Enhancement of jellyfish (Aurelia aurita) populations by extensive aquaculture rafts in a coastal lagoon in Taiwan
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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.
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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 com-
munities 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: purcelj3@wwu.edu.
Introduction Arai, 2001; Purcell et al., 2007). Briefly, more nutrients increase
Recently, problems related to jellyfish have captured the public’s production, shift nutrient ratios, and appear to shift the plankton
attention (e.g. Whiteman, 2002; Carpenter, 2004; De Pastino, foodweb towards flagellates and small zooplankton (e.g. Sommer
2006, 2007; Owen, 2006). The increase in jellyfish blooms is indi- et al., 2002). Aurelia spp. jellyfish, in particular, inhabit highly
cated by more frequent reports of injuries caused by stinging, and eutrophic waters (e.g. Graham, 2001; Ishii, 2001; Mills, 2001).
interference with fishing activities and power plant operations. They have a complex surface-ciliary feeding method (Southward,
Most fishers from the Seto Inland Sea, Japan, believe that 1955) and are known to eat microplankton (Stoecker et al.,
Aurelia aurita jellyfish populations have increased since the 1987). Recent stable isotope analyses placed A. aurita at a slightly
1980s, and most dramatically in the past 10 years (Uye and higher trophic level than copepods, confirming their utilization of
Ueta, 2004). Certainly, reports of jellyfish-related problems in microplanktonic foods (R. D. Brodeur, pers. comm.).
Japan have increased in recent years (Purcell et al., 2007). Eutrophication is often associated with low levels of dissolved
The Seto Inland Sea is heavily affected by human activity, includ- oxygen (DO) (hypoxia), particularly in bottom waters (e.g.
ing eutrophication, fishing, aquaculture, and construction. Breitburg et al., 2003). Aurelia labiata jellyfish were reported to
Concerns that jellyfish populations are increasing have stimu- have great tolerance to low levels of DO (Rutherford and
lated speculation about the possible causes, including climate Thuesen, 2005). Jellyfish polyps are also tolerant of low oxygen
change, eutrophication, overfishing, invasions, marine construc- levels (Condon et al., 2001) and may find additional habitat
tion, and water diversion (e.g. Arai, 2001; Mills, 2001; Oguz, where other epifauna are reduced in dysoxic waters (Ishii, 2006).
2005a, b; Purcell, 2005; Hay, 2006; Graham and Bayha, 2007). Eutrophication and development also reduce water clarity
Possibly, global warming is causing the increase in jellyfish. Most and light penetration, which may alter the feeding environment
coastal jellyfish are budded asexually from an attached stage to benefit non-visual gelatinous predators over visually feeding
(polyp) in the life cycle. In temperate scyphozoans, heightened fish.
temperatures increased the asexual production of new jellyfish in Aquaculture may accidentally benefit jellyfish populations in
Aurelia labiata: both temperature and salinity had significant several ways. First, if additional feed is provided, eutrophication
effects and strong interaction (Purcell et al., 2007). can lead to the conditions described earlier. Second, culture rafts
Several effects of eutrophication of coastal waters on the provide substrate on which benthic polyps may form large colo-
environment are potentially beneficial for jellyfish (reviewed in nies and produce more jellyfish. Aurelia spp. polyps are known
# 2008 International Council for the Exploration of the Sea. Published by Oxford Journals. All rights reserved.
For Permissions, please email: journals.permissions@oxfordjournals.org454 W-T. Lo et al.
