Marine Pollution Bulletin 97 (2015) 199–208
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Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Jellyfish (Cyanea nozakii) decomposition and its potential influence on marine environments studied via simulation experiments Chang-Feng Qu a,b, Jin-Ming Song a,⇑, Ning Li a, Xue-Gang Li a, Hua-Mao Yuan a, Li-Qin Duan a, Qing-Xia Ma a,b a b
Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China University of Chinese Academy of Sciences, Beijing 100049, China
a r t i c l e
i n f o
Article history: Received 22 January 2015 Revised 4 June 2015 Accepted 8 June 2015 Available online 15 June 2015 Keywords: Cyanea nozakii Decomposition Jellyfish blooms Nutrient recycling Oxygen pH
a b s t r a c t A growing body of evidence suggests that the jellyfish population in Chinese seas is increasing, and decomposition of jellyfish strongly influences the marine ecosystem. This study investigated the change in water quality during Cyanea nozakii decomposition using simulation experiments. The results demonstrated that the amount of dissolved nutrients released by jellyfish was greater than the amount of particulate nutrients. NH+4 was predominant in the dissolved matter, whereas the particulate matter was dominated by organic nitrogen and inorganic phosphorus. The high N/P ratios demonstrated that jellyfish decomposition may result in high nitrogen loads. The inorganic nutrients released by C. nozakii decomposition were important for primary production. Jellyfish decomposition caused decreases in the pH and oxygen consumption associated with acidification and hypoxia or anoxia; however, sediments partially mitigated the changes in the pH and oxygen. These results imply that jellyfish decomposition can result in potentially detrimental effects on marine environments. Ó 2015 Elsevier Ltd. All rights reserved.
1. Introduction Jellyfish are conspicuous marine zooplanktons that play critical roles in the exchange of material and energy in marine ecosystems. Studies have confirmed that jellyfish populations are increasing worldwide (Brotz et al., 2012; Lynam et al., 2006; Purcell and Arai, 2001; Uye and Ueta, 2004). Jellyfish blooms can cause numerous negative consequences, including breaking fishing nets, interfering with fisheries and aquaculture, stinging swimmers and clogging power plant water intakes. These consequences result in ecological and economic losses and could eventually damage the normal composition and function of marine ecosystems (Dong et al., 2010; Mills, 2001; Purcell et al., 2007; Richardson et al., 2009). Jellyfish blooms are generally short-lived, and the large biomasses of jellyfish gradually die and sink after blooming. Jellyfish blooms represent significant stocks of nutrients (Lebrato et al., 2011; Pitt et al., 2009), and the large amounts of nutrients from jellyfish blooms have been recognized as an important functional component of marine ecosystems (Purcell, 2012). Studies have
⇑ Corresponding author at: Institute of Oceanology, Chinese Academy of Sciences, 7, Nanhai Road, Qingdao 266071, China. E-mail address: [email protected] (J.-M. Song). http://dx.doi.org/10.1016/j.marpolbul.2015.06.016 0025-326X/Ó 2015 Elsevier Ltd. All rights reserved.
reported that jellyfish carrion can serve as a carbon source in marine environments (Billett et al., 2006; Hansson and Norrman, 1995; Lebrato et al., 2013), and jellyfish decomposition also has potentially significant effects on microbial plankton (Tinta et al., 2010; Titelman et al., 2006). Studies have also demonstrated that jellyfish decomposition is an important pathway for nitrogen (N) and phosphorus (P) recycling (Li et al., 2012; West et al., 2009b). However, few studies have examined the influence of jellyfish decomposition on the composition of and dynamic changes in nutrients, and there are few comprehensive assessments of the influence of jellyfish decomposition on marine environments. Determination of the nutrients released by jellyfish decomposition is a key for understanding this process’s possible effects on microbial populations and primary production. A significant increase in the incidence of jellyfish blooms in Chinese seas has been observed since the late 1990s (Cheng et al., 2004; Dong et al., 2010; Sun, 2012). Cyanea nozakii is one of the dominant scyphozoan species responsible for most jellyfish blooms in Chinese seas, which occur in relatively warm (17–25 °C) and saline (33–34) water (Cheng et al., 2005; Zhang et al., 2012). C. nozakii blooms have been observed in the Bohai Sea, Yellow Sea and East China Sea and can have abundant populations of 4000–6000 in d km2 (Zhang et al., 2005). The blooms of C. nozakii have resulted in significant problems for fisheries. For example,
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C. nozakii overflow into coastal fisheries in northern Zhejiang and Jiangsu (Dong, 2000) caused an 85% decline in edible jellyfish in the Liaodong Bay in 2004 (Ge and He, 2004). Additionally, when the large amounts of C. nozakii die and decompose, it can have serious effects on the surrounding environments. However, at present, reports regarding C. nozakii decomposition are still relatively scarce. Therefore, to clarify the impact of C. nozakii decomposition on marine environments, it is necessary to investigate the processes and characteristics of its decomposition. Using simulations in the form of incubation experiments, the objective of this study was to examine the process of C. nozakii decomposition and evaluate its effects on the ambient water column, including the recycling of nutrients and variations in the dissolved oxygen (DO) and pH. Additionally, the influence of C. nozakii decomposition on marine ecosystems is discussed. The results provide basic information regarding the mechanisms of jellyfish decomposition. 