453
Enhancement of jellyfish (Aurelia aurita) populations by
extensive aquaculture rafts in a coastal lagoon in Taiwan
Wen-Tseng Lo, Jennifer E. Purcell, Jia-Jang Hung, Huei-Meei Su, and Pei-Kai Hsu
Lo, W-T., Purcell, J. E., Hung, J-J., Su, H-M., and Hsu, P-K. 2008. Enhancement of jellyfish (Aurelia aurita) populations by extensive aquaculture rafts
in a coastal lagoon in Taiwan. – ICES Journal of Marine Science, 65: 453–461.
Blooms of the moon jellyfish, Aurelia aurita, often occur in coastal waters that are heavily affected by human construction, such as harbours.
Tapong Bay is a hypertrophic lagoon in southwestern Taiwan that was studied between August 1999 and September 2004. The removal of
extensive oyster-culture rafts in June 2002 provided a “natural” experiment to examine the effects of aquaculture on processes and communities in the lagoon. The removal caused many changes in the ecosystem, including increases in flushing, light penetration, dissolved
oxygen, salinity, chlorophyll a, primary production, and zooplankton, but decreases in nutrients, periphyton, and dramatically reduced
populations of bivalves, zooplanktivorous fish, and jellyfish (A. aurita). We conclude that environmental and trophic conditions were
favourable for jellyfish throughout the study period. Therefore, we believe that aquaculture rafts enhanced jellyfish populations by
three probable mechanisms: the rafts provided substrate and shading for the larval settlement and polyp colony formation, and the
rafts restricted water exchange in the lagoon. Aquaculture is increasing rapidly in Asia, and the problems associated with jellyfish may
also increase.
Keywords: bivalve, circulation, eutrophication, fish, nutrients, oyster, phytoplankton, water budget, zooplankton.
Received 6 July 2007; accepted 19 October 2007; advance access publication 24 January 2008.
W-T. Lo, J. E. Purcell, H-M. Su, and P-K. Hsu: Department of Marine Biotechnology and Resources, Asian-Pacific Ocean Research Centre, Kuroshio
Research Group, National Sun Yat-Sen University, 70 Lienhai Road, Kaohsiung, Taiwan 804, Republic of China. J-J. Hung: Institute of Marine Geology
and Chemistry, National Sun Yat-Sen University, 70 Lienhai Road, Kaohsiung, Taiwan 804, Republic of China. J. E. Purcell: Western Washington
University, Shannon Point Marine Center, 1900 Shannon Point Road, Anacortes, WA 98221, USA. Correspondence to J. E. Purcell: tel: þ1 360
2932188; fax: þ1 360 2931083; e-mail: [email protected].
Introduction
Recently, problems related to jellyfish have captured the public’s
attention (e.g. Whiteman, 2002; Carpenter, 2004; De Pastino,
2006, 2007; Owen, 2006). The increase in jellyfish blooms is indicated by more frequent reports of injuries caused by stinging, and
interference with fishing activities and power plant operations.
Most fishers from the Seto Inland Sea, Japan, believe that
Aurelia aurita jellyfish populations have increased since the
1980s, and most dramatically in the past 10 years (Uye and
Ueta, 2004). Certainly, reports of jellyfish-related problems in
Japan have increased in recent years (Purcell et al., 2007).
The Seto Inland Sea is heavily affected by human activity, including eutrophication, fishing, aquaculture, and construction.
Concerns that jellyfish populations are increasing have stimulated speculation about the possible causes, including climate
change, eutrophication, overfishing, invasions, marine construction, and water diversion (e.g. Arai, 2001; Mills, 2001; Oguz,
2005a, b; Purcell, 2005; Hay, 2006; Graham and Bayha, 2007).
Possibly, global warming is causing the increase in jellyfish. Most
coastal jellyfish are budded asexually from an attached stage
(polyp) in the life cycle. In temperate scyphozoans, heightened
temperatures increased the asexual production of new jellyfish in
Aurelia labiata: both temperature and salinity had significant
effects and strong interaction (Purcell et al., 2007).
Several effects of eutrophication of coastal waters on the
environment are potentially beneficial for jellyfish (reviewed in
# 2008
Arai, 2001; Purcell et al., 2007). Briefly, more nutrients increase
production, shift nutrient ratios, and appear to shift the plankton
foodweb towards flagellates and small zooplankton (e.g. Sommer
et al., 2002). Aurelia spp. jellyfish, in particular, inhabit highly
eutrophic waters (e.g. Graham, 2001; Ishii, 2001; Mills, 2001).
They have a complex surface-ciliary feeding method (Southward,
1955) and are known to eat microplankton (Stoecker et al.,
1987). Recent stable isotope analyses placed A. aurita at a slightly
higher trophic level than copepods, confirming their utilization of
microplanktonic foods (R. D. Brodeur, pers. comm.).
Eutrophication is often associated with low levels of dissolved
oxygen (DO) (hypoxia), particularly in bottom waters (e.g.
Breitburg et al., 2003). Aurelia labiata jellyfish were reported to
have great tolerance to low levels of DO (Rutherford and
Thuesen, 2005). Jellyfish polyps are also tolerant of low oxygen
levels (Condon et al., 2001) and may find additional habitat
where other epifauna are reduced in dysoxic waters (Ishii, 2006).
Eutrophication and development also reduce water clarity
and light penetration, which may alter the feeding environment
to benefit non-visual gelatinous predators over visually feeding
fish.
Aquaculture may accidentally benefit jellyfish populations in
several ways. First, if additional feed is provided, eutrophication
can lead to the conditions described earlier. Second, culture rafts
provide substrate on which benthic polyps may form large colonies and produce more jellyfish. Aurelia spp. polyps are known
International Council for the Exploration of the Sea. Published by Oxford Journals. All rights reserved.
