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Marine Biology (2005) 147: 863–868
DOI 10.1007/s00227-005-1579-8
R ES E AR C H A RT I C L E
J. Shoji Æ R. Masuda Æ Y. Yamashita Æ M. Tanaka
Effect of low dissolved oxygen concentrations on behavior and predation
rates on red sea bream Pagrus major larvae by the jellyfish
Aurelia aurita and by juvenile Spanish mackerel Scomberomorus
niphonius
Received: 1 September 2004 / Accepted: 15 January 2005 / Published online: 21 June 2005
Ó Springer-Verlag 2005
Abstract A shift in outcomes of predator-prey inter- during summer have the potential to increase the
actions in plankton community may occur at sublethal relative importance of jellyfish as predator of fish
dissolved oxygen concentrations that commonly occur larvae and to change the importance of alternative
in coastal waters. Laboratory experiments were con- trophic pathways in estuarine ecosystems.
ducted to investigate how a decline in dissolved oxy-
gen concentration alters the predation rate on fish
larvae by two estuarine predators. Behavior and con- Introduction
sumption of larval fish by moon jellyfish Aurelia aurita
(103.1±12.4 mm in bell diameter) and by a juvenile Low dissolved oxygen concentrations induced by
piscivore, Spanish mackerel Scomberomorus niphonius anthropogenic, physical and/or biological factors com-
(30.1±2.1 mm in standard length: SL), were observed monly occur in many aquatic habitats such as estuaries,
under four oxygen concentration treatments (1, 2 and lakes, fjords, coastal waters, and in the deep sea (Renaud
4 mg lÀ1 and air-saturated: 5.8 mg lÀ1). Larvae of a 1986; Suzuki and Matsukawa 1987; Nixon 1988).
coastal marine fish species, red sea bream Pagrus Occurrence of low dissolved oxygen in stratified waters
major (7.21±0.52 mm SL), were used as prey for the of shallow marine systems during summer can cause
experiment. Bell contraction rate of the jellyfish did lethal effects on benthic and pelagic organisms (Officer
not vary among the oxygen concentrations tested, et al. 1984; Aoki 1999). Even though the effect is not
indicating a tolerance to low oxygen concentration. lethal, oxygen concentrations in the range of 1–4 mg lÀ1
Gill ventilation rate of the Spanish mackerel increased (moderate levels of hypoxia) are physiologically stressful
and swimming speed decreased as the oxygen con- (Rombough 1988) and disturb growth and survival of
centration decreased, indicating that oxygen concen- many fish species (van der Veer and Bergman 1986;
trations £ 4 mg lÀ1 are physiologically stressful for Kramer 1987). Fish larvae would be more vulnerable to
this species. The number of larvae consumed in mortality when oxygen concentration declines to a
15 min. by jellyfish increased whereas those consumed stressful level since they are less tolerant of low dissolved
by Spanish mackerel decreased with the decrease in oxygen concentration due to undeveloped physiological
oxygen concentration. Low oxygen concentrations that function (Rombough 1988). Declines in dissolved oxy-
are commonly observed in coastal waters of Japan gen to moderate levels of hypoxia, which is not lethal
during short-term exposure, can reduce larval ability to
escape from predators and increase vulnerability to
Communicated by T. Ikeda, Hakodate
predation (Breitburg et al. 1994). However, there is
J. Shoji (&) Æ M. Tanaka
much less information on the effects of low dissolved
Laboratory of Estuarine Ecology,
oxygen on larval survival compared to those on adults
Field Science Education and Research Center,
and immature fishes.
Kyoto University, Sakyo, 606–8502 Kyoto, Japan
E-mail: shog@kais.kyoto-u.ac.jp The Seto Inland Sea is the largest area with reduced
Tel.: +81-75-7536225 salinity water in Japan and has many industrialized
Fax: +81-75-7536229
areas along its coast. Excess nutritional loading from the
R. Masuda Æ Y. Yamashita land exacerbates the depletion of oxygen concentration
Maizuru Fisheries Research Station,
in the coastal waters (Okaichi et al. 1996). In the Sea of
Field Science Education and Research Center,
Hiuchi, the central Seto Inland Sea, dissolved oxygen
Kyoto University, Nagahama, Maizuru,
concentration commonly declines to <1 mg lÀ1 during
625–0086 Kyoto, Japan
864
sea bream larvae were consumed by a moon jellyfish 66–
summer (Ochi et al. 1978). Recently, an increase in the
80 mm BD under laboratory conditions.
moon jellyfish Aurelia aurita population has lead to
The Spanish mackerel is widely distributed in south-
significant impacts, ecologically on the plankton com-
western coastal waters of Japan and spawns in May and
munity through its predation on zooplankton in the Seto
June (Kishida and Aida 1989) in the Seto Inland Sea,
Inland Sea and economically on industries, by hamper-
one of the major spawning area of the species. Young-
ing fishery activities and by preventing power plants
of-the-year Spanish mackerel inhabit the central Seto
from taking cooling water (Uye and Ueta 2004; Yasuda
Inland Sea throughout the summer until the wintering
2003). Uye et al. (2003) observed moon jellyfish aggre-
gated at a mean abundance of 250 mÀ2 and which migration out of the Seto Inland Sea (Kishida 1989).