2. Materials and methods 2.1. Experimental design The experiments were conducted in a laboratory from 30 August, 2012 to 13 September, 2012. The cultured seawater used in the experiments was collected from the Huiquan Bay in Qingdao at a depth of approximately 10 cm below the sea surface and filtered through a 200-lm-mesh net. Individual jellyfish and sediments were collected from the Jiaozhou Bay. After collection, the jellyfish were stored in foam boxes with blocks of ice to prevent spoilage and transported to the laboratory within two hours. Jellyfish were rinsed three times with filtered seawater to remove sand and other impurities immediately prior to the incubation experiment. Each incubation was conducted in a transparent plastic rectangular tub (55 cm 38 cm 37 cm). To determine the effects of C. nozakii decomposition, the following four experimental setups were assessed: seawater (S); seawater and sediment (SS); seawater and jellyfish (SJ); and seawater, sediment and jellyfish (SSJ). In the S treatment, 30 l of natural filtered seawater were transferred to the incubator. In the SS treatment, well-mixed sediments were homogeneously placed on the bottom of the incubator (with a layer thickness of 5 cm), and then 30 l of filtered seawater were slowly and gently introduced into the incubator. In the SJ treatment, the first step was the same as in the S treatment; subsequently, 800 g of processed C. nozakii tissue (include umbrellas, tentacles and oral arms) were added to the incubator. In the SSJ treatment, the first two steps were the same as in the SS treatment; subsequently, processed jellyfish tissue was placed on the sediment surface. All treatments were stabilized 24 h after adding 30 l of seawater to avoid turbulence and re-establish balance. Jellyfish were added simultaneously, and the treatments without jellyfish served as controls. All incubators were covered with gauze nets to prevent introduction of impurities. The simulated decomposition experiments were conducted under ambient laboratory conditions. Three replicate experiments were randomly assigned to each treatment. 2.2. Sampling The experiments commenced on 30 August, 2012, and the experiments were monitored for 15 days and sampled every 24 h. The day prior to the addition of the jellyfish to the incubators was considered to be the first day of the experiments. Water samples (300 ml each) were taken from each incubator after analysis of the DO and pH and filtered through a 0.70-lm GF/F filter membrane which were combusted (450 °C) and weighted. The filters
were dried and weighted to determine the particulate nitrogen and phosphorus. The filtrate was divided into two subsamples that were bottled separately. One subsample (150 ml) was used to measure the total dissolved nitrogen and phosphorus (TDN and TDP), and the other was used to analyse the ammonium (NH+4), nitrate 3 (NO 3 ), nitrite (NO2 ) and phosphate (PO4 ) concentrations. 2.3. Water analyses During the experiment, the pH and DO concentrations of the water were measured using an electrochemistry meter (ORION VERSA STAR) daily at 09:00 until the end of the experiment. The concentrations of inorganic nutrients were measured using a continuous flow analyser (Model: SKALAR SANplus). Using Skalar meth ods, the concentration of NOx (NO 3 + NO2 ) was determined using the cadmium–copper reduction and Griess reaction, NH+4 was quantified using a modified Berthelot reaction, and PO3 was 4 determined using phosphomolybdenum blue colorimetry. The DIN concentration was calculated as the sum of the NOx and NH+4 concentration, and the DIP concentration was equal to the concentration of PO3 4 . TDN and TDP were determined by total ultraviolet (UV) digestion with an oxidation solution (K2S2O8 + NaOH), which 3 automatically digested the TDN and TDP into NO 3 and PO4 , respectively. The concentration of dissolved organic nitrogen (DON) and phosphorus (DOP) was calculated by subtracting the DIN from the TDN and the DIP from the TDP, respectively. To determine the particulate nutrient content, the filters and blank membranes were immediately transferred into polypropylene centrifuge tubes, and 25 ml of 0.1-mol l1 HCl were added. The tubes were vibrated for 2 h and then centrifuged. The supernatants were used to determine the particulate inorganic nitrogen (PIN) and phosphorus (PIP) (Fang, 2004; Ruttenberg, 1992) using the analyser. After washing with Milli-Q water, the residual membranes were autoclaved at 124 °C for 1 h with 25 ml of a potassium peroxodisulfate (K2S2O8) and sodium hydroxide (NaOH) solution to digest the particulate organic nitrogen (PON) and phosphorus 3 (POP) into NO 3 and PO4 , respectively (Bronk et al., 2000; Thien and Myers, 1992). After natural cooling, the water samples were also tested using the analyser. The total particulate nitrogen (TPN) was calculated by summing the PIN and PON, and the total particulate phosphorus (TPP) was calculated by summing the PIP and POP, respectively. The total nitrogen (TN) was calculated by summing the TDN and TPN, and the total phosphorous (TP) was calculated by summing the TDP and TPP, respectively. The analyser detection limits for NH+4, NOx, PO3 4 , TDN and TDP were 1, 1, 1, 5 and 10 lg l1, respectively. 3. Results 3.1. The decomposition characteristics of C. nozakii The experiments demonstrated that C. nozakii decomposed completely within 14 days. The jellyfish tissue exhibited no obvious changes at the beginning of incubation. Beginning on the 3rd day, the blocks of jellyfish became smaller pieces with an unpleasant odour and then decomposed rapidly. As the jellyfish decomposed, the tissue pieces gradually reduced in size, and a white/transparent membrane appeared on the surface of the water, causing the water to become turbid, sticky and foul-smelling. The phenomenon lasted for 6 days, after which the blocks of jellyfish were no longer visible and only some floccules were found in the water. From that time until the end of the experiment, the jellyfish tissue decomposed completely, and the environments became visually similar to the controls; however, they retained a pungent odour.
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3.2. Influence of C. nozakii decomposition on the pH
with sediment recovered faster from the minimum value than did that of the water without sediment.
The two jellyfish treatments exhibited similar changes but were significantly different from the controls (Fig. 1). The pH values of the two control treatments changed slightly and exhibited almost linear, with average values of 8.03–8.07; these values were greater than those of the jellyfish treatments throughout the entire experiments. In the first 5 days, the pH in the jellyfish treatments decreased sharply (0.77–0.92 units). The lowest pH of the jellyfish treatments occurred on the 5th day, representing a 9.4–11.4% decrease compared with the controls. The maximum diurnal variation was observed at the beginning of decomposition, with values of 0.35–0.41 units. After the first 5 days, the pH increased continuously until the 12th day and then remained stable until the end of the experiment. When the decomposition was complete, the pH values of the jellyfish treatments were 7.55–7.77; these values were less than those of the controls. Although the pH values of the SJ and SSJ treatments exhibited a similar trend, the degree of variation was different. At a later incubation time (from day 9), the pH difference (4pH) in the SJ treatment was significantly lower than that in the SSJ treatment (p < 0.05); during decomposition, the pH values of the treatments with sediment recovered faster than those of the treatments without sediment.
