Download Fitting into Food Webs: Behavioral and

J. Great Lakes Res. 30 (Supplement 1):300–314
Internat. Assoc. Great Lakes Res., 2004
Fitting into Food Webs: Behavioral and Functional Response
of Young Lake Trout (Salvelinus namaycush) to an Introduced Prey,
the Spiny Cladoceran (Bythotrephes cederstroemi)
D. Rae Barnhisel† and W. Charles Kerfoot*
Lake Superior Ecosystem Research Center and Department Of Biological Sciences
Michigan Technological University
Houghton, Michigan 49931
ABSTRACT. Functional response experiments with alternative prey demonstrate how an exotic zooplankter co-exists with salmonid fish in Lake Superior. Young lake trout (Salvelinus namaycush) response
to Daphnia, a typical prey genus, and to Bythotrephes, a spined invertebrate predator that invaded North
America in the mid-1980s, is examined in a variety of laboratory experiments that span various prey densities, frequencies, experience, and consumer size. Bythotrephes’ caudal spine protects the animal from
small fish predation. At intermediate densities, the spiny cladoceran also disrupts foraging behavior of
young-of-year fish. Lake trout response to Bythotrephes is dependent on the length of the spine and fish
size. The degree to which lake trout are able to discriminate between prey and resume their prior attack
rate on Daphnia depends on the absolute density of Daphnia and the frequency with which fish encounter
Bythotrephes. For both experienced and naïve fish, aversive behavior to Bythotrephes occurs after a certain threshold of encounters. Under conditions of high encounter rates, once aversive behavior is established in YOY fish, foraging efficiency on Daphnia improves because Bythotrephes is recognized and
ignored. The density-dependent behavioral and functional responses resemble classical predator reactions to unpalatable prey.
INDEX WORDS:
Bythotrephes, functional response, lake trout, Lake Superior, Keweenaw Bay.
1966) influenced a predator’s functional response.
The “disk” or functional response equation served
as the basis for optimal foraging models (Charnov
1976), and is equivalent to the steady-state version
of the Michaelis-Menten enzyme kinetics equation
(Real 1977, DeAngelis 1992). When incorporated
into Lotka-Volterra logistic models of population
dynamics, the functional response equation produces stable solution trajectories (Canale 1970,
Berryman 1992). Although the functional response
equation describes short-term behavior, it is the primary ingredient in single-patch models that has the
potential to stabilize prey populations (Murdoch
1969, Murdoch and Bence 1987).
Murdoch (1973) expanded the “disk” equation to
describe a multiple prey system for its application
in pest management. The number of species i consumed by a predator, rj, is given by
INTRODUCTION
Understanding the effects of alternative prey on a
predator’s foraging behavior gives insight into how
generalist predators rank prey items, and whether a
predator changes its behavior to accommodate a
new prey item. In the case where exotic prey
species invade a system such as the Great Lakes,
functional response theory helps us understand how
new species fit into lake food webs, and whether
they will interact strongly or weakly with pre-existing species.
Functional response theory is firmly grounded in
ecology. Solomon (1949) introduced the concept of
a consumer’s “functional” response to resources according to resource density. Holling (1959) described a predator’s response to prey density with
the “disk” equation, and explored how mimicry, unpalatability (Holling 1965), and hunger (Holling
ai ni T
ri =
*Corresponding
author. E-mail: [email protected]
†Current Address: Marine Studies Consortium, 900 Washington St.,
Wellesley, MA 02482-5725
m
a jn jhj
∑
j =1
1
300
(1)
Trout Functional Response to Bythotrephes
where ai is predator attack rate on species i, hi is
predator handling time on species i, ni is density of
species i, T is the total time available for foraging,
and m is the number of species available to the
predator. Chesson (1989) developed alternative
prey theory by suggesting that Eq. 1 could be used
as a null model to test for qualitative changes in a
predator’s behavior toward a target prey in the presence of an alternative prey.
In alternative prey theory, the addition of any
prey item into a predator’s diet is likely to decrease
the predation risk of other prey and alter the foraging dynamics of the predator (e.g., Murdoch 1969,
Chesson 1989). In its simplest form, an additional
prey spreads predation risk through decreases in encounter probabilities, i.e., two prey have 1/2 the
chance of being eaten first than when present alone.
In terms of predator foraging dynamics, a predator
can either choose its diet according to encounter
probabilities or select prey according to taste, conspicuousness, size, etc. However, regardless of selectivity, the time spent encountering, capturing and
handling an individual prey item will decrease the
probability of encountering other prey. Thus,
adding an alternative prey, n2, to a predator’s diet
could result in a reduction in consumption of the
initial or target prey, n1, due to density effects of the
alternative prey and not necessarily due to a change
in predator attack rate, ai. However, if density effects can be accounted for, the model can potentially highlight changes in attack rate due to the
presence of the alternative prey (Chesson 1989).
Barnhisel (1990) suggested that attack rate could
be estimated by rearranging Eq. 1:
ai =
ri
ni (T − hi ri )
(2)
and solving the equation for the case where the target prey is offered singly. The resulting attack rate
can then be used to set up the null case, i.e. that
predator attack rate on species 1 will not change in
the presence of species 2, a procedure useful in
simple laboratory experiments.
Attack rate is a complex parameter that encompasses search, encounter and capture time (Holling
1959, Murdoch 1973). Any changes in a predator’s
attack rate independent of prey density might signal
a fundamental change in a predator’s behavior because it is an indication that the predator’s perception of prey has been altered. The introduction of
unpalatable prey species is likely to initiate transitory changes in interactions (Holling 1965). How-
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ever, to what degree is the nature of the original interaction eventually altered by a third species, or
does behavior allow accommodation (Abrams
1983, Miller and Kerfoot 1987)? Miller and Kerfoot
(1987) emphasized the potential importance of “indirect” food web effects, but also opened the possibility of “higher order” interactions. Worthen and
Moore (1991) suggested that the effect of a third
species on the interaction between two species due
to density be termed an “indirect effect,” whereas
the term “higher order interaction” be limited to circumstances in which the effect is independent of
any changes in density.
Bythotrephes cederstroemi is a predaceous cladoceran native to European and Asian Palearctic
freshwaters. The species was first reported from the
Laurentian Great Lakes in the mid-1980s (Lake
Huron 1984), then expanded to all Laurentian Great
Lakes by 1987 (Bur et al. 1986, Lange and Cap
1986, Lehman 1987, Evans 1988). Bythotrephes
was first recorded from Lake Superior waters in
1987 and from the Keweenaw Peninsula in 1988
(Cullis and Johnson 1988, Garton and Berg 1990).
