MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 280: 163?172, 2004 Published October 14
INTRODUCTION
The persistent or episodic occurrence of low dis-
solved oxygen (DO, hypoxia) is an important physical
feature of many aquatic habitats including estuaries,
lakes, nearshore coastal waters, fjords and the oxygen
minimum layer of the deep-sea. In shallow marine sys-
tems, hypoxia (i.e. dissolved oxygen concentrations
<2 mg l?1) generally occurs during summer when den-
sity stratification of the water column limits re-aeration
of bottom waters (Renaud 1986, Turner et al. 1987,
Swanson & Parker 1988, Rabalais et al. 1991). Sub-
pycnocline waters can become severely hypoxic or
anoxic during summer due to microbial respiration,
while oxygen concentrations at the surface can be sat-
urated or supersaturated as a result of algal photosyn-
thesis (Taft et al. 1980, Sanford et al. 1990, Jonas 1992,
Rabalais et al. 2002). Oxygen depletion in estuaries
and coastal waters is often exacerbated by excess
nutrient loadings (Officer et al. 1984, Elmgren 1989,
Rosenburg et al. 1990, Boesch et al. 2001, Rabalais et
al. 2002), and is a major threat to the ecology and fish-
eries of coastal waters worldwide (Caddy 1993). The
range and occurrence of oxygen depletion appear to
be increasing in shallow coastal and estuarine regions
(Diaz 2001) and hypoxia is predicted to become more
common as a result of global warming (Kennedy 1990).
A large proportion of the water in Chesapeake Bay
and its tributaries becomes hypoxic or anoxic for peri-
ods lasting hours to months in summer (Sanford et al.
? Inter-Research 2004 ? www.int-res.com*Email: marybeth.decker@yale.edu
Effects of low dissolved oxygen on zooplankton 
predation by the ctenophore Mnemiopsis leidyi
Mary Beth Decker1,*, Denise L. Breitburg2, Jennifer E. Purcell3
1Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut 06520-8106, USA
2Smithsonian Environmental Research Center, PO Box 28, Edgewater, Maryland 21037, USA
3Western Washington University, Shannon Point Marine Center, 1900 Shannon Point Road, Anacortes, Washington 98221, USA
ABSTRACT: The occurrence of low dissolved oxygen (DO), caused by vertical stratification and
excess nutrient inputs, is an important and widely occurring physical feature in aquatic systems.
Because some gelatinous species, such as the lobate ctenophore Mnemiopsis leidyi are more tolerant
of low DO concentrations than their prey and competitors, hypoxia may have profound effects on
trophic interactions. Predation, clearance and digestion rates of ctenophores feeding on zooplankton
(primarily Acartia tonsa) were measured at 1.0, 2.0, 3.0 mg l?1 and air-saturated (approximately
7 mg l?1) DO. Clearance of zooplankton by large ctenophores (mean 22.5 ml, range 7 to 46 ml) was
greater at low DO concentrations than under normoxic conditions. In contrast, consumption of zoo-
plankton by small (mean 2.9 ml, range 1 to 10 ml) M. leidyi did not differ among DO levels. Similarly,
ctenophore digestion rates were unchanged at oxygen concentrations as low as 1 mg l?1. Jumping
frequency of A. tonsa copepods decreased significantly with decreasing DO concentration (1.0, 2.0,
3.0 mg l?1 and air-saturated). Such changes in prey behavior in low DO could affect both encounter
and capture rates, potentially making less-tolerant prey more vulnerable to predation in hypoxic
waters. Gelatinous species, which are more tolerant of hypoxia than fishes, may be able to inhabit
regions of low oxygen that are avoided by zooplanktivorous fishes with high oxygen requirements.
This could lead to dominance of gelatinous predators in areas affected by severe hypoxia and might
alter energy pathways in these systems.
KEY WORDS:  Hypoxia ? Feeding ? Digestion ? Zooplankton ? Acartia tonsa ? Copepod ? Chesapeake
Bay
Resale or republication not permitted without written consent of the publisher
Mar Ecol Prog Ser 280: 163?172, 2004
1990). On average, about 62% of the subpycnocline
water volume in the main Chesapeake Bay (including
Mobjack Bay, but excluding Tangier Sound) is <5 mg
l?1, and about 19% of the subpycnocline volume is
<2 mg l?1 (M. Olson, Chesapeake Bay Program, pers.
comm.). Thus, hypoxia is a stress that is encountered
by many organisms in this ecosystem.
Not only does low DO have direct effects on mortal-
ity of organisms (reviewed in Marcus 2001 and Breit-
burg et al. 2001, Miller et al. 2002), but it can have
indirect effects on mortality through predator?prey
interactions. Motile species may shift their horizontal
or vertical distribution in both freshwater and coastal
systems influenced by hypoxia (Rudsam & Magnuson
1985, Kolar & Rahel 1993, Roman et al. 1993, Breitburg
et al. 1994, Howell & Simpson 1994, Keister et al. 2000,
Bell et al. 2003). Such differential shifts in the distribu-
tions of predators and prey potentially change the rates
at which they encounter each other (Breitburg et al.
