Journal of
Plankton Research
plankt.oxfordjournals.org
J. Plankton Res. (2014) 36(5): 1298 – 1309. First published online June 5, 2014 doi:10.1093/plankt/fbu047
Apparent diel feeding by the ctenophore
Mnemiopsis leidyi A. Agassiz 1865
(Ctenophora, Lobata)
LINDSAY J. SULLIVAN*
ROMBERG TIBURON CENTER FOR ENVIRONMENTAL STUDIES, SAN FRANCISCO STATE UNIVERSITY,
3152 PARADISE DRIVE, TIBURON, CA 94920-1205, USA
*CORRESPONDING AUTHOR: [email protected]
Received October 9, 2013; accepted May 5, 2014
Corresponding editor: Roger Harris
The ctenophore Mnemiopsis leidyi A. Agassiz (1865) is not generally believed to exhibit diel feeding. As a result, the majority of studies documenting feeding of M. leidyi have been performed during the day, which may underestimate or
overestimate daily clearance and ingestion rates if feeding changes over the diel cycle. Here, diel feeding by M. leidyi
was examined during seven separate 24-h periods using gut content analysis. The total prey abundance and number
of prey consumed per ctenophore did not differ between day and night; however, the percent of ctenophores with
empty guts was higher during the day. These data show that, although fewer ctenophores consumed prey during the
day, those that did consumed a larger number than at night. Additionally, the composition of the prey assemblage and
the diet of M. leidyi did not differ between day and night; however, the composition of the prey assemblage differed
from that observed in ctenophore guts, indicating selective feeding. Despite the lack of an overall difference in prey
abundance and diet composition, isopods, cumaceans, decapod shrimp larvae and mantis shrimp larvae were
observed in ctenophore guts only at night. These observations emphasize the importance of both day and night sampling, especially in ecosystems where prey availability changes significantly over the diel cycle.
KEYWORDS: gut contents; diet composition; prey selection; nocturnal demersal zooplankton; diurnal feeding
rhythm
I N T RO D U C T I O N
Diel feeding rhythms are well documented in both crustacean zooplankton (Fuller, 1937; Gauld, 1953; Kouassi
et al., 2001) and nekton (Gurney et al., 2002; Marnane
and Bellwood, 2002). These characteristic day – night patterns in feeding are frequently coupled with diel vertical
migration, and are most often influenced by changes in
prey availability and risk of predation (Haney, 1988).
available online at www.plankt.oxfordjournals.org
# The Author 2014. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]
L. J. SULLIVAN
j
DIEL FEEDING BY THE CTENOPHORE MNEMIOPSIS LEIDYI
Gelatinous zooplankton have also been reported to
exhibit diel patterns in behavior, including migration and
feeding. However, relatively few studies have investigated
diel rhythms in this group compared with crustacean
zooplankton and nekton, and with mixed results. Both
regular (e.g. migration to the surface at night) and reverse
(e.g. migration to the surface during the day) diel vertical
migrations have been reported for several species of
hydromedusae (Mills, 1983; Roe et al., 1984; Benović
et al., 2005) and siphonophores (Mackie et al., 1987). Diel
vertical migration has also been observed in some scyphomedusae and in the ctenophore, Beroe ovata (Roe et al.,
1984).
While feeding of siphonophores is regularly restricted
to day or night based on vertical migration patterns
(Mackie et al., 1987), feeding rhythms, or lack thereof,
within other gelatinous groups appear to vary among
species. Wintzer (Wintzer, 2010) observed no day– night
difference in the number of prey ingested by two species
of hydromedusae, Maeotias marginata and Moerisia lyonsi.
Conversely, Purcell and Nemazie (Purcell and Nemazie,
1992) observed an increase in the number of prey
ingested at night by the hydromedusa, Nemopsis bachei,
despite the absence of diel vertical migration in this
species or diel changes in prey availability. Additionally,
Arkett (Arkett, 1984) observed diel changes in the diet of
the hydromedusa, Polyorchis penicillatus, coincident with its
own diel vertical migration and the emergence of nocturnal demersal zooplankton. Spadinger and Maier
(Spadinger and Maier, 1999) also reported an increase in
the number of prey ingested at night by the hydromedusa, Craspedacusta sowerbyi, coincident with its own
diel vertical migration.
Fancett and Jenkins (Fancett and Jenkins, 1988)
observed no light – dark difference in clearance rate for
two species of scyphomedusae, Cyanea capillata and
Pseudorhiza haekeli, in laboratory feeding experiments.
Martinussen and Båmstedt (Martinussen and Båmstedt,
1995) also found no difference in ingestion rate or daily
ration between day and night for C. capillata. Kremer
(Kremer, 2005) reported no day – night difference in the
number of prey ingested or clearance rates of the scyphomedusa, Linuche unguiculata, as well as no difference in
prey availability. Similarly, Uye and Shimauchi (Uye and
Shimauchi, 2005) reported no day – night difference in
the number of prey ingested by another scyphomedusa,
Aurelia aurita. In contrast, Olesen et al. (Olesen et al., 1994)
reported an increase in the number of prey ingested at
night by A. aurita, coincident with increases in prey availability. Purcell (Purcell, 1992) also observed an increase
in the number of prey ingested at night by the scyphomedusa, Chrysaora quinquecirrha, coincident with increases in
prey availability. Similarly, Carr and Pitt (Carr and Pitt,
2008) reported differences in the diet of the scyphomedusa, Catostylus mosaicus, coincident with changes in the
prey assemblage.
Finally, Anderson (Anderson, 1974) reported no
diurnal difference in the number of prey ingested by the
ctenophore, Pleurobrachia pileus, despite changes in the
prey assemblage. In contrast, Hirota (Hirota, 1974)
reported changes in the diet composition of Pleurobrachia
bachei. Unfortunately, day– night differences in the prey
assemblage were not investigated or reported in many of
these studies. This makes interpretation of the differences
within groups difficult to interpret.
Despite conflicting evidence of diel feeding patterns
among Pleurobrachia spp. (Anderson, 1974; Hirota, 1974),
diurnal rhythms have been reported for the ctenophore,
Mnemiopsis leidyi A. Agassiz (1865), including suggestions
of diel feeding. Several studies have reported maximum
abundances of M. leidyi in surface waters at night (Zaika
and Sergeyeva, 1992; Haraldsson et al., 2014). Minkina
and Pavlova (Minkina and Pavlova, 1995) observed a
nighttime maximum in respiration, and spawning of this
species occurs only at night (Freeman and Reynolds,
1973; Zaika and Revkov, 1995). Additionally, Kovalev
et al. (Kovalev et al., 1996) suggested that maximum
feeding of M. leidyi occurs at night, but did not present
direct observations of feeding to support this claim. The
presence of these diurnal rhythms suggests that M. leidyi
possess adaptations for monitoring changes in light
levels, and while presumptive photoreceptor cells have
been observed in other ctenophores (Horridge, 1964;
Aronova, 1979), the role of these cells in light reception
has not yet been confirmed. Cumulatively, these observations support the possibility of a diel feeding rhythm in
M. leidyi, but the majority of studies to investigate feeding
in this species have been performed during daylight
hours, most likely due to ease of sampling. As a result,
total daily clearance and ingestion rates of M. leidyi, as
well as its potential predation impacts, may be underestimated or overestimated if feeding changes over the diel
cycle. Here, M. leidyi gut contents were examined during
seven separate 24-h periods in order to document the
presence/absence of a diel feeding rhythm.