By 1990, the species was established in Keweenaw
Bay and has persisted for over a decade. During
May–June, overwintering diapause eggs hatch into
a morphologically diminutive first generation
(Table 1), that occurs at very low density during
TABLE 1. Lengths of Bythotrephes cederstroemi around the Keweenaw Penninsula.
Lengths are in millimeters (SD). First generation
individuals were extermely scarce, as these totals
for May/June came from 0.8-km horizontal tows
with a 100 µm net. Later generation individuals
were used in the laboratory experiments.
Total
Body
Instar
length
length
First generation Keweenaw Bay 5/20/95–6/1/95
1st (N = 37)
2.6(0.2)
1.1(0.1)
2nd (N = 13)
3.7(0.3)
1.2(0.1)
Spine
length
1.6(0.1)
2.6(0.2)
Later generations Keweenaw Bay 8/12/91–9/5/91
1.8(0.3)
5.5(0.5)
7.3(0.6)
1st (N = 47)
2nd (N = 31)
8.6(0.5)
2.2(0.2)
6.4(0.4)
3rd (N = 26)
10.6(0.7)
2.6(0.3)
8.0(0.6)
Later generations Keweenaw Waterway
(Portage Lake) 9/12/91
1st (N = 32)
7.7(0.4)
2.0(0.2)
2nd (N = 21)
9.0(0.6)
2.4(0.3)
3rd (N = 9)
10.7(0.5)
2.8(0.4)
5.7(0.2)
6.6(0.5)
8.1(0.3)
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Barnhisel and Kerfoot
May and June. Subsequent parthenogenetic generations produce larger individuals with longer spines
that become abundant by late summer. Epilimnetic
temperatures and Bythotrephes densities for various
Keweenaw Bay stations are given in Figure 1. Densities of spiny cladocerans seem to peak around
15°C. In the relatively shallow L’Anse Bay (KB1,
30 m) portion of Keweenaw Bay, Bythotrephes increased up to 100 individuals/m2 by late September,
whereas densities were higher (200–300 individuals/m2) earlier at mid-bay (KB5, 102 m) and deeper
(KB7, 111 m; KB8, 135 m) stations. Submersible
studies documented that the spiny cladoceran is
present throughout the warm epilimnion, but adults
often concentrate deep within the thermocline region where Daphnia also congregate. To date, the
highest abundance recorded for Bythotrephes in
Lake Superior is 122 individuals/m 3 (Garton and
Berg 1990), which seems exceptionally dense, emphasizing the spatial tendency to clump. Our 19901991 Keweenaw Bay samples averaged 18
individuals m–3, although sampling in subsequent
years (1993–1994, 1998–2000) had some AugustSeptember values as high as 48–69 individuals/m 3
(Barnhisel and Harvey 1995, Compton and Kerfoot
2004).
Fish sampling in Keweenaw Bay documented the
incidence of Bythotrephes in fish gut contents. A
total of eight bottom trawl tows were taken on 20
September 1991 from the U.S. Fish and Wildlife
(now National Biological Survey) Bete Grise Station. Age-0 to age-1 rainbow smelt (Osmerus mordax) were caught in the first six tows. Age-1
rainbow smelt, age-0 lake herring (Coregonus artedii) and age-0 to age-2 lake whitefish (Coregonus
clupeaformis) and lake trout (Salvelinus
namaycush) were caught in remaining tows over
greater depths. Stomach content results for rainbow
smelt, lake herring, and lake whitefish were published in Barnhisel and Harvey (1995). All youngof-the-year (YOY) contained Bythotrephes, but not
until fish had attained total lengths of 7–10 cm. Between 8–20 cm total length, the number of spiny
cladocerans in guts increased linearly, although
larger fish had a tendency to switch to bigger, alternative prey (Mysis, insects, fish). Daphnia mendotae concentrations ranged between 81–372
individuals/m3, and were most abundant in rainbow
smelt and lake herring stomachs (Barnhisel and
Harvey 1995), emphasizing that YOY fish in the
range 3–7 cm total length were capable of ingesting
items similar in size to Bythotrephes core body
length (2–3 mm). Here we concentrate on
FIG. 1. Abundance of Bythotrephes cederstroemi in Keweenaw Bay 1990. Epilimnion temperatures are plotted in top graph; number of individuals per m 2 is plotted in the bottom graph.
Stations are: KB1, 46°46940 , 88°289100 W, middle
of L’Anse Bay; KB5, 46°539100N, 88°239300W,
NW Pequaming; KB7, 46°59900N, 88°14950W, W
Point Abbaye; KB8, 47°49500N, 88°29100W, E Traverse Island.
Bythotrephes interactions with lake trout, using this
species as a generalized salmonid.
To gain insight into the complex zooplanktonfish interactions in nature, Barnhisel and Kerfoot
(1994) applied alternative prey models to laboratory
experiments in which YOY yellow perch (Perca
flavescens) were fed Daphnia pulicaria in the presence of Bythotrephes. All three species (perch, D.
pulicaria, Bythotrephes) occurred in Lake Michigan
in the mid-80s, although the dominant Daphnia was
D. mendotae. Bythotrephes’ unpalatability was due
to a long, barbed caudal spine that presented ingestion difficulties to fish < 10 cm in length (Barnhisel
Trout Functional Response to Bythotrephes
1991a, 1991b). The null hypothesis was that although the consumption rate by perch (5–6 cm total
length) would change in the presence of
Bythotrephes, the perch attack rate on Daphnia
would remain constant. The model’s prediction of
the expected number of Daphnia consumed differed
significantly from observed consumption. The
model predicted a 13% decrease, whereas a 51%
decrease was observed. Not only was the spine an
effective defense for Bythotrephes, but we concluded that fish behavior toward Daphnia had fundamentally changed in the presence of
Bythotrephes, reducing Daphnia consumption.
Although consumption of a target prey can vary
in the presence of an alternative prey independent
of changes in prey density (Miller and Kerfoot
1987), responses are usually dependent upon prey
density, prey frequency, and/or predator experience.
At low densities of both palatable and unpalatable
prey types, a predator’s attack rate on both types
would be low because encounter rates are low.