1999). In addition, prey-capture rates can be affected
by hypoxia due to decreased foraging activity of
predators (Bejda et al. 1987, Breitburg et al. 1994,
Petersen & Pihl 1995, Taylor & Eggleston 2000) and
changes in the behaviors of prey that make them more
susceptible to predation (Poulin et al. 1987, Rahel &
Kolar 1990, Pihl et al. 1992, Kolar & Rahel 1993, Breit-
burg et al. 1997, Taylor & Eggleston 2000). For exam-
ple, predation by Chrysaora quinquecirrha medusae
feeding on fish larvae was greater at low DO, presum-
ably because the larvae escaped poorly when stressed;
however, medusa predation on fish eggs, which cannot
escape, was unaffected by low DO. In contrast, preda-
tion by juvenile striped bass Morone saxatilis feeding
on fish larvae was reduced at low DO (Breitburg et al.
1994, 1997). 
Hypoxia has differential effects on Chesapeake Bay
organisms. For example, the lobate ctenophore Mne-
miopsis leidyi is more tolerant of hypoxia than its prey
and than other predators in the Chesapeake food web
(Purcell et al. 2001a, Breitburg et al. 2003). Ctenophore
survival was 100% at DO concentrations ? 0.5 mg l?1 in
both 30 h and 72 h trials. In contrast, 24 h LC50 esti-
mates for the calanoid copepod Acartia tonsa range
from 0.95 to 1.4 mg l?1 (Roman et al. 1993, Stalder &
Marcus 1997). In addition, LC50 estimates for most Chesa-
peake Bay fishes range between 0.5 and 2.5 mg l?1
(reviewed in Breitburg et al. 2001, 2003). Because
gelatinous and non-gelatinous species differ in their
physiology and their oxygen demand, their behavior
(i.e. predatory or escape capabilities) may be affected
differently by low DO concentrations. It is possible that
ctenophores may increase prey consumption or out-
compete potential competitors such as the scyphome-
dusa Chrysaora quinquecirrha and the bay anchovy
Anchoa mitchilli in hypoxic waters where they co-
occur. Thus, the effects of low DO on ctenophores, as
well as on their prey and competitors, may dramati-
cally impact trophic interactions in the water column
(Breitburg et al. 1999, Purcell et al. 2001a). 
Mnemiopsis leidyi is an important predator of zoo-
plankton and ichthyoplankton in Chesapeake Bay and
its tributaries (Cowan & Houde 1992, 1993, Purcell et
al. 1994a,b, 2001b, Purcell & Decker 2005). M. leidyi
is a cruising predator that captures prey within their
outstretched lobes and tentillae (Waggett & Costello
1999). Consumption by M. leidyi at some times and
regions may reduce copepod populations in the main-
stem Chesapeake Bay, particularly when its preda-
tor Chrysaora quinquecirrha is scarce (Purcell et al.
2001b, Purcell & Decker 2005). 
The vertical distributions of Mnemiopsis leidyi cteno-
phores and Acartia tonsa copepods overlap in hypoxic
waters. M. leidyi and zooplankton are abundant in
bottom waters when bottom oxygen concentrations are
> 2 mg l?1 (Keister et al. 2000). Copepods are present in
the bottom layer when DO <2.5 to 3.0 mg l?1, but at
reduced densities, and M. leidyi can be abundant at
DO concentrations as low as 1.3 mg l?1. The influence
of hypoxia on the predatory behavior of M. leidyi has
recently been investigated in the laboratory (S. Kolesar
et al. unpubl. data). We are only beginning to under-
stand how interactions between this key predator and
its planktonic prey are influenced by low DO concen-
trations. 
In this study, we examine the effects of low DO on
zooplankton predation by Mnemiopsis leidyi. Inter-
actions between this important predator and its major
summer prey, Acartia tonsa, are typical of food webs in
the mesohaline regions of Chesapeake Bay as well as
in other estuaries along the Atlantic coast. Results from
our work can be used to predict effects of hypoxia on
plankton dynamics in seasonally-hypoxic estuaries. 
MATERIALS AND METHODS
Experimental animals. Ctenophores were collected
with a dip-net from the mesohaline Patuxent River 1 to
4 d prior to experiments. Test individuals were held at
ambient conditions (23?C, 13 to 15 salinity) in 75 l
aquaria that were gently mixed by surface paddles.
Ctenophores were fed zooplankton (mainly Acartia
tonsa and Artemia sp.), but not fed for 24 h prior to all
experiments. 
Zooplankton reared in 1 m3 mesocosms at the Acad-
emy of Natural Sciences Estuarine Research Center
were used as prey in predation and digestion experi-
ments. The mesocosms were filled with raw water from
the Patuxent River flowing through a 1 mm mesh,
which allowed eggs and other stages from natural field
164
Decker et al.: Hypoxia and zooplankton predation by ctenophores
assemblages of zooplankton to enter the mesocosms.
To promote algal growth and zooplankton reproduc-
tion, nutrients were added to the mesocosm at levels of
16 ?mol l?1 nitrogen and 1 ?mol l?1 phosphorus. There
was a 10% water change d?1 and nutrients were added
daily to maintain desired levels. On the day prior to
the experiments, zooplankton (dominated by Acartia
tonsa) were collected from mesocosms with a 202 ?m
net and held overnight in aquaria at 23?C, 13 to 15
salinity in the laboratory. 
Field-collected adult and late copepodite stages of
Acartia tonsa were used for the behavioral studies.
Copepods were collected from the mesohaline Chop-
tank River 1 to 2 d prior to behavioral observations by
slowly towing a 178 ?m mesh net horizontally at 0 to
2 m depth. Copepods from the solid 1 l cod-end bucket
were diluted immediately in a 20 l container and then
transferred to 75 l aquaria filled with 1 ?m filtered
Choptank water (25?C, 15 salinity). 