3.3. Dynamic variations in the DO
3.4.1. Release of particulate nitrogen and phosphorus During the decomposition of C. nozakii, the concentrations of particulate N and P in the control treatments remained low and changed little throughout the experiments (Fig. 3). In the treatments with addition of jellyfish, the PIN values reached their maxima on day 7 and then decreased gradually to the normal level until the end of the experiment. However, the PIP increased sharply after the addition of the jellyfish. The PIP in the SJ treatment decreased gradually until the end of the experiment. In the SSJ treatment, the PIP decreased sharply from a peak of 165.5 ± 27.2 lg l1 on the 5th day to 49.1 ± 11.4 lg l1 on the 6th day and then decreased gradually until the end of the experiment. The PIN was significantly greater in the SJ treatment than in the S treatment from the 3th day until the 15th day (p < 0.05). In the SSJ treatment, the PIN was greater than in the SS treatment from the 2nd day until the 9th day (p < 0.01) and exhibited a slightly longer lag phase compared with the SJ treatment. The PIP values of both jellyfish treatments were significantly greater than those of the controls (p < 0.01) for the whole incubation period. The PON and POP exhibited similar trends, sharply increasing to a maximum after the addition of the jellyfish and then decreasing until the end of the experiment. There was a significant correlation between the PON and POP (RSJ = 0.977, RSSJ = 0.977, p < 0.01) during the whole incubation period. However, after the maximum values were obtained, the change in the PON was greater than that in the POP. The maximum values of the PON and POP in the treatments without sediment lagged behind the values in the treatments with sediment. The concentrations of PON and POP in both jellyfish treatments were significantly greater than those of the controls during the whole incubation period (SJ: pN < 0.01, pP < 0.01; SSJ: pN < 0.05, pP < 0.01). The average PIN, PIP, PON and POP values for the whole incubation period were 6–11, 9–15, 6– 11 and 8–23 times higher than those of the controls, respectively. The dynamic change in the TPN exhibited a pattern similar to the PON because the PON was nearly one order of magnitude greater than the PIN. The TPP included both the PIP and POP. Both the TPN and TPP values in the treatments with jellyfish were significantly greater than those of the controls throughout the entire incubation period (p < 0.01). 3.4.2. Release of dissolved nitrogen and phosphorus The dissolved nutrient changes were quite different from those of the particulate phases (Fig. 4). However, for both control
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Fig. 2 shows the variation in the DO and DO differences (4DO) caused by the decomposition of C. nozakii. The DO in both control incubations remained high for the duration of the entire experiments; however, the control with sediment had a lower DO than did the control with seawater alone. For the jellyfish treatments, the DO concentrations decreased sharply and were significantly less than those of the controls from the 2nd day (p < 0.01). The DO concentrations in both jellyfish incubations reached a minimum on the 3rd day (which lasted for 7 days), with a range from 17.7 ± 4.2 lmol l1 (mean ± SE) to 36.4 ± 14.8 lmol l1; these values were one-eighth to one-sixth of those of the controls. During the last 6 days, the DO concentrations increased gradually. Compared with the SJ treatment, the DO concentrations of the SSJ exhibited a higher increase in amplitude from day 10, but no significant differences were detected. The DO consumption reached maximum values of 5550.8–7378.9 lmol kg1 d1 in the jellyfish treatments. The difference in the DO consumption between the SJ and SSJ treatment was large, and the DO consumption in the SJ was significantly greater than that in the SSJ from the 10th day until the 14th day (p < 0.05). In short, the addition of C. nozakii prolonged the consumption of DO, and the DO of the water
3.4. Nutrient dynamics
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Fig. 4. Changes in the concentrations of dissolved nitrogen and phosphorus (lg l1) during Cyanea nozakii incubation.
treatments, all forms of dissolved nutrients remained low and changed little throughout the incubation period. In all cases, NH+4 was the dominant form of DIN, and small quantities of NOx were released by the jellyfish. Therefore, the dynamic changes in the NH+4 concentrations were similar to the changes in the DIN values. The same trend was evident for the DIN and TDN, which increased continuously after the initial addition of the jellyfish, peaked, and then decreased in the final 1–2 days. Following the addition of the jellyfish, there was a continuous release of DIN and TDN. The DIN reached a maximum of 9674.5–10117.1 lg l1 in the jellyfish treatments, which was 8–9 times greater than in the controls. The TDN reached a maximum of 10213.9–11093.2 lg l1, which was approximately 8 times greater than in the controls. The DON comprised a small part of the TDN (6.9–31.9%). The DON values of the jellyfish treatments were significantly greater than those of the controls from the 4th day until the end of the experiment. The trend in the DON values differed from the trend in the DIN
and TDN values; the DON peaked before the DIN and TDN. The DON reached a maximum of 2567–3329.0 lg l1 in the jellyfish treatments and was 8–11 times greater than in the controls. The DIN, DON and TDN values of the jellyfish treatments were 5–6, 5 and 7 times higher than those of the controls, respectively, when integrated over the 14 incubation days. Regarding the dissolved phosphorus, the changes in the DIP differed from those in the TDP. In the SJ treatment, the DIP increased slightly but steadily until day 9, rose sharply from day 10 to 13, and then decreased in the last two days. The DIP of the SJ treatment reached a maximum of 501.9 ± 25.0 lg l1 on 13th day, which was 10 times greater than that of the S treatment. In the SSJ treatment, the DIP increased sharply from day 5 to day 13, and then decreased in the following days. The DIP of the SSJ reached a maximum value of 599.9 ± 60.0 lg l1 by day 13; this value was 14 times greater than that of the SS treatment. The TDP values of both jellyfish treatments exhibited similar variation, gradually increasing after the