Larvae and juveniles exhibit strong piscivory (Shoji and
consumed almost 100% of mesozooplankton in coastal
Tanaka 2001) and high consumption of fish larvae (90–
waters of southwestern Japan in summer. An increase in
127% body weight dayÀ1: Shoji et al. 2001). The Spanish
the moon jellyfish population would have significant
effects on the recruitment of coastal fishery resources in mackerel is considered to be the most important pred-
the Seto Inland Sea through increasing the predation ator in the summer ichthyoplankton community since
impact and/or compensation. In addition, predation on no other pelagic juvenile fish has been reported to be
fish larvae by moon jellyfish would be more important piscivorous in the area.
during summer hypoxia if moon jellyfish are tolerant to
moderate hypoxia, a decline in oxygen concentrations
to 1–4 mg lÀ1 that commonly occurs in the central Seto Materials and methods
Inland Sea during summer. Investigation on the effect of
dissolved oxygen concentration on larval predation Rearing of prey larvae
mortality in relation to prey-predator interactions would
lead to a better understanding of how changes in envi- Red sea bream eggs naturally spawned and fertilized at
ronmental conditions directly and indirectly affect larval the Kyoto Prefecture Sea-Farming Center (KPSFC)
survival in estuarine ecosystems. However, there is no were transported to the Maizuru Fisheries Research
information on predation on fish larvae by moon Station (MFRS), Kyoto University Field Science Edu-
jellyfish in coastal waters of Japan, although the jelly- cation and Research Center, and were maintained in
fish’s life history (Toyokawa et al. 2000) and predation 500-l tanks with aerated seawater. Larvae were fed with
on invertebrate zooplankton (Ishii and Tanaka 2001; rotifer Brachionus plicatilis and Artemia spp. at 16.1–
Uye et al. 2003) have been well documented. 19.5°C under natural light conditions. Age and mean
In the present study, we describe results from experi- (±SD) standard length (SL) of larvae used for the
ments conducted to examine how low dissolved oxygen experiments were day 23 and 7.21 (±0.52) mm (post-
concentrations affect the predation on fish larvae by two flexion stage).
predators, moon jellyfish and a juvenile piscivore, Spanish
mackerel Scomberomorus niphonius. Behavior and con-
sumption rates of the predators under low oxygen con-
Rearing and husbandry of predators
centrations were observed under laboratory conditions.
Larvae of red sea bream Pagrus major was used as
Moon jellyfish were collected at the pier of MFRS using
prey in the predation experiments. The red sea bream is
a 10-l plastic bucket and were kept in 100-l tanks with
widely distributed and is one of the most important
filtered sea water. Considering the size of moon jellyfish
fishery resources in coastal waters of Japan. Pelagic
abundant in the Seto Inland Sea during summer (Uye
larvae and juveniles are abundant from March to May
2004), moon jellyfish in mean BD (±SD) of 103.1
in Shijiki Bay, Nagasaki (Tanaka 1980), and in May and
(±13.1) mm (n=24) were used for the predation
June in the Seto Inland Sea (Shoji et al. 2002). Late
experiments. The moon jellyfish were fed with Artemia
larvae and early juveniles migrate from coastal open
spp. and were starved for overnight before the experi-
waters in May and June to settle in shallow waters of
ments.
bays (Azeta et al. 1980).
Artificially fertilized eggs were obtained from a pair
The moon jellyfish is widely distributed in coastal wa-
of adults of Spanish mackerel fished by a gill net in the
ters of the world (Yasuda 2003) and is reported to have
Sea of Harima, eastern Seto Inland Sea. The eggs were
recently increased in abundance in coastal waters of Japan
transported from the Yashima Branch, Japan Sea
such as Tokyo Bay (Ishii 2001) and the Seto Inland Sea
Farming Association (JASFA), to MFRS and were
(Uye and Ueta 2004). Moon jellyfish has been considered
maintained in 500-l tanks with aerated seawater. Larvae
as an important predator of zooplankton (Bailey and
were fed with yolk-sac red sea bream larvae (day 0–3)
Batty 1984; van der Veer and Oorthuysen 1986; Sullivan
under natural light conditions with water temperature
et al. 1994; Matanoski et al. 2004) because of its high
ranging from 15.8 to 19.5°C. Early juveniles
consumption rates. Moller (1984) observed that 68
¨
(30.1±2.1 mm SL, day 28) were used as the predators
Atlantic herring Clupea harengus larvae were eaten by a
for the predation experiment. The juveniles were starved
moon jellyfish 42 mm in bell diameter (BD) in Kiel Fjord.
overnight before the experiment.