Effects of dissolved oxygen on ctenophore preda-
tion on zooplankton. We filled 8 experimental contain-
ers (plastic garbage cans) to 90 l with 0.2 ?m filtered
water from the mesohaline Patuxent River. Lids were
taped shut, and water in the containers was bubbled
with either N2 (low-oxygen treatments) or air (air-
saturated treatments) to obtain the desired DO concen-
trations. DO concentrations were monitored using YSI
(Models 52 and 85) dissolved oxygen meters. When a
container reached its target DO concentration, the air-
stone was removed from the water and allowed to
hang in the airspace above the water. The leakage of
N2 into the airspace ensured displacement of air and
maintenance of stable water-oxygen concentrations.
Consumption of zooplankton by ctenophores was mea-
sured at 1.0, 2.0, 3.0 mg l?1 and air-saturated (approxi-
mately 7 mg l?1) DO concentrations. The 1.0 mg l?1 DO
treatment was tested to include the lower portion of
the DO range at which ctenophores and copepods
occasionally co-occur (Keister et al. 2000). DO concen-
trations below 1.0 mg l?1 were not tested because in-
creased mortality of Acartia tonsa is observed when
they are held at or below 0.9 mg l?1 for 24 h (Stalder
& Marcus 1997). The experiment was conducted on
June 4, 9 and 16, 1999 and on August 2 and 30, 2000;
2 replicates of each DO concentration were completed
on each date.
Prey used in the predation experiment were pre-
dominantly adult and late copepodite stages of Acartia
tonsa. Zooplankton were divided into 8 portions with
an unbiased plankton splitter and 1?8 added into each
of the experimental containers once the target oxygen
concentrations had been attained. We then placed 8 to
12 ctenophores gently into a 2 l acclimation chamber
that excluded zooplankton (mesh size 35 ?m) within
each experimental tank, the containers were resealed,
and the ctenophores and zooplankton were allowed to
acclimate for 1 h. Ctenophores were then released into
the test arena and allowed to feed for 1 h. Experiment
duration was limited to 1 h because this is the average
time it takes for Mnemiopsis mccradyi (possibly the
same species as M. leidyi, K. Bayha pers. comm.) to
digest 1 to 10 adult Acartia sp. (Larson 1987). During
the course of the experiments, DO concentrations in
the low-oxygen treatments were maintained within a
mean of 0.09 mg l?1 (?0.01 SE) of the targeted levels. 
At the end of the experiment, both predators and
prey were removed from the experimental containers.
Ctenophores were dipped from the containers with an
aquarium net, their individual displacement volumes
were measured, and they were immediately preserved
in 5% buffered formalin. Water was siphoned from
each container, and zooplankton were collected in a
35 ?m mesh bag. Prior to preservation in 5% formalin,
zooplankton were stained with neutral red (Dressel et
al. 1972, Fleming & Coughlan 1978) so that their con-
dition during the experiment could later be scored as
alive or dead. The number of living copepods plus
those found in the ctenophores? gut contents was used
to calculate prey density in each experimental con-
tainer. Ctenophore volumes, prey densities, DO con-
centrations and temperatures for each treatment are
reported in Table 1. The number of prey added to
1 of the 2.0 mg l?1containers on June 16, 1999 was
anomalously high due to an error made while splitting
the zooplankton, and these results were excluded from
analyses on predation rates.
Consumption rates were measured by examining
ctenophore gut contents. Prey items consumed were
identified and counted while viewing the entire gut
contents with a dissecting microscope. Size-specific
predation rates were calculated for each ctenophore as
the number of prey items eaten h?1 ml?1 ctenophore
volume. The mean predation rate of ctenophores
within each experimental container was calculated
and used as the response variable in statistical analy-
ses. We also calculated clearance rates (l cleared h?1
ctenophore?1) by dividing predation rates (no. prey
eaten individual?1 h?1) by initial prey densities (no. prey
l?1). Size-specific clearance rates (l cleared h?1 ml?1
ctenophore) were calculated for each ctenophore by
dividing the liters cleared h?1 ctenophore?1 by the
individual ctenophore volume (ml). 
Nested analysis of variance (ANOVA) was conducted
to examine variance in predation rates between DO
treatments, prey densities and days. We employed the
model ?predation rate = prey density + DO + prey den-
sity ? DO + date(DO)?. After ensuring that the slopes
were not heterogeneous (i.e. a non-significant inter-
action term) and that there was no effect of day, the
nested ANOVA was simplified to an analysis of covari-
165
Mar Ecol Prog Ser 280: 163?172, 2004
ance (ANCOVA) to allow examination of variation in
predation rates due to DO and prey density. In addi-
tion, we used 1-way ANOVA to examine variance in
clearance rates between DO treatments. Rank trans-
formations were used where log- and square-root
transformations still left variances heterogeneous. 