For Permissions, please email: [email protected]
454
to thrive on the undersurfaces of floating structures (e.g. Miyake
et al., 2002; Hoover, 2005). Third, zooplanktivorous fish are harvested for fishmeal in aquaculture feed (e.g. Kristofersson and
Anderson, 2006), which may provide opportunities for population
growth of gelatinous competitors.
Tapong Bay is a tropical lagoon located on the southwest coast
of Taiwan. It is relatively shallow and has been used extensively for
aquaculture for decades, during which the lagoon was occupied by
oyster hanging-culture rafts and fish net-pens. The lagoon ecosystem has undergone eutrophication as a result of poor circulation
and continuous inputs of nutrients and organic matter from
internal (cultured oysters and fish) and external (urban and aquaculture) sources (Hung and Hung, 2003; Hung et al., 2008). The
lagoon environment was cleaned with the complete removal of
the culture rafts and pens between June and December 2002.
One striking result of the culture raft removal was the disappearance of A. aurita jellyfish from Tapong Bay (Lo et al.,
2004). The obvious explanation for this was the removal of the
culture rafts, which had attached A. aurita polyps (H. J. Lin and
H. L. Hsieh, pers. comm.). Nevertheless, many other changes in
the lagoon could also have affected the jellyfish. Here, we
compare conditions in the lagoon before and after removal of
the culture rafts to determine why the jellyfish disappeared.
Material and methods
Study site
Tapong Bay is a small, semi-enclosed coastal lagoon in southwestern Taiwan (22827’N 120826’E; Figure 1). Its total area is
5.32 km2 and volume 11.6106 m3. Its depth ranges from
1 m near the tidal inlet to 6 m in the inner bay (mean depth =
2.2 m). Water exchange between Tapong Bay and Taiwan Strait
W-T. Lo et al.
is driven primarily by a semi-diurnal tide, which is somewhat
restricted by the narrow tidal inlet. In addition to direct freshwater input by precipitation, the terrestrial water input via the
Lipan Dike is derived mainly from urban and aquacultural wastewater with a moderate salinity (,20). The lagoon contained many
oyster rafts (19 166) and fish pens (3837) that were removed between
June and December 2002; the rafts were made of bamboo, and
measured ca. 2–4 m by 5–10 m (Hung et al., 2008).
Conditions in Tapong Bay are affected by the northeastern and
southwestern monsoons during the dry (October–April) and wet
(May –September) seasons, respectively, which also affect the
mixing of lagoon water. Total inputs of precipitation and wastewater are much greater in the wet than in the dry season.
Because of its small volume, salinity in the lagoon reflects this
seasonal variability, ranging from 25 in the wet season to 35 in
the dry season. Atmospheric temperature ranges from 228C in
winter (dry season) to 328C in summer (wet season; Hung and
Hung, 2003).
Sampling and analytical methods
Sampling in Tapong Bay was conducted monthly or bimonthly
from August 1999 to December 2002; after complete removal of
the culture rafts (January 2003), sampling was conducted either
bimonthly or quarterly at several stations in the lagoon (Figure 1,
Table 1). Data on hydrography, nutrients, chlorophyll a (Chl a)
production, phyto- and zooplankton, and jellyfish were collected
according to the methods described below.
Previous analyses of Tapong Bay before removal of the aquaculture rafts revealed both seasonal and spatial heterogeneity in all
variables (Hung and Hung, 2003; Lo et al., 2004; Su et al., 2004;
Lin et al., 2005; Hung et al., 2008; Hsu et al., in press).
Seasonal and spatial patterns were similar before and after
removal of the rafts (Hung et al., 2008; Hsu et al., in press;
H. J. Lin, pers. comm.). Here, we are concerned with differences
in the lagoon before and after removal of the culture rafts and
do not consider seasonal or spatial patterns. For this analysis,
data from all stations were averaged for each date. Dates before
removal were compared with dates after removal using the
Mann–Whitney rank sum tests.
Hydrography and nutrients
Near-surface temperatures were measured with a portable
conductivity-temperature sensor WTW, LF597. DO was measured
in situ with a portable DO meter (YSI 52); only measurements
from the bottom of the water column, where DO levels were
Table 1. Numbers of stations and sampling days in analyses in
Tapong Bay, southwestern Taiwan, before (August 1999 to July
2002) and after (February 2003 to September 2004) complete
removal of culture rafts by January 2003.
Figure 1. Structure of Tapong Bay, southwestern Taiwan, and
sampling station locations. Major wastewater inputs are from Lipan
Dike (far right) and Mangrove Creek (top centre). Tidal exchange
with the Taiwan Strait is restricted to a narrow canal (far left).
Stations for hydrographic (salinity, DO, and pH) and nutrient
sampling (Hung and Hung, 2003) are marked by triangles; stations
for phytoplankton, Chl a, and primary production sampling (Su et al.,
2004) are marked by circles; stations for temperature, zooplankton,
and jellyfish sampling are marked by squares. Locations of
aquaculture rafts in the bay (hatched areas) and aquaculture ponds
(light grey) surrounding the bay.
Number of
Days before
Days after
stations
(No.)
(No.)
Hydrography
(T,
S)
3
11
12
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . .
(T,
S,
pH,
DO)
10
9
5
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . .
Nutrients
10
9
5
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . .
Phytoplankton, Chl a,
6
9
5
IGP,
light
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . .
Zooplankton and jellyfish 3
11
12
Station locations are in Figure 1. Abbreviations are as follow: T, temperature;
S, salinity; DO, bottom dissolved oxygen; Chl a, integrated chlorophyll a.
455
Enhancement of jellyfish populations
lowest, were tested here. Water column pH was measured in situ
with a portable pH meter (Mettler MP-120) with reproducibility
better than +0.02. Data on monthly precipitation (rain in mm)
were obtained from the Central Weather Bureau of Taiwan
(http://www.cwb.gov.tw/). Photosynthetically active radiation
(PAR) was measured at the surface, mid-depth, and bottom of
the water column using a Li-Cor Quantum Li-189 meter.
