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JPR Advance Access published November 21, 2012
Journal of
Plankton Research
plankt.oxfordjournals.org
J. Plankton Res. (2012) 0(0): 1 – 7. doi:10.1093/plankt/fbs082
Predation by the scyphozoan Pelagia
noctiluca on Mnemiopsis leidyi ctenophores
in the NW Mediterranean Sea
UXUE TILVES1*, JENNIFER E. PURCELL2, MACARENA MARAMBIO1, ANTONIO CANEPA1, ALEJANDRO OLARIAGA1 AND
VERÓNICA FUENTES1
1
37-49 08003 BARCELONA, SPAIN AND 2SHANNON POINT MARINE CENTER,
1900 SHANNON POINT ROAD, ANACORTES, WA 98221, USA
INSTITUT DE CIENCIES DEL MAR, CSIC, P. MARÍTIM DE LA BARCELONETA,
WESTERN WASHINGTON UNIVERSITY,
*CORRESPONDING AUTHOR: [email protected]
Received March 19, 2012; accepted October 23, 2012
Corresponding editor: Marja Koski
The invasive ctenophore Mnemiopsis leidyi, which now may be established in the
NW Mediterranean, is a voracious predator of zooplankton and ichthyoplankton.
Pelagia noctiluca, an abundant scyphomedusa there, eats other gelatinous species.
We measured predation, digestion and escape when different sizes of medusae fed
on ctenophores. Clearance rates increased with predator size and ingestion rates
increased with prey concentration. Digestion times were longer when medusae
were smaller than the ctenophores. All large ctenophores escaped from the
medusae, but small ctenophores were ingested completely. Pelagia noctiluca is potentially an important predator of M. leidyi that may help control populations of this
ctenophore.
KEYWORDS: jellyfish; invasive; escape; functional response; feeding rates
The invasive ctenophore Mnemiopsis leidyi was reported
for the first time along the entire Catalan coast (Spain),
in the northwestern Mediterranean Sea in the summer
of 2009 (Fuentes et al., 2009). Its reappearance in large
numbers in subsequent years suggests its potential establishment (Marambio et al., unpublished data). This
ctenophore species has invaded all European seas
(reviewed in Costello et al., 2012) and it is known for
doi:10.1093/plankt/fbs082, available online at www.plankt.oxfordjournals.org
# The Author 2012. Published by Oxford University Press. All rights reserved. For permissions, please email: [email protected]
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and reduce capture stress. Adult medusae released
gametes in experimental aquaria at the Institut de
Ciències del Mar (ICM-CSIC) in Barcelona, Spain,
where ephyrae and juveniles were raised. Specimens of
Mnemiopsis leidyi were gently collected in jars from the
Ebro River Delta. Immediately after collection, specimens were transferred to 25-L plastic containers filled
with ambient seawater and transported to the
laboratory.
Specimens were kept 1 week before the experiments
in 200-L flow-through tanks with natural filtered seawater (temperature: 208C + 0.5, salinity: 37.8). These
conditions were maintained during the experiments.
Pelagia noctiluca medusae were fed daily with frozen crustaceans and fresh jellyfish, either Aurelia aurita or
Rhizostoma pulmo. Mnemiopsis leidyi individuals were fed
Artemia salina nauplii. Medusae were kept without food
for 24 h before the experiments.
To estimate the feeding rates of P. noctiluca, individual
medusae of different sizes and stages were incubated
with different concentrations of M. leidyi (Table I).
Experiments with adult and juvenile medusae were conducted in 100-L flow-through tanks with a water flow of
300 L h21. The ctenophore length (oral– aboral axis
including the lobes) was measured before each experiment; the bell diameter of P. noctiluca was measured after
each experiment to minimize stress to the animals.
Medusae were allowed 1 h to acclimatize until the tentacles were completely extended before incubations;
then the ctenophores were added to the experimental
tanks. Pelagia noctiluca ephyrae and M. leidyi larvae were
incubated together in 1.4-L bottles that were placed in
a plankton wheel to keep the organisms in suspension.
After incubation, the number of remaining ctenophores
was recorded. Controls ensured that the ctenophores
disappeared only due to the predation by the ephyrae.
