 1976).
Vinyard and O’Brien (1976) calculated light
levels typically limiting to planktivorous
fish. Although the light levels for fathead
minnows are unknown,
I assumed that
bluegills are representative
of pumpkinseeds, which are in the same genus. Light
levels at maximal sampling depth in the
pond with fish were equivalent to the larvae
being hidden from view on the bottom of
the enclosures, with only 1.O x 1O-7 % surface light in early summer and 0.2% in late
summer. The overall pattern in the field trials was that larvae from both the + fish and
the -fish ponds showed a significantly
greater intensity of migration under the fish
treatment than in the fish-free treatment.
In June both the source of the larvae and
the treatment of presence or absence of fish
cue had a significant effect on larval distribution in the water column (Table 2). I used
further analyses of variance, with noon and
midnight means as repeated measures, to
compare the mean number of larvae in the
water colu.mn between treatments.
Although there was no difference in the number of larvae from the fish-free pond up at
noon between treatments (Table l), significantly more of these larvae (3 X) were up
at night in the pond with fish compared to
the fish-free pond (P -C 0.01). The larvae
from the fish-free pond seemed to spend
more time at the surface at noon in the + fish
treatment than in the -fish treatment, but
the treatment means did not differ significantly. The larvae from the pond with fish
in June were 4 times more likely to be up
at noon in the -fish treatment compared
to those in the +fish treatment (P < 0.05)
(Table 1). At midnight, larvae from both
1461
Chemically induced migration
June:
No-Fish Pond
No Fish->
No Fish --> No Fish
Fish
# larvae / liter
0
4
1
2
3
I 1 I I I I I//.
//
6
7
8
I I I I I
1
2
3
4
0
-I ’ I ’ I ’ ’ ’ I
5
6
7
’ ’ ’ ’ ’ ’
Max
Inferred
Bottom
Fish Pond
0
Sur
5
OW
Mid
Fish -> No Fish
Fish -> Fish
1
I.1
2
*
3
4
I.1
5
rn I
rn
6
7
I.
1
1
2
3
4
0
4 ’ I . I m I ’ I
B
P
5
6
7
’ I ’ I ’ 1
E
Max
Inferred
Bottom
I
P
i
Fig. 2. A comparison of the early summer vertical distribution of the average number of larvae outside cages
with the number inside cages across treatments. For the treatments, each bar is the mean (+ 1 SE) of three
replicate cages. The bottom layer is an extrapolation from the three sample layers, given the stocking density
of 1.0 larva liter-‘. The bottom layer could not be extrapolated for the samples outside the enclosures because
absolute density was not known.
ponds were at least twice as abundant in the
water when exposed to the + fish treatment
than those in the -fish treatment (P <
0.001). As expected, no larvae were up in
the water column at noon outside the enclosures in the pond with fish (Table 1). The
densities and vertical distributions
within
the enclosures are similar to those outside
in the ponds, suggesting that there was no
confounding effect of enclosures on Chaoborus migration behavior (Fig. 2).
The late-summer enclosures were again
stocked with 1.O larva liter-l. In August, the
early summer pattern of greater intensity of
migration in + fish treatments was still present regardless of the source of the larvae
(Table 1). Unlike early summer, however,
the source of the larvae was no longer a
significant factor, and the larvae from the
fish-free pond showed no significant difference in vertical distribution
between treatments at night (Table 2). In addition, the
larvae from the pond with fish did not show
a significant increase in the water column
at noon in the -fish treatment. Further
ANOVA with noon and night as repeated
measures showed significantly more larvae
were up in the + fish treatment at night (P
< 0.01) compared to the -fish treatment.
In late summer the vertical distribution
pattern outside the cages was still similar to
that inside the cages. Larval abundance
above the sediments increased outside the
enclosures compared to that inside the enclosures (Fig. 3), despite the census data (Fig.
1) showing a slight decrease in the overall
Tjossem
1462
August:
No Fish ->
No-Fish Pond
# larvae/ liter
12
’ ’
Fish -> No Fish
Fish --> Fish
Fish Pond
0
No Fish --> Fish
No Fish
1 c-1
3
40
12
3
4
0.