to thrive on the undersurfaces of floating structures (e.g. Miyake is driven primarily by a semi-diurnal tide, which is somewhat
et al., 2002; Hoover, 2005). Third, zooplanktivorous fish are har- restricted by the narrow tidal inlet. In addition to direct fresh-
vested for fishmeal in aquaculture feed (e.g. Kristofersson and water input by precipitation, the terrestrial water input via the
Anderson, 2006), which may provide opportunities for population Lipan Dike is derived mainly from urban and aquacultural waste-
growth of gelatinous competitors. water with a moderate salinity (,20). The lagoon contained many
Tapong Bay is a tropical lagoon located on the southwest coast oyster rafts (19 166) and fish pens (3837) that were removed between
of Taiwan. It is relatively shallow and has been used extensively for June and December 2002; the rafts were made of bamboo, and
aquaculture for decades, during which the lagoon was occupied by measured ca. 2–4 m by 5–10 m (Hung et al., 2008).
oyster hanging-culture rafts and fish net-pens. The lagoon ecosys- Conditions in Tapong Bay are affected by the northeastern and
tem has undergone eutrophication as a result of poor circulation southwestern monsoons during the dry (October–April) and wet
and continuous inputs of nutrients and organic matter from (May –September) seasons, respectively, which also affect the
internal (cultured oysters and fish) and external (urban and aqua- mixing of lagoon water. Total inputs of precipitation and waste-
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culture) sources (Hung and Hung, 2003; Hung et al., 2008). The water are much greater in the wet than in the dry season.
lagoon environment was cleaned with the complete removal of Because of its small volume, salinity in the lagoon reflects this
the culture rafts and pens between June and December 2002. seasonal variability, ranging from 25 in the wet season to 35 in
One striking result of the culture raft removal was the dis- the dry season. Atmospheric temperature ranges from 228C in
appearance of A. aurita jellyfish from Tapong Bay (Lo et al., winter (dry season) to 328C in summer (wet season; Hung and
2004). The obvious explanation for this was the removal of the Hung, 2003).
culture rafts, which had attached A. aurita polyps (H. J. Lin and
H. L. Hsieh, pers. comm.). Nevertheless, many other changes in Sampling and analytical methods
the lagoon could also have affected the jellyfish. Here, we Sampling in Tapong Bay was conducted monthly or bimonthly
compare conditions in the lagoon before and after removal of from August 1999 to December 2002; after complete removal of
the culture rafts to determine why the jellyfish disappeared. 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)
Material and methods production, phyto- and zooplankton, and jellyfish were collected
Study site according to the methods described below.
Tapong Bay is a small, semi-enclosed coastal lagoon in southwest- Previous analyses of Tapong Bay before removal of the aquacul-
ern Taiwan (22827’N 120826’E; Figure 1). Its total area is ture rafts revealed both seasonal and spatial heterogeneity in all
5.32 km2 and volume 11.6106 m3. Its depth ranges from variables (Hung and Hung, 2003; Lo et al., 2004; Su et al., 2004;
1 m near the tidal inlet to 6 m in the inner bay (mean depth = Lin et al., 2005; Hung et al., 2008; Hsu et al., in press).
2.2 m). Water exchange between Tapong Bay and Taiwan Strait 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 Number of Days before Days after
sampling station locations. Major wastewater inputs are from Lipan stations (No.) (No.)
Dike (far right) and Mangrove Creek (top centre). Tidal exchange Hydrography (T, S) 3 11 12
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . .
with the Taiwan Strait is restricted to a narrow canal (far left). (T, S, pH, DO) 10 9 5
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . .
Stations for hydrographic (salinity, DO, and pH) and nutrient Nutrients 10 9 5
sampling (Hung and Hung, 2003) are marked by triangles; stations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . .
for phytoplankton, Chl a, and primary production sampling (Su et al., Phytoplankton, Chl a, 6 9 5
2004) are marked by circles; stations for temperature, zooplankton, IGP, light
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . .
and jellyfish sampling are marked by squares. Locations of Zooplankton and jellyfish 3 11 12
aquaculture rafts in the bay (hatched areas) and aquaculture ponds Station locations are in Figure 1. Abbreviations are as follow: T, temperature;
(light grey) surrounding the bay. S, salinity; DO, bottom dissolved oxygen; Chl a, integrated chlorophyll a.Enhancement of jellyfish populations 455
lowest, were tested here. Water column pH was measured in situ stoichiometrically from DDIP and the carbon to phosphate ratio
with a portable pH meter (Mettler MP-120) with reproducibility (C:P) of organic matter being produced or consumed in the
better than +0.02. Data on monthly precipitation (rain in mm) lagoon. Therefore,
were obtained from the Central Weather Bureau of Taiwan
(http://www.cwb.gov.tw/). Photosynthetically active radiation ½ p r ¼ DDICO ¼ DDIP ðC : PÞparticulate ;
(PAR) was measured at the surface, mid-depth, and bottom of
the water column using a Li-Cor Quantum Li-189 meter. where DDICO is the change in dissolved inorganic carbon. The
Water samples were collected from Tapong Bay (Stations 1 –10, particulate organic C:P ratio in the lagoon was not determined,
Figure 1), Lipan Dike, and the adjacent coastal sea, before (from and the Redfield ratio (106) was adopted for stoichiometric calcu-
August 1999 to July 2002) and after (from February 2003 to lation, because phytoplankton was the primary producer in the
September 2004) removal of the culture rafts (Table 1). Three lagoon (Lin et al., 2005). Further details of methods and the result-
replicate water samples were collected from upper, middle, and ing values are reported by date in Hung et al. (2008) and are used
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bottom layers using a peristaltic pump and a precleaned silicone in the current analysis.
tube. Salinity was determined using an Autosal salinometer
(Guildine 8400B) in the laboratory to gain precise salinity values Phytoplankton, Chl a, and productivity
(+0.002) for deriving salt and water budgets. An additional Water samples were collected in triplicate at low tide for each site
four litres from each station were stored in a polyethylene bottle every 2 –3 months from October 1999 to July 2004 (Table 1). An
and brought back to the laboratory immediately for further aliquot from each station was fixed in Lugol’s solution after fil-
analyses. tration through a 200 mm net. Taxa were identified and counted
In the laboratory, the water sample was filtered through from two 0.5 ml subsamples of the concentrated sample using a
precombusted GF/F filters (at 4508C, 4 h). The filtered water light microscope under phase and DIC contrast at 400 after
was used to measure dissolved nutrients, including dissolved settlement on a scaled slide. For this analysis, miscellaneous flagel-
inorganic nitrogen (NO3+NO2+NH4, hereafter DIN), dissolved lates (Chlorophyta, Raphidophyta, and Euglenophyta) were
inorganic phosphate (PO4, hereafter DIP), dissolved silicate grouped. Chl a concentrations were determined spectrophotome-
(H4SiO4, hereafter DSi), dissolved organic carbon (DOC), trically by immediately filtering water samples in triplicate through
nitrogen (DON), and phosphorus (DOP). Generally, three repli- Whatman GF/F filters in the field and extracting them in 90%
cate measurements were processed for each chemical analysis. acetone for 24 h at 48C in the dark (Parsons et al., 1984).
Particulate organic carbon (POC) and nitrogen (PON) were Productivity incubations were performed with bay water collected
measured from the filtered samples, placed in tin boats, then at low tide in the early morning using a 2 l Van Dorn bottle. Three
combusted in a C/N/S analyser (Fisons NCS 1500) after removing light and three dark 300 ml BOD bottles were incubated in flowing
the inorganic carbon with 2 M hydrochloric acid (Hung et al., seawater tanks adjacent to Tapong Bay. Net production and respir-
1999). The blank value attributed to precombusted GF/F filter ation rates were derived from changes in DO concentrations over
and tin boat demonstrated a precision of +0.3 mM C and time, as determined by a modified Winkler method (Pai et al.,
+0.2 mM N. 1993), in illuminated and dark bottles, respectively. Rates rep-
The biogeochemical fluxes and metabolism of nutrients and resent community rates.