Here, the null model (Barnhisel and Kerfoot 1994)
would be unlikely to detect changes in a predator’s
foraging response because foraging time is not limiting. At higher densities, attack rates would increase as encounter rates and predator experience
increase. However, at some threshold prey densities, attack rates on both prey types would begin to
show differences because fish encounter the more
conspicuous, yet unpalatable, item more often and
spend increasing amounts of time trying to ingest it.
Confusion by YOY fish could benefit Bythotrephes,
which also prey on Daphnia. As density and encounter increases, contacts become frequent enough
so that the predator (fish) may learn to discriminate
between prey types, ignoring Bythotrephes, after
which predator foraging efficiency (fish and
Bythotrephes) might return to typical levels on
Daphnia.
The purpose of this investigation is to examine
the changes in fish foraging behavior toward a target palatable prey in the presence of an alternative
unpalatable prey according to prey density, prey
frequency and predator experience. Here we examine in the laboratory the factors associated with fish
consumption of Daphnia in the presence of
Bythotrephes. The series of short-term and longterm foraging and functional response experiments
involve lake trout, a laboratory surrogate for native
salmonid responses in Lake Superior. The alternative prey model is used to determine to what extent
the negative effect of Bythotrephes on fish foraging
303
(Daphnia removal) is sensitive to changes in prey
density.
MATERIALS AND METHODS
For laboratory experiments, more than 200 age-0
lake trout (Isle Royale lean strain) were obtained
from the Michigan Department of Natural Resources Hatchery, Marquette, MI, in June 1992.
Fish were held in a large flow-through chamber
maintained around 6.0°C by a 1 hp chilling unit for
approximately two months and fed commercial
food pellets (Biodry). In August 1992, twelve 40 L
flow-through aquaria were set up under fluorescent
lights in a 12 h light-dark cycle and divided in
halves. Light levels were approximately 20 µEinsteins/m2/s. Each half received one fish and approximately 20 liters of chilled water from a large
chamber. Water was replenished daily by a system
that pumped water from the holding chamber to a
large head tank above the aquaria. Chilled water
was then distributed to each half through a pipe system at 5 min intervals. The amount distributed was
controlled by valves to maintain similar temperatures between halves and among aquaria. Each half
aquarium had its own overflow system to control
water level. Water in each half was completely replaced at least once a day. All loose material (e.g.,
detritus, feces) was removed from aquaria prior to a
trial. Although a control and an experimental fish
were contained within the same aquarium, the division did not allow fish to view each other nor water
to be exchanged between the two halves. During
the total period of experimentation (7 August–20
October 1992; September 1993), the holding chamber temperature was ca. 7.6°C; the experimental
aquaria were slightly warmer as each aquarium half
ranged from 10.1 to 12.9°C, depending on its distance from the head tank, and thus the amount of
chilled water it received.
Four groups of 24 hatchery fish were used in the
system described above. A second system consisted
of two 120 L aquaria each chilled by an internal
unit, divided in half, and lit by an overhead fluorescent light on a 12h light-dark cycle. Light levels
were ca. 15 µEinsteins/m2/s. Twenty-four hatchery
fish were distributed to each half, four at a time
from 27 August to 19 September 1992 for 1 d feeding trials. The aquaria were cleaned and the water
changed before adding fish. Although the division
did not allow fish to view each other, water could
be exchanged between halves. Fish were acclimated
304
Barnhisel and Kerfoot
to aquaria at least 48 hours prior to trials. The temperature in this system ranged from 11.9 to 12.9°C.
Two prey types were offered to fish: adult Daphnia pulicaria, ca. 2 mm in size, taken from Lancaster Lake, Cheboygan County, MI, and adult
Bythotrephes cederstroemi, ca. 10 mm in size, taken
from Portage Lake, Houghton, MI. Both prey were
maintained at 5°C and brought slowly (12h) to at
least 10°C before being offered to fish. Daphnia
were maintained on hydrated broken cell Chlorella
capsules; Bythotrephes were collected fresh as
needed. Daphnia pulicaria was used instead of naturally occurring D. mendotae because 1) the species
was easier to maintain in laboratory culture, and 2)
D. pulicaria was used previously in Lake Michigan
experiments at the UM Biological Station, allowing
cross-comparisons with previous rainbow trout and
yellow perch experiments. YOY lake trout were
used as a surrogate for native Lake Superior
salmonid behavior, because this species was easier
to maintain in the laboratory than other resident
species (e.g., lake herring) and provided a salmonid
alternative to rainbow trout used in initial experiments (Barnhisel 1991a).
Feeding trials were conducted at various times of
the day whenever sufficient Bythotrephes could be
collected, but all fish were fed within one hour of
each other. Control and experimental fish were fed
consecutively, but randomized as to which was fed
first. Fish were distributed so that lengths and
weights differed very little between control and experimental groups. To initiate a trial, prey were
added simultaneously to the top of the aquarium. A
trial began when a fish captured its first prey item
and ended after 2 min unless otherwise specified.
Identification of prey captured and various components of fish behavior were recorded using a video
camera/recorder (Panasonic WV-3400 Color Video
Camera, NV-8950 Video Cassette Recorder with
variable speed playback) and microphone. The
camera documented fish foraging responses and,
upon playback, the video timer relayed the time at
which each prey was captured and a behavior was
observed. Statistical tests followed Sokal and Rohlf
(1995).
To ensure positive growth, three food pellets
were given to each fish each day. Each pellet
weighed ca. 0.013 g. Three pellets represented ca.
1.5% of the average fish wet weight. On days when
trials were conducted, fish were fed the three pellets
immediately following the trial to check for satiation, unless otherwise specified. Fish always ate the
pellets offered. Details of specific experiments are
treated below.
Despined Bythotrephes Experiments
Hatchery fish were distributed to the two large
(120 L) self-contained aquaria, each divided in half,
from 19 September to 27 October 1992. One-day
trials were conducted with a total of twenty-four
fish, four at a time. Fish ranged in size from 7.4 cm
to 9.8 cm total length. Each fish was acclimated to
its aquarium for at least 48 hours, and fed three
food pellets each day. On the trial day, fish in one
half of the aquaria received paired presentations of
Daphnia and despined Bythotrephes, whereas fish
on the other half received paired presentations of
Daphnia and intact Bythotrephes. To despine
Bythotrephes, forceps were used to cauterize and
then sever the spine at the base anterior to the first
pair of caudal barbs (Barnhisel 1991a, 1991b). Up
to 50 presentations were attempted with each fish
and paired prey type. Again, efforts were made to
ensure that fish fed despined or intact Bythotrephes
were similar in length and weight.