METHOD
Gut content analysis
During 2003 and 2004, M. leidyi were collected for gut
content analysis from the University of Rhode Island’s
Graduate School of Oceanography dock, located in the
lower West Passage of Narragansett Bay, RI, USA
(418290 32.1300 N, 718250 08.0200 W). Ctenophores were
1299
JOURNAL OF PLANKTON RESEARCH
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VOLUME 36
collected with vertically integrated tows using a 0.5-m
diameter, 1-mm mesh ring net. Tows were taken at 4-h
intervals over seven separate 24-h periods at approximately 09:00 (day), 13:00 (day), 17:00 (day), 21:00
(night), 01:00 (night), 05:00 (night) and 09:00 (day)
(Table I). Because digestion of most prey items takes less
than 2 h at similar temperatures (Sullivan, 2010), samples
were collected 2 h after sunrise (day) and sunset (night).
Following each tow, the contents of the cod end were
gently transferred to a 5 gallon bucket containing in situ
water. Randomly selected ctenophores were removed
from the bucket with a scoop and transferred in a petri
dish to a dockside Olympus SZ-ST dissecting microscope. During each time interval, the guts of 20– 30 live
individuals were examined and the contents were identified and enumerated. The maximum amount of time
between collection and gut content examination was
,10 min. Approximately 140 individuals were examined
during each study. Tintinnid ciliates were identified
according to Lee et al. (Lee et al., 2000). All other zooplankton taxa were identified according to Gerber
(Gerber, 2000). Surface water temperature (8C) was measured with a digital thermometer. Ctenophore total
length (cm), which includes lobes, was measured with a
ruler.
Prey abundance
During each time interval, the prey assemblage was
sampled in conjunction with the gut content observations
with a vertically integrated tow using a 0.25-m diameter,
64-mm mesh ring net equipped with a General Oceanics
flowmeter. Zooplankton samples were preserved in 4%
formaldehyde buffered with 1 – 2% sodium borate.
Subsamples containing at least 100 – 200 individuals of
the most abundant prey taxa were counted at a magnification of 50 under a Nikon SMZ-U Zoom 1:10 dissecting microscope (Venrick, 1978). Approximately 300
j
NUMBER 5
j
PAGES 1298 – 1309
j
2014
individuals of the most abundant prey taxa and 600 total
prey items were identified and counted from each
sample. Zooplankton were identified as above. The numerical abundance (no. L21) of each prey category was
calculated according to Postel et al. (Postel et al., 2000).
Data analysis
Because samples collected within the same 24-h period
were highly correlated, day (n ¼ 4) and night (n ¼ 3)
samples from each sampling date were averaged prior to
analysis. Differences in depth (m), surface temperature
(8C) and ctenophore total length (cm) between day and
night were examined with paired Student’s t-tests. Differences in the total prey abundance (no. L21), total number
of prey consumed per ctenophore (no. ctenophore21) and
percent of ctenophores with empty guts between day and
night were also examined with paired Student’s t-tests.
Paired Student’s t-tests were performed with the R#
2.12.1 software package (The R Foundation for Statistical
Computing).
The percent composition of the prey assemblage and
the diet of M. leidyi during the day and night were
compared with a two-way, crossed analysis of similarities
(ANOSIM) based on the Bray – Curtis similarity measure.
ANOSIM tests for differences between groups of samples
using a nonparametric permutation procedure, and is
analogous to a multivariate analysis of variance (Clarke
and Green, 1988). A multidimensional scaling (MDS)
plot, also based on the Bray – Curtis similarity measure,
was then used to graphically display the observed differences. The more similar samples were to one another,
the closer they appeared in the MDS plot. If ANOSIM
detected differences, an analysis of similarity percentages
(SIMPER) was performed to determine the relative contribution of individual prey categories to the similarity/
dissimilarity within and among samples (Clarke and
Gorley, 2006). ANOSIM, MDS and SIMPER were
Table I: Sampling dates, day and night depth (m) (mean + 95% CI), surface water temperatures (8C)
(mean + 95% CI) and Mnemiopsis leidyi total lengths (cm) (mean + 95% CI)
Depth (m)
Surface temperature (8C)
Ctenophore total length
(cm)
Study number
Sampling dates
Day
Night
Day
Night
Day
Night
1
2
3
4
5
6
7
7– 8 August 2003
21 –22 August 2003
6– 7 July 2004
27 –28 July 2004
17 –18 August 2004
11 –12 September 2004
2– 3 October 2004
7.5 + 1.7
6.3 + 0.6
4.9 + 1.0
5.3 + 0.5
7.3 + 3.1
6.0 + 0.0
6.3 + 0.5
8.3 + 1.3
7.1 + 1.2
5.3 + 0.7
5.7 + 0.7
8.5 + ND
5.8 + 0.9
6.0 + 0.0
23.6 + 0.6
25.8 + 0.9
20.1 + 0.6
21.6 + 1.0
21.5 + 1.2
21.5 + 1.6
19.2 + 0.5
23.3 + 0.3
24.5 + 0.4
20.1 + 0.3
21.8 + 0.5
21.5 + 0.7
20.8 + 0.3
18.8 + ND
2.4 + 2.6
3.6 + 3.4
1.2 + 2.2
1.1 + 0.8
1.4 + 1.5
1.8 + 2.5
1.8 + 2.6
2.4 + 2.5
3.0 + 3.3
1.5 + 2.9
1.1 + 0.7
1.3 + 1.9
2.0 + 2.6
1.0 + 1.6
ND, no data.