Water samples were collected from Tapong Bay (Stations 1 –10,
Figure 1), Lipan Dike, and the adjacent coastal sea, before (from
August 1999 to July 2002) and after (from February 2003 to
September 2004) removal of the culture rafts (Table 1). Three
replicate water samples were collected from upper, middle, and
bottom layers using a peristaltic pump and a precleaned silicone
tube. Salinity was determined using an Autosal salinometer
(Guildine 8400B) in the laboratory to gain precise salinity values
(+0.002) for deriving salt and water budgets. An additional
four litres from each station were stored in a polyethylene bottle
and brought back to the laboratory immediately for further
analyses.
In the laboratory, the water sample was filtered through
precombusted GF/F filters (at 4508C, 4 h). The filtered water
was used to measure dissolved nutrients, including dissolved
inorganic nitrogen (NO3+NO2+NH4, hereafter DIN), dissolved
inorganic phosphate (PO4, hereafter DIP), dissolved silicate
(H4SiO4, hereafter DSi), dissolved organic carbon (DOC),
nitrogen (DON), and phosphorus (DOP). Generally, three replicate measurements were processed for each chemical analysis.
Particulate organic carbon (POC) and nitrogen (PON) were
measured from the filtered samples, placed in tin boats, then
combusted in a C/N/S analyser (Fisons NCS 1500) after removing
the inorganic carbon with 2 M hydrochloric acid (Hung et al.,
1999). The blank value attributed to precombusted GF/F filter
and tin boat demonstrated a precision of +0.3 mM C and
+0.2 mM N.
The biogeochemical fluxes and metabolism of nutrients and
carbon in the lagoon were evaluated using the LOICZ biogeochemical budget model (Smith et al., 1991; Gordon et al., 1996).
Details of modelling can be found at the LOICZ website (http://
www.nioz.Nl/loicz/) or from Hung and Hung (2003) for the
period before removal. This biogeochemical budget model is a
box model from which non-conservative nutrient and carbon
budgets can be constructed from non-conservative distributions
of nutrients and water budgets, which in turn are constrained
from the salt balance under a steady-state assumption. The nonconservative flux of a material is estimated from the flux deviation
between inputs and outputs, based on salt and water balances. The
non-conservative flux of dissolved inorganic phosphorus is
assumed to be an approximation of net metabolism, because
phosphorus is not involved in gas-phase reactions. Nitrogen and
carbon both have other major pathways, such as denitrification,
nitrogen fixation, gas exchange across the air–sea interface, and
calcification. The biogeochemical pathways of carbon can be
approximated from non-conservative phosphorus flux and C:P
stoichiometric ratio of reactive particles in the lagoon. Because
of the distinct variability in wastewater and material inputs with
time, water and nutrient budgets estimated from a box model
for the lagoon can only be valid within a season. Therefore,
carbon budgets were made for each sampling period before they
were integrated as annual budgets.
The net ecosystem metabolism (NEP) [difference between
gross production and respiration (p – r)] can be estimated
stoichiometrically from DDIP and the carbon to phosphate ratio
(C:P) of organic matter being produced or consumed in the
lagoon. Therefore,
½ p r ¼ DDICO ¼ DDIP ðC : PÞparticulate ;
where DDICO is the change in dissolved inorganic carbon. The
particulate organic C:P ratio in the lagoon was not determined,
and the Redfield ratio (106) was adopted for stoichiometric calculation, because phytoplankton was the primary producer in the
lagoon (Lin et al., 2005). Further details of methods and the resulting values are reported by date in Hung et al. (2008) and are used
in the current analysis.
Phytoplankton, Chl a, and productivity
Water samples were collected in triplicate at low tide for each site
every 2 –3 months from October 1999 to July 2004 (Table 1). An
aliquot from each station was fixed in Lugol’s solution after filtration through a 200 mm net. Taxa were identified and counted
from two 0.5 ml subsamples of the concentrated sample using a
light microscope under phase and DIC contrast at 400 after
settlement on a scaled slide. For this analysis, miscellaneous flagellates (Chlorophyta, Raphidophyta, and Euglenophyta) were
grouped. Chl a concentrations were determined spectrophotometrically by immediately filtering water samples in triplicate through
Whatman GF/F filters in the field and extracting them in 90%
acetone for 24 h at 48C in the dark (Parsons et al., 1984).
Productivity incubations were performed with bay water collected
at low tide in the early morning using a 2 l Van Dorn bottle. Three
light and three dark 300 ml BOD bottles were incubated in flowing
seawater tanks adjacent to Tapong Bay. Net production and respiration rates were derived from changes in DO concentrations over
time, as determined by a modified Winkler method (Pai et al.,
1993), in illuminated and dark bottles, respectively. Rates represent community rates.
Zooplankton and jellyfish abundance
Samples were collected monthly (before removal) and bimonthly
(after removal; Table 1) by towing a NorPac net with 100 mm
mesh and flowmeter near-surface (0– 1 m). Samples were immediately preserved in 5 –10% formalin solution. In the laboratory,
each sample was subsampled with a Folsom plankton splitter,
and a minimum of 500 organisms were identified and counted
by use of a dissecting microscope.
Results
Lagoon-wide averages of hydrographic measurements revealed a
few significant differences before and after removal of the
culture rafts (Table 2). Temperature, pH, and DO were similar
in both periods. Salinity was significantly higher in the period
after (32.6) removal than before (31.8); however, rain revealed
no significant difference between periods. Water clarity increased
significantly after removal, and the amounts of light penetrating
the water column also increased, but not significantly. Lagoonwide water residence times were significantly longer (10 d) when
the culture rafts were present than after (6 d).
Before removal of the culture rafts, lagoon-wide averaged concentrations of DSi (20.3 mM), DIN (16.4 mM), and DIP (4.0 mM)
were greater than after the removal (DSi = 10.0 mM; DIN =
11.4 mM; DIP = 1.5 mM); differences were significant at the 0.05
probability level for DSi and DIP, but not for DIN (Table 2).