Long-term Foraging Responses
A complex long-term experiment assessed reaction of fish to various Bythotrephes densities and
ratios of Bythotrephes to Daphnia. The design incorporated autocorrelated series, balanced by controls (Fig. 2). Results were compared with
model-driven predictions. The long-term feeding
trials were intended to simulate a seasonal scenario
in which juvenile fish grew accustomed to feeding
on Daphnia, and then encountered Bythotrephes in
increasing densities and Bythotrephes/Daphnia ratios.
Twenty-four hatchery fish (7.4 ± 0.5 SD cm total
length; 2.9 ± 0.5 SD g) were distributed into twelve
divided small (40 L) aquaria on 7 August 1992.
Twelve fish in one half of each aquaria were designated as controls (Daphnia Only “Controls”) and
fed 50 Daphnia each day as a 50 mL aliquot (ca. 50
individuals per aliquot; N = 18) and three food pellets per day for 21 days.
In a separate series (Seasonal Sequence), beginning on 19 August, fish were fed various ratios of
Bythotrephes and Daphnia in a single trial once a
day, again for a total duration of 21 days (Fig. 2).
On days 1–3, the twelve experimental fish were fed
0 Bythotrephes and 50 Daphnia each day. On days
4–9, experimental fish were fed 5 Bythotrephes and
Trout Functional Response to Bythotrephes
305
FIG. 2. Diagrammatic representation of the 21-day experimental design in which 24 fish were fed
various ratios of Daphnia and Bythotrephes. Twelve fish were in the control group (C); twelve fish
were in the experimental group (B).
50 Daphnia each day. On day 10, experimental fish
were split into two groups of 6 fish each. Average
temperatures differed by no more than 0.3°C between aquarium halves and no more than 1.1°C
among aquaria. Individual fish were measured and
weighed to the nearest 0.1 g on day 1 and again on
day 21. One group (first group, low) continued to
be fed 5 Bythotrephes and 50 Daphnia a day for
three additional days, and then on days 13–21, was
fed 5 Bythotrephes and 25 Daphnia a day. The other
group (first group, high) was fed 10 Bythotrephes
and 50 Daphnia a day from day 10–18, and then
fed Daphnia and Bythotrephes in a 1:1 ratio from
day 19–21. In the 1:1 prey ratio trials, fish were
presented with paired Daphnia and Bythotrephes
(60 presentations a day).
To examine the effect of experience with
Bythotrephes on Bythotrephes consumption, both
Daphnia control (naïve) and Seasonal Sequence
(experienced) fish were fed 30 Bythotrephes on 3
October (N = 12 fish) and 10 Bythotrephes on 4 October (N = 6 fish). Behavioral probabilities of attack given encounter and ingestion given attack,
and average time spent handling Bythotrephes were
calculated and compared between the two groups
(Three-day Experiment). To check for satiation,
presentations were followed by three food pellets
on days 1 and 2. To control for hunger, three food
pellets preceded presentations on day 3. Fish consumed all pellets,
Functional Response Experiments:
Abundance and Ratio Considerations
In a long-term experiment, a second group of
hatchery fish (group 2, 8.3 ± 0.5 SD cm; 4.2 ± 0.5
SD g) was distributed to the twelve divided small
(40 L) aquaria on 9 September. Twelve control fish
were fed Daphnia once a day in increasing densities
of 25, 50, and 75, respectively, over 3 days. From
Barnhisel and Kerfoot
306
23 September to 2 October, controls were fed 20,
40, or 60 Daphnia in a trial, whereas experimental
fish were fed 20, 40, or 60 Daphnia paired with 5,
10, or 15 Bythotrephes. The first two trials (5 and
10 Bythotrephes added) were run consecutively.
Trial 3 (15 Bythotrephes) was conducted according
to Bythotrephes availability. Control and experimental fish were always fed on the same day. Temperatures did not differ between trials nor between
control and experimental halves.
Two other groups of hatchery fish (groups 3 and
4, naïve fish) were fed various ratios of Daphnia
(20, 40, 60) and Bythotrephes (5, 10, 15, 20) in a
short-term, 3 × 4 design. Group 3 (8.3 ± 0.5 SD cm;
4.2 ± 0.5 SD g) was distributed to the 12 divided
small (40 L) aquaria on 5 October and fed 8 October; Group 4 (8.7 ± 0.5 SE cm; 4.8 ± 0.5 SE g) was
distributed to the small aquaria on 9 October and
fed 14 October. For each group, 12 fish acted as
controls and were fed 20, 40, or 60 Daphnia and 0
Bythotrephes (N = 4). Twelve fish were fed one of
the twelve prey combinations. Since both groups
were given the same experimental treatment, they
were combined to replicate each combination (N =
2). Average temperatures differed by no more than
0.2°C between aquaria halves and no more than
2.2°C among aquaria for Group 3. For Group 4, average temperatures differed by no more than 0.6°C
between aquaria halves and no more than 2.1°C
among aquaria.
RESULTS
Despined Bythotrephes Experiment
Fish responded differently to presentations of
spined and unspined Bythotrephes. For fish fed intact Bythotrephes (N = 12), the spined prey was rejected on average at the 7th encounter (mean 7.4 ±
1.5SE), and avoided on average at the 20 th encounter (mean 19.9 ± 2.7SE). For fish fed despined
Bythotrephes, only one fish rejected a Bythotrephes
at the 48th encounter and two fish rejected a Daphnia at the 36th and 47th encounter. The probability
that fish would attack a despined (0.50 ± 0.05SE) or
an intact Bythotrephes (0.43 ± 0.06SE) before a
Daphnia was arcsine transformed (Sokal and Rohlf
1995) and compared to each other and to the arcsine transformed value of 0.5. According to a onetail t-test, probabilities for Bythotrephes and
Daphnia of comparable core body length did not
differ from each other nor from 0.5 (e.g., intact vs.
despined, d.f. = 10, t = 1.3, p = .19 N.S.). Behaviors
seen in fish fed spined Bythotrephes but not in fish
FIG. 3. Short-term experiments (1 day) in which
24 fish were fed either an intact or despined
Bythotrephes paired with a Daphnia. The figure
shows the number of encounters to A) rejection
and B) aversion for fish fed intact Bythotrephes
according to fish length. The number of encounters to rejection was significantly correlated with
fish length according to a Spearman Rank Correlation analysis (see text).
fed despined Bythotrephes included nudging, hesitation, multiple rejections of live and dead
Bythotrephes, and opercular flaring. A Spearman
rank correlation analysis indicated that the number
of encounters to rejection (item spit out) for spined
Bythotrephes was significantly correlated with fish
length (rs = 0.59; d.f. = 11, p < 0.04*); although the
number of encounters to aversion (ignoring item)
was not (Fig. 3; rS = 0.35; d.f. = 11; p > 0.10 N.S.).