New animals were used in each incubation. The
negative effects on the invaded ecosystems, including reduction and changed composition of the zooplankton,
and collapse of fisheries (Shiganova, 1998; Shiganova
and Bulgakova, 2000; Roohi et al., 2010; Riisgård et al.,
2011). Mnemiopsis leidyi has had devastating effects especially where no native predators were present, such as
in the Black and Caspian seas (Purcell et al., 2001).
Predators control the ctenophores to some degree in
native environments (Purcell et al., 2001); in fact M. leidyi
was controlled in the Black Sea (reviewed in Costello
et al., 2012) when Beroe ovata was accidentally introduced.
Moreover, Shiganova and Malej (Shiganova and Malej,
2009) suggested possible predatory control of M. leidyi by
Beroe spp. in the northern Adriatic Sea. In this context,
predators and their potential to control M. leidyi populations in the Mediterranean Sea are of particular interest.
In addition to Beroe spp., some scyphomedusae consume
M. leidyi, including Chrysaora quinquecirrha in the USA
(Purcell and Cowan, 1995; Kreps et al., 1997) and Cyanea
capillata in the North Sea (Hosia and Titelman, 2011).
The scyphozoan Pelagia noctiluca is a potential predator of ctenophores. This jellyfish is abundant in the
northwestern Mediterranean (Sabatés et al., 2010) and is
an opportunistic predator that consumes a wide variety
of prey, including gelatinous species (Malej, 1989;
Sabatés et al., 2010). It occurs widely in the open ocean
and often is reported in high numbers in coastal areas
(Doyle et al., 2008; Licandro et al., 2010). Our objective
was to evaluate the predation potential of P. noctiluca on
M. leidyi. We measured feeding and digestion rates of
ephyrae, juvenile and adult medusae feeding on ctenophores in the laboratory and videotaped interactions
between medusae and ctenophores to quantify the frequency of escape.
Pelagia noctiluca jellyfish were collected off the northeastern Spanish coast during September– December
2010 in plastic bags or buckets to minimize damage
Table I: Experimental conditions for Pelagia noctiluca medusae feeding on Mnemiopsis leidyi
ctenophores
Experiment type
Feeding
Feeding
Feeding
Digestion
Digestion
Digestion
Digestion
Digestion
Digestion
Behaviour
Medusa diameter (mm)
a
40 –55
20 –25b
3.8 –4.2c
32 –35a
32 –35a
40 –47a
40 –47a
50 –56a
50 –56a
51 –62a
Ctenophore length (mm)
e
8 – 16
8 – 12e
1 – 3d
30 –36e
40 –49e
30 –36e
40 –49e
30 –36e
40 –49e
42 –50e
Prey container21
Replicates
Incubation time
Tank volume (L)
3,5,7,10,15
7,10,15,20,30
5,7,15
1
1
1
1
1
1
6
3,3,4,3,3
3
3
3
3
3
3
3
3
6
30 min
30 min
2h
Until complete
Until complete
Until complete
Until complete
Until complete
Until complete
4h
100
100
1.4
100
100
100
100
100
100
200
One predator was in each container aadults; bjuveniles; cephyrae; dlarvae, elobate stage.
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Two analyses of DT data were performed: (i) to test
the effects of predator and prey sizes on the DT separately, data were rank transformed to pass normality and
homoscedasticity assumptions and linear regressions
then fitted; (ii) untransformed data were analysed in
three groups to test if the relative sizes of the predator
and the prey affected the DT. The groups were:
predator . prey (medusa bell diameter was at least
5 mm greater than ctenophore length); predator ¼ prey
(size difference was 2 – 3 mm), and predator , prey
(medusa bell diameter was at least 10 mm less than
ctenophore length). No homoscedasticity of the data
required the use of Kruskal –Wallis and Wilcoxon
rank-sum tests.
All analyses were performed using the R 2.15 software (R Development Core Team, 2012). Data are
given as mean + standard deviation.