1
3
2
!
Sur
Mid
9
e
a
Ii--Max
I
Inferred
Bottom
1
Fig. 3. As Fig. 2, but for late summer.
outside population size. The number per
liter outside the enclosures suggests that a
decreased proportion of the pond population may have stayed close to the pond bottom (Fig. 3).
I see an interesting pattern emerging from
the proportion
of larvae up in the water
(Table 3), as calculated from the average
number of larvae up in the water column
over all depths (Figs. 2-3). In early summer,
more chaoborids were up in the water column in the + fish treatment than in the -fish
treatment, regardless of their source pond.
The probability that larvae from the fish-
Table 1. Mean number of larvae per liter (-c 1 SE, y1= 9) up in the water column in the cages compared with
the number of larvae per liter outside the cages for the reciprocal transfer experiment with Chaoborusflavicuns.
Source (S) refers to the pond from which the larvae came; treatment (T) refers to the pond in which they were
placed.
Outside cages
Avg No. up inside cages
Early summer
s
T
Day
Night
-fish
+ fish
-fish
+fish
-fish
+ fish
-fish
+ fish
--fish
0.56(0.19)
0.40(0.09)
0.06(0.04)
0.59(0.12)
0.12(0.10)
0.28(0.11)
0.12(0.07)
0.12(0.07)
1.27(0.14)
0.34(0.08)
2.50(0.38)
0.99(0.20)
1.85(0.33)
1.39(0.2 1)
1.94(0.44)
1.1 l(O.18)
+ fish
Late summer
- tish
+ fish
Day
Night
0.34(0.09)
0.00(0.00)
0.43(0.18)
2.56(0.7 1)
1.48(0.73)
0.03(0.03)
3.21(0.51)
5.34(0.89)
Chemically induced migration
Table 2. Two-factor ANOVA using the difference
between midnight and noon values as a measure of
intensity of migration for Chaoborus ji’uvicans in the
reciprocal transfer experiment.
Source of
variation
Early summer
Source pond
Treatment
(+F, -F)
Source X
treatment
Error
Late summer
Source pond
Treatment
(+F, -F)
Source X
treatment
Error
df
MS
1
34.4
26.8
0.0008
1
73.4
57.3
0.000 1
1
8
10.1
1.3
7.9
0.023
0.004
0.95
8.9
0.02
0.19
0.67
1
1
1
8
F
0.009
20.5
0.44
2.3
P
free pond were up in the water column (surface, middle, and maximum depths combined), day and night, was about two times
higher in the + fish treatment than in the
-fish one (Table 3). They were more evenly
distributed by depth in the -fish treatment
than in the + fish treatment, but most larvae
were still on the bottom (Fig. 2). All populations were mostly on the bottom, even
though larvae from the fish-free pond migrated less than the larvae from the pond
with fish. In late summer, the proportion of
larvae in the water column increased to at
least 3/4of the larvae at all times (Table 3).
Nevertheless, most were at the maximal
sampling depth during the day and rose in
the column at night (Fig. 3).
Laboratory trials-The density of larvae
up in the water column did not differ sigTable 3. The average proportion of larvae up in the
water column in the enclosures.
Proportion up
Early summer
Source
Treatment
Day
Night
-fish
+fish
-fish
+fish
-fish
+fish
-fish
+fish
-fish
0.6
0.3
0.7
0.4
0.75
0.75
0.75
0.75
0.5
0.2
1.0
0.4
0.75
0.75
1.0
1.0
+fish
Late summer
-fish
+fish
1463
nificantly within treatments between trials
(ANOVA, P > 0.05), thus results of trials
were pooled for further analysis. The presence of fish chemical cues affected the migratory behavior of Chaoborus larvae in both
the lab and the field by altering the intensity
of migration. In contrast to the field, however, a somewhat greater fraction of larvae
were up in the water column in the -fish
treatment than in the + fish treatment. Although the fish cue did not measurably alter
the behavior of Chaoborus from the fishfree pond (Fig. 4A), the lack of cue did alter
the behavior of the larvae from the pond
with fish (Fig. 4B), so that more larvae were
up in the water column during the day, and
intensity of migration decreased. The laboratory experiments cannot rule out the
possibility that the lack of mechanical stimulus (fish movement) produced this response, but it can be ruled out by the field
trials because larval behavior changed in the
field where it was unlikely that any mechanical cue came through the large enclosures. Migration was quantified by comparing the number of larvae per liter in the
top 90 cm of the column with the number
in the bottom 10 cm covered in black plastic, but the treatment effects reported were
also evident at 30- or 50-cm divisions.