Effects of dissolved oxygen on ctenophore diges-
tion rates. Because gut-content analyses were used to
estimate predation rates, it was necessary to determine
whether DO concentrations influenced the time re-
quired by ctenophores to digest zooplankton. In order
to measure digestion rates of Mnemiopsis leidyi feed-
ing on zooplankton (primarily Acartia tonsa), eight 11 l
glass aquaria were filled with 0.2 ?m filtered Patuxent
River water. Conditions were constant in each treat-
ment (mean water temperature = 21.8?C, SE = 0.2, mean
salinity = 14.5, SE = 0.2). Prior to the addition of cteno-
phores and zooplankton, the aquaria were sealed and
bubbled with either N2 (low-oxygen treatments) or air
(air-saturated treatments) to obtain the desired DO
concentrations. Digestion rates were measured at 1.0,
2.0 and 3.0 mg l?1 and air-saturated DO. Once the
target DO levels had been attained, 50 ctenophores
(mean individual volume 1.5 ml) were gently added to
each of 4 aquaria. Ctenophores were allowed to accli-
mate for 1 h before copepods were added at a density
of roughly 200 l?1. After ctenophores had fed for
10 min, they were removed with an aquarium net, gen-
tly dipped in filtered Patuxent River water to remove
any uneaten copepods, and then transferred into
another 4 aquaria with the same 4 DO concentrations as
the feeding containers. At 25 min
intervals, 5 to 6 ctenophores were
removed from each of the diges-
tion containers and the number of
whole copepods and intact cara-
paces in their guts were counted
with a dissecting microscope.
Martinussen & B?mstedt (1999)
showed no significant relation-
ships between digestion time and
size of a similar lobate cteno-
phore, Bolinopsis infundibulum.
Use of small, transparent cteno-
phores allowed easy visual in-
spection of gut contents. Differ-
ent individuals were sampled at
each 25 min interval. We calcu-
lated the average number of prey
items present ctenophore?1 at the
initial sampling period and then
at each 25 min interval thereafter.
This experiment was run twice,
on July 2 and 9, 1999. The results
of the digestion experiment were
analyzed using the model ?no. prey ctenophore?1 =
Time + DO + Time ? DO + Date? to allow examination
of variation in digestion rates due to DO and date and
to test for differences in digestion rates among DO
treatments. 
In order to ensure that ctenophores were digesting
prey in hypoxic water and not simply expelling their
gut contents, we continuously observed digestion by
individual ctenophores in a 1.5 l watch-glass at a range
of DO concentrations. The watch-glass and an 11 l
aquarium were filled with 0.2 ?m-filtered Patuxent
River water (21 to 23?C, 11 to 12 salinity), covered with
clear Plexiglas and sealed, and DO concentrations (1.0,
2.0, 3.0 mg l?1 and air-saturated) were obtained as
before. We used a peristaltic pump to fill the sealed
watch-glass and gently circulate water between the
aquarium and the watch-glass to maintain target oxy-
gen levels. DO concentrations in the watch-glass were
monitored with an oxygen microelectrode throughout
the observation period. Ctenophores were fed until
they had consumed 2 to 12 adult Acartia tonsa, and
then 2 were gently placed in the watch-glass. Diges-
tion of copepods was observed at 1 low-DO treatment
and 1 air-saturated control on 3 d in July 2000. Ob-
servations continued until gut contents were no longer
recognizable. 
Effects of dissolved oxygen on copepod behavior.
The swimming behavior of Acartia tonsa in filtered
water has been described as monotonic jumping
(Tiselius & Jonsson 1997). To assess how normal
swimming behavior of Acartia tonsa may have been
166
Table 1. Mnemiopsis leidyi. Conditions in experiments testing predation by cteno-
phores on prey, primarily Acartia tonsa copepods. Values are means ? 1 SE of the
mean. Air-sat: air-saturated (approximately 7 mg l?1 dissolved oxygen)
Experimental conditions Date
4 Jun 9 Jun 16 Jun 2 Aug 30 Aug 
1999 1999 1999 2000 2000 
Target O2 conc. 1 1 1 1 1
(mg l?1) for 2 2 2 2 2
4 treatments 3 3 3 3 3
Air-sat Air-sat Air-sat Air-sat Air-sat
Measured O2 conc. 1.0 ? 0.0 1.1 ? 0.1 1.1 ? 0.0 1.0 ? 0.1 1.1 ? 0.0
(mg l?1) for 1.9 ? 0.1 2.0 ? 0.1 2.0 ? 0.0 2.0 ? 0.0 2.1 ? 0.0
4 treatments 2.9 ? 0.1 2.9 ? 0.1 2.9 ? 0.0 3.0 ? 0.0 3.1 ? 0.0
7.0 ? 0.0 7.2 ? 0.1 6.7 ? 0.0 7.7 ? 0.1 7.6 ? 0.2
Water temperature (?C) 21.9 ? 0.10 22.8 ? 0.10 22.9 ? 0.10 21.6 ? 0.10 22.6 ? 0.00
Salinity 13 13.5 14 10 12
No. of replicates 2 2 2 2 2
No. ctenophores tank?1 12 12 12 12 8
Ctenophore volume (ml) 21.1 ? 0.90 23.6 ? 0.90 22.8 ? 0.80 2.3 ? 0.1 3.9 ? 0.3
(range) (7?45) (12?46) (10?44) (1?3) (1?10)
Copepod density range 23?35 49?95 28?64 27?55 22?66
(no. l?1)
Decker et al.: Hypoxia and zooplankton predation by ctenophores
affected during our predation experiments, we exam-
ined how jumping frequency of free-swimming cope-
pods was influenced by DO concentrations. An aquar-
ium (36 cm ? 14 cm ? 10 cm, 5 l) filled with 1 ?m-filtered
Choptank River water was sealed, and target DO con-
centrations were obtained as before. Observations
were conducted at 1.0, 2.0, 3.0 mg l?1 and air-saturated
DO. Copepods (approximately 200 l?1) were then placed
in the aquarium and allowed to acclimate for 1 h.