CR and IR of Pelagia noctiluca were significantly
related to prey concentration (F1,41 ¼ 34.6; P , 0.0001)
(Fig. 1A– F). Individual CR of all sizes of P. noctiluca
ranged from 0.4 + 0.1 to 103.2 + 32.6 L medusa21
h21. We analysed the CR and IR separately for P. noctiluca of different sizes.
The slope of the regression between CR of adults
and prey concentration was not significantly different
from 0 (Fig. 1A). IR increased with increasing ctenophore concentration (1.6 – 11.5 prey medusa21 h21,
Fig. 1D). Adult P. noctiluca ate more when more prey
were available, and no saturation point was observed
(functional response Type I; Holling, 1959), as observed
for C. capillata medusae feeding on M. leidyi (Hosia and
Titelman, 2011). Data were fitted by the use of linear
models.
The CR of juveniles ranged between 38 and 80 L
medusa21 h21. The CR increased over the lower prey
concentrations, but decreased at the highest two prey
densities (Fig. 1B). The IR increased with ctenophore
concentration and ranged from 3.6 to 10.1 prey
medusa21 h21. Juvenile P. noctiluca ate more when
more prey were available. No clear saturation point was
detected with the concentrations of prey used, but
the best fit was the negative exponential model corresponding to a functional response Type II (Fig. 1B CR
and E IR).
Ephyrae showed a Type II functional response and
the best fit was the Michaelis– Menten model (Fig. 1C
and F). The CR decreased with increasing prey concentration from 0.5 to 0.3 L medusa21 h21 and the IR
increased from 1.8 to 3.4 prey medusa21 h21 (Fig. 1C–F).
The CR of P. noctiluca ephyrae were higher than those of
C. quinquecirrha ephyrae ,4 mm (0.03 L h21) (Olesen
et al., 1996); in our P. noctiluca experiments, the containers were larger, the ephyrae generally larger and the
incubation times were short (30 min) to prevent severe
reduction of the prey available. During all incubations,
fewer than 40% of the prey were consumed.
Feeding was calculated as the clearance rate (CR)
according to the equation of Purcell and Cowan
(Purcell and Cowan, 1995) (CR: the volume of water filtered in L medusa21 h21):
V
Co
;
ln
CR ¼
Ct
ðn tÞ
where V is the container volume (L), n is the number of
predators (medusae), t is the incubation time (h), and Co
and Ct are the number of prey (ctenophores) at the beginning and at the end of the incubation, respectively.
The ingestion rate (IR, defined as: number of prey
eaten medusa21 h21) was calculated according to the
equation of MØller and Riisgård (MØller and Riisgård,
2007):
IR ¼ CR Cm ;
where Cm is the geometric mean of the prey concentration during the incubation and was calculated from the
equation
Cm ¼ exp
lnðCo Ct Þ
:
2
Digestion times (DTs) of 18 P. noctiluca of different sizes
feeding on M. leidyi were measured (Table I). Each
measurement began when one ctenophore was put into
the oral arms of one P. noctiluca. Predator and prey conditions were visually checked every 15 min and DT was
defined as when no prey tissue could be seen inside the
medusa.
Interactions between P. noctiluca and M. leidyi were
observed by videotaping (Table I). Encounters between
medusae and ctenophores were recorded with a
Prosilica GE 4900C (Allied Vision Technologies) CCD
high-resolution camera at a frequency of one picture
every 10 s with the focal distance held constant.
“Encounters” were defined as when a ctenophore
touched the medusa tentacles or oral arms. The
encounters were grouped as “short encounters” (,20 s)
and “long encounters” (.20 s), even if the prey later
escaped.
For analyses of the CR and IR of P. noctiluca feeding
on M. leidyi, the data were processed according to functional response (FR) models. Data were fitted to different models based on the best likelihood (highest R 2
value), according to Holling (Holling, 1959; Gentelman
et al., 2003).
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Fig. 1. Functional responses of Pelagia noctiluca feeding on Mnemiopsis leidyi ctenophores. Symbols show the clearance rates (CR) and ingestion
rates (IR) of each medusa size according to the prey concentration. Three replicates were made for each concentration; if two symbols appear,
then two replicates have the same IR or CR). The hatched line shows the relationship between the CR and the IR and prey concentration. (A
and D) Functional response for adults: Type I; CR: y ¼ 100.75 þ 31x, R 2 ¼ 0.07, P-value ¼ 0.88; IR: y ¼ 70.14x, R 2 ¼ 0.98, P-value , 0.001.