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addition of the jellyfish, peaking and then decreasing until the end of the experiment. The DOP values in both jellyfish treatments increased from the 4th day, remained steady until the last 1–2 days, and then decreased until the end of the experiment. 3.4.3. Composition and percentages of nitrogen and phosphorus The ranges and mean of N and P in the water column released by the jellyfish are summarized in Table 1. The average concentration of the TN during jellyfish decomposition was 8364–8500 lg l1, which was 12 times higher than the TP, with values of 695– 706 lg l1. The dissolved nutrient concentrations were greater than those of the particulate nutrient: the TDN and TDP accounted for 91.2–94.4% of the TN and 74.8–96.5% of the TP, respectively (Fig. 5). DIN, especially NH+4, was the dominant form in all treatments and contributed 81.7–85.9% of the TDN in the water column. In the control treatments, the DON occupied the smallest proportion, just 14.1–16.0%. In contrast, NOx occupied the smallest proportion in the treatments with the jellyfish, only 2.5–2.7%. Regarding phosphorus compounds, the DOP was the dominant component of the TP in the control treatments, whereas the DIP and DOP were equivalent in the jellyfish treatments. The proportions of PIP and POP in the jellyfish treatments were greater than those of the controls. During jellyfish decomposition, the forms and proportions of N and P in the water column were continually changing. Compared with the control treatments, the percentages of NH+4 and PON in the water column increased with the addition of jellyfish, whereas NOx and PIN decreased; the DON changed little. Similarly, the percentages of DIP, PIP and POP in the jellyfish treatments increased compared with the controls, whereas the percentage of DOP decreased. Generally, the nutrients released by jellyfish were mainly in dissolved phases, especially NH+4 and DIP, and were approximately 72.2–75.2% of the TN and 34.9–43.1% of the TP. NH+4 exhibited a significant positive correlation with TN (RSJ = 0.9862, RSSJ = 0.9856, p < 0.01), and DIP exhibited a significant positive correlation with TP (RSJ = 0.7788, RSSJ = 0.8860, p < 0.01). 3.4.4. Ratios of N/P during jellyfish decomposition During the jellyfish incubation, the PON/POP ratios had average values of 26–28, which were less than those of the controls but greater than the Redfield ratios throughout the decomposition time (Fig. 6). In contrast, the TPN/TPP ratios of the jellyfish treatments reached average values of 10, which were less than the Redfield ratios. Moreover, the primary difference between the SJ and SSJ treatments was that the PON/POP and TPN/TPP ratios in the SJ were lower than in the SSJ from the beginning until the 8th day; however, they were greater from the 8th day until the end of the experiment. Regarding the dissolved nutrients, the DIN/DIP ratios of both jellyfish treatments were much greater than those of the controls from the initial time until the 10th day, with average values of 73–96, but were less than those of the controls from the 11th day until the end of the experiment, with values of 39–43 (reaching a maximum of 136–138 by day 3). The TDN/TDP of the treatments with jellyfish
were approximately 2 times greater than those of the controls, which increased gradually, peaked to 36–39 by day 8, and then decreased until the end of the experiment. Overall, the average ratios of DIN/DIP and TDN/TDP of the jellyfish treatments were 69 and 29, which were much greater than the Redfield ratio. Moreover, both the DIN/DIP and TDN/TDP ratios in the SJ treatment were greater than those in the SSJ treatment during the entire incubation period. 4. Discussion 4.1. Jellyfish decomposition after blooming Jellyfish populations accumulate and form blooms, which last for just a few days, weeks or months because of limitations of food and space, changes in temperature and oxygen, and jellyfish life cycles. When jellyfish die, their carcasses may decompose in the water column or on the seabed, depending on the depth of water and the sinking rate of the jellyfish. The rate of jellyfish falling to the seabed is rapid and varies from 850 to 1500 m d1, and the rate is influenced by the jellyfish size, elemental composition, delay rate, carcass geometry, orientation adopted, and seawater temperature (Lebrato et al., 2013). This fast sinking rate implies that jellyfish carcasses are deposited on the seafloor in a few days (at most) or a few hours (at least), which is less than the time required for jellyfish decomposition. In general, dead jellyfish sink to the seabed while decomposing, and the processes of decomposition primarily occur on the seafloor. Some authors have observed this phenomenon with videos or photography (Lebrato et al., 2010). The C. nozakii decomposition observed in our experiment indicated that decomposition in the water column and on the seabed is different. The results demonstrated that sediment was beneficial in recovering from acidification and hypoxia, and it may act to mitigate changes in marine environments. The decomposition of jellyfish is very rapid. Titelman et al. (2006) reported that jellyfish decomposition was exponential, with decay-coefficients of 0.67–1.12 d1, and decomposition had a negative correlation with the jellyfish size. In our study, the time of decomposition was 14 days for C. nozakii (wet weight 800 g) in laboratory experiments, which was longer than the time for other jellyfish species. For example, it took 4.1 to 7 days for Periphylla periphylla (42.6–300 g) (Titelman et al., 2006), 6–7 days for Nemopilema nomurai (5000 g) (Song et al., 2012) and 9 days for Catostylus mosaicus (1600 g) (West et al., 2009b). These results suggest that the processes of decomposition after jellyfish blooms are transitory; however, they also exert a strong influence on the ambient environment. 4.2. Poor water quality during jellyfish decomposition Decomposition is always associated with poor water quality. In this study, a foul odour due to the jellyfish decomposition was present throughout the entire incubation; this odour may be the result
Table 1 Ranges and means of nitrogen (N) and phosphorus (P) (lg l1) in the water column during jellyfish incubation when integrated over 14 days. Treatment
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Range Average Range Average Range Average Range Average
N (lg l1)
P (lg l1)
NH+4
NOx
DON
PIN
PON
TN
DIP
DOP
PIP
POP
TP
803–1150 973 1549–9576 6038 601–915 789 1945–9567 6429
83–282 194 57–546 193 201–333 280 54–602 210
113–275 191 783–2329 1393 83–325 203 465–2668 1336
11–21 17 19–83 43 11–22 17 13–97 36
31–109 64 223–1185 697 49–133 85 129–1146 523
1252–1640 1439 2886–11,660 8364 1170–1558 1373 3077–11,735 8500
49–60 54 38–502 237 33–63 51 59–600 310
136–215 181 165–346 283 133–204 161 175–321 277
2–11 4.5 17–197 118 4–13 8.6 30–166 77
2–7 4.0 17–102 57 2–8 4.8 12–96 42
202–277 243 278–937 695 197–262 225 310–952 706
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Fig. 5. Percentage of nitrogen (NH+4, NOx, DON, PIN, and PON) in the TN and phosphorus (DIP, DOP, PIP, and POP) in the TP during Cyanea nozakii decomposition when integrated over 14 days.
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Fig. 6. Ratios of N/P (mol/mol) in the treatments during jellyfish decomposition.
of spoilage by-products, such as biogenic amines and sulphide compounds (Gram and Dalgaard, 2002). Our studies also demonstrated that jellyfish decomposition led to some water acidification. The pH of water decreased at the initial stage of jellyfish decomposition, then increased and levelled off. We speculate that a large amount of jellyfish decomposition would likely lead to rapid release of some acidic substances. Although the substances are unknown at present and require further investigation, we speculate that the release of amino acids and fatty acids from proteins and lipid metabolism of jellyfish tissue is likely one of the main sources of these substances (Liu et al., 2007, 2004). As jellyfish decompose, the organic acids consumed by microorganisms exceed those released from the jellyfish, which induces an increase in the pH. Until the jellyfish decompose completely, the remaining organic acids cause relative acidification of the seawater.