carbon in the lagoon were evaluated using the LOICZ biogeo-
chemical budget model (Smith et al., 1991; Gordon et al., 1996). Zooplankton and jellyfish abundance
Details of modelling can be found at the LOICZ website (http:// Samples were collected monthly (before removal) and bimonthly
www.nioz.Nl/loicz/) or from Hung and Hung (2003) for the (after removal; Table 1) by towing a NorPac net with 100 mm
period before removal. This biogeochemical budget model is a mesh and flowmeter near-surface (0– 1 m). Samples were immedi-
box model from which non-conservative nutrient and carbon ately preserved in 5 –10% formalin solution. In the laboratory,
budgets can be constructed from non-conservative distributions each sample was subsampled with a Folsom plankton splitter,
of nutrients and water budgets, which in turn are constrained and a minimum of 500 organisms were identified and counted
from the salt balance under a steady-state assumption. The non- by use of a dissecting microscope.
conservative flux of a material is estimated from the flux deviation
between inputs and outputs, based on salt and water balances. The Results
non-conservative flux of dissolved inorganic phosphorus is Lagoon-wide averages of hydrographic measurements revealed a
assumed to be an approximation of net metabolism, because few significant differences before and after removal of the
phosphorus is not involved in gas-phase reactions. Nitrogen and culture rafts (Table 2). Temperature, pH, and DO were similar
carbon both have other major pathways, such as denitrification, in both periods. Salinity was significantly higher in the period
nitrogen fixation, gas exchange across the air–sea interface, and after (32.6) removal than before (31.8); however, rain revealed
calcification. The biogeochemical pathways of carbon can be no significant difference between periods. Water clarity increased
approximated from non-conservative phosphorus flux and C:P significantly after removal, and the amounts of light penetrating
stoichiometric ratio of reactive particles in the lagoon. Because the water column also increased, but not significantly. Lagoon-
of the distinct variability in wastewater and material inputs with wide water residence times were significantly longer (10 d) when
time, water and nutrient budgets estimated from a box model the culture rafts were present than after (6 d).
for the lagoon can only be valid within a season. Therefore, Before removal of the culture rafts, lagoon-wide averaged con-
carbon budgets were made for each sampling period before they centrations of DSi (20.3 mM), DIN (16.4 mM), and DIP (4.0 mM)
were integrated as annual budgets. were greater than after the removal (DSi = 10.0 mM; DIN =
The net ecosystem metabolism (NEP) [difference between 11.4 mM; DIP = 1.5 mM); differences were significant at the 0.05
gross production and respiration (p – r)] can be estimated probability level for DSi and DIP, but not for DIN (Table 2).456
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Table 2. Physical variables, nutrients, and ecosystem properties measured before vs. after removal of oyster-culture rafts from Tapong Bay, Taiwan.
Physical variables
Temp (88 C) Surface salinity pH DO2 (mg l21) Rain (mm) Resid (d)a Water motion (g d21)
Before 26.9 31.8 8.18 4.0 169 10.0 10.2
vs. , . ,
after 27.2 32.6 8.14 4.5 168 6.1 16.1
p-value NS ,0.01 NS NS NS ,0.01 ,0.1
Nutrients
DSi (mM)a DIN (mM)a DIP (mM)a DON (mM)a DOP (mM)a DOC (mM)a
Before 20.3 16.4 4.0 24.4 2.4 162.4
vs. . .
after 10.0 11.4 1.5 39.8 1.2 232.3
p-value ,0.05 0.1 0.01 ,0.1 ,0.1 ,0.1
Ecosystem properties
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
Before 6 12 197 1.4 5.6
vs. ,
after 13 19 225 5.4 11.6
p-value 0.01 0.1 NS NS NS
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.Enhancement of jellyfish populations 457
Lagoon-wide averaged concentrations of DON and DOC were
Oysters (g ww m23)a
Aurelia (ind. m23)
greater before removal (24.4 and 162.4 mM) than after (39.8 and
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
232.3 mM), but DOP concentrations were greater before
sampling stations. Abbreviations for variables represent: Phytopl, total phytoplankton; Cyano, cyanobacteria; Dinoflag, dinoflagellates; Flagellates, sum of miscellaneous flagellates (Euglenophyta, Chlorophyta,
(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.