1300
Table II: Mean (+95% CI) abundances of zooplankton in Mnemiopsis leidyi guts (number ctenophore21) during the day and night of each
study
1
2
3
4
7 –8 August 2003
21 –22 August 2003
6 –7 July 2004
27 –28 July 2004
Day
Night
Day
Night
Day
Night
Tintinnid ciliates
Rotifers
Scyphozoan medusae
Hydrozoan medusae
Chaetognaths
Mollusc veligers
Polychaete larvae
Copepod nauplii
Calanoid copepods
Cyclopoid copepods
Poecilostomatoid copepods
Harpacticoid copepods
Isopods
Amphipods
Barnacle larvae
Cladocerans
Cumaceans
Crab larvae
Decapod shrimp larvae
Mantis shrimp larvae
Echinoderm pluteus larvae
Ascidian tadpole larvae
Larvaceans
Fish eggs
–
–
–
–
–
0.38 + 0.33
–
–
3.25 + 5.89
–
–
0.03 + 0.05
–
0.01 + 0.02
0.09 + 0.14
–
–
0.41 + 0.35
–
–
–
–
0.19 + 0.37
0.01 + 0.02
0.03 + 0.03
–
–
–
–
0.48 + 0.33
–
–
0.68 + 0.57
–
–
0.03 + 0.03
–
0.15 + 0.25
0.07 + 0.07
–
–
0.78 + 0.54
–
–
–
–
0.02 + 0.03
0.02 + 0.03
0.94 + 0.89
–
–
–
–
0.43 + 0.38
–
0.06 + 0.11
0.09 + 0.13
0.01 + 0.02
–
0.08 + 0.06
–
–
0.04 + 0.02
0.03 + 0.04
–
0.52 + 0.35
–
–
–
0.16 + 0.26
–
–
1.17 + 1.03
–
–
–
–
0.15 + 0.13
0.02 + 0.04
0.01 + 0.02
0.06 + 0.06
–
–
0.14 + 0.12
–
0.06 + 0.04
–
–
–
0.72 + 0.07
–
0.02 + 0.04
–
0.01 + 0.02
–
–
–
–
–
–
–
0.45 + 0.38
–
0.02 + 0.03
0.46 + 0.32
–
–
0.06 + 0.09
–
0.01 + 0.02
0.05 + 0.07
0.04 + 0.07
–
0.18 + 0.11
–
–
–
–
–
0.01 + 0.02
–
–
–
–
–
0.57 + 0.66
–
–
0.85 + 1.37
0.02 + 0.03
–
0.10 + 0.15
–
0.03 + 0.03
0.12 + 0.13
–
–
0.20 + 0.34
–
–
–
–
–
0.05 + 0.06
0.06 + 0.05
–
–
–
–
0.60 + 0.30
–
0.03 + 0.03
0.01 + 0.02
–
–
0.03 + 0.05
–
–
–
–
–
0.04 + 0.05
–
–
–
0.03 + 0.05
–
–
0.27 + 0.21
–
–
–
–
1.48 + 0.09
–
0.03 + 0.07
0.17 + 0.09
–
–
0.05 + 0.10
–
0.02 + 0.03
0.02 + 0.03
–
–
0.07 + 0.07
–
0.02 + 0.03
–
–
–
–
Taxon
5
17 –18 August 2004
Day
Night
6
11 –12 September 2004
Day
Night
7
2 –3 October 2004
Day
Night
Tintinnid ciliates
Rotifers
Scyphozoan medusae
Hydrozoan medusae
Chaetognaths
Mollusc veligers
Polychaete larvae
Copepod nauplii
Calanoid copepods
Cyclopoid copepods
Poecilostomatoid copepods
Harpacticoid copepods
0.31 + 0.37
0.15 + 0.14
–
–
–
0.07 + 0.09
–
0.17 + 0.25
0.42 + 0.42
0.01 + 0.02
–
0.01 + 0.02
0.08 + 0.03
0.02 + 0.03
–
–
–
0.66 + 0.46
–
0.25 + 0.27
1.10 + 1.52
–
–
0.17 + 0.10
0.53 + 0.42
0.01 + 0.02
–
–
–
1.64 + 0.90
0.01 + 0.02
0.24 + 0.14
0.34 + 0.40
–
–
0.02 + 0.05
0.14 + 0.11
–
–
–
–
0.70 + 0.55
0.03 + 0.03
0.17 + 0.17
0.28 + 0.24
–
–
0.15 + 0.17
0.03 + 0.05
–
–
–
–
0.62 + 0.53
–
0.15 + 0.11
0.05 + 0.09
–
–
0.99 + 0.94
0.11 + 0.17
–
–
–
–
1.82 + 1.11
–
0.21 + 0.17
0.97 + 0.51
–
–
0.41 + 0.33
Continued
DIEL FEEDING BY THE CTENOPHORE MNEMIOPSIS LEIDYI
Night
j
Day
L. J. SULLIVAN
1301
Taxon
JOURNAL OF PLANKTON RESEARCH
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VOLUME 36
Night
–
0.02 + 0.03
0.02 + 0.03
–
–
0.28 + 0.14
0.03 + 0.06
0.02 + 0.03
–
–
0.02 + 0.03
–
White rows contain zooplankton present in the water column and in ctenophore guts. Grey rows contain zooplankton present only in the water column.
–
–
0.02 + 0.03
–
–
0.12 + 0.15
–
–
–
–
–
–
Isopods
Amphipods
Barnacle larvae
Cladocerans
Cumaceans
Crab larvae
Decapod shrimp larvae
Mantis shrimp larvae
Echinoderm pluteus larvae
Ascidian tadpole larvae
Larvaceans
Fish eggs
–
–
0.04 + 0.07
–
–
0.04 + 0.02
–
–
–
–
0.01 + 0.02
–
Day
Day
Taxon
0.02 + 0.03
0.02 + 0.03
0.02 + 0.03
–
0.13 + 0.25
0.13 + 0.26
–
0.03 + 0.06
–
–
–
–
–
0.04 + 0.05
0.04 + 0.07
–
–
–
–
–
–
0.03 + 0.05
–
–
–
–
0.04 + 0.05
–
–
–
–
–
–
–
–
–
Day
Day
21 –22 August 2003
7 –8 August 2003
Night
2
Night
6 –7 July 2004
j
PAGES 1298 – 1309
j
2014
R E S U LT S
Night
27 –28 July 2004
4
3
NUMBER 5
performed with the PRIMER# 6.1 software package
(Primer-E, Plymouth, UK).
1
Table II: Continued
j
The following did not differ significantly between day
and night: depth (6 + 2 m mean + 95% CI, paired
Student’s t-test: df ¼ 6, t ¼ 22.14, P ¼ 0.08); temperature (22 + 28C, paired Student’s t-test: df ¼ 6, t ¼ 1.84,
P ¼ 0.11); ctenophore total length (2 + 5 cm, paired
Student’s t-test: df ¼ 6, t ¼ 0.93, P ¼ 0.39); total number
of prey L21 (16 + 25 L21, paired Student’s t-test: df ¼ 6,
t ¼ 20.06, P ¼ 0.96); and total number of prey consumed per ctenophore (2 + 15 ctenophore21, paired
Student’s t-test: df ¼ 6, t ¼ 20.77, P ¼ 0.47). The
percent of ctenophores with empty guts was significantly
higher during the day than at night (49 + 42% and
29 + 29% respectively, paired Student’s t-test: df ¼ 6,
t ¼ 5.32, P , 0.01).
Mnemiopsis leidyi consumed tintinnid ciliates, rotifers,
mollusc veligers, polychaete larvae, the copepodid and
naupliar stages of calanoid, cyclopoid and harpacticoid
copepods, isopods, amphipods, barnacle larvae, cladocerans, cumaceans, crab larvae, decapod shrimp larvae,
mantis shrimp larvae, ascidian larvae, larvaceans and
fish eggs (Table II). Scyphomedusae, hydromedusae,
chaetognaths, poecilostomatoid copepods and echinoderm pluteus larvae were present in the water column,
but were not consumed (Tables II and III). All prey consumed were present in the water column during both day
and night, except mantis shrimp larvae, which occurred
only at night (Tables II and III). All prey consumed were
present in ctenophore guts during both day and night,
except isopods, cumaceans, decapod shrimp larvae and
mantis shrimp larvae, which were ingested only at night
(Table II).