Nakayama et al. (2003) described that more than 110 red
865
Table 1 Aurelia aurita and Scomberomorus niphonius. Mean±SD
dissolved oxygen concentrations (mg lÀ1) in the tanks with
moon jellyfish (MJ) and juvenile Spanish mackerel (SM) as pred-
ator of red sea bream larvae. Four oxygen concentrations (1, 2 and
4 mg lÀ1 and air-saturated) were set for the predation experiments
Oxygen level desired Predator
MJ SM
1 mg lÀ1 1.02±0.04 1.04±0.06
2 mg lÀ1 1.96±0.11 1.97±0.10
4 mg lÀ1 3.94±0.05 3.97±0.08
Air-saturated 5.75±0.01 5.78±0.09
Predation experiment
Fig. 1 Aurelia aurita. Bell contraction rate (no. minÀ1) of moon
Observations on the behavior of the predators and jellyfish Aurelia aurita under reduced and air-saturated (5.8 mg lÀ1)
measurements of predation rates on fish larvae were oxygen concentrations. Six replicates were conducted at each
conducted under four oxygen concentration treatments oxygen concentration. Vertical bars indicate SD
(1, 2, 4 mg lÀ1 and air-saturated: 5.8 mg lÀ1). Water
temperature, salinity, and oxygen concentration were
27.7±2.5 at 4 mg lÀ1 and 29.0±2.8 at 2 mg lÀ1 during
recorded with an Environmental Monitoring System
the experiment. There was no significant effect of the
(YSI 650 MDS, YSI, USA). Water temperature ranged
oxygen treatment on the bell contraction rate (Kruskal-
between 19.5 and 20.3°C and salinity between 33.2–
Wallis test, P=0.86). Overall mean (n=24) of bell
33.5 psu both in the stocking and experimental tanks.
contraction rate was 28.3±2.4.
The desired oxygen concentrations were obtained by
Consumption rate by moon jellyfish was higher under
bubbling filtered seawater with nitrogen and air. Oxygen
the two lowest oxygen concentrations (Fig. 2). More
concentrations within ±4% of the desired concentration
than 80% of red sea bream larvae were predated on by
were obtained (Table 1).
moon jellyfish at oxygen concentration of 1 and 2 mg
Either of 1 moon jellyfish or 1 Spanish mackerel with 30
lÀ1. About half of the larvae survived under the two
red sea bream larvae were introduced to a 10-l circular
highest oxygen concentrations. Effect of the oxygen
experimental tank surrounded with a black plastic sheet to
concentration treatment on consumption rate was sig-
minimize the effect of the influence of the observer. A
nificant (Kruskal-Wallis followed by Dunnett test,
relatively shallow depth of the water (14 cm) prevented the
P<0.05).
moon jellyfish from vertical distribution. The tank was
sealed and the behavior of the predators was videotaped.
Observations on the behavior of the predators were star-
Spanish mackerel behavior and consumption rate
ted 5 min after the beginning of the experiments. The
number of contractions of the moon jellyfish bell was
The gill ventilation rate of juvenile Spanish mackerel
counted for 3 min by direct observations. Cruise swim-
increased with the decrease in dissolved oxygen con-
ming speed (cm secÀ1) and gill ventilation rate (no. minÀ1)
centration (Fig. 3). Mean gill ventilation rate (±SD)
of the Spanish mackerel were measured using the video-
taped records. The number of red sea bream larvae pre-
dated on by the two predators for 15 min was counted at
the end of each experiment. The larvae ingested or cap-
tured on the umbrella surface and with tentacles by moon
jellyfish were defined as predated. The moon jellyfish were
measured in BD and the Spanish mackerel in SL. The
predators were not reused. Six replicates were made for
each predator and oxygen treatment. All experiments were
conducted from 0900 to 1500 hours.
Results
Fig. 2 Aurelia aurita. Number of red sea bream larvae predated on
Moon jellyfish behavior and consumption rate in 15 min by one moon jellyfish under reduced and air-saturated
(5.8 mg lÀ1) oxygen concentrations. Six replicates were conducted
at each oxygen concentration. Different letters indicate significant
The bell contraction rate of moon jellyfish did not vary
differences among oxygen concentration treatments (Kruskal-
among the oxygen concentrations tested (Fig. 1). Mean Wallis followed by Dunnett test, P<0.05). Vertical bars indicate
bell contraction rate (no. minÀ1 ±SD) ranged between SD
866
and air-saturated oxygen concentration treatments
(Kruskal-Wallis followed by Dunnett test, P<0.05).
Consumption rate of larvae by Spanish mackerel
juvenile increased with the increase in oxygen concen-
tration (Fig. 4). Only one red sea bream larva was pre-
dated on by the Spanish mackerel under the 1 mg lÀ1
treatment. There was a significant effect of oxygen
concentration on the consumption rate (Kruskal-Wallis
followed by Dunnett test, P<0.05).
Discussion
The present experiments showed that a decline in oxygen
concentration had different effects on the consumption
rate by the different predators, moon jellyfish and
juvenile Spanish mackerel. Differences in tolerances to
low dissolved oxygen concentration between the two
predators are attributable to the difference in the pattern
of change in consumption under the oxygen concentra-
tions between 1.04–5.75 mg lÀ1. Bell contraction rate of
moon jellyfish did not vary under the oxygen concen-
trations tested whereas gill ventilation rate of Spanish
mackerel increased and cruise swimming speed de-
Fig. 3 Scomberomorus niphonius. Gill ventilation rate (no. minÀ1)
creased as the oxygen concentrations decreased. These
and cruising swimming speed (cm sÀ1) of juvenile Spanish mackerel
under reduced and air-saturated (5.8 mg lÀ1) oxygen concentra- observations suggest that moon jellyfish has a higher
tolerance to low oxygen concentrations ( £ 2 mg lÀ1)
tions. Six replicates were conducted at each oxygen concentration.