243.5
0.001
NT
0.3
.
.
Nutrient and carbon budgets were determined principally by
0
0
water budget, nutrient and carbon distributions, and internal bio-
geochemical processes (Hung et al., in 2008). The water budget
Periphyton (g ww m23)a
was derived from the salt balance. For a nutrient budget, the differ-
ence between total inputs and total outputs indicates source
Oithona (ind. m23)
(inputs , outputs) or sink (inputs . outputs) in the ecosystem.
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The system DDIP may be used to approximate the NEP of the
,1.7–14.5
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 . res-
NT
NS
70
30
.
0
piration). The NEP in Tapong Bay was all positive except for one
negative and two near 0 (Hung et al., 2008). Thus, Tapong Bay is
Flagellates (cells l21)
an autotrophic system. The mean value of NEP increased by 37%
Acartia (ind. m23)
after removal of the culture rafts; however, the difference was not
statistically significant.
Lagoon-wide averaged phytoplankton cell numbers, biomass
30 103
(Chl a), and integrated gross primary production (IGP) were
3 103
0.002
3100
greater after removal of the culture rafts than before (Tables 2
0.02
600
,
,
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
Dinoflag (cells l21)
Nauplii (ind. m23)
Cryptophyta, Raphidophyta); Copepods, total copepods; Pcalanus, Paracalanus; Nauplii, copepod nauplii; NT, not tested.
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
28 103
4 103
Table 3. Organisms sampled before and after removal of culture rafts from Tapong Bay, Taiwan.
(cyanobacteria, diatoms, dinoflagellates, and miscellaneous flagel-
1600
800
lates) were similar (22 –31%). NS
NS
,
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 Bestolina (ind. m23)
Diatoms (cells l21)
species combined (a sixfold increase) and for all of the predomi-
nant species individually, except for Oithona spp. Copepod
nauplii abundance doubled, but was not significant.
2 104
4 104
Lagoon-wide averaged abundances of the jellyfish, A. aurita, 0.002
2000
changed from high values (Figure 2; mean 0.3 ind. m23) with
NS
20
,
,
the culture rafts to the complete absence of jellyfish after
removal (Table 3).
Pcalanus (ind. m23)
Cyano (cells l21)
Discussion
Physical changes following culture raft removal
30 103
5 103
An important consequence of the culture raft removal was
0.002
improved circulation in Tapong Bay. Dominant semi-diurnal
300
NS
50
,
,
and diurnal tides controlled primary water exchange and sub-
sequently drove the lagoon circulation. Two sub-anticlockwise
Copepods (ind. m23)
circulation patterns were separated generally from the middle
Phytopl (cells l21)
area of the lagoon in a northeast–southwest direction (Yu,
Phytoplankton
2001). The hydrochemistry and water budgets in Tapong Bay
Zooplankton
before removal of the culture rafts were described by Hung and
13 104
Hung (2003). Briefly, the water residence time ranged from 7 d
From Lin et al. (2005).
3 104
(summer) to 13 d (winter) with a mean of 10 d. It was longer in
3000
0.05
500
0.1
,
,
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
p-value
p-value
Before
Before
major circulation pattern remained the same, the water residence
after
after
vs.
vs.
time in the inner and outer lagoon after removal was reduced
a458 W-T. Lo et al.