456
Table 2. Physical variables, nutrients, and ecosystem properties measured before vs. after removal of oyster-culture rafts from Tapong Bay, Taiwan.
Physical variables
Before
vs.
after
p-value
Surface salinity
31.8
,
32.6
,0.01
pH
8.18
8.14
NS
DO2 (mg l21)
4.0
4.5
NS
Rain (mm)
169
168
NS
Resid (d)a
10.0
.
6.1
,0.01
DSi (mM)a
DIN (mM)a
DIP (mM)a
DON (mM)a
DOP (mM)a
DOC (mM)a
20.3
.
10.0
,0.05
16.4
11.4
0.1
4.0
.
1.5
0.01
24.4
39.8
,0.1
2.4
1.2
,0.1
162.4
232.3
,0.1
Chl a (mg m23)
IGP (mmol O2 m23 h21)
Light at bottom (mE m22 s21)
nfix-denit (mol m22 year21)a
NEP (mol m22 year21)a
6
,
13
0.01
12
19
0.1
197
225
NS
1.4
5.4
NS
5.6
11.6
NS
Temp (88 C)
26.9
27.2
NS
Water motion (g d21)
10.2
,
16.1
,0.1
Nutrients
Before
vs.
after
p-value
Ecosystem properties
Before
vs.
after
p-value
p-values are results from Mann–Whitney rank sum tests comparing variables (means of all stations for each sampling date) before (1999–2002) and after (2003–2004) culture raft removal. Figure 1 shows the
sampling stations. Abbreviations for variables represent: Rain, monthly total; D, dissolved; O2, oxygen; Resid, water residence time; I, inorganic; O, organic; Si, silica; N, nitrogen; P, phosphate; C, carbon; D, change;
NEP, net ecosystem metabolism; nfix-denit, nitrogen fixation vs. denitrification.
a
Data from (Hung et al., 2008).
W-T. Lo et al.
0.3
.
0
0.001
70
30
NS
600
,
3100
0.002
800
1600
NS
20
,
2000
0.002
50
,
300
0.002
Pcalanus (ind. m23)
Copepods (ind. m23)
Zooplankton
500
,
3000
0.05
Acartia (ind. m23)
Bestolina (ind. m23)
Nauplii (ind. m23)
Dinoflag (cells l21)
4 103
,
28 103
NS
Diatoms (cells l21)
2 104
,
4 104
NS
Cyano (cells l21)
5 103
,
30 103
NS
Before
vs.
after
p-value
Before
vs.
after
p-value
Aurelia (ind. m23)
Oithona (ind. m23)
243.5
.
0
NT
Flagellates (cells l21)
3 103
,
30 103
0.02
,1.7–14.5
.
0
NT
Oysters (g ww m23)a
Phytopl (cells l21)
3 104
,
13 104
0.1
An important consequence of the culture raft removal was
improved circulation in Tapong Bay. Dominant semi-diurnal
and diurnal tides controlled primary water exchange and subsequently drove the lagoon circulation. Two sub-anticlockwise
circulation patterns were separated generally from the middle
area of the lagoon in a northeast–southwest direction (Yu,
2001). The hydrochemistry and water budgets in Tapong Bay
before removal of the culture rafts were described by Hung and
Hung (2003). Briefly, the water residence time ranged from 7 d
(summer) to 13 d (winter) with a mean of 10 d. It was longer in
the inner lagoon (7–24 d) than in the outer lagoon (4–12 d).
After removal of the rafts, the water residence time decreased to
4 –9 d with a mean of 6 d (Hung et al., 2008). Because the
major circulation pattern remained the same, the water residence
time in the inner and outer lagoon after removal was reduced
Periphyton (g ww m23)a
Physical changes following culture raft removal
Phytoplankton
Discussion
Table 3. Organisms sampled before and after removal of culture rafts from Tapong Bay, Taiwan.
Lagoon-wide averaged concentrations of DON and DOC were
greater before removal (24.4 and 162.4 mM) than after (39.8 and
232.3 mM), but DOP concentrations were greater before
(2.4 mM) removal than after (1.2 mM); however, these differences
were not significant at the 5% probability level but were significant
at the 10% level.
Nutrient and carbon budgets were determined principally by
water budget, nutrient and carbon distributions, and internal biogeochemical processes (Hung et al., in 2008). The water budget
was derived from the salt balance. For a nutrient budget, the difference between total inputs and total outputs indicates source
(inputs , outputs) or sink (inputs . outputs) in the ecosystem.
The system DDIP may be used to approximate the NEP of the
lagoon (Hung and Hung, 2003). A system with a negative DDIP is
generally regarded as autotrophic and a net CO2-consuming
system via a net production of organic matter (production . respiration). The NEP in Tapong Bay was all positive except for one
negative and two near 0 (Hung et al., 2008). Thus, Tapong Bay is
an autotrophic system. The mean value of NEP increased by 37%
after removal of the culture rafts; however, the difference was not
statistically significant.
Lagoon-wide averaged phytoplankton cell numbers, biomass
(Chl a), and integrated gross primary production (IGP) were
greater after removal of the culture rafts than before (Tables 2
and 3). Significant differences were seen only for Chl a and
numbers of miscellaneous flagellates at the 5% level, and for IGP
and total cell numbers at the 10% level. The proportions of the
various phytoplankton groups also changed. Before culture raft
removal, diatoms predominated, with 62.5% of the total
numbers; after raft removal, the contributions of the groups
(cyanobacteria, diatoms, dinoflagellates, and miscellaneous flagellates) were similar (22 –31%).
Lagoon-wide averaged abundance of copepods increased
greatly after removal of the culture rafts (Table 3). Differences
between abundances before and after were significant for all
species combined (a sixfold increase) and for all of the predominant species individually, except for Oithona spp. Copepod
nauplii abundance doubled, but was not significant.