(B and E) Functional response for juveniles: Type III; best fit regression for CR: y ¼ 86.61e(22.1x), Deviance explained: 31.54%, P-value , 0.05;
best fit regression for IR: y ¼ 17.35x/(0.18 þ x), R 2 ¼ 0.73, P-value , 0.05. (C and F) Functional response for ephyrae: Type II; best
fit regression for CR: y ¼ 0.22 x/(22.82 þ x), R 2 ¼ 0.74, P-value , 0.05; best fit regression for IR: y ¼ 5.39 x/(10.39 þ x), R 2 ¼ 0.87,
P-value , 0.05
of 4.1 mm diameter clearing 0.4 + 0.1 L h21 juveniles
of 20– 25 mm diameter clearing 62.1 + 19.9 L h21 and
medusae of 40– 45 mm diameter clearing 103.2 +
32.6 L h21 . The CR for P. noctiluca adults were higher
ctenophore densities lower, all of which could have contributed to the higher CR for that species.
Medusa size was an important factor affecting the individual CRs (F1,41 ¼ 94.53; P , 0.0001) with ephyrae
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Table II: Experimentally measured clearance rates of scyphomedusae (Chrysaora quinquecirrha,
Cyanea capillata, Pelagia noctiluca) feeding on Mnemiopsis leidyi
Predator
Predator stage
and diameter (mm)
Prey length (mm)
Prey L21
Clearance
(L ind21 h1)
Container
volume (L)
Reference
C. capillata
C. quinquecirrha
C. quinquecirrha
C. quinquecirrha
P. noctiluca
P. noctiluca
P. noctiluca
Adult 75 + 13
Adult 81 + 15
Adult 75 + 21
Ephyra , 4
Adult 40 –55
Juvenile 20 –25
Ephyra 3.8 – 4.2
28.7 + 55
14.1 + 38 mL
10.5 + 44 mL
1.5 + 4; 1.6 + 0.4
8– 16
8– 12
1– 3d
0.0053 –0.0421
0.0063 + 0.0032
0.0074 + 0.0025
10 –40
0.03– 0.15
0.07– 0.3
5–15
40 + 11
69 +55
29 + 27
0.03
103 + 33
62 + 20
0.4
380
3200
1000
0.5 –1
100
100
1.4
(Hosia and Titelman, 2011)
(Purcell and Cowan, 1995)
(Purcell and Cowan, 1995)
(Olesen et al., 1996)
This study
This study
This study
Data are given as mean + SD.
than those for other scyphomedusan species eating
M. leidyi (Table II), even though the other predators
(C. capillata 75 mm; C. quinquecirrha 81 mm) were larger
than P. noctiluca medusae (45 mm) and their containers
were larger than in our study.
The relatively small container size in our experiments
may have affected the feeding rates, which may be consistently underestimated in experiments conducted in
containers (Purcell, 2009). Purcell and Cowan (Purcell
and Cowan, 1995) obtained a lower CR in 1000-L than
in 3200-L mesocosms (Table I). Our experiments were
conducted in flow-through tanks; however, the possible
efficacy of water circulation in reducing container size
effects on feeding is untested.
Ctenophore size was significantly correlated with the
DT (R 2 ¼ 0.24, t ¼ 2.246, P-value ¼ 0.039). Regardless
of the predator’s size, DT increased with larger prey
(Fig. 2A). In contrast, medusa size did not significantly
affect the DT, although an inverse trend was observed
(R 2 ¼ 0.071, t ¼ 21.105, P ¼ 0.29). Although the DT
were not significantly different among all relative-size
groups of predators and prey (P ¼ 0.762), the DTs of
the groups “predator . prey” and “predator , prey”
were significantly different (P ¼ 0.027), with the DT
being longer when the predator is smaller than the prey
(Fig. 2B).