There was no significant day – night difference in the
percent composition of M. leidyi gut contents or the prey
assemblage between day and night (two-way ANOSIM,
global R ¼ 20.11, P ¼ 0.97). This appears in the MDS
plot as a lack of spatial separation between day (triangle)
and night (circle) samples (Fig. 1). However, there was a
significant difference in the percent composition of
M. leidyi gut contents and the prey assemblage (two-way
ANOSIM, global R ¼ 0.61, P ¼ 0.001). This appears in
the MDS plot as a clear spatial separation between gut
(closed symbols) and water (open symbols) samples
(Fig. 1). SIMPER analysis indicated that tintinnid ciliates,
veligers, polychaete larvae, copepod nauplii, calanoid
copepods, harpacticoid copepods, crab larvae and ascidian larvae accounted for 90% of the dissimilarity in the
percent composition of species between ctenophore guts
1302
Table III: Mean (+95% CI) abundances of zooplankton in the water column (number L21) during the day and night of each study
1
2
3
4
7–8 August 2003
21 –22 August 2003
6– 7 July 2004
27 – 28 July 2004
Day
Night
Day
Night
Day
Night
Tintinnid ciliates
Rotifers
Scyphozoan medusae
Hydrozoan medusae
Chaetognaths
Mollusc veligers
Polychaete larvae
Copepod nauplii
Calanoid copepods
Cyclopoid copepods
Poecilostomatoid copepods
Harpacticoid copepods
Isopods
Amphipods
Barnacle larvae
Cladocerans
Cumaceans
Crab larvae
Decapod shrimp larvae
Mantis shrimp larvae
Echinoderm pluteus larvae
Ascidian tadpole larvae
Larvaceans
Fish eggs
5.24 + 6.49
–
–
–
0.001 + 0.002
0.60 + 0.47
0.29 + 0.03
16.39 + 11.81
1.20 + 1.78
0.12 + 0.15
–
0.96 + 0.72
–
0.01 + 0.01
0.18 + 0.11
–
–
0.02 + 0.01
–
–
–
0.28 + 0.32
0.06 + 0.07
0.003 + 0.004
2.00 + 1.52
–
–
–
0.002 + 0.002
0.49 + 0.29
0.29 + 0.35
11.04 + 8.46
3.04 + 2.71
0.12 + 0.06
–
2.36 + 2.54
–
0.01 + 0.01
0.24 + 0.21
–
–
0.14 + 0.14
0.01 + 0.01
0.001 + 0.001
–
0.11 + 0.13
0.07 + 0.06
0.002 + 0.002
15.95 + 10.04
0.08 + 0.08
–
–
–
0.28 + 0.09
0.15 + 0.11
6.75 + 1.58
0.52 + 0.45
0.15 + 0.14
–
0.28 + 0.19
–
0.001 + 0.001
0.08 + 0.14
–
–
0.10 + 0.10
–
–
0.001 + 0.002
0.05 + 0.08
0.001 + 0.001
–
14.31 + 9.59
0.14 + 0.15
–
–
–
0.15 + 0.11
0.22 + 0.16
8.14 + 3.44
1.18 + 0.69
0.10 + 0.08
–
0.75 + 0.38
0.001 + 0.001
0.002 + 0.002
–
–
–
0.05 + 0.03
0.002 + 0.003
–
–
0.08 + 0.06
0.01 + 0.01
0.01 + 0.01
–
–
0.001 + 0.002
–
0.001 + 0.002
0.08 + 0.04
0.14 + 0.12
0.16 + 0.12
0.17 + 0.12
0.03 + 0.02
0.005 + 0.002
0.11 + 0.09
–
–
0.04 + 0.02
–
–
0.01 + 0.01
0.001 + 0.003
–
0.002 + 0.003
0.01 + 0.01
–
0.01 + 0.01
0.001 + 0.003
–
–
–
–
0.17 + 0.25
0.09 + 0.11
0.11 + 0.07
0.15 + 0.12
0.05 + 0.07
0.006 + 0.002
0.14 + 0.03
–
0.006 + 0.002
0.03 + 0.02
–
0.002 + 0.002
0.01 + 0.01
0.01 + 0.01
–
0.001 + 0.003
0.01 + 0.01
0.001 + 0.003
0.01 + 0.01
0.66 + 0.52
0.07 + 0.14
–
–
0.001 + 0.002
0.78 + 0.63
0.18 + 0.18
1.65 + 1.28
0.36 + 0.52
0.08 + 0.05
–
0.09 + 0.08
0.004 + 0.008
–
0.09 + 0.10
–
–
0.02 + 0.02
0.001 + 0.002
–
–
0.57 + 0.58
0.001 + 0.002
–
0.77 + 0.93
0.04 + 0.04
–
–
–
1.20 + 1.29
0.08 + 0.04
1.27 + 1.19
0.45 + 0.39
0.09 + 0.05
–
0.29 + 0.57
0.002 + 0.002
0.005 + 0.006
0.01 + 0.01
–
–
0.06 + 0.05
0.005 + 0.009
–
–
0.58 + 0.41
–
0.002 + 0.004
Taxon
5
17– 18 August 2004
Day
6
11 –12 September 2004
Day
Night
7
2– 3 October 2004
Day
Night
15.19 + 13.78
0.32 + 0.25
–
–
–
3.28 + 2.88
0.45 + 0.18
13.37 + 10.71
0.63 + 0.24
0.09 + 0.03
–
0.74 + 0.46
–
0.22 + 0.24
0.06 + 0.07
–
–
–
0.51 + 0.71
0.71 + 1.01
5.60 + 6.44
0.67 + 0.44
0.18 + 0.17
–
2.06 + 0.60
–
0.12 + 0.09
–
–
–
–
0.52 + 0.54
0.43 + 0.32
7.34 + 8.65
1.24 + 1.41
0.21 + 0.25
–
4.07 + 0.99
–
Tintinnid ciliates
Rotifers
Scyphozoan medusae
Hydrozoan medusae
Chaetognaths
Mollusc veligers
Polychaete larvae
Copepod nauplii
Calanoid copepods
Cyclopoid copepods
Poecilostomatoid copepods
Harpacticoid copepods
Isopods
Night
1.89 + 1.13
1.07 + 1.29
6.72 + 7.14
0.08 + 0.08
0.29 + 0.18
0.16 + 0.09
4.61 + 3.53
2.27 + 1.60
0.31 + 0.37
–
0.002 + 0.002
–
1.87 + 1.42
0.48 + 0.53
7.78 + 7.26
6.47 + 3.63
0.74 + 0.66
–
0.95 + 0.69
0.004 + 0.005
–
–
–
–
0.36 + 0.30
0.003 + 0.004
5.32 + 1.39
0.29 + 0.29
–
–
–
2.04 + 0.36
0.58 + 0.14
11.14 + 5.98
1.64 + 0.65
0.10 + 0.01
–
1.84 + 0.93
–
Continued
DIEL FEEDING BY THE CTENOPHORE MNEMIOPSIS LEIDYI
Night
j
Day
L. J. SULLIVAN
1303
Taxon
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PAGES 1298 – 1309
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White rows contain zooplankton present in the water column and in ctenophore guts. Grey rows contain zooplankton present only in the water column.