This simple experiment demonstrated that reaction
Trout Functional Response to Bythotrephes
of fish to spined Bythotrephes versus Daphnia is related to the presence of the spine and its attributes,
not to the bulk, visibility, palatability, or other characteristics of the alternative prey’s (Bythotrephes)
body, per se.
Long-term Foraging Responses
In the complex, long-term feeding experiment
(Fig. 2), trials were intended to simulate a seasonal
scenario in which juvenile fish grew accustomed to
feeding on Daphnia, and then encountered increased densities of Bythotrephes and Bythotrephes/
Daphnia ratios. Over the 21 days of the experiment,
100% of Daphnia attacked were ingested, whereas
96% of Bythotrephes attacked were ingested.
In Figure 4a, the average number of Daphnia (±
SE) attacked by fish in the “Daphnia Only Control”
307
series is graphed versus the “Seasonal Sequence
Experimental” series. There was no significant difference (p > .05) between the 5 Bythotrephes and
10 Bythotrephes treatment groups, so these were
combined for a simple paired comparison. Only
those fish fed 50 Daphnia are shown (Daphnia
Only “Control” series versus “Seasonal Sequence”
series fish fed to day 18) and compared using a
paired Student’s t-test (* p < .05; ** p < .01) on
daily values. The conservative statistical procedure
(paired Student’s t-test) was applied, rather than a
more complex design (e.g., featuring time × treatment interactions), because of variable sample
sizes, autocorrelation between treatments, and the
complex sequential setup. Also, because of the numerous paired comparisons (> 18), only the twolevel outcome (* p < .05; ** p < .01) of the
statistical test is shown, rather than the t-values.
FIG. 4. Long-term feeding trials, comparing attacks on controls (Daphnia only) with observed and
expected (model) results in the presence of alternative prey (Bythotrephes): (a) Average number of Daphnia and Bythotrephes (± SE) attacked by fish during the 21-day long-term experiment. All fish were fed
50 Daphnia and either 5 or 10 Bythotrephes per day. Open squares indicate the average number of Daphnia attacked in controls (Daphnia only, N = 12). Closed triangles indicate the number of Daphnia
attacked in experimental trials (Bythotrephes present, N = 6–12). Average number of Daphnia attacked by
fish in controls was compared to the number attacked by fish fed Daphnia in the presence of
Bythotrephes using paired Student’s t-tests (**p < 0.01; *p <0.05). Fish fed 50 Daphnia and 5
Bythotrephes provide data for days 4–9 (N = 12). On days 10–12, 6 fish were fed 5 Bythotrephes and 6
fish were fed 10 Bythotrephes. A Student’s t-test indicated that Daphnia attack did not differ between the
two Bythotrephes treatments, so they were combined to provide data for days 10-12 (N = 12). On days
13–18, fish fed 50 Daphnia and 10 Bythotrephes provided average Daphnia consumption data (N = 6).
Fish fed 25 Daphnia and 5 Bythotrephes are excluded from the figure. Average number of Bythotrephes
attacked (± SE) is shown for those fish fed 5 or 10 Bythotrephes combined. (b) Expected Daphnia consumption estimated using the alternative prey model (Eqns. 1&2) compared to observed Daphnia consumption for fish fed 50 Daphnia and either 0, 5, or 10 Bythotrephes. Comparisons were made using a
one sample Student’s t-test (3 symbols: p < 0.001; two symbols: p < 0.01; one symbol: p < 0.05), with series
distinguished by different symbols.
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Barnhisel and Kerfoot
Consumption of Daphnia did not differ between
“Controls” and “Seasonal Sequence” groups on
days 1–3 when both groups were fed only 50 Daphnia, merely illustrating that fish in both series had
initially similar responses. However, on days 4–9,
when 50 Daphnia were paired with Bythotrephes in
the “Seasonal Sequence” series, Daphnia consumption declined significantly compared with the “Control” series; Fig. 4a). For reference, the number of
Bythotrephes attacked is plotted at the bottom of the
figure, and increased slightly throughout the experiment with increased Bythotrephes presentations.
The low level of Daphnia consumption on day 16
can be attributed to the small size of Daphnia offered. Fresh collections from Lancaster Lake on
that date contained a high proportion of young
Daphnia < 2 mm in size. In summery, observed results clearly show that attacks on Daphnia were depressed in the presence of Bythotrephes, an
alternative prey.
Behavioral probabilities of attack given encounter (pAlE) of Bythotrephes were calculated to
examine how relative and absolute densities of prey
affect foraging behavior. Probabilities were arcsinetransformed to meet the assumption of normality.
The probability of attack given encounter for
Bythotrephes between fish fed 5 Bythotrephes and
fish fed 10 Bythotrephes differed significantly on
day 10 when the two groups split off from each
other, and again on day 18, according to a paired
Student’s t-test (**p < 0.01). Six fish fed equal ratios of Bythotrephes and Daphnia in the final 3 days
of the experiment (Three-day Experiment) showed
no difficulty ingesting Daphnia, but often extreme
difficulty ingesting Bythotrephes (Fig. 5a). Behaviors observed in all fish at least one time included
body convulsions when trying to ingest a Bythotrephes, rejecting both dead and alive Bythotrephes
or only the spine, hoarding Bythotrephes in the
mouth rather than ingesting them (one fish rejected
up to 6 Bythotrephes at one time), capturing a
Bythotrephes but having the spine protrude from the
mouth, attacking or nudging a Bythotrephes but not
capturing it, approaching a Bythotrephes but not attacking it, and hesitating to attack Daphnia. Rejection of Bythotrephes first occurred at the 7–10 th
encounter over the three days. Aversion (approaching a Bythotrephes without capture) was apparent at
ca. the 40th encounter on days 1 and 2, and at the
20th encounter on day 3 (Fig. 5a).