Acidification from jellyfish decomposition is more serious in some situations, such as when there is a temperature decrease, pH change or salinity change (Ma et al., 2012). In this study, the decomposition of jellyfish significantly reduced the DO concentrations of the seawater. The results demonstrated that the duration of low DO was at least half of the total decomposition time, and the recovery processes were relatively slow. Therefore, the large DO consumption and long duration of low DO could result in localized hypoxic (
Contents lists available at ScienceDirect
Marine Pollution Bulletin journal homepage: www.elsevier.com/locate/marpolbul
Jellyfish (Cyanea nozakii) decomposition and its potential influence on marine environments studied via simulation experiments Chang-Feng Qu a,b, Jin-Ming Song a,⇑, Ning Li a, Xue-Gang Li a, Hua-Mao Yuan a, Li-Qin Duan a, Qing-Xia Ma a,b a b
Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China University of Chinese Academy of Sciences, Beijing 100049, China
a r t i c l e
i n f o
Article history: Received 22 January 2015 Revised 4 June 2015 Accepted 8 June 2015 Available online 15 June 2015 Keywords: Cyanea nozakii Decomposition Jellyfish blooms Nutrient recycling Oxygen pH
a b s t r a c t A growing body of evidence suggests that the jellyfish population in Chinese seas is increasing, and decomposition of jellyfish strongly influences the marine ecosystem. This study investigated the change in water quality during Cyanea nozakii decomposition using simulation experiments. The results demonstrated that the amount of dissolved nutrients released by jellyfish was greater than the amount of particulate nutrients. NH+4 was predominant in the dissolved matter, whereas the particulate matter was dominated by organic nitrogen and inorganic phosphorus. The high N/P ratios demonstrated that jellyfish decomposition may result in high nitrogen loads. The inorganic nutrients released by C. nozakii decomposition were important for primary production. Jellyfish decomposition caused decreases in the pH and oxygen consumption associated with acidification and hypoxia or anoxia; however, sediments partially mitigated the changes in the pH and oxygen. These results imply that jellyfish decomposition can result in potentially detrimental effects on marine environments. Ó 2015 Elsevier Ltd. All rights reserved.
1. Introduction Jellyfish are conspicuous marine zooplanktons that play critical roles in the exchange of material and energy in marine ecosystems. Studies have confirmed that jellyfish populations are increasing worldwide (Brotz et al., 2012; Lynam et al., 2006; Purcell and Arai, 2001; Uye and Ueta, 2004). Jellyfish blooms can cause numerous negative consequences, including breaking fishing nets, interfering with fisheries and aquaculture, stinging swimmers and clogging power plant water intakes. These consequences result in ecological and economic losses and could eventually damage the normal composition and function of marine ecosystems (Dong et al., 2010; Mills, 2001; Purcell et al., 2007; Richardson et al., 2009). Jellyfish blooms are generally short-lived, and the large biomasses of jellyfish gradually die and sink after blooming. Jellyfish blooms represent significant stocks of nutrients (Lebrato et al., 2011; Pitt et al., 2009), and the large amounts of nutrients from jellyfish blooms have been recognized as an important functional component of marine ecosystems (Purcell, 2012). Studies have
⇑ Corresponding author at: Institute of Oceanology, Chinese Academy of Sciences, 7, Nanhai Road, Qingdao 266071, China. E-mail address: [email protected] (J.-M. Song). http://dx.doi.org/10.1016/j.marpolbul.2015.06.016 0025-326X/Ó 2015 Elsevier Ltd. All rights reserved.
reported that jellyfish carrion can serve as a carbon source in marine environments (Billett et al., 2006; Hansson and Norrman, 1995; Lebrato et al., 2013), and jellyfish decomposition also has potentially significant effects on microbial plankton (Tinta et al., 2010; Titelman et al., 2006). Studies have also demonstrated that jellyfish decomposition is an important pathway for nitrogen (N) and phosphorus (P) recycling (Li et al., 2012; West et al., 2009b). However, few studies have examined the influence of jellyfish decomposition on the composition of and dynamic changes in nutrients, and there are few comprehensive assessments of the influence of jellyfish decomposition on marine environments. Determination of the nutrients released by jellyfish decomposition is a key for understanding this process’s possible effects on microbial populations and primary production. A significant increase in the incidence of jellyfish blooms in Chinese seas has been observed since the late 1990s (Cheng et al., 2004; Dong et al., 2010; Sun, 2012). Cyanea nozakii is one of the dominant scyphozoan species responsible for most jellyfish blooms in Chinese seas, which occur in relatively warm (17–25 °C) and saline (33–34) water (Cheng et al., 2005; Zhang et al., 2012). C. nozakii blooms have been observed in the Bohai Sea, Yellow Sea and East China Sea and can have abundant populations of 4000–6000 in d km2 (Zhang et al., 2005). The blooms of C. nozakii have resulted in significant problems for fisheries. For example,
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C. nozakii overflow into coastal fisheries in northern Zhejiang and Jiangsu (Dong, 2000) caused an 85% decline in edible jellyfish in the Liaodong Bay in 2004 (Ge and He, 2004). Additionally, when the large amounts of C. nozakii die and decompose, it can have serious effects on the surrounding environments. However, at present, reports regarding C. nozakii decomposition are still relatively scarce. Therefore, to clarify the impact of C. nozakii decomposition on marine environments, it is necessary to investigate the processes and characteristics of its decomposition. Using simulations in the form of incubation experiments, the objective of this study was to examine the process of C. nozakii decomposition and evaluate its effects on the ambient water column, including the recycling of nutrients and variations in the dissolved oxygen (DO) and pH. Additionally, the influence of C. nozakii decomposition on marine ecosystems is discussed. The results provide basic information regarding the mechanisms of jellyfish decomposition. 