Lagoon-wide averaged abundances of the jellyfish, A. aurita,
changed from high values (Figure 2; mean 0.3 ind. m23) with
the culture rafts to the complete absence of jellyfish after
removal (Table 3).
p-values are results from Mann–Whitney rank sum tests comparing variables (means of all stations for each sampling date) before (1999– 2002) and after (2003–2004) culture raft removal. Figure 1 shows the
sampling stations. Abbreviations for variables represent: Phytopl, total phytoplankton; Cyano, cyanobacteria; Dinoflag, dinoflagellates; Flagellates, sum of miscellaneous flagellates (Euglenophyta, Chlorophyta,
Cryptophyta, Raphidophyta); Copepods, total copepods; Pcalanus, Paracalanus; Nauplii, copepod nauplii; NT, not tested.
a
From Lin et al. (2005).
457
Enhancement of jellyfish populations
458
W-T. Lo et al.
Figure 2. Jellyfish (Aurelia aurita) abundance in Tapong Bay, southwestern Taiwan, from August 1999 to December 2004. Samples were
collected on a bimonthly schedule (February/April/June/August/October/December). Extensive aquaculture rafts were removed in the
second half of 2002, as indicated by the vertical grey line. Station locations are marked by squares in Figure 1.
proportionately to 5 –13 d and 3 –7 d, respectively. An independent estimate of water motion revealed a significant increase
after removal (Su et al., 2004; H. J. Lin, pers. comm.).
Apparently, the culture rafts reduced water flow in the lagoon.
This affected some aspects of the conditions in the lagoon.
Specifically, DO concentrations were somewhat higher after
removal. DO in the bottom water seldom was as low as
2 mg O2 l21 (Hung and Hung, 2003; Hung et al., 2008),
suggesting that hypoxia was not a serious problem in Tapong
Bay, either before or after removal. Increased salinity after
removal may have been caused by improved flushing by ocean
water.
Decreasing ocean pH is one effect of climate warming (Caldeira
and Wickett, 2003). Attrill et al. (2007) confirmed a significant
negative correlation between nematocyst occurrence in continuous plankton recorder (CPR) samples and pH (range 8.0 –8.3)
during the period 1971–1995, and suggested that pelagic cnidarians may benefit from this change because of the detrimental
effects of high pH on calcifying organisms; however, insignificant
changes in pH (20.04) were observed following removal of the
culture rafts, and probably had no effect on jellyfish populations.
Changes in nutrients, production, and the foodweb
following culture raft removal
Decreased nutrients were observed after removal of the culture
rafts, which could be attributed to many changes in Tapong Bay.
Removal of the oysters eliminated that source of excreted nutrients. The removal of fish-pen cultures also would have eliminated
nutrient additions from excess feed and fish waste products;
however, the magnitudes of such additions are unknown. The
oysters were estimated to consume 44% of the production in
the lagoon (Lin et al., 2006). Removal of the oysters eliminated a
major consumer of suspended particulate matter from the ecosystem, resulting in increased availability of particulate food in the
water column. Increases in phytoplankton, Chl a, and IGP were
observed. These increases would have required additional nutrients. Increased flushing may also have contributed to lower nutrient concentrations (Hung et al., 2008).
The DIN:DIP ratio ranged between 1.5 and 9.2 throughout the
study, which is much lower than the Redfield ratio of 16 (Redfield
et al., 1963). The low DIN:DIP ratios were probably caused by
P-contaminated wastewater inputs from the Lipan Dike with
very low DIN:DIP ratios (,2.5). Because both DIN and DIP concentrations were much greater than the critical levels (DIN ,
1 mM; DIP , 0.1 mM; DSi , 2 mM) of nutrient limitation (e.g.
Justič et al., 1995), the lagoon appears to have excess DIP (Hung
and Hung, 2003; Hung et al., 2008).
Environmental conditions that seem to favour jellyfish have
high nutrients, but low Si:N ratios, characteristic of eutrophic
coastal waters (Sommer et al., 2002). This is associated with a predominance of small flagellates over diatoms and a strong microbial
foodweb that is fuelled heterotrophically by bacteria rather than
autotrophically. Such changes occurred in Tapong Bay following
removal of the culture rafts. Despite an apparent decrease in nutrients, levels before and after culture raft removal were comparable
with other eutrophic systems (Tada et al., 2001; Hung and Kuo,
2002; Newton et al., 2003). The Si:N ratio decreased from 1.24
to 0.88, with the proportion of diatoms being halved and the proportion of small flagellates increasing 2.5-fold. Tapong Bay was
previously reported to be an autotrophic ecosystem, a sink for
carbon dioxide, and to have net nitrogen fixation (Hung and
Hung, 2003). On the basis of the nutrient changes, jellyfish populations might have been expected to increase after culture raft
removal rather than disappear.
Phytoplankton abundance and community composition
changed after removal of the oyster cultures. Total phytoplankton
abundance increased, mainly as a result of more miscellaneous flagellates, although increases were seen in cyanobacteria, diatoms,
and dinoflagellates as well. After culture raft removal, the
proportion of diatoms was halved, and the proportion of miscellaneous flagellates had increased 2.5-fold. These changes probably
reflect several influences, including the shift in main consumers
from oysters to copepods, improved light availability brought
about by the elimination of shading by the rafts, improved water
circulation, and altered nutrient ratios.
The lack of statistical significance for some phytoplankton
groups probably is the result of substantial spatial and seasonal
Enhancement of jellyfish populations
variations. The number of phytoplankton cells, Chl a, and IGP
increased consistently from the tidal inlet to the inner lagoon,
and the increase was more pronounced after removal than
before (Hung et al., 2008). Distributions of Chl a were significantly
inversely correlated with total suspended matter, but not with
nutrients, causing Hung et al. (2008) to conclude that IGP and
Chl a may be controlled primarily by light availability and temperature in Tapong Bay, which has high turbidity and abundant
nutrients.
Copepod abundance increased sixfold in Tapong Bay after
removal of the culture rafts, probably the result of increased availability of phytoplankton and reduction of zooplanktivorous fish
(H. J. Lin, pers. comm.) and jellyfish (Lo and Chen, 2008).