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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 indepen- The DIN:DIP ratio ranged between 1.5 and 9.2 throughout the
dent estimate of water motion revealed a significant increase study, which is much lower than the Redfield ratio of 16 (Redfield
after removal (Su et al., 2004; H. J. Lin, pers. comm.). et al., 1963). The low DIN:DIP ratios were probably caused by
Apparently, the culture rafts reduced water flow in the lagoon. P-contaminated wastewater inputs from the Lipan Dike with
This affected some aspects of the conditions in the lagoon. very low DIN:DIP ratios (,2.5). Because both DIN and DIP con-
Specifically, DO concentrations were somewhat higher after centrations were much greater than the critical levels (DIN ,
removal. DO in the bottom water seldom was as low as 1 mM; DIP , 0.1 mM; DSi , 2 mM) of nutrient limitation (e.g.
2 mg O2 l21 (Hung and Hung, 2003; Hung et al., 2008), Justič et al., 1995), the lagoon appears to have excess DIP (Hung
suggesting that hypoxia was not a serious problem in Tapong and Hung, 2003; Hung et al., 2008).
Bay, either before or after removal. Increased salinity after Environmental conditions that seem to favour jellyfish have
removal may have been caused by improved flushing by ocean high nutrients, but low Si:N ratios, characteristic of eutrophic
water. coastal waters (Sommer et al., 2002). This is associated with a pre-
Decreasing ocean pH is one effect of climate warming (Caldeira dominance of small flagellates over diatoms and a strong microbial
and Wickett, 2003). Attrill et al. (2007) confirmed a significant foodweb that is fuelled heterotrophically by bacteria rather than
negative correlation between nematocyst occurrence in continu- autotrophically. Such changes occurred in Tapong Bay following
ous plankton recorder (CPR) samples and pH (range 8.0 –8.3) removal of the culture rafts. Despite an apparent decrease in nutri-
during the period 1971–1995, and suggested that pelagic cnidar- ents, levels before and after culture raft removal were comparable
ians may benefit from this change because of the detrimental with other eutrophic systems (Tada et al., 2001; Hung and Kuo,
effects of high pH on calcifying organisms; however, insignificant 2002; Newton et al., 2003). The Si:N ratio decreased from 1.24
changes in pH (20.04) were observed following removal of the to 0.88, with the proportion of diatoms being halved and the pro-
culture rafts, and probably had no effect on jellyfish populations. portion 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
Changes in nutrients, production, and the foodweb Hung, 2003). On the basis of the nutrient changes, jellyfish popu-
following culture raft removal lations might have been expected to increase after culture raft
Decreased nutrients were observed after removal of the culture removal rather than disappear.
rafts, which could be attributed to many changes in Tapong Bay. Phytoplankton abundance and community composition
Removal of the oysters eliminated that source of excreted nutri- changed after removal of the oyster cultures. Total phytoplankton
ents. The removal of fish-pen cultures also would have eliminated abundance increased, mainly as a result of more miscellaneous fla-
nutrient additions from excess feed and fish waste products; gellates, although increases were seen in cyanobacteria, diatoms,
however, the magnitudes of such additions are unknown. The and dinoflagellates as well. After culture raft removal, the
oysters were estimated to consume 44% of the production in proportion of diatoms was halved, and the proportion of miscel-
the lagoon (Lin et al., 2006). Removal of the oysters eliminated a laneous flagellates had increased 2.5-fold. These changes probably
major consumer of suspended particulate matter from the ecosys- reflect several influences, including the shift in main consumers
tem, resulting in increased availability of particulate food in the from oysters to copepods, improved light availability brought
water column. Increases in phytoplankton, Chl a, and IGP were about by the elimination of shading by the rafts, improved water
observed. These increases would have required additional nutri- circulation, and altered nutrient ratios.
ents. Increased flushing may also have contributed to lower nutri- The lack of statistical significance for some phytoplankton
ent concentrations (Hung et al., 2008). groups probably is the result of substantial spatial and seasonalEnhancement of jellyfish populations 459
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 temp-
erature 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 avail-
ability of phytoplankton and reduction of zooplanktivorous fish
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(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 disappear-
ance is opposite to expectations. 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
Probable effects of ecosystem changes on jellyfish aquaculture rafts. After removal of the rafts, no jellyfish or ephyrae
in Tapong Bay were found, but water residence times are shown (open circles) on
Hydrographic conditions in Tapong Bay were favourable for the the x-axis for six dates between February 2003 and September 2004.
survival and reproduction of A. aurita, both before and after Zero values of abundance are shown as 0.01, so that they appear on
culture raft removal. DO was not at stressful levels either before the log scale.