0.001 + 0.002
0.012 + 0.004
0.003 + 0.003
0.002 + 0.003
0.02 + 0.02
–
–
0.006 + 0.004
3.10 + 2.86
0.01 + 0.01
–
0.01 + 0.01
0.0023 + 0.0003
0.0004 + 0.0008
–
0.15 + 0.10
0.002 + 0.004
–
–
0.38 + 0.34
0.001 + 0.003
0.001 + 0.002
Amphipods
Barnacle larvae
Cladocerans
Cumaceans
Crab larvae
Decapod shrimp larvae
Mantis shrimp larvae
Echinoderm pluteus larvae
Ascidian tadpole larvae
Larvaceans
Fish eggs
0.001 + 0.001
0.02 + 0.03
–
–
0.05 + 0.01
0.0005 + 0.0009
–
–
0.07 + 0.05
0.001 + 0.001
–
Day
Taxon
Day
Night
0.007 + 0.001
0.02 + 0.01
0.004 + 0.005
0.02 + 0.03
0.03 + 0.04
0.001 + 0.002
–
–
1.57 + 0.21
0.004 + 0.005
0.001 + 0.002
–
0.02 + 0.01
–
0.001 + 0.002
–
–
–
0.004 + 0.005
0.28 + 0.38
0.02 + 0.01
–
0.01 + 0.01
0.04 + 0.05
0.002 + 0.004
0.003 + 0.007
0.003 + 0.004
0.003 + 0.004
–
–
0.16 + 0.18
0.01 + 0.01
0.001 + 0.002
Day
Day
6– 7 July 2004
21 –22 August 2003
7–8 August 2003
1
Table III: Continued
Night
3
2
Night
27 – 28 July 2004
4
Night
JOURNAL OF PLANKTON RESEARCH
Fig. 1. Similarity between the percent composition of Mnemiopsis leidyi
gut contents and the prey assemblage during day and night. The graph
was constructed with non-metric MDS from a similarity matrix based
on the Bray– Curtis similarity measure (Primer v6). Stress ¼ 0.15. The
axes of MDS plots do not have units. Closed triangles represent the
combined prey composition of ctenophore guts during the day. Open
triangles represent the combined prey composition in the water column
during the day. Closed circles represent the combined prey composition
of ctenophore guts during the night. Open circles represent the
combined prey composition in the water column during the night.
Fig. 2. Daily percent difference in prey composition between
Mnemiopsis leidyi guts and the water column. Boxplots represent the
mean (closed circle), median (line) and quartiles (box). The upper and
lower whiskers extend to the highest and lowest value that is within 1.5
times the inter-quartile range of the corresponding quartile. Data
beyond the end of the whiskers are considered outliers (open circles)
(Tukey, 1977).
and the water column. Mnemiopsis leidyi selected for veligers, calanoid copepods and crab larvae, and selected
against tintinnid ciliates, polychaete larvae, copepod
nauplii, harpacticoid copepods and ascidian larvae
(Fig. 2).
Although overall trends showed no specific day– night
differences in the percent composition, the proportion of
some prey categories in ctenophore guts and the prey
1304
L. J. SULLIVAN
j
DIEL FEEDING BY THE CTENOPHORE MNEMIOPSIS LEIDYI
Fig. 3. Percent composition of the prey assemblage (black) and gut contents of Mnemiopsis leidyi (gray) over time: (a) tintinnid ciliates, (b) rotifers, (c)
mollusc veligers, (d) polychaete larvae, (e) copepod nauplii, (f ) calanoid copepods, (g) cyclopoid copepods, (h) harpacticoid copepods, (i) isopods,
( j) amphipods, (k) barnacle larvae, (l) cladocerans, (m) cumaceans, (n) crab larvae, (o) decapod shrimp larvae, ( p) mantis shrimp larvae, (q)
ascidian tadpole larvae, (r) larvaceans, and (s) fish eggs. Boxplots represent the mean (closed circle), median (line) and quartiles (box). The upper
and lower whiskers extend to the highest and lowest value that is within 1.5 times the inter-quartile range of the corresponding quartile. Data
beyond the end of the whiskers are considered outliers (open circles) (Tukey, 1977).
assemblage varied over the diel cycle (Fig. 3). The proportion of tintinnid ciliates, rotifers, veligers, polychaete
larvae, copepod nauplii, calanoid copepods, cyclopoid
copepods, barnacle larvae, cladocerans, ascidian larvae,
larvaceans and fish eggs in ctenophore guts and the prey
assemblage exhibited no obvious diel patterns (Fig. 3).
The proportion of harpacticoid copepods, isopods,
amphipods, cumaceans, crab larvae, decapod shrimp
larvae and mantis shrimp larvae in ctenophore guts and
in the prey assemblage peaked during the night (Fig. 3).
DISCUSSION
The total number of identified prey in ctenophore guts
and the water column did not differ between day and
night. Additionally, no day– night patterns were observed
in the specific composition of the prey assemblage or the
diet of M. leidyi, indicating the absence of a diel cycle in
prey abundance or ctenophore feeding activity. Despite
the overall lack of a diel feeding pattern in prey composition, isopods, cumaceans, decapod shrimp larvae and
mantis shrimp larvae were observed in ctenophore guts
only at night. However, even when present, the abundances of these prey categories in the assemblage and in
ctenophore guts were low, and they did not influence the
overall analysis. These data may support suggestions by
Kovalev et al. (Kovalev et al., 1996) that maximum
feeding of M. leidyi occurs at night if the reported
maximum was due to changes in prey availability, rather
than changes in feeding rate. As a result, in ecosystems
where prey availability changes markedly over the diel
cycle, surveys of M. leidyi feeding should include nighttime sampling.
The total prey abundance and number of prey consumed per ctenophore did not differ between day and
1305
JOURNAL OF PLANKTON RESEARCH
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VOLUME 36
night; however, the percent of ctenophores with empty
guts was higher during the day. These data suggest that,
although fewer ctenophores consumed prey during the
day, those that did consumed a larger number than at
night. Despite being transparent, M. leidyi has been
reported to elicit a shadow response in some prey
(Forward, 1976). Decreases in encounter rates as the
result of a shadow response could account for the
observed decrease in feeding incidence during the day.
Nevertheless, predator avoidance cannot account for the
suggested daytime increase in the number of prey consumed. Interactions with daytime aggregations of prey,
which are common among pelagic invertebrates (Ritz,
1994), would increase encounter rates of ctenophores
with prey. As a result, increases in the number of prey
ingested would only occur in ctenophores that encountered aggregations.