2. Materials and methods 2.1. Experimental design The experiments were conducted in a laboratory from 30 August, 2012 to 13 September, 2012. The cultured seawater used in the experiments was collected from the Huiquan Bay in Qingdao at a depth of approximately 10 cm below the sea surface and filtered through a 200-lm-mesh net. Individual jellyfish and sediments were collected from the Jiaozhou Bay. After collection, the jellyfish were stored in foam boxes with blocks of ice to prevent spoilage and transported to the laboratory within two hours. Jellyfish were rinsed three times with filtered seawater to remove sand and other impurities immediately prior to the incubation experiment. Each incubation was conducted in a transparent plastic rectangular tub (55 cm 38 cm 37 cm). To determine the effects of C. nozakii decomposition, the following four experimental setups were assessed: seawater (S); seawater and sediment (SS); seawater and jellyfish (SJ); and seawater, sediment and jellyfish (SSJ). In the S treatment, 30 l of natural filtered seawater were transferred to the incubator. In the SS treatment, well-mixed sediments were homogeneously placed on the bottom of the incubator (with a layer thickness of 5 cm), and then 30 l of filtered seawater were slowly and gently introduced into the incubator. In the SJ treatment, the first step was the same as in the S treatment; subsequently, 800 g of processed C. nozakii tissue (include umbrellas, tentacles and oral arms) were added to the incubator. In the SSJ treatment, the first two steps were the same as in the SS treatment; subsequently, processed jellyfish tissue was placed on the sediment surface. All treatments were stabilized 24 h after adding 30 l of seawater to avoid turbulence and re-establish balance. Jellyfish were added simultaneously, and the treatments without jellyfish served as controls. All incubators were covered with gauze nets to prevent introduction of impurities. The simulated decomposition experiments were conducted under ambient laboratory conditions. Three replicate experiments were randomly assigned to each treatment. 2.2. Sampling The experiments commenced on 30 August, 2012, and the experiments were monitored for 15 days and sampled every 24 h. The day prior to the addition of the jellyfish to the incubators was considered to be the first day of the experiments. Water samples (300 ml each) were taken from each incubator after analysis of the DO and pH and filtered through a 0.70-lm GF/F filter membrane which were combusted (450 °C) and weighted. The filters
were dried and weighted to determine the particulate nitrogen and phosphorus. The filtrate was divided into two subsamples that were bottled separately. One subsample (150 ml) was used to measure the total dissolved nitrogen and phosphorus (TDN and TDP), and the other was used to analyse the ammonium (NH+4), nitrate 3 (NO 3 ), nitrite (NO2 ) and phosphate (PO4 ) concentrations. 2.3. Water analyses During the experiment, the pH and DO concentrations of the water were measured using an electrochemistry meter (ORION VERSA STAR) daily at 09:00 until the end of the experiment. The concentrations of inorganic nutrients were measured using a continuous flow analyser (Model: SKALAR SANplus). Using Skalar meth ods, the concentration of NOx (NO 3 + NO2 ) was determined using the cadmium–copper reduction and Griess reaction, NH+4 was quantified using a modified Berthelot reaction, and PO3 was 4 determined using phosphomolybdenum blue colorimetry. The DIN concentration was calculated as the sum of the NOx and NH+4 concentration, and the DIP concentration was equal to the concentration of PO3 4 . TDN and TDP were determined by total ultraviolet (UV) digestion with an oxidation solution (K2S2O8 + NaOH), which 3 automatically digested the TDN and TDP into NO 3 and PO4 , respectively. The concentration of dissolved organic nitrogen (DON) and phosphorus (DOP) was calculated by subtracting the DIN from the TDN and the DIP from the TDP, respectively. To determine the particulate nutrient content, the filters and blank membranes were immediately transferred into polypropylene centrifuge tubes, and 25 ml of 0.1-mol l1 HCl were added. The tubes were vibrated for 2 h and then centrifuged. The supernatants were used to determine the particulate inorganic nitrogen (PIN) and phosphorus (PIP) (Fang, 2004; Ruttenberg, 1992) using the analyser. After washing with Milli-Q water, the residual membranes were autoclaved at 124 °C for 1 h with 25 ml of a potassium peroxodisulfate (K2S2O8) and sodium hydroxide (NaOH) solution to digest the particulate organic nitrogen (PON) and phosphorus 3 (POP) into NO 3 and PO4 , respectively (Bronk et al., 2000; Thien and Myers, 1992). After natural cooling, the water samples were also tested using the analyser. The total particulate nitrogen (TPN) was calculated by summing the PIN and PON, and the total particulate phosphorus (TPP) was calculated by summing the PIP and POP, respectively. The total nitrogen (TN) was calculated by summing the TDN and TPN, and the total phosphorous (TP) was calculated by summing the TDP and TPP, respectively. The analyser detection limits for NH+4, NOx, PO3 4 , TDN and TDP were 1, 1, 1, 5 and 10 lg l1, respectively. 3. Results 3.1. The decomposition characteristics of C. nozakii The experiments demonstrated that C. nozakii decomposed completely within 14 days. The jellyfish tissue exhibited no obvious changes at the beginning of incubation. Beginning on the 3rd day, the blocks of jellyfish became smaller pieces with an unpleasant odour and then decomposed rapidly. As the jellyfish decomposed, the tissue pieces gradually reduced in size, and a white/transparent membrane appeared on the surface of the water, causing the water to become turbid, sticky and foul-smelling. The phenomenon lasted for 6 days, after which the blocks of jellyfish were no longer visible and only some floccules were found in the water. From that time until the end of the experiment, the jellyfish tissue decomposed completely, and the environments became visually similar to the controls; however, they retained a pungent odour.
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3.2. Influence of C. nozakii decomposition on the pH
with sediment recovered faster from the minimum value than did that of the water without sediment.
The two jellyfish treatments exhibited similar changes but were significantly different from the controls (Fig. 1). The pH values of the two control treatments changed slightly and exhibited almost linear, with average values of 8.03–8.07; these values were greater than those of the jellyfish treatments throughout the entire experiments. In the first 5 days, the pH in the jellyfish treatments decreased sharply (0.77–0.92 units). The lowest pH of the jellyfish treatments occurred on the 5th day, representing a 9.4–11.4% decrease compared with the controls. The maximum diurnal variation was observed at the beginning of decomposition, with values of 0.35–0.41 units. After the first 5 days, the pH increased continuously until the 12th day and then remained stable until the end of the experiment. When the decomposition was complete, the pH values of the jellyfish treatments were 7.55–7.77; these values were less than those of the controls. Although the pH values of the SJ and SSJ treatments exhibited a similar trend, the degree of variation was different. At a later incubation time (from day 9), the pH difference (4pH) in the SJ treatment was significantly lower than that in the SSJ treatment (p < 0.05); during decomposition, the pH values of the treatments with sediment recovered faster than those of the treatments without sediment.