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. at the shortest time; also, jellyfish were not collected on two dates
Moreover, measured temperature had a greater range before with moderate residence times (8.6 –10.1 d; Figure 3). Ephyrae
(16.9– 31.88C) than after (23.0 –31.48C) removal, suggesting that were present at long water residence times of 9.3 –13.2 d; they
neither unusually low nor high temperatures were probable were absent at resident times of 5.8 – 12.4 d. The water residence
causes for jellyfish disappearance. times calculated for after-culture raft removal are shorter
Salinity near surface did change significantly, and the effect on (3.8 – 9.2 d) than before, but overlapped with residence times
A. aurita is unclear. Ephyrae were sampled in Tapong Bay from when jellyfish, but not ephyrae, were present in Tapong Bay
April 1999 to April 2002 (W-TL, unpublished data). They (Figure 3). Water residence times were longer in the deeper
occurred during October–April, but were abundant between (6 m) inner lagoon than in the outer lagoon before and after
November and February. Therefore, they were present (1 – removal (Hung et al., 2008), and jellyfish abundance was greater
328 ephyrae m23) during the coolest (24.1 + 3.18C) months there (Figure 2). Therefore, we conclude that increased water
with the highest surface salinities (31.7 + 2.5). Additionally, the exchange could have promoted transport of jellyfish and their
seasonal rains before culture raft removal changed surface salinities planula larvae and ephyrae from the lagoon. The importance of
by as much as 10 (Lo et al., 2004), but this did not eradicate the A. transport is unknown.
aurita population. Another direct consequence of culture raft removal was
Results for other scyphozoan species suggest tolerance of chan- increased solar radiation in the water column, which may have
ging salinities. Salinity had significant effects on A. labiata polyps been detrimental to the A. aurita population. The planula larvae
(Purcell, 2007). In combinations of low temperature (78C) and of the jellyfish prefer to settle on poorly illuminated undersurfaces
high (34) and low (20) salinity, polyps had 83 – 92% survival, in the water (Brewer, 1978). Light levels reaching the bottom of
but few jellyfish were produced; however, in combinations of Tapong Bay after culture raft removal averaged 225 mE m22 s21,
high temperature (158C) and high and low salinity, polyps had which was considerably higher than those measured underneath
83 –100% survival and high jellyfish production (Purcell, 2007). covered marina floats (2– 6 mE m22 s21) where A. labiata polyps
In contrast, the combination of high salinity (30) and temperature flourished (Purcell et al., 2007). When the culture rafts were
(31.2– 33.18C) from an El Niño was detrimental to Mastigias sp. removed from the surface, the larvae were deprived of settling sur-
jellyfish in a marine lake in Palau (normal 30.88C, 25.5 salinity); faces, and any remaining hard surface may have been exposed to
however, although Aurelia spp. in the lake appeared damaged at light levels that are detrimental to or inhibitory for settlement of
the same time, their population did not decrease (Dawson et al., the planulae.
2001). In addition, Mastigias sp. polyps were alive and asexually We believe that aquaculture rafts provided shaded surfaces for
reproducing during this period (Dawson et al., 2001). We larval settlement and polyp colony expansion and increased reten-
believe that the overall salinity increase of 0.8 in Tapong Bay tion of the planulae, ephyrae, and jellyfish in Tapong Bay. Removal
probably would not have caused the jellyfish to disappear. of favourable polyp substrate with the culture rafts probably was
Water exchange in Tapong Bay increased after removal of the the main cause for the disappearance of jellyfish, perhaps acting
culture rafts, which may have increased transport of the jellyfish together with increased light and water exchange in the lagoon.
and ephyrae from the bay. Jellyfish were present at lagoon-wide Therefore, we observed three probable mechanisms by which
water residence times of 5.8 –13.2 d, with the greatest abundances aquaculture rafts enhanced jellyfish populations; the rafts provided460 W-T. Lo et al.
substrate and shading for the polyps, and the rafts restricted water 1 – 26. International Food Policy Research Institute, Washington,
exchange in the lagoon. DC.