The present study is the first report of mantis shrimp
larvae in the guts of M. leidyi. Many of the other prey categories observed are known to be common components
of the diet including tintinnid ciliates, veligers, the copepodid and naupliar stages of copepods, barnacle larvae,
cladocerans and crab larvae (Burrell and Van Engel,
1976; Larson, 1987; Tsikhon-Lukanina et al., 1991, 1992;
Mutlu, 1999; Purcell and Decker, 2005; Javidpour et al.,
2009). Rare instances of predation on isopods, amphipods, cumaceans and decapod shrimp have also been
reported (Burrell and Van Engel, 1976; Larson, 1987;
Tsikhon-Lukanina et al., 1992). Prey categories of M. leidyi
reported previously, but not consumed in this study,
include diatoms, flagellates, aloricate ciliates, planula
larvae, chaetognaths, other ctenophores, ostracods,
mysids, tanaids and fish larvae (Burrell and Van Engel,
1976; Larson, 1987; Tsikhon-Lukanina et al., 1992;
Mutlu, 1999; Purcell and Decker, 2005; Javidpour et al.,
2009; Sullivan, 2010). Chaetognaths were present in the
water column during this study, but in low abundance.
All of the other missing prey categories occur in
Narragansett Bay; however, sampling may not have overlapped temporally or spatially with their distributions.
Additionally, small soft-bodied prey, such as aloricate ciliates, may be digested too rapidly (,2 min) for consumption to be observed using gut content analysis (Sullivan,
2010).
Ctenophore feeding rates increase with size
(Monteleone and Duguay, 1988; Sullivan and Gifford,
2004), and diet composition and capture efficiency also
change during development (Rapoza et al., 2005;
Waggett and Sullivan, 2006). Specifically, M. leidyi have
been reported to shift from a diet dominated by protistan
microplankton to a more diverse diet of metazoan mesoplankton during the transition from the cydippid to
lobate stage (Rapoza et al., 2005). Additionally, capture
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PAGES 1298 – 1309
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2014
efficiency of metazoans, including nauplii and copepods,
within the cydippid stage increases with size until reaching a maximum; and ctenophores ,0.80 mm are incapable of consuming copepods (Waggett and Sullivan,
2006). Differences in size, and potentially stage, among
sampling dates in this study may account for some of the
variability observed in the number of prey items consumed or the percent composition of ctenophore gut contents. However, ctenophore size, and thus stage, did not
differ between day and night, and are unlikely to have
influenced our day – night analysis. Similarly, ctenophore
feeding rates increase with temperature (Kremer, 1979).
Although water temperature varied among sampling
dates, there was also no day – night difference in water
temperature.
Positive selection of veligers and calanoid copepods,
and negative selection of tintinnid ciliates and copepod
nauplii have been reported previously in M. leidyi (Burrell
and Van Engel, 1976; Larson, 1987; Sullivan and
Gifford, 2004). These differences in selection are likely
the result of the lower encounter rates with less active
prey categories (Larson, 1987; Waggett and Costello,
1999). Strong positive selection for crab larvae has not
previously been reported, and may have resulted from
their extremely long digestion times, which can range
from 3 to 6 h (Chang, 2004). The same may also be true
for veligers, which also have longer digestion times
(2 h) than most other prey categories (Chang, 2004;
Sullivan, 2010).
No overall temporal difference was observed in the
specific composition of the prey assemblage or ctenophore guts. Narragansett Bay is a shallow (8.3 m) weakly
stratified estuary (Pilson, 1985). This may result in fairly
even distributions of plankton, including M. leidyi
(Kremer and Nixon, 1976). However, some patterns were
observed within individual prey categories. The most
obvious difference was due to the presence of mantis
shrimp larvae in the water column and in ctenophore
guts only at night. Additionally, although isopods, cumaceans and decapod shrimp larvae were present in the
water column during both day and night, they were
observed in ctenophore guts only at night when their
abundance increased. The proportion of harpacticoid
copepods, amphipods and crab larvae in the water
column and in ctenophore guts also increased at night.
Nocturnal demersal zooplankton, including mantis
shrimp larvae, are inactive during the day, resting on the
bottom or attached to substrates, and emerge into the
water column at night (Reaka and Manning, 1981).
Patterns of daily emergence/dispersal are well documented for other benthic marine invertebrates, including harpacticoid copepods, isopods, amphipods, cumaceans and
decapod larvae (Saigusa, 2001), and are probably a
1306
L. J. SULLIVAN
j
DIEL FEEDING BY THE CTENOPHORE MNEMIOPSIS LEIDYI
mechanism for avoiding predation (Robertson and
Howard, 1978; Alldredge and King, 1985). Nocturnal
demersal zooplankton can be important components of
coastal marine ecosystems. They are often major contributors to the diets of both bottom and midwater feeding
fish (Robertson and Howard, 1978; Marnane and
Bellwood, 2002), and can be economically important
themselves as adults, specifically decapods. Because the
majority of studies documenting feeding by M. leidyi have
been performed during daylight hours, reports of nocturnal demersal zooplankton in ctenophore guts are rare.
Nocturnal demersal zooplankton have the potential to
be important undocumented components of the diet of
M. leidyi, and will be observed only if sampling is performed over the entire diel cycle. In this study, even when
present in the water column, nocturnal demersal zooplankton, including isopods, amphipods, cumaceans and
mantis shrimp larvae, were rare (0.01 L21). As a result,
they did not contribute significantly to diet composition
in this study, but they may be important dietary components at times of year or in locations where they are more
abundant. Other potential nocturnal demersal zooplankton that might have been missed in this study include
mysids, ostracods and tanaids, which have previously
been reported in the guts of M. leidyi, as well as lobster
larvae, which have not be reported in the guts of M. leidyi
or any other gelatinous zooplankton.
The nighttime ingestion of nocturnal demersal zooplankton by gelatinous species, including hydromedusae
and scyphomedusae, has been noted in other studies
(Mills, 1983; Arkett, 1984; Olesen et al., 1994; Pitt et al.,
2008), and may contribute significantly to diet. Pitt et al.
(Pitt et al., 2008) reported that the scyphomedusa,
C. mosaicus, consistently derived most of its carbon from
nocturnal demersal zooplankton, including emergent
copepods, decapod shrimp (Lucifer sp.) and mysids.
Similarly, Olesen et al. (Olesen et al., 1994) suggested that
increased consumption of harpacticoid copepods at
night, when their abundance in the water column
increased, could account for discrepancies between prey
abundance and growth of the scyphomedusa, A. aurita.
The consumption of nocturnal demersal zooplankton
could be especially advantageous when daytime prey
biomass is low, or when relatively large taxa are consumed. Thus, some estimate of the prevalence of nocturnal demersal zooplankton should be made before relying
solely on daytime collections to estimate diet composition
and carbon ingestion by M. leidyi.
In conclusion, no overall day –night differences were
observed in the composition of the prey assemblage or
diet of M. leidyi. In spite of this, the taxonomic composition of ctenophore guts and the prey field differed over
the diel cycle. The most obvious difference was due to
the presence of mantis shrimp larvae in the water column
and in ctenophore guts only at night. These observations
suggest that it may not be necessary to examine ctenophore gut contents over the diel cycle in locations where
the day and night prey distributions are the same.