Therefore, a major competitor (oysters) and major predators
(fish and jellyfish) of copepods were reduced or removed from
Tapong Bay. The increased abundance of suitable food (copepods)
indicates favourable conditions for jellyfish, and their disappearance is opposite to expectations.
Probable effects of ecosystem changes on jellyfish
in Tapong Bay
Hydrographic conditions in Tapong Bay were favourable for the
survival and reproduction of A. aurita, both before and after
culture raft removal. DO was not at stressful levels either before
or after removal. Aurelia spp. jellyfish and polyps appear to be
very tolerant of hypoxic conditions (Rutherford and Thuesen,
2005; Ishii, 2006). Temperature did not change appreciably.
Moreover, measured temperature had a greater range before
(16.9– 31.88C) than after (23.0 –31.48C) removal, suggesting that
neither unusually low nor high temperatures were probable
causes for jellyfish disappearance.
Salinity near surface did change significantly, and the effect on
A. aurita is unclear. Ephyrae were sampled in Tapong Bay from
April 1999 to April 2002 (W-TL, unpublished data). They
occurred during October–April, but were abundant between
November and February. Therefore, they were present (1 –
328 ephyrae m23) during the coolest (24.1 + 3.18C) months
with the highest surface salinities (31.7 + 2.5). Additionally, the
seasonal rains before culture raft removal changed surface salinities
by as much as 10 (Lo et al., 2004), but this did not eradicate the A.
aurita population.
Results for other scyphozoan species suggest tolerance of changing salinities. Salinity had significant effects on A. labiata polyps
(Purcell, 2007). In combinations of low temperature (78C) and
high (34) and low (20) salinity, polyps had 83 – 92% survival,
but few jellyfish were produced; however, in combinations of
high temperature (158C) and high and low salinity, polyps had
83 –100% survival and high jellyfish production (Purcell, 2007).
In contrast, the combination of high salinity (30) and temperature
(31.2– 33.18C) from an El Niño was detrimental to Mastigias sp.
jellyfish in a marine lake in Palau (normal 30.88C, 25.5 salinity);
however, although Aurelia spp. in the lake appeared damaged at
the same time, their population did not decrease (Dawson et al.,
2001). In addition, Mastigias sp. polyps were alive and asexually
reproducing during this period (Dawson et al., 2001). We
believe that the overall salinity increase of 0.8 in Tapong Bay
probably would not have caused the jellyfish to disappear.
Water exchange in Tapong Bay increased after removal of the
culture rafts, which may have increased transport of the jellyfish
and ephyrae from the bay. Jellyfish were present at lagoon-wide
water residence times of 5.8 –13.2 d, with the greatest abundances
459
Figure 3. Numbers of Aurelia aurita jellyfish (solid circles) and
ephyrae (triangles) in relation to water residence time in Tapong Bay
before (on nine dates from August 1999 to July 2002) removal of
aquaculture rafts. After removal of the rafts, no jellyfish or ephyrae
were found, but water residence times are shown (open circles) on
the x-axis for six dates between February 2003 and September 2004.
Zero values of abundance are shown as 0.01, so that they appear on
the log scale.
at the shortest time; also, jellyfish were not collected on two dates
with moderate residence times (8.6 –10.1 d; Figure 3). Ephyrae
were present at long water residence times of 9.3 –13.2 d; they
were absent at resident times of 5.8 – 12.4 d. The water residence
times calculated for after-culture raft removal are shorter
(3.8 – 9.2 d) than before, but overlapped with residence times
when jellyfish, but not ephyrae, were present in Tapong Bay
(Figure 3). Water residence times were longer in the deeper
(6 m) inner lagoon than in the outer lagoon before and after
removal (Hung et al., 2008), and jellyfish abundance was greater
there (Figure 2). Therefore, we conclude that increased water
exchange could have promoted transport of jellyfish and their
planula larvae and ephyrae from the lagoon. The importance of
transport is unknown.
Another direct consequence of culture raft removal was
increased solar radiation in the water column, which may have
been detrimental to the A. aurita population. The planula larvae
of the jellyfish prefer to settle on poorly illuminated undersurfaces
in the water (Brewer, 1978). Light levels reaching the bottom of
Tapong Bay after culture raft removal averaged 225 mE m22 s21,
which was considerably higher than those measured underneath
covered marina floats (2– 6 mE m22 s21) where A. labiata polyps
flourished (Purcell et al., 2007). When the culture rafts were
removed from the surface, the larvae were deprived of settling surfaces, and any remaining hard surface may have been exposed to
light levels that are detrimental to or inhibitory for settlement of
the planulae.
We believe that aquaculture rafts provided shaded surfaces for
larval settlement and polyp colony expansion and increased retention of the planulae, ephyrae, and jellyfish in Tapong Bay. Removal
of favourable polyp substrate with the culture rafts probably was
the main cause for the disappearance of jellyfish, perhaps acting
together with increased light and water exchange in the lagoon.
Therefore, we observed three probable mechanisms by which
aquaculture rafts enhanced jellyfish populations; the rafts provided
460
substrate and shading for the polyps, and the rafts restricted water
exchange in the lagoon.
Implications for the future
The current world human population is projected to increase 46%
by 2050 (US Census Bureau, 2006). Human influences and
demands on the ocean will increase with population growth.
Global bivalve aquaculture (mussels, oysters, scallops) increased
fivefold between 1980 and 2005; the Asian share of the world production increased from 60% in 1980 to 93% in 2005 (FAO, 2007).
Similarly, global marine fish production has increased ninefold
since 1980, with Asia’s share high (80% in 2005; FAO, 2007).
Global fish production is projected to double between 1997 and
2020, with especially large increases in developing nations and in
aquaculture (Delgado et al., 2003). Therefore, we conclude that
floating aquaculture structures probably will increase in the
future, increase favourable habitat for jellyfish polyps, and
locally increase jellyfish populations, especially in areas where
water flow is restricted. The problems are likely to occur in Asia.