Copepods were filmed using a Sony CCD TR400 Hi8
video-recorder with a variable focus lens (5.4 to 64.8
mm). The aquarium was illuminated from behind
using an infrared light (IR) source (STA Model Mir 3
Infra-red, wavelength > 700 nm, Aspect Technology
and Equipment) because zooplankton are most sensi-
tive to light with <700 nm wavelengths (Sterns & For-
ward 1984, Forward 1988) and therefore, IR should not
have influenced copepod behavior. The positions of
the camcorder and IR light were moved horizontally
every 10 minutes in order to film copepods in a differ-
ent region of the aquarium. We filmed for a total of 2 h
at each DO treatment. 
Jumping frequencies were determined by counting
the number of jumps of an individual copepod for 1
min or until it left the field of view. We chose 100 indi-
viduals arbitrarily from the videotape footage for each
DO treatment. Container size was large compared
with the size of the copepods (ca 0.5 mm carapace
length), and no copepods near the aquarium walls
were used to minimize the effects of the container on
their behavior. To test for the effect of DO on copepod
jumping frequencies, we conducted a linear regres-
sion on the mean jumping frequency in each DO
treatment. It is unlikely that in a relatively large con-
tainer the behavior of one copepod would affect the
behavior of other copepods, thus each observation
was considered to be an independent measure of
jumping frequency. 
RESULTS
Effects of low dissolved oxygen on ctenophore
predation on zooplankton
Large ctenophores were unavailable for collection
in 2000; thus, ctenophore sizes differed dramatically
in 1999 and 2000 predation experiment replicates
(Table 1). Because small ctenophores ingest more per
unit volume than large ctenophores (Kremer 1979,
Kremer & Reeve 1989), we examined DO effects on
ctenophore predation and clearance rates separately
for 1999 and 2000. Neither date nor interactions
(between prey density and DO) were significant in
either year (all p > 0.28) in tests using the full ANOVA
model; therefore we present results of the simplified
ANCOVA model testing only the main effects. In-
spection of statistical analyses indicated significant
effects of prey density (F = 71.48, df = 1, p < 0.001), and
a trend toward higher predation rates at moderate lev-
els of hypoxia (2.0 and 3.0 mg l?1) than at 1 mg l?1 and
air-saturation during 1999 (Fig. 1A; F = 3.12, df = 3,
p = 0.052). In contrast, neither prey density (F = 3.43,
167
Prey density (no. l-1)
20 40 60 80 100
0
2
4
6
8
10
12
 P
re
y 
ea
te
n 
(n
o.
 h
?1
 m
l?1
 c
te
no
ph
or
e)
0
2
4
6
8
10
12 A
B
Air sat
3.0 mg l-1
2.0 mg l-1
1.0 mg l-1
Fig. 1. Mnemiopsis leidyi. Numbers of zooplankton prey (pri-
marily Acartia tonsa adults and copepodites) consumed by
ctenophores during 1 h experiment in reduced (1.0, 2.0 and
3.0 mg l?1) and air-saturated (approximately 7 mg l?1) dis-
solved oxygen concentrations in (A) 1999 and (B) 2000. Data
points: average no. of prey eaten h?1 ml?1 ctenophore vol ver-
sus experimental prey densities (no. l?1) for each replicate;
lines: relationships between prey consumption and prey den-
sity for each oxygen treatment (1999: y1.0 = 0.06x + 0.28,
R2 = 0.95, t = 8.41, df = 4, p = 0.001; y2.0 = 0.06x + 0.77, R2 = 0.61,
t = 2.18, df = 3, p = 0.12; y3.0 = 0.07x + 0.15, R2 = 0.78, t = 3.76,
df = 4, p = 0.02; yAir-sat = 0.05x ? 0.07, R2 = 0.93, t = 7.34, df = 4,
p = 0.002. 2000: y1.0 = 0.02x + 4.36, R2 = 0.01, t = 0.11, df = 2,
p = 0.92; y2.0 = 0.15x ? 1.75, R2 = 0.29, t = 0.90, df = 2, p = 0.46;
y3.0 = 0.08x + 0.80, R2 = 0.71, t = 2.24, df = 2, p = 0.15; yAir-sat =
0.13x ? 0.73, R2 = 0.64, t = 1.89, df = 2, p = 0.20). Experimental 
conditions summarized in Table 1
Mar Ecol Prog Ser 280: 163?172, 2004
df = 1, p = 0.09), nor DO (F = 0.06, df = 3, p = 0.98) had
significant effects on predation rate in 2000. 
The results of the predation experiment showed no
ctenophore satiation in hypoxic conditions at the range
of prey densities tested (Fig. 1). We therefore examined
variation in ctenophore clearance rates (l cleared h?1
ml?1 ctenophore volume) among DO treatments using
ANOVA. A 1-way ANOVA on ranks indicated differ-
ences in clearance rates among DO treatments in 1999
(F = 4.87, df = 3, p = 0.01), but not in 2000 (F = 0.02, df = 3,
p = 0.99) (Table 2). A Student-Newman-Keuls multiple-
comparison test revealed that in 1999 clearance rates in
all low-DO treatments were higher than those in the air-
saturated controls (Table 2). Thus, our data indicate that
predation by large ctenophores (mean = 22.5 ml, range =
7 to 46 ml) was greater at low-DO concentrations than in
air-saturated conditions; however, small ctenophores
(mean 2.9 ml, range = 1 to 10 ml) showed no differences
in predation among DO treatments. 