The attack rate model (Daphnia + Bythotrephes
alternative prey) was applied to the 21-day foraging
response experiment (Fig. 4b). Fish attack rate on
FIG. 5. Fish reaction (Three-day Experiment) to
Bythotrephes when presented in a 1:1 ratio with
Daphnia in the final 3 days of the long-term foraging experiment. Up to 60 paired presentations
were made: a) The average number of encounters
(± SE) at which fish (N = 6) begin to reject (open
squares) and show aversion (closed squares) to
Bythotrephes. b) The average behavioral probability of attack given encounter (pAlE ± SE) for
fish preying on 5, 10, and 15 Bythotrephes plotted
against Daphnia density. The probability of fish
attacking Bythotrephes significantly decreased
with increasing Daphnia density at densities of 10
and 15 Bythotrephes (*p < 0.05, ANOVA).
Daphnia, aD, was estimated for each day using Eq.
2, and the average removal rate, rD , estimated from
control fish for that day. Handling time, hD, was estimated using the average handling time of Daphnia
by control and experimental fish during days 1-3
when both groups received Daphnia offered alone.
Handling time was defined as the average capture
Trout Functional Response to Bythotrephes
interval between Daphnia and the next prey item.
Daphnia density, nD, was the number of Daphnia
offered to fish. Total time, T, was 160 s. Expected
Daphnia consumption, rD, was calculated for each
day using Eq. 1 and the same variables used in calculating Eq. 2, and compared to observed Daphnia
consumption by experimental fish. As a check of
the model and its assumptions, r D expected was
compared to rD observed of experimental fish on
days 1-3 using a Student’s one sample t-test. There
were no significant differences. This indicated that
the model had the potential to accurately predict
lake trout consumption of Daphnia, attack rate of
the controls and average handling time of both
groups.
Variables for Bythotrephes in Eq. 1 were estimated using data from the day in question averaged
over all experimental fish. Attack rate, aB, was calculated for each day using Eq. 2. Handling time, hB,
was estimated using the average capture interval
between Bythotrephes capture and the next prey
item. Density, nB, and T were calculated for various
Daphnia numbers (Fig. 2). Variables a B, h B, n B,
were then included in Eq. 1 to calculate expected
consumption of Daphnia when both prey items
were offered.
Average handling time (capture interval) for
Daphnia, hD, was 3.9 ± 0.3 seconds. All other variables except for T varied with the day. Expected
Daphnia consumption, rD, was calculated for days
4-9 and compared to observed Daphnia consumption of experimental fish fed 50 Daphnia and 5
Bythotrephes (Fig. 4b). Expected rD was calculated
for days 10–12 when 6 fish were fed 50 Daphnia
and 5 Bythotrephes and 6 fish were fed 50 Daphnia
and 10 Bythotrephes. There were significant differences between expected and observed Daphnia
consumption for most days (Fig. 4b, ***p < 0.001;
**p < 0.01; *p < 0.05). Expected rD calculated for 6
fish fed 50 Daphnia and 10 Bythotrephes on days
13–18 was significantly different from “observed”
on all days except day 13. There were no significant
differences in fish length or weight between control
and experimental groups at the end of the experiment. For both groups combined, average ending
length was 8.7(± 0.1 SE) cm, and average ending
weight was 4.8(± 0.1 SE) g.
That is, in both control versus experimental (Fig.
4a) and model (expected) versus observed comparisons (Fig. 4b), fish foraging on Daphnia was reduced relative to expectations. The alternative prey
model (Daphnia + Bythotrephes) predicted attack
levels at intermediate Bythotrephes densities and
309
frequencies, yet the observed attack levels were
below the predictions. In other words, the observed
risk to Daphnia was reduced below that expected
from numeric risk-spreading (i.e. more prey items).
In contrast, increasing density and frequency of
Bythotrephes increased Bythotrephes rejection and
promoted aversion conditioning on Bythotrephes
and increased risk to Daphnia.
Functional Response Experiments:
Abundance, Ratio, and
Experience Considerations
Fish from the 21-day experiment (experienced
fish) were used in further functional response experiments. Figure 6 illustrates the functional response of fish to various densities of Daphnia
offered alone (25, 50, 75, N = 12; and 20, 40, 60;
N = 4), and with increasing densities of
Bythotrephes (5, 10, 15; N = 4). According to Student’s t-tests, Daphnia consumption was significantly different between control fish and fish fed 5
or 10 Bythotrephes in five of six paired comparisons (e.g., d.f. = 10; 5 Bytho, 60 Daphnia, t = 6.3,
p < .001**; 10 Bytho, 20 Daphnia, t = 2.4, p = .04*;
40 Daphnia, t = 2.8, p = .02*; 20 Daphnia, t = 2.7,
p = .02*). However, there were no significant differences between control fish and fish fed 15
Bythotrephes (d.f. = 10; 15 Bytho, 20 Daphnia, t =
1.0, p = 0.3 N.S.; 40 Daphnia, t = 0.5, p>0.5 N.S.;
60 Daphnia, t = 0.7, p = 0.5 N.S.). That is, relative
Daphnia consumption was reduced at intermediate
Bythotrephes densities, but the results suggest that
experienced fish returned to typical foraging behavior at high densities of Bythotrephes when aversion
conditioning occurred in fish.
Behavioral probabilities of attack given encounter (pAlE, Fig. 5b) and ingestion given attack
(pIlA) for fish preying on Bythotrephes at various
Daphnia densities were inversely correlated with
Bythotrephes densities (Barnhisel 1994). That is,
experience with Bythotrephes decreased the probability of attack (e.g., at 40 Daphnia, 5 vs. 10, t =
3.0; 10 vs. 15, t = 2.4; 5 vs 15, t = 7.0; all p < .05*).
The pAlE for Bythotrephes when 5 were offered
was negatively related to Daphnia density, and this
trend also was evident when 10 and 15
Bythotrephes were offered.
The average time fish spent on Bythotrephes was
measured as the interval between the capture of a
Bythotrephes and the next prey item. Initially, for
12 fish fed intact Bythotrephes during a total of 96
observations, fish spent 8.5(± 1.0SE) seconds. By
310
Barnhisel and Kerfoot
the end of the experiment, that interval had increased. Fish spent 10.0(± 2.0SE) seconds at densities of 10 Bythotrephes and 13.8 ± 1.4 seconds at
densities of 30 Bythotrephes (d.f. = 10, t = 2.4, p =
.04*). The interval at high Bythotrephes density was
greater, although most Bythotrephes were bypassed
between captures (aversion conditioning). Behav-
iors observed for all Bythotrephes presentations included whole body convulsing after capturing an
individual, nudging a Bythotrephes with the mouth
but not capturing it, having the spine protrude from
the mouth after capture, and looking at a
Bythotrephes but not attacking or capturing it. In
summary, functional response experiments with experienced fish showed a clear density dependent response. At low encounter rates (5,10 Bythotrephes),
fish were confused and exhibited reduced removal
rates of Daphnia. At high encounter levels (15
Bythotrephes), the fish ignored Bythotrephes and
the Daphnia removal rates returned to normal.