We recommend additional research into materials that may
inhibit settlement by jellyfish larvae (e.g. Hoover, 2005).
Acknowledgements
This research was supported by grants from the National Science
Council to J-JH, W-TL, and H-MS and from the Ministry of
Education of the Republic of China to W-TL [94-C030220
(Kuroshio project)] and J-JH [95-C030214 (Kuroshio project)].
We thank H-HC for obtaining information on the numbers of
oyster rafts and fish pens.
References
Arai, M. N. 2001. Pelagic coelenterates and eutrophication: a review.
Hydrobiologia, 451: 69– 87.
Attrill, M. J., Wright, J., and Edwards, M. 2007. Climate-related
increases in jellyfish frequency suggest a more gelatinous future
for the North Sea. Limnology and Oceanography, 52: 480 – 485.
Breitburg, D. L., Adamack, A., Rose, K. A., Kolesar, S. E., Decker, M.
B., Purcell, J. E., Keister, J. E., et al. 2003. The pattern and influence
of low dissolved oxygen in the Patuxent River, a seasonally hypoxic
estuary. Estuaries, 26: 280 – 297.
Brewer, R. H. 1978. Larval settlement behavior in the jellyfish Aurelia
aurita (Linnaeus) (Scyphozoa: Semaeostomeae). Estuaries, 1:
120– 122.
Caldeira, K., and Wickett, M. E. 2003. Anthropogenic carbon and
ocean pH. Nature, 425: 385.
Carpenter, B. 2004. Feeling the sting: warming oceans, depleted fish
stocks, dirty water—they set the stage for a jellyfish invasion.
U. S. News and World Report, 137: 68– 69. http://www.usnews.
com/culture/article/040816/16jelly.html
Condon, R. H., Decker, M. B., and Purcell, J. E. 2001. Effects of low
dissolved oxygen on survival and asexual reproduction of scyphozoan polyps (Chrysaora quinquecirrha). Hydrobiologia, 451:
89 – 95.
Dawson, M. N., Martin, L. E., and Penland, L. K. 2001. Jellyfish
swarms, tourists, and the Christ-child. Hydrobiologia, 451:
131– 144.
De Pastino, B. 2006. Giant jellyfish invade Japan. http://news.nationalgeographic.com/news/2006/01/0119_060119_jellyfish.html
De Pastino, B. 2007. Blue jellyfish invade Australia beaches. http://
news.nationalgeographic.com/news/2007/01/
070123-blue-jellyfish.html
Delgado, C. L., Wada, N., Rosegrant, M. W., Meijer, S., and Ahmed, M.
2003. Outlook for Fish to 2020: Meeting Global Demand. A 2020
Vision for Food, Agriculture, and the Environment Initiative, pp.
W-T. Lo et al.
1 – 26. International Food Policy Research Institute, Washington,
DC.
FAO. 2007. Fisheries and Aquaculture Department Website. http://
www.fao.org. Accessed 28 March 2007.
Gordon, D. C., Boudreau, P. R., Mann, K. H., Ong, K. H., Silvert,
W. L., Smith, S. V., Wattayakorn, G., et al. 1996. LOICZ
Biogeochemical Modelling Guidelines. LOICZ Reports and
Studies, 5. LOICZ, Texel, The Netherlands. 96 pp.
Graham, W. M. 2001. Numerical increases and distributional shifts of
Chrysaora quinquecirrha (Desor) and Aurelia aurita (Linné)
(Cnidaria: Scyphozoa) in the northern Gulf of Mexico.
Hydrobiologia, 451: 97– 111.
Graham, W. M., and Bayha, K. M. 2007. 14 Biological invasions by
marine jellyfish. In Ecological Studies, 193. Biological Invasions,
pp. 240– 255. Ed. by W. Nentwig. Springer-Verlag, Berlin.
Hay, S. 2006. Marine ecology: gelatinous bells may ring change in
marine ecosystems. Current Biology, 16: R679– R682.
Hoover, R. A. 2005. Population characteristics of the scyphozoan
Aurelia labiata and predation by nudibranchs. MSc thesis,
Western Washington University, Bellingham, WA.
Hsu, P. K., Lo, W. T., and Shih, C. T. The coupling of copepod assemblages and hydrography in a eutrophic lagoon in Taiwan: seasonal
and spatial variations. Zoological Studies, in press.
Hung, J. J., and Hung, P. Y. 2003. Carbon and nutrient dynamics in a
hypertrophic lagoon in southwestern Taiwan. Journal of Marine
Systems, 42: 97 – 114.
Hung, J. J., and Kuo, F. 2002. Temporal variability of carbon and nutrient budgets from a tropical lagoon in Chiku, southwestern Taiwan.
Estuarine Coastal and Shelf Science, 54: 887– 900.
Hung, J-J., Hung, C-S., and Su, H. M. 2008. Biogeochemical responses
to the removal of maricultural structures from an eutrophic lagoon
(Tapong Bay) in Taiwan. Marine Environmental Research, 65:
1 – 17.
Hung, J-J., Lin, C-S., Hung, G-W., and Chung, C. 1999. Lateral transport of lithogenic particles from the continental margin of the
southern East China Sea. Estuarine, Coastal and Shelf Science,
49: 483– 499.
Ishii, H. 2001. The influence of environmental changes upon the
coastal plankton ecosystems, with special reference to mass occurrence of jellyfish. Bulletin of the Plankton Society of Japan, 48:
55 – 61.
Ishii, H. 2006. Adaptation to coastal environmental changes in the
polyp stage in relation to jellyfish blooms in Tokyo Bay. PICES
XV abstract S2-3117. Yokohama, 13 October 2006.
Justič, D., Rabalais, N. N., and Turner, R. E. 1995. Stoichiometric
nutrient balance and origin of coastal eutrophication. Marine
Pollution Bulletin, 30: 41 – 46.