However, when estimating predator impacts or defining
the diet of M. leidyi, specific prey items may be missed entirely if sampling does not occur over the entire diel cycle.
AC K N OW L E D G E M E N T S
The research reported here was performed in partial fulfillment of the requirements for the degree of Doctor of
Philosophy at the University of Rhode Island’s Graduate
School of Oceanography, Narragansett, RI, USA. I
thank J.H. Costello, D.J. Gifford, A. Slaughter,
B.K. Sullivan and two anonymous reviewers for their
helpful comments regarding the manuscript. I thank
J. Heltshe, W. Kimmerer, N. Miller and J. Moderan for
statistical advice. Additionally, I am grateful to A. Allen,
M.B. Heaton, R.A. Thibeault and R.J. Waggett for help
with overnight sampling, and D.E. Van Keuren for assistance with zooplankton identification.
FUNDING
This work was partially supported by an award from the
National Science Foundation (OCE-0115177) to B.K.
Sullivan and D. J. Gifford.
REFERENCES
Alldredge, A. L. and King, J. M. (1985) The distance demersal zooplankton migrate above the benthos: implications for predation. Mar.
Biol., 84, 253– 260.
Anderson, E. (1974) Trophic Interactions among Ctenophores and
Copepods in St. Margaret’s Bay, Nova Scotia. PhD dissertation,
Dalhousie University, Halfax, Nova Scotia.
Arkett, S. A. (1984) Diel vertical migration and feeding behavior of a demersal hydromedusan (Polyorchis penicillatus). Can. J. Fish. Aquat. Sci.,
41, 1837–1843.
Aronova, M. Z. (1979) Electron microscopic study of presumptive
photoreceptor cells in the aboral organ of the ctenophore, Beroe
cucumis. Zh. Evol. Biokhim. Fiziol., 15, 596–601.
Benović, A., Lučić, D., Onofri, V. et al. (2005) Bathymetric distribution
of medusae in the open waters of the middle and south Adriatic Sea
during spring 2002. J. Plankton Res., 27, 79–89.
Burrell, V. G. and Van Engel, W. A. (1976) Predation by and distribution
of a ctenophore, Mnemiopsis leidyi A. Agassiz, in the York River
Estuary. Est. Coast. Mar. Sci., 4, 235– 242.
1307
JOURNAL OF PLANKTON RESEARCH
j
VOLUME 36
Carr, E. F. and Pitt, K. A. (2008) Behavioural responses of zooplankton
to the presence of predatory jellyfish. J. Exp. Mar. Biol. Ecol., 354,
101–110.
Chang, H. (2004) Studies on the digestion rates of the lobate ctenophore, Mnemiopsis leidyi A. Agassiz (Ctenophora, Lobata). MS thesis,
University of Rhode Island, Kingston, RI.
Clarke, K. R. and Gorley, R. N. (2006) PRIMER v6: User Manual/
Tutorial. Plymouth Marine Laboratories, Plymouth.
Clarke, K. R. and Green, R. H. (1988) Statistical design and analysis
for a “biological effects’ study. Mar. Ecol. Prog. Ser., 46, 213–226.
Fancett, M. S. and Jenkins, G. P. (1988) Predatory impact of scyphomedusae on ichthyoplankton and other zooplankton in Port Phillip Bay.
J. Exp. Mar. Biol. Ecol., 116, 63–77.
Forward, R. B. (1976) A shadow response in a larval crustacean. Biol.
Bull. (Woods Hole), 151, 126– 140.
Freeman, G. and Reynolds, G. T. (1973) The development of bioluminescence in the ctenophore Mnemiopsis leidyi. Dev. Biol., 31,
61– 100.
Fuller, J. L. (1937) The feeding of Calanus pacificus in relation to environmental conditions. Biol. Bull. (Woods Hole), 72, 233– 246.
Gauld, J. L. (1953) Diurnal variation in the grazing of planktonic copepods. J. Mar. Biol. Assoc. UK, 31, 461– 473.
Gerber, R. P. (2000) An Identification Manual to the Coastal and Estuarine
Zooplankton of the Gulf of Maine Region From Passamaquoddy Bay to Long
Island Sound. Acadia Productions, Brunswick, ME.
Gurney, L. J., Froneman, P. W., Pakhomov, E. A. et al. (2002) Diel
feeding patterns and daily ration estimates of three subantarctic
euphausiids in the vicinity of the Prince Edward Islands (Southern
Ocean). Deep-Sea Res. II, 35, 222– 225.
Haney, J. F. (1988) Diel patterns of zooplankton behavior. Bull. Mar. Sci.,
43, 583–603.
Haraldsson, M., Båmstedt, U., Tiselius, P. et al. (2014) Evidence of diel
vertical migration in Mnemiopsis leidyi. PLoS ONE, 9, e86595.
Hirota, J. (1974) Quantitative natural history of Pleurobrachia bachei in La
Jolla Bight. Fish. Bull., 72, 295–335.
Horridge, G. A. (1964) Presumed photoreceptive cilia in a ctenophore.
Quart. J. Micr. Sci., 105, 311– 317.
Javidpour, J., Molinero, J. C., Lehmann, A. et al. (2009) Annual assessment of the predation of Mnemiopsis leidyi in a new invaded environment, the Kiel Fjord (Western Baltic Sea): a matter of concern?
J. Plankton Res., 31, 729 –738.
Kouassi, E., Pagano, M., Saint-Jean, L. et al. (2001) Vertical migrations
and feeding rhythms of Acartia clausi and Pseudodiaptomus hessei
(Copepods: Calanoida) in a tropical lagoon (Ebrié, Côte d’Ivoire).
Est. Coast Shelf Sci., 52, 715– 728.
Kovalev, A. V., Saika, V. Y., Ostrovskaya, N. A. et al. (1996) Mnemiopsis
mccradyi, a new inhabitant of the Black Sea. Hydrobiol. J., 32, 25–29.
Kremer, P. (1979) Predation by the ctenophore Mnemiopsis leidyi in
Narragansett Bay, Rhode Island. Estuaries, 2, 97–105.
Kremer, P. (2005) Ingestion and elemental budgets for Linuche ungulculata,
a scyphomedusa with zooxanthellae. J. Mar. Biol. Assoc. UK, 85,
613–625.
j
NUMBER 5
j
PAGES 1298 – 1309
j
2014
Lee, J. J., Leedale, G. F. and Bradbury, P. (2000) An Illustrated Guide to the
Protozoa, Second Edition. Allen Press Inc., Lawrence, KS.
Mackie, G. O., Pugh, P. R. and Purcell, J. E. (1987) Siphonophore
biology. Adv. Mar. Biol., 24, 97–262.
Marnane, M. J. and Bellwood, D. R. (2002) Diet and nocturnal foraging
in cardinalfishes (Apogonidae) at One Tree Reef, Great Barrier Reef,
Australia. Mar. Ecol. Prog. Ser., 231, 261–268.