FAO. 2007. Fisheries and Aquaculture Department Website. http://
Implications for the future www.fao.org. Accessed 28 March 2007.
The current world human population is projected to increase 46% Gordon, D. C., Boudreau, P. R., Mann, K. H., Ong, K. H., Silvert,
by 2050 (US Census Bureau, 2006). Human influences and W. L., Smith, S. V., Wattayakorn, G., et al. 1996. LOICZ
Biogeochemical Modelling Guidelines. LOICZ Reports and
demands on the ocean will increase with population growth.
Studies, 5. LOICZ, Texel, The Netherlands. 96 pp.
Global bivalve aquaculture (mussels, oysters, scallops) increased
Graham, W. M. 2001. Numerical increases and distributional shifts of
fivefold between 1980 and 2005; the Asian share of the world pro- Chrysaora quinquecirrha (Desor) and Aurelia aurita (Linné)
duction increased from 60% in 1980 to 93% in 2005 (FAO, 2007). (Cnidaria: Scyphozoa) in the northern Gulf of Mexico.
Similarly, global marine fish production has increased ninefold Hydrobiologia, 451: 97– 111.
since 1980, with Asia’s share high (80% in 2005; FAO, 2007). Graham, W. M., and Bayha, K. M. 2007. 14 Biological invasions by
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Global fish production is projected to double between 1997 and marine jellyfish. In Ecological Studies, 193. Biological Invasions,
2020, with especially large increases in developing nations and in pp. 240– 255. Ed. by W. Nentwig. Springer-Verlag, Berlin.
aquaculture (Delgado et al., 2003). Therefore, we conclude that Hay, S. 2006. Marine ecology: gelatinous bells may ring change in
floating aquaculture structures probably will increase in the marine ecosystems. Current Biology, 16: R679– R682.
future, increase favourable habitat for jellyfish polyps, and Hoover, R. A. 2005. Population characteristics of the scyphozoan
locally increase jellyfish populations, especially in areas where Aurelia labiata and predation by nudibranchs. MSc thesis,
Western Washington University, Bellingham, WA.
water flow is restricted. The problems are likely to occur in Asia.
Hsu, P. K., Lo, W. T., and Shih, C. T. The coupling of copepod assem-
We recommend additional research into materials that may
blages and hydrography in a eutrophic lagoon in Taiwan: seasonal
inhibit settlement by jellyfish larvae (e.g. Hoover, 2005). and spatial variations. Zoological Studies, in press.
Hung, J. J., and Hung, P. Y. 2003. Carbon and nutrient dynamics in a
Acknowledgements hypertrophic lagoon in southwestern Taiwan. Journal of Marine
This research was supported by grants from the National Science Systems, 42: 97 – 114.
Council to J-JH, W-TL, and H-MS and from the Ministry of Hung, J. J., and Kuo, F. 2002. Temporal variability of carbon and nutri-
Education of the Republic of China to W-TL [94-C030220 ent budgets from a tropical lagoon in Chiku, southwestern Taiwan.
(Kuroshio project)] and J-JH [95-C030214 (Kuroshio project)]. Estuarine Coastal and Shelf Science, 54: 887– 900.
We thank H-HC for obtaining information on the numbers of Hung, J-J., Hung, C-S., and Su, H. M. 2008. Biogeochemical responses
oyster rafts and fish pens. to the removal of maricultural structures from an eutrophic lagoon
(Tapong Bay) in Taiwan. Marine Environmental Research, 65:
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