Different letters indicate significant differences among oxygen than juvenile Spanish mackerel does.
concentration treatments (Kruskal-Wallis followed by Dunnett
The increase in consumption on the larvae (7.21 mm
test, P<0.05). Vertical bars indicate SD
SL) by moon jellyfish under oxygen concentrations £ 2
mg lÀ1 supports results from another experiment in which
ranged from 207.8±7.7 at 1 mg lÀ1 and 159.8±7.3 un-
the consumption by moon jellyfish on red sea bream larvae
der the control condition. There was a significant effect
(6.19 and 8.60 mm SL) increased at £ 2 mg lÀ1 (Shoji
of oxygen concentration on the gill ventilation rate
et al. 2005). Fukuhara (1985) observed under laboratory
(Kruskal-Wallis followed by Dunnett test, P<0.05).
conditions that the cruising swimming speed rapidly in-
Mean cruise swimming speed was higher in the higher
creased in red sea bream larvae >6 mm SL at which size
oxygen concentration treatments (Fig. 3). All Spanish
the development of unpaired fins begins. Nakayama et al.
mackerel were at the bottom of experimental tank hav-
(2003) reported that time to capture by moon jellyfish
ing stopped swimming at 5 min after the start of
significantly increased in red sea bream larvae >7 mm SL
experiment in 1 mg lÀ1 treatment. There was a signifi-
in aquaria. These observations suggest that red sea bream
cant difference in the swimming speed between 1 mg lÀ1
larvae >7 mm SL are less vulnerable to predation by
moon jellyfish than smaller larvae are apparently due to
their increased swimming ability.
Fish larvae are considered more vulnerable to phys-
iological stress by a decline in the oxygen concentration
since they are less physiologically developed (Rombough
1988). Dissolved oxygen concentrations £ 2 mg lÀ1 are
not considered lethal for short-term exposure, but re-
duce the ability of fish larvae to react to and escape from
jellyfish predators and to recover from contact with
jellyfish (Breitburg et al. 1994). Therefore, the vulnera-
bility of fish larvae to predation by jellyfish predators
increases under low dissolved oxygen concentrations
that are not lethal during short-term exposure. We
Fig. 4 Scomberomorus niphonius. Number of red sea bream larvae
conclude that red sea bream larvae >7 mm SL are
predated on in 15 min by one juvenile Spanish mackerel under
reduced and air-saturated (5.8 mg l-1) oxygen concentrations. Six highly vulnerable to predation by moon jellyfish under
replicates were conducted at each oxygen concentration. Different dissolved oxygen concentration £ 2 mg lÀ1 in nature; at
letters indicate significant differences among oxygen concentration
oxygen concentrations ‡ 4 mg lÀ1 they are potentially
treatments (Kruskal-Wallis followed by Dunnett test, P<0.05).
able to avoid moon jellyfish.
Vertical bars indicate SD
867
Costello and Colin (1994) examined the mechanisms zooplankton have been replaced by moon jellyfish in the
of prey capture by moon jellyfish under laboratory food web since the moon jellyfish biomass increased in
conditions and suggested that moon jellyfish can capture the Seto Inland Sea. The excess nutritional loading from
prey organisms with slower escape speeds than flow land is considered as one of the major factors that
velocity at the bell margin of moon jellyfish. In the caused the dominance by moon jellyfish in the summer
present study, bell contraction rate did not vary under plankton community in the Seto Inland Sea since it
oxygen concentrations between 1.04 and 5.75 mg lÀ1. promotes production of small zooplankton which is a
This result indicates that the volume of water filtered by major prey organism of the moon jellyfish (Mills 2001;
Uye and Ueta 2004). We suggest, based on present re-
moon jellyfish and their ability to capture prey did not
decrease under oxygen concentrations £ 2 mg lÀ1. sults, another possible mechanism for the increase in
Moon jellyfish survival was 100% at 1 mg lÀ1 in 3-h abundance of the moon jelly fish: the excess nutritional
experiments (Shoji, unpublished data). We conclude that loading has contributed to the increase in abundance of
the moon jellyfish is highly tolerant to low dissolved moon jellyfish through exacerbating the depletion in
oxygen concentrations and under these conditions there oxygen concentration which is advantageous to feeding
would be enhanced flow from ichthyoplankton to moon of the moon jellyfish.
jellyfish.
In contrast to the consumption by moon jellyfish, Acknowledgements We express our thanks to Dr. D.L. Breitburg,
consumption by juvenile Spanish mackerel decreased as Smithsonian Environmental Research Center, for teaching the
experimental protocol and Dr. E.D. Houde, Chesapeake Biological
dissolved oxygen concentration decreased. Early life
Laboratory, University of Maryland, Dr. Mark Wuenschel,
stages of scombrid fishes (including Scomberomorus fish)
NOAA Beaufort Laboratory, and two anonymous reviewers for
are considered to have a high oxygen requirement due to providing valuable comments on the manuscript. Thanks are due
the high swimming and metabolic rates (Hunter 1981). to Mr. A. Iwamoto and staff of JASFA for providing Spanish
The increase in gill ventilation rate and decrease in mackerel eggs and Dr. H. Motoh and staff of KPSFC for providing
red sea bream eggs. All experiments were conducted in Japan, and
swimming speed of juvenile Spanish mackerel with the
were in compliance with the current laws.