3.3. Dynamic variations in the DO
3.4.1. Release of particulate nitrogen and phosphorus During the decomposition of C. nozakii, the concentrations of particulate N and P in the control treatments remained low and changed little throughout the experiments (Fig. 3). In the treatments with addition of jellyfish, the PIN values reached their maxima on day 7 and then decreased gradually to the normal level until the end of the experiment. However, the PIP increased sharply after the addition of the jellyfish. The PIP in the SJ treatment decreased gradually until the end of the experiment. In the SSJ treatment, the PIP decreased sharply from a peak of 165.5 ± 27.2 lg l1 on the 5th day to 49.1 ± 11.4 lg l1 on the 6th day and then decreased gradually until the end of the experiment. The PIN was significantly greater in the SJ treatment than in the S treatment from the 3th day until the 15th day (p < 0.05). In the SSJ treatment, the PIN was greater than in the SS treatment from the 2nd day until the 9th day (p < 0.01) and exhibited a slightly longer lag phase compared with the SJ treatment. The PIP values of both jellyfish treatments were significantly greater than those of the controls (p < 0.01) for the whole incubation period. The PON and POP exhibited similar trends, sharply increasing to a maximum after the addition of the jellyfish and then decreasing until the end of the experiment. There was a significant correlation between the PON and POP (RSJ = 0.977, RSSJ = 0.977, p < 0.01) during the whole incubation period. However, after the maximum values were obtained, the change in the PON was greater than that in the POP. The maximum values of the PON and POP in the treatments without sediment lagged behind the values in the treatments with sediment. The concentrations of PON and POP in both jellyfish treatments were significantly greater than those of the controls during the whole incubation period (SJ: pN < 0.01, pP < 0.01; SSJ: pN < 0.05, pP < 0.01). The average PIN, PIP, PON and POP values for the whole incubation period were 6–11, 9–15, 6– 11 and 8–23 times higher than those of the controls, respectively. The dynamic change in the TPN exhibited a pattern similar to the PON because the PON was nearly one order of magnitude greater than the PIN. The TPP included both the PIP and POP. Both the TPN and TPP values in the treatments with jellyfish were significantly greater than those of the controls throughout the entire incubation period (p < 0.01). 3.4.2. Release of dissolved nitrogen and phosphorus The dissolved nutrient changes were quite different from those of the particulate phases (Fig. 4). However, for both control
8.2
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Fig. 2 shows the variation in the DO and DO differences (4DO) caused by the decomposition of C. nozakii. The DO in both control incubations remained high for the duration of the entire experiments; however, the control with sediment had a lower DO than did the control with seawater alone. For the jellyfish treatments, the DO concentrations decreased sharply and were significantly less than those of the controls from the 2nd day (p < 0.01). The DO concentrations in both jellyfish incubations reached a minimum on the 3rd day (which lasted for 7 days), with a range from 17.7 ± 4.2 lmol l1 (mean ± SE) to 36.4 ± 14.8 lmol l1; these values were one-eighth to one-sixth of those of the controls. During the last 6 days, the DO concentrations increased gradually. Compared with the SJ treatment, the DO concentrations of the SSJ exhibited a higher increase in amplitude from day 10, but no significant differences were detected. The DO consumption reached maximum values of 5550.8–7378.9 lmol kg1 d1 in the jellyfish treatments. The difference in the DO consumption between the SJ and SSJ treatment was large, and the DO consumption in the SJ was significantly greater than that in the SSJ from the 10th day until the 14th day (p < 0.05). In short, the addition of C. nozakii prolonged the consumption of DO, and the DO of the water
3.4. Nutrient dynamics
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treatments, all forms of dissolved nutrients remained low and changed little throughout the incubation period. In all cases, NH+4 was the dominant form of DIN, and small quantities of NOx were released by the jellyfish. Therefore, the dynamic changes in the NH+4 concentrations were similar to the changes in the DIN values. The same trend was evident for the DIN and TDN, which increased continuously after the initial addition of the jellyfish, peaked, and then decreased in the final 1–2 days. Following the addition of the jellyfish, there was a continuous release of DIN and TDN. The DIN reached a maximum of 9674.5–10117.1 lg l1 in the jellyfish treatments, which was 8–9 times greater than in the controls. The TDN reached a maximum of 10213.9–11093.2 lg l1, which was approximately 8 times greater than in the controls. The DON comprised a small part of the TDN (6.9–31.9%). The DON values of the jellyfish treatments were significantly greater than those of the controls from the 4th day until the end of the experiment. The trend in the DON values differed from the trend in the DIN
and TDN values; the DON peaked before the DIN and TDN. The DON reached a maximum of 2567–3329.0 lg l1 in the jellyfish treatments and was 8–11 times greater than in the controls. The DIN, DON and TDN values of the jellyfish treatments were 5–6, 5 and 7 times higher than those of the controls, respectively, when integrated over the 14 incubation days. Regarding the dissolved phosphorus, the changes in the DIP differed from those in the TDP. In the SJ treatment, the DIP increased slightly but steadily until day 9, rose sharply from day 10 to 13, and then decreased in the last two days. The DIP of the SJ treatment reached a maximum of 501.9 ± 25.0 lg l1 on 13th day, which was 10 times greater than that of the S treatment. In the SSJ treatment, the DIP increased sharply from day 5 to day 13, and then decreased in the following days. The DIP of the SSJ reached a maximum value of 599.9 ± 60.0 lg l1 by day 13; this value was 14 times greater than that of the SS treatment. The TDP values of both jellyfish treatments exhibited similar variation, gradually increasing after the
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addition of the jellyfish, peaking and then decreasing until the end of the experiment. The DOP values in both jellyfish treatments increased from the 4th day, remained steady until the last 1–2 days, and then decreased until the end of the experiment. 3.4.3. Composition and percentages of nitrogen and phosphorus The ranges and mean of N and P in the water column released by the jellyfish are summarized in Table 1. The average concentration of the TN during jellyfish decomposition was 8364–8500 lg l1, which was 12 times higher than the TP, with values of 695– 706 lg l1. The dissolved nutrient concentrations were greater than those of the particulate nutrient: the TDN and TDP accounted for 91.2–94.4% of the TN and 74.8–96.5% of the TP, respectively (Fig. 5). DIN, especially NH+4, was the dominant form in all treatments and contributed 81.7–85.9% of the TDN in the water column. In the control treatments, the DON occupied the smallest proportion, just 14.1–16.0%. In contrast, NOx occupied the smallest proportion in the treatments with the jellyfish, only 2.5–2.7%. Regarding phosphorus compounds, the DOP was the dominant component of the TP in the control treatments, whereas the DIP and DOP were equivalent in the jellyfish treatments. The proportions of PIP and POP in the jellyfish treatments were greater than those of the controls. During jellyfish decomposition, the forms and proportions of N and P in the water column were continually changing. Compared with the control treatments, the percentages of NH+4 and PON in the water column increased with the addition of jellyfish, whereas NOx and PIN decreased; the DON changed little. Similarly, the percentages of DIP, PIP and POP in the jellyfish treatments increased compared with the controls, whereas the percentage of DOP decreased. Generally, the nutrients released by jellyfish were mainly in dissolved phases, especially NH+4 and DIP, and were approximately 72.2–75.2% of the TN and 34.9–43.1% of the TP. NH+4 exhibited a significant positive correlation with TN (RSJ = 0.9862, RSSJ = 0.9856, p < 0.01), and DIP exhibited a significant positive correlation with TP (RSJ = 0.7788, RSSJ = 0.8860, p < 0.01). 