Martinussen, M. B. and Båmstedt, U. (1995) Diet, estimated daily food
ration and predator impact by the scyphozoan jellyfishes Aurelia aurita
and Cyanea capillata. In Skjoldal, H. R., Hopkins, C., Erikstad, K. E.
and Leinaas, H. P. (eds), Ecology of Fjords and Coastal Waters. Elsevier,
New York, NY, pp. 127 –145.
Mills, C. E. (1983) Vertical migration and diel activity patterns of hydromedusae: studies in a large tank. J. Plankton Res., 5, 619– 635.
Minkina, N. I. and Pavlova, E. V. (1995) Diurnal changes of the respiration rate in the comb jelly Mnemiopsis leidyi in the Black Sea.
Oceanology, 35, 222–225.
Monteleone, D. M. and Duguay, L. E. (1988) Laboratory studies of predation by the ctenophore Mnemiopsis leidyi on the early stages in the
life history of the bay anchovy, Anchoa mitchilli. J. Plankton Res., 10,
359 –372.
Mutlu, E. (1999) Distribution and abundance of ctenophores and their
zooplankton food in the Black Sea. 2. Mnemiopsis leidyi. Mar. Biol.,
135, 603– 613.
Olesen, N. J., Frandsen, K. and Riisgård, H. U. (1994) Population dynamics, growth and energetics of jellyfish Aurelia aurita in a shallow
fjord. Mar. Ecol. Prog. Ser., 105, 9 –18.
Pilson, M. E. Q. (1985) On the residence time of water in Narragansett
Bay. Estuaries, 8, 2 –14.
Pitt, K. A., Clement, A. L., Connolly, R. M. et al. (2008) Predation by
jellyfish on large and emergent zooplankton: implications for
benthic-pelagic coupling. Est. Coast. Shelf Sci., 76, 827 –833.
Postel, L., Fock, H. and Hagen, W. (2000) Biomass and abundance. In
Harris, R. P., Wiebe, P., Lenz, J., Skjoldal, H. R. and Huntley, M.
(eds), ICES Zooplankton Methodology Manual. Academic Press, London,
pp. 83–192.
Purcell, J. E. (1992) Effects of predation by the scyphomedusan Chrysaora
quinquecirrha on zooplankton populations in Chesapeake Bay, USA.
Mar. Ecol. Prog. Ser., 87, 65–76.
Purcell, J. E. and Decker, M. B. (2005) Effects of climate on relative predation by scyphomedusae and ctenophores on copepods in
Chesapeake Bay during 1987– 2000. Limnol. Oceanogr., 50, 376–387.
Purcell, J. E. and Nemazie, D. A. (1992) Quantitative feeding ecology of
the hydromedusan Nemposis bachei in Chesapeake Bay. Mar. Biol., 113,
305 –311.
Rapoza, R., Novak, D. and Costello, J. H. (2005) Life-stage dependent,
in situ dietary patterns of the lobate ctenophore Mnemiopsis leidyi
Agassiz 1865. J. Plankton Res., 27, 951–956.
Reaka, M. L. and Manning, R. B. (1981) The behavior of stomatopod
Crustacea and its relationship to rates of evolution. J. Crustac. Biol., 1,
309 –327.
Ritz, D. A. (1994) Social aggregations in pelagic invertebrates. Adv. Mar.
Biol., 30, 155– 216.
Kremer, P. and Nixon, S. (1976) Distribution and abundance of the
ctenophore, Mnemiopsis leidyi in Narragansett Bay. Est. Coast. Mar. Sci.,
4, 627– 639.
Robertson, A. I. and Howard, R. K. (1978) Diel trophic interactions
between vertically-migrating zooplankton and their fish predators in
an eelgrass community. Mar. Biol., 48, 207 –213.
Larson, R. J. (1987) In situ feeding rates of the ctenophore Mnemiopsis
mccradyi. Estuaries, 10, 87– 91.
Roe, H. S. J., James, P. T. and Thurston, M. H. (1984) The diel migrations and distributions within a mesopelagic community in the North
1308
L. J. SULLIVAN
j
DIEL FEEDING BY THE CTENOPHORE MNEMIOPSIS LEIDYI
East Atlantic. 6. Medusae, ctenophores, amphipods and euphausiids.
Prog. Oceanogr., 13, 425– 460.
Uye, S. and Shimauchi, H. (2005) Population biomass, feeding, respiration and growth rates, and carbon budget of the scyphomedusa
Aurelia aurita in the Inland Sea of Japan. J. Plankton Res., 27, 237– 248.
Saigusa, M. (2001) Daily rhythms of emergence of small invertebrates
inhabiting shallow subtidal zones: a comparative investigation at four
locations in Japan. Ecol. Res., 16, 1– 28.
Venrick, E. L. (1978) How many cells to count? In Sournia, A. (ed.),
Phytoplankton Manual. UNESCO, Paris, pp. 167–180.
Spadinger, R. and Maier, G. (1999) Prey selection and diel feeding of
the freshwater jellyfish, Craspedacusta sowerbyi. Freshw. Biol., 41,
567–573.
Waggett, R. and Costello, J. H. (1999) Capture mechanisms used by the
lobate ctenophore, Mnemiopsis leidyi, preying on the copepod Acartia
tonsa. J. Plankton Res., 21, 2037– 2052.
Sullivan, L. J. (2010) Gut evacuation of larval Mnemiopsis leidyi
A. Agassiz (Ctenophora, Lobata). J. Plankton Res., 32, 69–74.
Waggett, R. J. and Sullivan, L. J. (2006) Feeding efficiency of the larval
ctenophore Mnemiopsis leidyi A. Agassiz (Ctenophora, Lobata).
J. Plankton Res., 28, 719– 723.
Sullivan, L. J. and Gifford, D. J. (2004) Diet of the larval ctenophore
Mnemiopsis leidyi A. Agassiz (Ctenophora, Lobata). J. Plankton Res., 26,
417–431.
Tsikhon-Lukanina, E. A., Reznichenko, O. G. and Lukasheva, T. A.
(1991) Quantitative patterns of feeding of the Black Sea ctenophore
Mnemiopsis leidyi. Oceanology, 31, 196–199.
Tsikhon-Lukanina, Y. A., Reznichenko, O. G. and Lukasheva, T. A.
(1992) Diet of the ctenophore Mnemiopsis in inshore waters of the
Black Sea. Oceanology, 32, 496– 500.
Tukey, J. W. (1977) Exploratory Data Analysis. Addison-Wesley, Reading.
Wintzer, A. P. (2010) Ecology of non-native hydrozoans in the
San Francisco Estuary: implications for pelagic organism decline
fishes. PhD dissertation, University of California, Davis, CA.
Zaika, V. Y. and Revkov, N. K. (1995) Anatomy of the gonads and reproduction in Mnemiopsis ctenophores in the Black Sea. Hydrobiol. J., 31,
9 –14.
Zaika, V. Y. and Sergeyeva, N. G. (1992) Diurnal variations in population structure and vertical distribution of the ctenophore Mnemiopsis
maccradyi in the Black Sea. Hydrobiol. J., 28, 1 –6.
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