We estimated the average clearance by Mnemiopsis
leidyi (average size = 15.5 ml, size range 1 to 46 ml,
SE = 0.5) feeding on Acartia tonsa at 1.0 l cleared h?1
ctenophore?1 (SE = 0.1, range 0.1 to 2.4 l cleared h?1
ctenophore?1). At experimental prey densities ranging
from 22 to 121 copepods l?1, this is equivalent to
0.3?10.5 % h?1 (average 2.5% h?1, SE = 0.3) or an aver-
age of 46.7 copepods eaten h?1 ctenophore?1. 
Effects of low dissolved oxygen on 
ctenophore digestion rates
Results of the ANCOVA revealed that there was
no effect of date on the number of prey consumed
ctenophore?1 throughout the timed digestion experi-
ment (Table 3); therefore, we combined data from both
days for further analyses. The numbers of prey present
in the ctenophore guts decreased over time, with few
prey remaining at 150 min (Fig. 2). The average num-
ber of prey present in ctenophores was 4.1 (SE = 0.5,
range 1 to 11) at the start of the experiment and 0.4
(SE = 0.1, range 0 to 4) after 150 min. In order for linear
models to be used in the regression and slope analyses,
data for the final time interval (i.e. 200 min) were omit-
ted. Data for all 4 DO treatments then fit significant lin-
ear regressions. The slopes of the regressions were not
significantly different (Table 4, ANOVA, heterogeneity
of slopes, F = 0.66, df = 21, p = 0.84), providing no evi-
dence for differences in digestion rates among the DO
treatments. 
Observations of 12 individual ctenophores digesting
copepods revealed that no ctenophores expelled their
gut contents after an average of 51.5 min (SE = 7.1,
range 25 to 91) in any treatment. During these obser-
vations, ctenophores ingested similar numbers of cope-
pods (6.3 ? 0.9, range 2 to 12) and conditions were sim-
ilar to those in the preceding experiment (water
temperature = 21.9?C ? 0.5, salinity = 11.6 ? 0.2) and in
all treatments. Temperatures during the observations
168
Table 2. Mnemiopsis leidyi. Mean (?SE) size-specific clear-
ance rates (l cleared h?1 ml?1 ctenophore) of ctenophores
eating zooplankton, primarily Acartia tonsa copepods, at
various dissolved oxygen treatments in 1999, 2000 and in both
years combined
Year 1.0 mg l?1 2.0 mg l?1 3.0 mg l?1 Air-saturated
1999 0.06 ? 0.00 0.08 ? 0.01 0.07 ? 0.01 0.05 ? 0.00
2000 0.13 ? 0.05 0.11 ? 0.04 0.10 ? 0.01 0.11 ? 0.03
Both 0.09 ? 0.02 0.09 ? 0.02 0.08 ? 0.01 0.07 ? 0.01
Table 3. Mnemiopsis leidyi. Variation in digestion rates of
copepods (Acartia tonsa) by ctenophores as a function of dis-
solved oxygen (DO) and date. Analysis tested for effects of
DO and date on number of prey present ctenophore?1
throughout the timed digestion experiment. The model ?no.
prey ctenophore?1 = time + DO + time ? DO + Date? was em-
ployed, whereby interaction term tests for heterogeneity of
slopes (i.e. differences in digestion rates among DO treatments)
Source df SS F p 
Time 7 156.10 10.7 <0.0001
DO 3 12.3 02.0 0.14
DO ? Time 0210 28.8 00.7 0.84
Date 1 0.03 0.01 0.90 
Time (min)
0 50 100 150 200
P
re
y 
pr
es
en
t c
te
no
ph
or
e-
1
0
2
4
6
8
10
Air-sat
3.0 mg l -1
2.0 mg l -1
1.0 mg l -1
Fig. 2. Mnemiopsis leidyi. Effects of dissolved oxygen (DO)
concentration on digestion of zooplankton by ctenophores.
Water temperature during experiment averaged 21.8?C
(?0.2 SE). Data points: average no. of prey present cteno-
phore?1 for each replicate during course of digestion experi-
ment; lines: relationships between number of prey cteno-
phore?1 and time (?175 min) for each oxygen treatment (y1.0 =
?0.04x + 5.98; y2.0 = ?0.02x + 3.27; y3.0 = ?0.03x + 4.47; yAir-sat =
?0.02x + 3.78). Parameters of regression analyses in Table 4
Decker et al.: Hypoxia and zooplankton predation by ctenophores
of individual ctenophores were not significantly differ-
ent from conditions in the preceding digestion experi-
ment (Student?s t = ?0.53, df = 12, p = 0.6); however,
salinities were lower than during the previous experi-
ment in 1999 (Mann-Whitney rank sum T6, 8 = 21, p =
0.001), and reflected differences in the salinity of the
Patuxent River during the time of the 2 experiments. 