decline in oxygen concentration to 4 mg lÀ1 in the
experiments indicate that the oxygen concentration
£ 4 mg lÀ1 was physiologically stressful for juvenile
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1685
DOI 10.1007/s00227-005-1579-8
R ES E AR C H A RT I C L E
J. Shoji Æ R. Masuda Æ Y. Yamashita Æ M. Tanaka
Effect of low dissolved oxygen concentrations on behavior and predation
rates on red sea bream Pagrus major larvae by the jellyfish
Aurelia aurita and by juvenile Spanish mackerel Scomberomorus
niphonius
Received: 1 September 2004 / Accepted: 15 January 2005 / Published online: 21 June 2005
Ó Springer-Verlag 2005
Abstract A shift in outcomes of predator-prey inter- during summer have the potential to increase the
actions in plankton community may occur at sublethal relative importance of jellyfish as predator of fish
dissolved oxygen concentrations that commonly occur larvae and to change the importance of alternative
in coastal waters. Laboratory experiments were con- trophic pathways in estuarine ecosystems.
ducted to investigate how a decline in dissolved oxy-
gen concentration alters the predation rate on fish
larvae by two estuarine predators. Behavior and con- Introduction
sumption of larval fish by moon jellyfish Aurelia aurita
(103.1±12.4 mm in bell diameter) and by a juvenile Low dissolved oxygen concentrations induced by
piscivore, Spanish mackerel Scomberomorus niphonius anthropogenic, physical and/or biological factors com-
(30.1±2.1 mm in standard length: SL), were observed monly occur in many aquatic habitats such as estuaries,
under four oxygen concentration treatments (1, 2 and lakes, fjords, coastal waters, and in the deep sea (Renaud
4 mg lÀ1 and air-saturated: 5.8 mg lÀ1). Larvae of a 1986; Suzuki and Matsukawa 1987; Nixon 1988).
coastal marine fish species, red sea bream Pagrus Occurrence of low dissolved oxygen in stratified waters
major (7.21±0.52 mm SL), were used as prey for the of shallow marine systems during summer can cause
experiment. Bell contraction rate of the jellyfish did lethal effects on benthic and pelagic organisms (Officer
not vary among the oxygen concentrations tested, et al. 1984; Aoki 1999). Even though the effect is not
indicating a tolerance to low oxygen concentration. lethal, oxygen concentrations in the range of 1–4 mg lÀ1
Gill ventilation rate of the Spanish mackerel increased (moderate levels of hypoxia) are physiologically stressful
and swimming speed decreased as the oxygen con- (Rombough 1988) and disturb growth and survival of
centration decreased, indicating that oxygen concen- many fish species (van der Veer and Bergman 1986;
trations £ 4 mg lÀ1 are physiologically stressful for Kramer 1987). Fish larvae would be more vulnerable to
this species. The number of larvae consumed in mortality when oxygen concentration declines to a
15 min. by jellyfish increased whereas those consumed stressful level since they are less tolerant of low dissolved
by Spanish mackerel decreased with the decrease in oxygen concentration due to undeveloped physiological
oxygen concentration. Low oxygen concentrations that function (Rombough 1988). Declines in dissolved oxy-
are commonly observed in coastal waters of Japan gen to moderate levels of hypoxia, which is not lethal
during short-term exposure, can reduce larval ability to
escape from predators and increase vulnerability to
Communicated by T. Ikeda, Hakodate
predation (Breitburg et al. 1994). However, there is
J. Shoji (&) Æ M. Tanaka
much less information on the effects of low dissolved
Laboratory of Estuarine Ecology,
oxygen on larval survival compared to those on adults
Field Science Education and Research Center,
and immature fishes.
Kyoto University, Sakyo, 606–8502 Kyoto, Japan
E-mail: shog@kais.kyoto-u.ac.jp The Seto Inland Sea is the largest area with reduced
Tel.: +81-75-7536225 salinity water in Japan and has many industrialized
Fax: +81-75-7536229
areas along its coast. Excess nutritional loading from the
R. Masuda Æ Y. Yamashita land exacerbates the depletion of oxygen concentration
Maizuru Fisheries Research Station,
in the coastal waters (Okaichi et al. 1996). In the Sea of
Field Science Education and Research Center,
Hiuchi, the central Seto Inland Sea, dissolved oxygen
Kyoto University, Nagahama, Maizuru,
concentration commonly declines to <1 mg lÀ1 during
625–0086 Kyoto, Japan
864
sea bream larvae were consumed by a moon jellyfish 66–
summer (Ochi et al. 1978). Recently, an increase in the
80 mm BD under laboratory conditions.
moon jellyfish Aurelia aurita population has lead to
The Spanish mackerel is widely distributed in south-
significant impacts, ecologically on the plankton com-
western coastal waters of Japan and spawns in May and
munity through its predation on zooplankton in the Seto
June (Kishida and Aida 1989) in the Seto Inland Sea,
Inland Sea and economically on industries, by hamper-
one of the major spawning area of the species. Young-
ing fishery activities and by preventing power plants
of-the-year Spanish mackerel inhabit the central Seto
from taking cooling water (Uye and Ueta 2004; Yasuda
Inland Sea throughout the summer until the wintering
2003). Uye et al. (2003) observed moon jellyfish aggre-
gated at a mean abundance of 250 mÀ2 and which migration out of the Seto Inland Sea (Kishida 1989).