A total of 838 encounters between large ctenophores
(45.6 + 4.6 mm) and P. noctiluca, resulting in 375 “short
encounters” and 463 “long encounters” were videotaped. The ctenophores escaped in 100% of the encounters, which is comparable with results for C. quinquecirrha
(97.2%; Kreps et al., 1997) and for C. capillata (90.8%;
Hosia and Titelman, 2011). Subsequent “short encounters” also resulted in escape. When a ctenophore
adhered to an oral arm or tentacle, it displayed escape
behaviour, consisting of rotation along the oral-aboral
axis and change in the swimming direction; pieces of
tissue left attached to the medusa’s oral arms or tentacles
(Supplementary data, Fig. S1) subsequently were
ingested by the medusa, as seen in previous studies
(Purcell and Cowan, 1995; Kreps et al., 1997; Hosia and
Titelman, 2011). Thus, the ctenophores were damaged
and partly consumed. After losing several parts of tissue,
the ability to change their swimming direction was
reduced. Damage was reflected by an increased frequency of “long encounters” during the incubations;
“long encounters” constituted 43.1% of the encounters,
during the first hour, but 70.6% in the last hour. M. leidyi
has a remarkable capacity to regenerate lost tissue and
damaged ctenophores healed quickly (Coonfield, 1936;
Purcell and Cowan, 1995). These abilities enhance the
survival of M. leidyi. Even though repeated encounters
could affect its health, the ctenophore was never
ingested, showing the high ability of large ctenophores
to escape.
Behaviour of P. noctiluca and DTs also influenced the
CR and the IR. Observations during the feeding
experiments, in which the ctenophores were smaller
than during videotaping, showed that small ctenophores
(19 + 8 mm) did not escape from the medusae. Small
ctenophores were transported from the tentacles or oral
arms to the manubrium, where they were enveloped
and could not escape; pieces of tissue attached to the
predator’s oral arms also were ingested (Supplementary
data, Fig. S2A – C). Parts of the ctenophores were visible
inside the medusa’s umbrella, with the ciliated comb
rows visible longest (Supplementary data, Fig. S2C).
When the DT was short, the medusae could feed more
without becoming saturated in high prey densities. In
each capture and ingestion event, the ctenophore was
considerably smaller than the medusa, as in other
studies (Purcell and Cowan, 1995; Kreps et al., 1997;
Hosia and Titelman, 2011).
Many species of gelatinous zooplankton are eaten
by other gelatinous species (Purcell, 1991). Although
several studies have been conducted to study these interactions, few were with P. noctiluca as the predator (Malej,
1989) and few with M. leidyi as the prey (Purcell and
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been occasionally reported together on the Mediterranean Spanish coast, in Denia (Alicante) (Fuentes et al.,
2010; M. Acevedo, ICM, Barcelona, personal communication) and in the Mar Menor lagoon (V. L. Fuentes,
ICM, Barcelona, personal communication). More
studies on the distribution of these species in the NW
Mediterranean are needed to understand the effect of
P. noctiluca on M. leidyi populations.
S U P P L E M E N TA RY DATA
Supplementary data can be found online at http://
plankt.oxfordjournals.org.
AC K N OW L E D G M E N T S
The experimental work was conducted as part of the
“Medusa project”, supported by the Catalan Water
Agency (ACA) and the LIFE CUBOMED project
(www.cubomed.eu). We thank Miriam Gentile for
helping us maintain the cultures, Paulo Casal for
helping to install the camera system and Eduardo Obis
for photography.
FUNDING
This research was supported by the European comission
(LIFE PROGRAM) by funding the CUBOMED
PROJECT. Also was supported by the Catalan government by funding from the ACA (Catalan Water Agency)
through the Medusa project.
Fig. 2. Digestion times of Pelagia noctiluca adults on different sizes of
Mnemiopsis leidyi ctenophores. (A) effect of the prey size on the DT; best
fit regression y ¼ 5.83x – 110.51, R 2 ¼ 0.19, P-value ¼ 0.039. (B)
Digestion times for three groups based on the relative sizes of the
predator
and
prey:
“predator , prey”,
“predator ¼ prey”,
“predator . prey”
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