For C. Jlavicans, either the source or the
treatment of the larvae significantly affected
the number of animals up in the water columns in the laboratory. Regardless of water
treatment, the C. flavicans larvae from the
fish-free pond were 2-3 times more abundant at noon than larvae from the pond with
fish. The mean numbers of larvae from the
fish-free pond that were up (Fig. 4A) were
not different between treatments during the
day, but the night averages showed slightly
more up in the +fish treatment (P > 0.05).
The larvae appeared to be sinking at night
when compared to daytime densities, perhaps due to their having abundant food in
the day. The C. Jlavicans larvae from the
fish-free pond were a third more abundant
in the water column in the day than at night.
At all times, more larvae from the fish-free
pond than from the pond with fish were up
in the water column. In contrast, for larvae
from the pond with fish (Fig. 4B), the presence of fish cue produced a significant de-
1464
Tjossem
Laboratory Columns:
Laboratory Columns:
A. Fishless Pond C. flavicans
Amot Forest 1988
0 Noon
H Midnight
0
T
-
With
Fish
Without
Fish
‘With Fish
Without
n
Noon
Midnight
Fish
Amot Forest 1989
B. Fish Pond C. flavicans
7
q
Noon
H Midnight
0 Noon
q Midnight
With Fish
With Fish
Without
Fish
Fig. 4. Treatment effects on the mean number (+ 1
SE) of Chaoborus.fluvicans larvae liter--’ in the upper,
lighted layer (top 90 cm) ofreplicate (n = 9) laboratory
columns containing 30 larvae each.
crease (P < 0.005) in the number of larvae
up in the water column during the day, with
no difference between treatments at night.
The larvae from both the fish and fish-free
sources were similar in the number up at
night.
Chaoborus albatus in the laboratory experiments from both 1988 and 1989 (Fig.
5) responded in a manner similar to C. fluvicans in the pond with fish. Removing the
fish cue resulted in more larvae up in the
water during the day and thus a lesser intensi ty of migration. Significantly more larvae (2-3 x ) stayed up in the water at noon
when exposed to fish-free water than when
they were treated with water circulated
through the aquarium with fish (P < 0.05).
At night there was no significant difference
Without
Fish
Fig. 5. Treatment effects on the mean number (+ 1
SE) of Chaoborus albatus larvae up in the laboratory
water columns at noon and midnight. The 1988 means
are from five replicate columns; the 1989 histograms
are based on y1= 9.
between the water treatments. These results
were thus consistent from year to year and
between species.
Discussion
This study documents an inducible modification of vertical migration behavior in
response to changes in some quality of the
water associated with the presence or absence of fish. The larvae used in the reciprocal transfer experiments came from source
ponds that were similar except for the presence or absence of fish. Both populations of
larvae showed a greater intensity of migration when exposed to fish water. Within this
similar pattern of response, the two populations showed different distributions in the
water column between day and night. The
Chemically induced migration
larvae from the pond with fish reacted as
predicted when transferred to a fish-free
pond by decreasing the intensity of their
migration. Nevertheless, when deprived of
fish cue they only lessened the intensity of
their migration rather than stopping it altogether. Why do chaoborids bother to migrate at all in the absence of a specific cue?