Larvae and juveniles exhibit strong piscivory (Shoji and
consumed almost 100% of mesozooplankton in coastal
Tanaka 2001) and high consumption of fish larvae (90–
waters of southwestern Japan in summer. An increase in
127% body weight dayÀ1: Shoji et al. 2001). The Spanish
the moon jellyfish population would have significant
effects on the recruitment of coastal fishery resources in mackerel is considered to be the most important pred-
the Seto Inland Sea through increasing the predation ator in the summer ichthyoplankton community since
impact and/or compensation. In addition, predation on no other pelagic juvenile fish has been reported to be
fish larvae by moon jellyfish would be more important piscivorous in the area.
during summer hypoxia if moon jellyfish are tolerant to
moderate hypoxia, a decline in oxygen concentrations
to 1–4 mg lÀ1 that commonly occurs in the central Seto Materials and methods
Inland Sea during summer. Investigation on the effect of
dissolved oxygen concentration on larval predation Rearing of prey larvae
mortality in relation to prey-predator interactions would
lead to a better understanding of how changes in envi- Red sea bream eggs naturally spawned and fertilized at
ronmental conditions directly and indirectly affect larval the Kyoto Prefecture Sea-Farming Center (KPSFC)
survival in estuarine ecosystems. However, there is no were transported to the Maizuru Fisheries Research
information on predation on fish larvae by moon Station (MFRS), Kyoto University Field Science Edu-
jellyfish in coastal waters of Japan, although the jelly- cation and Research Center, and were maintained in
fish’s life history (Toyokawa et al. 2000) and predation 500-l tanks with aerated seawater. Larvae were fed with
on invertebrate zooplankton (Ishii and Tanaka 2001; rotifer Brachionus plicatilis and Artemia spp. at 16.1–
Uye et al. 2003) have been well documented. 19.5°C under natural light conditions. Age and mean
In the present study, we describe results from experi- (±SD) standard length (SL) of larvae used for the
ments conducted to examine how low dissolved oxygen experiments were day 23 and 7.21 (±0.52) mm (post-
concentrations affect the predation on fish larvae by two flexion stage).
predators, moon jellyfish and a juvenile piscivore, Spanish
mackerel Scomberomorus niphonius. Behavior and con-
sumption rates of the predators under low oxygen con-
Rearing and husbandry of predators
centrations were observed under laboratory conditions.
Larvae of red sea bream Pagrus major was used as
Moon jellyfish were collected at the pier of MFRS using
prey in the predation experiments. The red sea bream is
a 10-l plastic bucket and were kept in 100-l tanks with
widely distributed and is one of the most important
filtered sea water. Considering the size of moon jellyfish
fishery resources in coastal waters of Japan. Pelagic
abundant in the Seto Inland Sea during summer (Uye
larvae and juveniles are abundant from March to May
2004), moon jellyfish in mean BD (±SD) of 103.1
in Shijiki Bay, Nagasaki (Tanaka 1980), and in May and
(±13.1) mm (n=24) were used for the predation
June in the Seto Inland Sea (Shoji et al. 2002). Late
experiments. The moon jellyfish were fed with Artemia
larvae and early juveniles migrate from coastal open
spp. and were starved for overnight before the experi-
waters in May and June to settle in shallow waters of
ments.
bays (Azeta et al. 1980).
Artificially fertilized eggs were obtained from a pair
The moon jellyfish is widely distributed in coastal wa-
of adults of Spanish mackerel fished by a gill net in the
ters of the world (Yasuda 2003) and is reported to have
Sea of Harima, eastern Seto Inland Sea. The eggs were
recently increased in abundance in coastal waters of Japan
transported from the Yashima Branch, Japan Sea
such as Tokyo Bay (Ishii 2001) and the Seto Inland Sea
Farming Association (JASFA), to MFRS and were
(Uye and Ueta 2004). Moon jellyfish has been considered
maintained in 500-l tanks with aerated seawater. Larvae
as an important predator of zooplankton (Bailey and
were fed with yolk-sac red sea bream larvae (day 0–3)
Batty 1984; van der Veer and Oorthuysen 1986; Sullivan
under natural light conditions with water temperature
et al. 1994; Matanoski et al. 2004) because of its high
ranging from 15.8 to 19.5°C. Early juveniles
consumption rates. Moller (1984) observed that 68
¨
(30.1±2.1 mm SL, day 28) were used as the predators
Atlantic herring Clupea harengus larvae were eaten by a
for the predation experiment. The juveniles were starved
moon jellyfish 42 mm in bell diameter (BD) in Kiel Fjord.
overnight before the experiment.