Kristofersson, D., and Anderson, J. L. 2006. Is there a relationship
between fisheries and farming? Interdependence of fisheries,
animal production and aquaculture. Marine Policy, 30: 721 – 725.
Lin, H. J., Dai, W. W., Shao, K. T., Su, H. M., Lo, W. T., Hsieh, H. L.,
Fang, L. S., et al. 2006. Trophic structure and functioning in a
eutrophic and poorly flushed lagoon in southwestern Taiwan.
Marine Environmental Research, 62: 61 – 82.
Lin, H. J., Wang, T. C., Su, H. M., and Hung, J. J. 2005. Relative
importance of phytoplankton and periphyton on oyster-culture
pens in a eutrophic tropical lagoon. Aquaculture, 243: 279– 290.
Lo, W. T., and Chen, I. L. 2008. Population succession and feeding of
scyphomedusae, Aurelia aurita, in a eutrophic tropical lagoon in
Taiwan. Estuarine, Coastal and Shelf Science, 76: 227 – 238.
Lo, W. T., Chung, C. L., and Shih, C. T. 2004. Seasonal distribution of
copepods in Tapong Bay, southwestern Taiwan. Zoological Studies,
43: 464– 474.
Mills, C. E. 2001. Jellyfish blooms: are populations increasing globally
in response to changing ocean conditions? Hydrobiologia, 451:
55 – 68.
Enhancement of jellyfish populations
Miyake, H., Terazaki, M., and Kakinuma, Y. 2002. On the polyps of the
common jellyfish Aurelia aurita in Kagoshima Bay. Journal of
Oceanography, 58: 451 –459.
Newton, A., Icely, J. D., Falcao, M., Nobre, A., Nunes, J. P., Ferreira,
J. G., and Vale, C. 2003. Evaluation of eutrophication in the Rio
Formosa coastal lagoon, Portugal. Continental Shelf Research, 23:
1945– 1961.
Oguz, T. 2005a. Black Sea ecosystem response to climatic teleconnections. Oceanography, 18: 122– 133.
Oguz, T. 2005b. Long-term impacts of anthropogenic forcing on the
Black Sea ecosystem. Oceanography, 18: 112– 121.
Owen, J. 2006. Jellyfish invasion puts sting on Europe beaches. http://
news.nationalgeographic.com/news/2006/08/
060818-jellyfish-spain.html.
Pai, S. C., Gong, G. C., and Liu, K. K. 1993. Determination of dissolved
oxygen in seawater by direct spectrophotometry of total iodine.
Marine Chemistry, 41: 343– 351.
Parsons, T. R., Maita, Y., and Lalli, C. M. 1984. A Manual of Chemical
and Biological Methods for Seawater Analysis. Pergamon Press,
Oxford. 173 pp.
Purcell, J. E. 2005. Climate effects on formation of jellyfish and ctenophore blooms. Journal of the Marine Biological Association of the
UK, 85: 461 –476.
Purcell, J. E. 2007. Environmental effects on asexual reproduction rates
of the scyphozoan, Aurelia aurita. Marine Ecology Progress Series,
348: 183 – 196.
Purcell, J. E., Uye, S. I., and Lo, W. T. 2007. Anthropogenic causes of
jellyfish blooms and their direct consequences for humans: a
review. Marine Ecology Progress Series, 350: 153– 174.
Redfield, A. C., Ketchum, B. H., and Rechard, F. A. 1963. The influence
of organisms on the composition of sea water. In The Sea, pp. 26 –
77. Ed. by M. H. Hill. Interscience, New York.
Rutherford, L. D., and Thuesen, E. V. 2005. Metabolic performance
and survival of medusae in estuarine hypoxia. Marine Ecology
Progress Series, 294: 189 – 200.
461
Smith, S. V., Hollibaugh, J. T., Dollar, S. J., and Vink, S. 1991. Tomales
Bay metabolism: C– N – P stoichiometry and ecosystem heterotrophy at the land – sea interface. Estuarine, Coastal and Shelf Science,
33: 223– 257.
Sommer, U., Stibor, H., Katechakis, A., Sommer, F., and Hansen, T.
2002. Pelagic food web configurations at different levels of nutrient
richness and their implications for the ratio fish production:primary production. Hydrobiologia, 484: 11 – 20.
Southward, A. J. 1955. Observations on the ciliary currents of the jellyfish, Aurelia aurita. Journal of the Marine Biological Association of
the UK, 34: 210– 216.
Stoecker, D. K., Michaels, A. E., and Davis, L. H. 1987. Grazing by the
jellyfish Aurelia aurita on microzooplankton. Journal of Plankton
Research, 9: 901– 915.
Su, H. M., Lin, H. J., and Hung, J. J. 2004. Effects of tidal flushing on
phytoplankton in a eutrophic tropical lagoon in Taiwan. Estuarine,
Coastal and Shelf Science, 61: 739– 750.
Tada, K., Morishita, M., Hamada, K. I., Montani, S., and Yamada, M.
2001. Standing stock and production rate of phytoplankton and a
red tide outbreak in a heavily eutrophic embayment, Dokai Bay,
Japan. Marine Pollution Bulletin, 42: 1177– 1186.
US Census Bureau. 2006. Total midyear population for the world:
1950– 2050. http://www.census.gov/idb/www/worldpop.html
Uye, S., and Ueta, Y. 2004. Recent increase of jellyfish populations and
their nuisance to fisheries in the Inland Sea of Japan. Bulletin of the
Japanese Society of Fisheries Oceanography, 68: 9 – 198 (in
Japanese with English abstract).
Whiteman, L. 2002. The blobs of summer. NRDC The Earth’s Best
Defense, 24: 14 – 19.
Yu, C. S. 2001. Dynamic interaction and numeric simulation among
Tapong Bay, Kaoping Estuary and Kaoping Canyon. Annual
Report of National Science Council, Taiwan (in Chinese).
doi:10.1093/icesjms/fsm185