One might think that, given the costs of
vertical migration, natural selection would
favor those larvae that migrate only when
a certain stimulus is present. The cost of
migration, however, is unknown, and if the
chemical cue is variable in its reliability, the
best compromise might be to maintain the
ability to migrate. This decline in migration
intensity suggests that in the absence of fish
the larvae gain some benefit, such as increased feeding, from staying up in the water
column during the day.
When the larvae from the fish-free pond
were transferred to the pond with fish, they
did not immediately disappear from the water column during the day in response to
fish cues. Instead, they showed a difference
in migration only at night, with more larvae
up in the water column in the + fish treatment compared to the -fish treatment. The
difference in migration response between the
two populations of C. flavicans suggests that
the long-term association of a population
with fish has a strong indirect or direct influence on migratory behavior. The fish
could indirectly affect migration behavior
by altering food availability
for the chaoborids, but this interpretation
seems unlikely for two reasons. First, when the enclosures were stocked with larvae they also
received some other zooplankton at the same
time, but this allocation was equal across
treatments. Second, during both field trials
the zooplankton densities outside the enclosures were very similar in the fish-free
pond, and increased in August in the pond
with fish. Because food levels for the larvae
were sufficient in both ponds during both
trials, a difference in food supply does not
appear likely to alter migration patterns over
the 3-d trials.
A direct response to predators is suggested by Dorazio et al. (1987), who found that
vertical migration
of Daphnia in Lake
Michigan increased between 19 8 3 and 19 8 5
1465
when predation intensity was thought to be
greatest. Such a quick response required either selection or a combination of selection
and an induced behavioral response. Because Chaoborus in the pond with fish had
been subject to selection pressure by fish
predation, an underlying genetic difference
in the two populations may have combined
with behavioral flexibility
to produce the
observed different responses of the two populations of larvae. Distinct genotypes could,
however, be maintained only by genotypicspecific habitat selection by the females when
they lay their eggs. Swift (1976) dismissed
such a process when he observed that Chaoborus trivittatus in Eunice Lake, British
Columbia, migrated without having any fish
in the lake at the time of the study. He discounted avoidance of fish predation as the
proximal cause for migration, although he
did not compare the intensity of migration
of the population in the fish-free lake to that
of a lake with fish. Instead, he suggested that
there was enough genetic exchange among
neighboring lakes with fish to maintain the
genetic basis for a migration pattern. The
relative importance of adaptation and behavioral response may differ between species or depend on local conditions. These
dynamics remain to be explained.
In the laboratory columns, an addition of
fish cue does not result in an increased intensity of migration for C. flavicans from
the fish-free pond, although an increase is
observed for larvae from the pond with fish.
The differences between laboratory and field
results may be due to differences in the concentration of fish cue, light regime, and depth
of the water column.
This study suggests that environmental
cues can change migratory behavior without
an attendent increase in mortality.
The
presence of fish chemical cues acts as a signal to the larvae to maintain a strong migratory response or suffer high predation. In
contrast, a loss of fish cue may signal a decline in the risk of predation and thus a
decreasing need to remain hidden in the
sediments. Induced behavioral responses
can have a short response time and act only
when a specific predator is present. Sih
(1987) reviewed major categories of antipredator traits and their evolution and sug-
1466
Tjossem
gested that the degree of environmental
variability
may determine when a species
relies more on behavioral than on morphological defenses. When the cost of a defense
is high, one would expect fixed morphological defenses mainly in an environment
of
consistent predation, but flexible behavioral
responses under variable predation pressure. The larvae of the phantom midge are
so small relative to many planktivorous fish
that morphological defenses such as spines
would be largely ineffective. An induced behavioral response may still be costly, with
lowered reproduction due to the energy requirement
of the behavior
or because
avoidance of predators causes the organisms to move to areas of lowered food concentrations. In addition, more time spent in
colder water may increase development
times (Swift 1976).
Generations of Chaoborus larvae may be
exposed to frequent fluctuations in selection
pressure because the flying adult females
may oviposit at ponds both with and without fish. They have not yet been found to
show any oviposition
site preference that
could lead to adaptations to local conditions. Regardless of this possibility,
any
ability of the larvae to escape predation by
altering their water-column
migration behavior would increase their chances of survival and eventual reproduction.