Nakayama et al. (2003) described that more than 110 red
865
Table 1 Aurelia aurita and Scomberomorus niphonius. Mean±SD
dissolved oxygen concentrations (mg lÀ1) in the tanks with
moon jellyfish (MJ) and juvenile Spanish mackerel (SM) as pred-
ator of red sea bream larvae. Four oxygen concentrations (1, 2 and
4 mg lÀ1 and air-saturated) were set for the predation experiments
Oxygen level desired Predator
MJ SM
1 mg lÀ1 1.02±0.04 1.04±0.06
2 mg lÀ1 1.96±0.11 1.97±0.10
4 mg lÀ1 3.94±0.05 3.97±0.08
Air-saturated 5.75±0.01 5.78±0.09
Predation experiment
Fig. 1 Aurelia aurita. Bell contraction rate (no. minÀ1) of moon
Observations on the behavior of the predators and jellyfish Aurelia aurita under reduced and air-saturated (5.8 mg lÀ1)
measurements of predation rates on fish larvae were oxygen concentrations. Six replicates were conducted at each
conducted under four oxygen concentration treatments oxygen concentration. Vertical bars indicate SD
(1, 2, 4 mg lÀ1 and air-saturated: 5.8 mg lÀ1). Water
temperature, salinity, and oxygen concentration were
27.7±2.5 at 4 mg lÀ1 and 29.0±2.8 at 2 mg lÀ1 during
recorded with an Environmental Monitoring System
the experiment. There was no significant effect of the
(YSI 650 MDS, YSI, USA). Water temperature ranged
oxygen treatment on the bell contraction rate (Kruskal-
between 19.5 and 20.3°C and salinity between 33.2–
Wallis test, P=0.86). Overall mean (n=24) of bell
33.5 psu both in the stocking and experimental tanks.
contraction rate was 28.3±2.4.
The desired oxygen concentrations were obtained by
Consumption rate by moon jellyfish was higher under
bubbling filtered seawater with nitrogen and air. Oxygen
the two lowest oxygen concentrations (Fig. 2). More
concentrations within ±4% of the desired concentration
than 80% of red sea bream larvae were predated on by
were obtained (Table 1).
moon jellyfish at oxygen concentration of 1 and 2 mg
Either of 1 moon jellyfish or 1 Spanish mackerel with 30
lÀ1. About half of the larvae survived under the two
red sea bream larvae were introduced to a 10-l circular
highest oxygen concentrations. Effect of the oxygen
experimental tank surrounded with a black plastic sheet to
concentration treatment on consumption rate was sig-
minimize the effect of the influence of the observer. A
nificant (Kruskal-Wallis followed by Dunnett test,
relatively shallow depth of the water (14 cm) prevented the
P<0.05).
moon jellyfish from vertical distribution. The tank was
sealed and the behavior of the predators was videotaped.
Observations on the behavior of the predators were star-
Spanish mackerel behavior and consumption rate
ted 5 min after the beginning of the experiments. The
number of contractions of the moon jellyfish bell was
The gill ventilation rate of juvenile Spanish mackerel
counted for 3 min by direct observations. Cruise swim-
increased with the decrease in dissolved oxygen con-
ming speed (cm secÀ1) and gill ventilation rate (no. minÀ1)
centration (Fig. 3). Mean gill ventilation rate (±SD)
of the Spanish mackerel were measured using the video-
taped records. The number of red sea bream larvae pre-
dated on by the two predators for 15 min was counted at
the end of each experiment. The larvae ingested or cap-
tured on the umbrella surface and with tentacles by moon
jellyfish were defined as predated. The moon jellyfish were
measured in BD and the Spanish mackerel in SL. The
predators were not reused. Six replicates were made for
each predator and oxygen treatment. All experiments were
conducted from 0900 to 1500 hours.
Results
Fig. 2 Aurelia aurita. Number of red sea bream larvae predated on
Moon jellyfish behavior and consumption rate in 15 min by one moon jellyfish under reduced and air-saturated
(5.8 mg lÀ1) oxygen concentrations. Six replicates were conducted
at each oxygen concentration. Different letters indicate significant
The bell contraction rate of moon jellyfish did not vary
differences among oxygen concentration treatments (Kruskal-
among the oxygen concentrations tested (Fig. 1). Mean Wallis followed by Dunnett test, P<0.05). Vertical bars indicate
bell contraction rate (no. minÀ1 ±SD) ranged between SD
866
and air-saturated oxygen concentration treatments
(Kruskal-Wallis followed by Dunnett test, P<0.05).
Consumption rate of larvae by Spanish mackerel
juvenile increased with the increase in oxygen concen-
tration (Fig. 4). Only one red sea bream larva was pre-
dated on by the Spanish mackerel under the 1 mg lÀ1
treatment. There was a significant effect of oxygen
concentration on the consumption rate (Kruskal-Wallis
followed by Dunnett test, P<0.05).
Discussion
The present experiments showed that a decline in oxygen
concentration had different effects on the consumption
rate by the different predators, moon jellyfish and
juvenile Spanish mackerel. Differences in tolerances to
low dissolved oxygen concentration between the two
predators are attributable to the difference in the pattern
of change in consumption under the oxygen concentra-
tions between 1.04–5.75 mg lÀ1. Bell contraction rate of
moon jellyfish did not vary under the oxygen concen-
trations tested whereas gill ventilation rate of Spanish
mackerel increased and cruise swimming speed de-
Fig. 3 Scomberomorus niphonius. Gill ventilation rate (no. minÀ1)
creased as the oxygen concentrations decreased. These
and cruising swimming speed (cm sÀ1) of juvenile Spanish mackerel
under reduced and air-saturated (5.8 mg lÀ1) oxygen concentra- observations suggest that moon jellyfish has a higher
tolerance to low oxygen concentrations ( £ 2 mg lÀ1)
tions. Six replicates were conducted at each oxygen concentration.