3.4.4. Ratios of N/P during jellyfish decomposition During the jellyfish incubation, the PON/POP ratios had average values of 26–28, which were less than those of the controls but greater than the Redfield ratios throughout the decomposition time (Fig. 6). In contrast, the TPN/TPP ratios of the jellyfish treatments reached average values of 10, which were less than the Redfield ratios. Moreover, the primary difference between the SJ and SSJ treatments was that the PON/POP and TPN/TPP ratios in the SJ were lower than in the SSJ from the beginning until the 8th day; however, they were greater from the 8th day until the end of the experiment. Regarding the dissolved nutrients, the DIN/DIP ratios of both jellyfish treatments were much greater than those of the controls from the initial time until the 10th day, with average values of 73–96, but were less than those of the controls from the 11th day until the end of the experiment, with values of 39–43 (reaching a maximum of 136–138 by day 3). The TDN/TDP of the treatments with jellyfish
were approximately 2 times greater than those of the controls, which increased gradually, peaked to 36–39 by day 8, and then decreased until the end of the experiment. Overall, the average ratios of DIN/DIP and TDN/TDP of the jellyfish treatments were 69 and 29, which were much greater than the Redfield ratio. Moreover, both the DIN/DIP and TDN/TDP ratios in the SJ treatment were greater than those in the SSJ treatment during the entire incubation period. 4. Discussion 4.1. Jellyfish decomposition after blooming Jellyfish populations accumulate and form blooms, which last for just a few days, weeks or months because of limitations of food and space, changes in temperature and oxygen, and jellyfish life cycles. When jellyfish die, their carcasses may decompose in the water column or on the seabed, depending on the depth of water and the sinking rate of the jellyfish. The rate of jellyfish falling to the seabed is rapid and varies from 850 to 1500 m d1, and the rate is influenced by the jellyfish size, elemental composition, delay rate, carcass geometry, orientation adopted, and seawater temperature (Lebrato et al., 2013). This fast sinking rate implies that jellyfish carcasses are deposited on the seafloor in a few days (at most) or a few hours (at least), which is less than the time required for jellyfish decomposition. In general, dead jellyfish sink to the seabed while decomposing, and the processes of decomposition primarily occur on the seafloor. Some authors have observed this phenomenon with videos or photography (Lebrato et al., 2010). The C. nozakii decomposition observed in our experiment indicated that decomposition in the water column and on the seabed is different. The results demonstrated that sediment was beneficial in recovering from acidification and hypoxia, and it may act to mitigate changes in marine environments. The decomposition of jellyfish is very rapid. Titelman et al. (2006) reported that jellyfish decomposition was exponential, with decay-coefficients of 0.67–1.12 d1, and decomposition had a negative correlation with the jellyfish size. In our study, the time of decomposition was 14 days for C. nozakii (wet weight 800 g) in laboratory experiments, which was longer than the time for other jellyfish species. For example, it took 4.1 to 7 days for Periphylla periphylla (42.6–300 g) (Titelman et al., 2006), 6–7 days for Nemopilema nomurai (5000 g) (Song et al., 2012) and 9 days for Catostylus mosaicus (1600 g) (West et al., 2009b). These results suggest that the processes of decomposition after jellyfish blooms are transitory; however, they also exert a strong influence on the ambient environment. 4.2. Poor water quality during jellyfish decomposition Decomposition is always associated with poor water quality. In this study, a foul odour due to the jellyfish decomposition was present throughout the entire incubation; this odour may be the result
Table 1 Ranges and means of nitrogen (N) and phosphorus (P) (lg l1) in the water column during jellyfish incubation when integrated over 14 days. Treatment
S SJ SS SSJ
Range Average Range Average Range Average Range Average
N (lg l1)
P (lg l1)
NH+4
NOx
DON
PIN
PON
TN
DIP
DOP
PIP
POP
TP
803–1150 973 1549–9576 6038 601–915 789 1945–9567 6429
83–282 194 57–546 193 201–333 280 54–602 210
113–275 191 783–2329 1393 83–325 203 465–2668 1336
11–21 17 19–83 43 11–22 17 13–97 36
31–109 64 223–1185 697 49–133 85 129–1146 523
1252–1640 1439 2886–11,660 8364 1170–1558 1373 3077–11,735 8500
49–60 54 38–502 237 33–63 51 59–600 310
136–215 181 165–346 283 133–204 161 175–321 277
2–11 4.5 17–197 118 4–13 8.6 30–166 77
2–7 4.0 17–102 57 2–8 4.8 12–96 42
202–277 243 278–937 695 197–262 225 310–952 706
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Fig. 5. Percentage of nitrogen (NH+4, NOx, DON, PIN, and PON) in the TN and phosphorus (DIP, DOP, PIP, and POP) in the TP during Cyanea nozakii decomposition when integrated over 14 days.
30
60
SJ S(y=37.0)
SJ S(y=21.9)
25
40
TPN/TPP
PON/POP
50
SSJ SS(y=41.8)
30 20
20 15 10 5
10
0
0 0
2
4
6
8
10
12
14
16
0
2
4
Incubation Time (Day)
6
8
10
12
14
16
Incubation Time (Day) 50
150
90 60
SJ SSJ S(y=13.0) SS(y=13.3)
40
TDN/TDP
SJ SSJ S(y=47.6) SS(y=47.9)
120
DIN/DIP
SSJ SS(y=16.6)
30 20 10
30
0
0 0
2
4
6
8
10
12
14
16
Incubation Time (Day)
0
2
4
6
8
10
12
14
16
Incubation Time (Day)
Fig. 6. Ratios of N/P (mol/mol) in the treatments during jellyfish decomposition.
of spoilage by-products, such as biogenic amines and sulphide compounds (Gram and Dalgaard, 2002). Our studies also demonstrated that jellyfish decomposition led to some water acidification. The pH of water decreased at the initial stage of jellyfish decomposition, then increased and levelled off. We speculate that a large amount of jellyfish decomposition would likely lead to rapid release of some acidic substances. Although the substances are unknown at present and require further investigation, we speculate that the release of amino acids and fatty acids from proteins and lipid metabolism of jellyfish tissue is likely one of the main sources of these substances (Liu et al., 2007, 2004). As jellyfish decompose, the organic acids consumed by microorganisms exceed those released from the jellyfish, which induces an increase in the pH. Until the jellyfish decompose completely, the remaining organic acids cause relative acidification of the seawater.
Acidification from jellyfish decomposition is more serious in some situations, such as when there is a temperature decrease, pH change or salinity change (Ma et al., 2012). In this study, the decomposition of jellyfish significantly reduced the DO concentrations of the seawater. The results demonstrated that the duration of low DO was at least half of the total decomposition time, and the recovery processes were relatively slow. Therefore, the large DO consumption and long duration of low DO could result in localized hypoxic (