Groups 3 and 4 (naïve) fish responded differently
to Daphnia offered alone versus in the presence of
Bythotrephes. Groups 3 and 4 response to Daphnia
offered alone were combined and compared to their
combined response to Daphnia offered with
Bythotrephes using an unpaired Student’s t-test.
Daphnia consumption differed significantly between control and experimental groups at Daphnia
densities of 20 (Fig. 7; d.f. = 10; t = 3.7, p, .004**),
but was not significant at higher densities (d.f. = 10,
40: t = 0.2, p >.50 N.S.; 60: t = 0.3, p > .5 N.S.).
Daphnia removal was modified at various
Bythotrephes densities (d.f = 10; 5 Bytho: t = 2.7; p
< 0.03*; 10 Bytho: t = 2.6, p < 0.03*; 15 Bytho:
t = 3.3, p < 0.01**; 20 Bytho: t = 4.5, p < 0.003**).
Group 3 and 4’s response as naïve fish also differed
significantly from Group 2’s response as experienced fish (d.f. = 10; 20 Daphnia, t = 3.1, p <
0.01**; for 40 Daphnia, t = 7.1, p < 0.001**; for 60
Daphnia, t = 4.7, p < 0.001**). Naïve fish generally
were more confused in the presence of
FIG. 6. Functional response experiment (experienced fish) with alternative prey, in which 24 fish
were fed various densities of Daphnia (20, 40, 60)
with increasing densities of Bythotrephes (panel a
= 5, B = 10, C = 15). Average number of prey consumed per predator (± SE) is plotted according to
Daphnia density. Open symbols represent consumption of Daphnia in controls (Daphnia only);
closed symbols represent consumption of Daphnia
(squares) and Bythotrephes (triangles) in experimental (alternative prey) experiments. Control
consumption is repeated for all three panels.
Daphnia consumption densities of 25, 50, and 75
(controls) were determined prior to the experimental trials in 1-day series using control fish.
Trout Functional Response to Bythotrephes
311
Bythotrephes and had lower removal rates of Daphnia (additional experiments, Barnhisel 1994).
The Group 3 & 4 (naïve fish) functional response
experiments underscore the importance of experience. Seasonal interactions are progressive and prolonged, as both Daphnia and Bythotrephes
populations simultaneously increase during summer. Aversion conditioning is very sensitive to density and the fine details are not captured if only
naïve fish are used in short-term experiments
(Barnhisel and Kerfoot 1994).
FIG. 7. Groups 3 and 4 fish (naïve fish) average
per fish consumption of Daphnia (± SE; N = 4)
over various Daphnia densities: a) Daphnia were
offered alone to fish which had no prior experience; b) Group 3 (squares) and Group 4 (triangles) average per fish consumption (± SE; N = 4)
of Daphnia (open symbols) and Bythotrephes
(closed symbols) over various Daphnia densities.
Consumption was averaged over 4 densities of
Bythotrephes (5, 10, 15, 20); standard error bars
indicate the variation of Daphnia consumption by
fish at the different Bythotrephes densities. Consumption of Daphnia without Bythotrephes
(panel a) differed significantly (p < .05, t-test)
from consumption of Daphnia with Bythotrephes
(panel b) only at Daphnia densities of 20.
DISCUSSION
Bythotrephes is a carnivorous crustacean that potentially competes with juvenile fish for zooplankton. The ecological function of Bythotrephes’
caudal spine appears to be protection, as emphasized by the spineless Bythotrephes experiments.
Although despined Bythotrephes do not occur in nature (although there are smaller, spineless, and related species, such as Polyphemus), the experiments
in which both intact and despined Bythotrephes
were offered to fish highlighted the importance of
the spine in defense. The adverse reaction of fish
emphasized the difficulty of swallowing spines. For
this reason, application of traditional terrestrial
model-mimic relationships to the fish-Bythotrephes
interaction seems appropriate, especially with small
YOY fish (Barnhisel and Kerfoot 1994). The interaction between small YOY fish and Bythotrephes is
qualitatively similar to a bluejay reacting to a distasteful monarch butterfly (Holling 1965, Huheey
1984). As the density of Bythotrephes increased in
paired-prey (Bythotrephes and Daphnia) feeding
trials, fish encountered the unpalatable prey more
often and spent increasing amounts of time trying
to ingest it. At higher prey densities and frequencies, contacts become frequent enough so that the
predator (fish) learned to discriminate between prey
types. Fish would ignore Bythotrephes and subsequently predator foraging efficiency returned to
typical levels on Daphnia.
Does the presence of Bythotrephes alter fish reaction to Daphnia and hence constitute a higher order
interaction? Our results indicate that the spine has
the potential to disrupt fish foraging behavior when
encounters with Bythotrephes are at intermediate
densities. The experiments were designed to simulate certain ecological scenarios among young fish,
Bythotrephes, and a shared resource such as Daphnia. The ratio of Daphnia: Bythotrephes offered to
fish was similar to invertebrate predator:prey ratios
312
Barnhisel and Kerfoot
observed during August-October, when
Bythotrephes was most abundant (Barnhisel and
Harvey 1995). The second group of experiments,
the long-term feeding trials, were intended to simulate a seasonal scenario in which juvenile fish grew
accustomed to feeding on Daphnia, and then encountered Bythotrephes in increasing densities. In
these experiments, interference at intermediate
Bythotrephes densities was demonstrated. However,
the functional response experiments, run at different densities of Bythotrephes, suggest that the interference with fish feeding on Daphnia is a transitory
effect related to density. Once fish encounter
Bythotrephes at high densities, they develop “aversion conditioning” and subsequently ignore the invertebrate predator, returning to more typical
consumption rates of Daphnia. This transitory response differs from what is expected from higherorder interactions, where the nature of the
interaction is changed (Case and Bender 1981,
Abrams 1983, Worthan and Moore 1991, Werner
1992).