Different letters indicate significant differences among oxygen than juvenile Spanish mackerel does.
concentration treatments (Kruskal-Wallis followed by Dunnett
The increase in consumption on the larvae (7.21 mm
test, P<0.05). Vertical bars indicate SD
SL) by moon jellyfish under oxygen concentrations £ 2
mg lÀ1 supports results from another experiment in which
ranged from 207.8±7.7 at 1 mg lÀ1 and 159.8±7.3 un-
the consumption by moon jellyfish on red sea bream larvae
der the control condition. There was a significant effect
(6.19 and 8.60 mm SL) increased at £ 2 mg lÀ1 (Shoji
of oxygen concentration on the gill ventilation rate
et al. 2005). Fukuhara (1985) observed under laboratory
(Kruskal-Wallis followed by Dunnett test, P<0.05).
conditions that the cruising swimming speed rapidly in-
Mean cruise swimming speed was higher in the higher
creased in red sea bream larvae >6 mm SL at which size
oxygen concentration treatments (Fig. 3). All Spanish
the development of unpaired fins begins. Nakayama et al.
mackerel were at the bottom of experimental tank hav-
(2003) reported that time to capture by moon jellyfish
ing stopped swimming at 5 min after the start of
significantly increased in red sea bream larvae >7 mm SL
experiment in 1 mg lÀ1 treatment. There was a signifi-
in aquaria. These observations suggest that red sea bream
cant difference in the swimming speed between 1 mg lÀ1
larvae >7 mm SL are less vulnerable to predation by
moon jellyfish than smaller larvae are apparently due to
their increased swimming ability.
Fish larvae are considered more vulnerable to phys-
iological stress by a decline in the oxygen concentration
since they are less physiologically developed (Rombough
1988). Dissolved oxygen concentrations £ 2 mg lÀ1 are
not considered lethal for short-term exposure, but re-
duce the ability of fish larvae to react to and escape from
jellyfish predators and to recover from contact with
jellyfish (Breitburg et al. 1994). Therefore, the vulnera-
bility of fish larvae to predation by jellyfish predators
increases under low dissolved oxygen concentrations
that are not lethal during short-term exposure. We
Fig. 4 Scomberomorus niphonius. Number of red sea bream larvae
conclude that red sea bream larvae >7 mm SL are
predated on in 15 min by one juvenile Spanish mackerel under
reduced and air-saturated (5.8 mg l-1) oxygen concentrations. Six highly vulnerable to predation by moon jellyfish under
replicates were conducted at each oxygen concentration. Different dissolved oxygen concentration £ 2 mg lÀ1 in nature; at
letters indicate significant differences among oxygen concentration
oxygen concentrations ‡ 4 mg lÀ1 they are potentially
treatments (Kruskal-Wallis followed by Dunnett test, P<0.05).
able to avoid moon jellyfish.
Vertical bars indicate SD
867
Costello and Colin (1994) examined the mechanisms zooplankton have been replaced by moon jellyfish in the
of prey capture by moon jellyfish under laboratory food web since the moon jellyfish biomass increased in
conditions and suggested that moon jellyfish can capture the Seto Inland Sea. The excess nutritional loading from
prey organisms with slower escape speeds than flow land is considered as one of the major factors that
velocity at the bell margin of moon jellyfish. In the caused the dominance by moon jellyfish in the summer
present study, bell contraction rate did not vary under plankton community in the Seto Inland Sea since it
oxygen concentrations between 1.04 and 5.75 mg lÀ1. promotes production of small zooplankton which is a
This result indicates that the volume of water filtered by major prey organism of the moon jellyfish (Mills 2001;
Uye and Ueta 2004). We suggest, based on present re-
moon jellyfish and their ability to capture prey did not
decrease under oxygen concentrations £ 2 mg lÀ1. sults, another possible mechanism for the increase in
Moon jellyfish survival was 100% at 1 mg lÀ1 in 3-h abundance of the moon jelly fish: the excess nutritional
experiments (Shoji, unpublished data). We conclude that loading has contributed to the increase in abundance of
the moon jellyfish is highly tolerant to low dissolved moon jellyfish through exacerbating the depletion in
oxygen concentrations and under these conditions there oxygen concentration which is advantageous to feeding
would be enhanced flow from ichthyoplankton to moon of the moon jellyfish.
jellyfish.
In contrast to the consumption by moon jellyfish, Acknowledgements We express our thanks to Dr. D.L. Breitburg,
consumption by juvenile Spanish mackerel decreased as Smithsonian Environmental Research Center, for teaching the
experimental protocol and Dr. E.D. Houde, Chesapeake Biological
dissolved oxygen concentration decreased. Early life
Laboratory, University of Maryland, Dr. Mark Wuenschel,
stages of scombrid fishes (including Scomberomorus fish)
NOAA Beaufort Laboratory, and two anonymous reviewers for
are considered to have a high oxygen requirement due to providing valuable comments on the manuscript. Thanks are due
the high swimming and metabolic rates (Hunter 1981). to Mr. A. Iwamoto and staff of JASFA for providing Spanish
The increase in gill ventilation rate and decrease in mackerel eggs and Dr. H. Motoh and staff of KPSFC for providing
red sea bream eggs. All experiments were conducted in Japan, and
swimming speed of juvenile Spanish mackerel with the
were in compliance with the current laws.
decline in oxygen concentration to 4 mg lÀ1 in the
experiments indicate that the oxygen concentration
£ 4 mg lÀ1 was physiologically stressful for juvenile
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