Effects of low dissolved oxygen on copepod behavior
Behavior of Acartia tonsa was significantly affected
by DO concentration (Fig. 3). Mean jump frequency
increased with increasing DO concentration from a
low of 38.3 jumps min?1 (SE = 1.8) in the 1.0 mg l?1
treatment to a high of 127.8 jumps min?1 (SE = 6.9) in
the air-saturated treatment. Linear regression of log-
transformed jump frequency against DO concentration
was significant (R2 = 0.996, t = 21.12, df = 2, p = 0.002). 
DISCUSSION
Results from this study indicate that consumption of
calanoid copepods by large Mnemiopsis leidyi cteno-
phores (mean = 22.5 ml, range = 7 to 46 ml) was greater
in low dissolved oxygen (DO) environments than under
normoxic conditions. In contrast, consumption by small
ctenophores (mean 2.9 ml, range = 1 to 10 ml) was not
influenced by DO concentrations ?1 mg l?1, just as
consumption of ichthyoplankton (fish eggs and larvae)
by M. leidyi (average volume = 15.6 ml, range = 7 to
25 ml) is not affected by oxygen concentrations greater
than or equal to 1.5 mg l?1 (S. Kolesar et al. unpubl.
data). Because consumption rates of large ctenophores
feeding on zooplankton prey appear to be affected by
the low DO at which they are found in the field, the
location within the water column at which encounters
occur, the size distribution of ctenophores, as well as
vertical overlap between predator and prey may all be
extremely important in determining the overall effect
that hypoxia has on trophic interactions (Keister et al.
2000, Breitburg et al. 2003). 
Bottom-layer hypoxia has a great influence on the
vertical distribution of zooplankton and gelatinous
predators in Chesapeake Bay and its tributaries, but
the DO concentration eliciting avoidance varies among
species (Breitburg et al. 2003, Decker et al. 2003). As a
result, the presence of low DO concentrations could
affect overlap of and encounters between Mnemiopsis
leidyi and Acartia tonsa copepods. Field sampling in
both the mainstem Chesapeake Bay (Roman et al.
1993) and the Patuxent River (Keister et al. 2000, J.
Purcell et al. unpubl. data) indicate that A. tonsa is less
abundant in the bottom layer when DO concentrations
are low than when they are high. The proportion of A.
tonsa found in the bottom layer of the Patuxent River
declines as DO concentrations fall below 2.5 to 3 mg l?1.
In contrast, high proportions of M. leidyi were found
in the bottom layer at DO concentrations as low as
1.3 mg l?1 (Keister et al. 2000, Breitburg et al. 2003). As
a result, vertical overlap between M. leidyi and A.
tonsa would be reduced when bottom DO concentra-
tions are 1 to 2 mg l?1. In addition, because A. tonsa
actively avoids the hypoxic bottom layer in a stratified
water column (Decker et al. 2003), per capita con-
sumption of this prey by ctenophores may be highest in
the volume of water within and above the pycnocline
and oxycline. 
169
Table 4. Mnemiopsis leidyi. Results of linear regressions of
number of prey (Acartia tonsa) present in ctenophore guts
over time during digestion in dissolved oxygen (DO) treat-
ments (Fig. 2). Fit of each linear regression was significant for
each DO treatment; therefore, comparisons were made be-
tween lines in order to test for effect of DO concentration on
digestion of prey. Heterogeneity of slopes analysis revealed
that slopes of the regressions were not significantly different,
indicating that M. leidyi digestion rates did not differ among 
DO treatments
Dissolved oxygen R2 Slope t df p
treatment
1.0 mg l?1 0.66 ?0.04 ?5.29 14 <0.001
2.0 mg l?1 0.57 ?0.02 ?4.31 14 <0.009
3.0 mg l?1 0.63 ?0.03 ?4.86 14 <0.001
Air-saturated 0.46 ?0.02 ?3.73 14 <0.002 
DO concentration (mg l?1)
0 1 2 3 4 5 6 7
Ju
m
p 
fre
qu
en
cy
 (l
og
10
 n
o.
 m
in
?1
)
1.4
1.5
1.6
1.7
1.8
1.9
2.0
2.1
Fig. 3. Acartia tonsa. Jump frequency of copepods under
reduced (1.0, 2.0 and 3.0 mg l?1) and air-saturated (approxi-
mately 7 mg l?1) dissolved oxygen (DO) concentrations. Sym-
bols represent the mean jumping frequency ?1 SE of mean.
Equation of line is y = 0.09x + 1.44, R2 = 0.99, t = 21.12, df = 2, 
p < 0.002
Mar Ecol Prog Ser 280: 163?172, 2004
Our estimate of average ctenophore clearance rates
of copepods (i.e. 1.0 l cleared h?1 ctenophore?1 or 23.3 l
cleared ctenophore?1 d?1, based on an average cteno-
phore volume of 15 ml) is comparable to estimates
measured by other investigators (reviewed in Purcell
et al. 2001b). Previous estimates standardized for a
40 ml ctenophore range from 16.8 to 52.8 l cleared
ctenophore?1 d?1, increasing with container size. Cteno-
phore volumes in our study ranged from 1 to 46 ml.
The wide size range of ctenophores used in the preda-
tion experiment may be responsible, in part, for the
scatter in the number of prey items consumed (Fig. 1).
The experimental containers used here were fairly
small (90 l), and our clearance estimate was more simi-
lar to those previously estimated in small containers. 
Martinussen & B?mstedt (1999, 2001) stressed the im-
portance of performing digestion experiments when-
ever gut contents are used to measure consumption
rates of gelatinous predators, because ambient condi-
tions can have significant effects on digestion rates.