Results from the long-term experiment indicate
that fewer Daphnia were consumed in the presence
of Bythotrephes, but beg the question of whether
the decrease is what one would expect given the
time fish spent on Bythotrephes. The alternative
prey null model predicted that Bythotrephes should
have only reduced fish consumption of Daphnia by
2%. However, observations indicate that fish decreased Daphnia consumption by 25%. This decrease is similar to, but not as great as, that
observed in yellow perch experiments (54-112% by
the 3-4th days; Barnhisel and Kerfoot 1994). Both
studies indicate that foraging time and absolute
Daphnia density play important roles in the degree
to which consumption is decreased in the presence
of Bythotrephes. Moreover, both absolute density
and relative frequency of Bythotrephes influence
fish responses to that taxon. Rather than increase,
fish tended to retain or lower consumption rates of
Bythotrephes under increased density of
Bythotrephes or prolonged exposure. Prolonged
summer exposure and runs of Bythotrephes encounters in nature (clumped distribution) probably reinforce aversion conditioning, although laboratory
video sequences were not scored to capture this
kind of information.
One would predict that vertebrate predators require certain thresholds of prey density and frequency before they are able to discriminate between
prey items. The short-term foraging response experiments conducted over a range of fish size indicate
that the number of encounters to rejection was significantly correlated with fish length, but that the
number of encounters to aversion was not (Fig. 2).
This suggests that rejection of prey is more likely a
physical constraint related to gape size whereas
aversion is a more complex behavioral decision related to prior experience. Once aversion kicks in,
there are dual consequences. Both fish and
Bythotrephes return to normal feeding behavior on
Daphnia and smaller cladocerans. Long-term observations suggest that the smaller Daphnia species
(D. retrocurva) in Keweenaw Bay is being replaced
by D. mendotae (Kerfoot et al. 2004), a larger-bodied species, as observed in southern Lake Michigan
when Bythotrephes became abundant (Lehman and
Cáceres 1993).
Other studies have attempted to use the multispecies functional response equation to predict
predator consumption using variables from only
single prey experiments (e.g., Colton 1987, Abrams
1990, Krylov 1992). These studies estimated alternative prey attack rate from single prey experiments
and assumed that attack rates on both prey would
remain constant in multiple prey experiments. Our
results suggest that attack rate should be estimated
from experiments in which the alternative prey is
offered in combination with the target prey, as expected and observed rates were significantly different. For time- and density-dependent responses,
Holling (1959) varied attack rates by adding an additional time-consuming component, c, to handling
time (Barnhisel and Kerfoot 1994). For Bythotrephes, hB could represent some minimum time required to mechanically process the animal, whereas
c could represent the time involved in other behaviors such as rejection and recapture, hesitation or
other aspects of indecision.
The degree to which Daphnia consumption is decreased in the presence of Bythotrephes is related to
density and frequency factors, specifically Daphnia
density and Bythotrephes frequency (ratio
Bythorephes:Daphnia). It appears that the density
of Daphnia affects Daphnia consumption according
to classical functional response theory, and it may
affect Bythotrephes consumption in that a certain
absolute density of Daphnia must be reached before
fish can distinguish between the two prey items.
The core bodies of both Daphnia and Bythotrephes
appear inherently equally conspicuous, although the
presence of the spine and the vigorous swimming
behavior of Bythotrephes make it more conspicuous
in nature (Jarnagin et al. 2004). Contrary to the prediction of Barnhisel and Kerfoot (1994) that Daph-
Trout Functional Response to Bythotrephes
nia removal would remain depressed at all prey
densities, these results indicate that fish can resume
their previous attack rate on Daphnia given sufficient encounters (experience) with both prey. Unfortunately, Bythotrephes foraging on Daphnia was
altered by laboratory confinement, so the complete
three-way interaction could not be evaluated.
The experiments here involved modest-sized
YOY (7–10 cm SL). The ability of larger size
classes (or older age classes) of several fish species
(late YOY or age-1) to consume numerous
Bythotrephes presents intriguing ramifications that
go beyond these experiments. Certainly, older
classes are much less abundant than YOY fish and
this aspect can be incorporated into risk modeling.
However, recently we discovered that another life
history stage of Bythotrephes is as well protected as
the free-swimming (pelagic) parthenogeneic generation, i.e., overwintering eggs were found to pass
through fish guts intact (Jarnagin 1998; Kerfoot et
al. 2000, Jarnagin et al. 2000, 2004). This revelation suggests that effects of heavy fish predation in
the fall may be muted. Moreover, fish-mediated diapause egg dispersal may be an evolved, intriguing
adaptation in native European or Black Sea/Caspian
waters that contain Bythotrephes and the related
genus Cercopagus (Kerfoot et al. 2000).
Our findings do not mean that higher order interactions cannot result from the presence of predators. Studies by Werner and colleagues (mentioned
in Miller and Kerfoot 1987; reviewed in Werner
1992, Anholt and Werner 1999) show that large fish
predators, by virtue of their presence (chemical
scent or pheromone) in lakes and not necessarily
their density, can 1) alter the foraging behavior of
smaller fish prey which spatially avoid encounter
and 2) induce morphological alterations in different
co-existing prey species. Some of these responses
meet the status of a higher order interaction because
they satisfy the criterion of a density-independent
indirect interaction put forth by Worthen and Moore
(1991). As we mentioned earlier, the Bythotrephesfish interaction seems more like a density-dependent analog of Mullerian mimicry, where distasteful
experience mediates avoidance. Rather than spatial
avoidance, the adaptations of Bythotrephes permit
spatial co-existence of a potential prey (invertebrate
predator) with a potential predator (fish).
ACKNOWLEDGMENTS
We thank Kevin Kirk, Heather Harvey, and John
Bauchat for help in field collections and laboratory
313
experiments. Thanks to the Michigan DNR Hatchery in Marquette for lake trout; Dr. Stephen Bowen,
David Wiitanen and the MTU facilities and grounds
crew for providing and maintaining Lakeside Laboratory facilities; James Selgeby, Charles Bronte,
and Timothy Edwards of the National Biological
Survey for specimens and expertise; Tony Sutterley
at the University of Michigan Biological Station for
canoe access to Lancaster Lake; and David Kimar
of Pirates Cove Marina for boat maintenance. DRB
also thanks other members of her thesis committee,
Drs. Stephen Bowen, Gopi Podila and Martin Auer,
for numerous suggestions. This research was supported by the Michigan Sea Grant College Program
(project number R/ES-10, under grant number
NA89AA-D-SG083 from the Office of Sea Grant,
National Oceanic and Atmospheric Administration
(NOAA), U.S. Department of Commerce, and funds
from the National Undersea Research Program
(NURP).
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Submitted: 7 July 2002
Accepted: 10 June 2004
Editorial handling: Martin T. Auer