In lakes
with fish, vertically migrating larvae are safest from fish predation, while in a fish-free
lake, larvae with a lower intensity of migration may encounter more prey in the surface waters or possibly develop sooner. The
latter possibility is countered by the observation that most larvae still remain at the
greatest depth. The cost of possible exposure to fish predation may be greater than
the cost of lost growth and reproduction due
to migration. The safest behavior is, thus,
for larvae to show some degree of migration
behavior that can be accentuated when triggered by fish chemical cues.
My experiments
cannot
determine
whether the behavioral differences between
the two populations of C. flavicans are genetically based. They do, however, strongly
support the hypothesis that a population can
have a significant amount of behavioral
flexibility in migratory behavior in response
to an envi:ronmental cue.
The lack of effect of source pond on the
vertical distribution
of C. flavicans in late
summer enclosures (Table 2) may have several causes. Because the larvae from the pond
with fish had been exposed to predation all
summer, those larvae that did not have a
strong migratory response probably suffered
high mortality.
This selective predation
could have reduced the number of larvae
up in the water, leaving only strong migrators in late summer. Yet if selection were
the only explanation, one would expect that
the intensity of migration would increase
only in the pond with fish and not also in
the fish-free pond as observed (Table 1).
The similar migration
patterns between
ponds in late summer may result from increased water transparency or earlier emergence of those larvae that had stayed up in
warm water during both day and night in
the fish-free pond (P. Dawidowicz
pers.
comm.). A second possibility is that the prolonged exposure to + fish water during summer had a lasting effect, causing larvae from
the pond with fish to continue to migrate
even when fish were absent. Thus larvae
that were exposed to the fish factor at a
particular stage migrated throughout their
lives. A third possibility is that as the risk
of visual predation grew larger throughout
the summer with older instars, the cost of
migration outweighed the earlier benefits of
being up in the water. Early in summer the
migrators traded the risk of being eaten at
dawn and dusk for the benefit of finding
prey. By late summer, they had less need
for food because they had reached a stage
where they could decrease food intake. Although older instars eat more prey per individual predator (Fedorenko 197 3, they
are also the stages that are capable of overwintering with very little available prey.
Predation risks could have remained the
same while the nutritional needs of the larvae decreased, leading to a reduction in the
number of larvae up in the water column
during the risky daylight hours. Lastly, it
should be pointed out that these factors
could act in concert.
The pred.ation hypothesis for vertical migration often depends on the assumption
Chemically induced migration
that changes observed in vertical migration
result from changes in the abundance of specific genotypes brought about by selective
mortality (Stich and Lampert 198 1; Luecke
1986). Luecke (1986) found that CJZavicans
in Lake Lenore migrated after the introduction of trout and he invoked natural selection to account for the change in distribution. On the basis of my results with the
same species, however, environmental
induction would explain equally well the pattern he observed.
The experiments reported here quantified
a population response, not the movement
of individuals.
Understanding
individual
responses would help to clarify how variation in migration is expressed. The differences in vertical distribution
could be due
either to some individuals staying up in the
water while others stay deep or to a continual shifting among all larvae between the
water column and the bottom. The marked
tendency for a large proportion of larvae to
stay down at all times may indicate that they
feed near the bottom or that migration may
have a periodicity > 1 d. Further comparisons of populations of the same species that
vary in their rate of encounter with fish may
reveal interesting variations in the ability of
larvae to respond to the presence of fish.
Chaoborus has been found to escape visual predation because of its great transparency, its low activity when not migrating, and its migrations out of well-lit water.
It now appears that the ability to migrate
can be influenced by fish chemical cues (or
their absence) inducing a change in behavior. This trait seems to be adaptive for the
midges, because over generations individuals may encounter habitats with or without
predatory fish. Behavioral modifications that
decrease the chances of being eaten are likely to persist in the populations.
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Submitted: 12 February 1990
Accepted: 8 May 1990
Revised: 6 August 1990