Because we used gut contents to measure consumption
by ctenophores in this study, we tested the effects of
DO concentration on the rate of extracellular digestion
in Mnemiopsis leidyi. DO concentration had no effect
on the rate at which copepods are broken down in
M. leidyi?s pharynx. In addition, hypoxia did not cause
ctenophores to expel undigested prey from their
mouths. 
Predation is the final outcome of the probability of
encounters between predator and prey and the proba-
bility of prey escape. In addition to the effect of shifts in
vertical distributions discussed above, rates of prey
encounter depend in part on relative swimming speeds
of predator and prey, with faster swimming prey being
encountered more frequently than slower prey (Gerrit-
sen & Strickler 1977). Low-DO concentrations reduced
the jumping frequencies of Acartia tonsa copepods.
Therefore, one would expect encounter rates of cope-
pods with predatory ctenophores also to decline with
decreasing DO concentrations. However, we showed
that predation rates of large ctenophores tended to
be higher in moderately hypoxic DO treatments, and
clearance rates of large ctenophores were higher at all
reduced oxygen concentrations tested than in air-
saturated controls (Fig. 1A, Table 2). It is possible that
the reduced jump rates we measured were a general
indication of reduced locomotory abilities of copepods
under hypoxic conditions and that escape behavior of
copepods is also compromised by low oxygen. If so, our
results suggest that hypoxia-induced changes in
escape rates are more important than changes in en-
counter rates in determining the ultimate effect of
hypoxia on consumption of copepods by large cteno-
phores. However, the relative importance of encounter
and escape rates may differ for small and large cteno-
phores, leading to a net result of no effect of hypoxia
on consumption by small ctenophores. In order to
resolve this issue, future research should investigate
the effects of DO concentrations on actual encounters
between ctenophores and zooplankton, including the
influence of DO on the swimming speeds of all cteno-
phore size classes and on the escape reactions of
A. tonsa.
Future studies should also consider the effects of
hypoxia on ctenophore predation of other dominant
zooplankters in the Chesapeake Bay system. For
example, the naupliar stages of Acartia tonsa are ex-
tremely abundant in summer (Roman et al. 1993) and
are important prey of Mnemiopsis leidyi in Chesa-
peake Bay (Purcell et al. 2001b). A. tonsa adults are
less tolerant of low DO than are nauplii (Stalder &
Marcus 1997). Therefore, the effect of hypoxia on
ctenophores feeding on adults and copepodites (this
study) may differ from that of ctenophores feeding on
nauplii. The mechanisms by which lobate ctenophores
encounter and capture their prey also differ, depend-
ing on prey type and prey behavior (Larson 1988,
Waggett & Costello 1999). Actively-swimming adult
A. tonsa first contact the inner surfaces of the cteno-
phore?s lobes, whereas, weakly-swimming A. tonsa
nauplii first contact the tentillae within the lobes of M.
leidyi (Wagget & Costello 1999). Due to these distinct
encounter mechanisms, low DO may affect capture
and escape of adult and naupliar stages of A. tonsa
differently. 
Low DO may have pronounced effects on the trophic
interactions involving gelatinous predators in Chesa-
peake Bay. Similar to what we observed for small Mne-
miopsis leidyi, predation by Chrysaora quinquecirrha
medusae on copepods was unaffected by DO concen-
trations ?1.5 mg l?1 (Breitburg et al. 1994, 1997). In con-
trast, C. quinquecirrha medusa predation on naked
goby larvae Gobiosoma bosc was much greater at low
DO concentrations (1.5 mg l?1) than in air-saturated
conditions, whereas predation on fish eggs (Anchoa
mitchilli) decreased in low DO (Breitburg et al. 1994,
1997). In striking contrast with the medusae, low DO
concentrations resulted in decreased consumption of
fish larvae by juvenile and adult fishes (Morone sax-
atilus and G. bosc, respectively) (Breitburg et al. 1994,
1997). These previous studies of C. quinquecirrha
along with studies of M. leidyi (this study, and S. Kole-
sar et al. unpubl. data) suggest that hypoxia tolerance
of M. leidyi ctenophores and C. quinquecirrha medusae
(as compared with hypoxia-sensitive fishes: Breitburg
et al. 2003) may enable gelatinous species to inhabit
and be effective predators in regions of low DO that
exclude vertebrate predators with high respiratory
demands. This may lead to dominance of gelatinous
predators over fishes in regions affected by severe
170
Decker et al.: Hypoxia and zooplankton predation by ctenophores
hypoxia, and could potentially alter energy pathways
in these systems (Breitburg et al. 1999, Purcell et al.
2001a). 
Acknowledgements. We thank, in particular, X. Ma as well as
L. Brink, R. Condon, K. Crawford, D. Davis, E. Haberkern, S.
Kolesar, C. Stringer and W. Yates, for their help in collecting
animals and conducting laboratory experiments. We also
thank M. Bundy, J. Costello, P. Kremer, M. Olson and P.
Turner for insightful discussions. This research was funded by
Environmental Protection Agency STAR award No. 827097-
01-0 to D.L.B., J.E.P., M.B.D. and K. A. Rose. 
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Editorial responsibility: Kenneth Sherman (Contributing Editor),
Narragansett, Rhode Island, USA
Submitted: September 1, 2003; Accepted: May 27, 2004
Proofs received from author(s): September 27, 2004