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Impact of jellyfish and mussels on algal blooms caused by seasonal oxygen depletion and nutrient release from the sediment in a Danish fjord
Journal of Experimental Marine Biology and Ecology 351 (2007) 92 – 105 www.elsevier.com/locate/jembe
Impact of jellyfish and mussels on algal blooms caused by seasonal oxygen depletion and nutrient release from the sediment in a Danish fjord Lene Friis Møller, Hans Ulrik Riisgård ⁎ Marine Biological Research Centre, University of Southern Denmark, Hindsholmvej 11, DK-5300 Kerteminde, Denmark Received 1 May 2007; received in revised form 1 June 2007; accepted 11 June 2007
Abstract The present case study in the heavily eutrophicated Skive Fjord (Denmark) provides an illustration of the potential links between primary production, oxygen deficiency, nutrients, mussels and jellyfish, and highlights the value of long-term monitoring and an experimental, integrative approach in the investigation of eutrophication processes. Skive Fjord suffers every summer from oxygen depletion in the near-bottom water causing large amounts of nutrients (phosphate and ammonia) to be released from the anoxic sediment. This subsequently stimulates a phytoplankton bloom, followed later on by an increase in the zooplankton. The surface chlorophyll a concentrations may become very high during periods with exceptionally severe oxygen depletion, and in certain years with mass occurrence of jellyfish (Aurelia aurita) peak concentrations as high as 60 to 80 μg chl a l− 1 have be measured in Skive Fjord because the jellyfish effectively eliminate the zooplankton-grazing impact on the phytoplankton bloom. Likewise, the grazing impact by dense populations of mussels (Mytilus edulis) can modify the phytoplankton biomass, especially in the near-bottom water. Here we combine available data on jellyfish and mussels with data on oxygen, nutrients, chlorophyll a, zooplankton, and other data from different studies conducted in Skive Fjord during the period 1996–2005. The study indicates that especially severe cases of oxygen depletion take place in years with mass occurrence of jellyfish because the blooming algae are not efficiently grazed, but settle to the bottom to be subsequently decomposed, leading to more severe oxygen depletion and killing of filter-feeding mussels, further escalation of the issue and severely impact of ecosystem services proved by the mussels. © 2007 Elsevier B.V. All rights reserved. Keywords: Aurelia aurita; Eutrophication; Grazing impact; Mytilus edulis; Oxygen depletion; Phytoplankton blooms; Zooplankton control
1. Introduction Eutrophication and subsequent near-bottom oxygen depletion in near shore and estuarine areas is an increasing environmental problem worldwide (Jørgensen and Richardson, 1996; Diaz, 2001). Eutro⁎ Corresponding author. Tel./fax: +45 6532 1433. E-mail address: [email protected] (H.U. Riisgård). 0022-0981/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2007.06.026
phication has been suggested to be an important environmental factor for increasing mass occurrence of jellyfish, possibly accelerated in combination with overfishing (Mills, 2001). Jellyfish are tolerant to low dissolved oxygen concentrations (Purcell et al., 2001; Rutherford and Thuesen, 2005) and they are therefore likely to take over oxygen depleted waters previously inhabited by zooplanktivorous fish. A new dominance of jellyfish alters the pathway of energy (Matsakis and
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Conover, 1991), and jellyfish respond quickly to changes in patches of food by exploiting their high feeding and growth rate potentials (Olesen et al., 1994; Olesen, 1995): during starvation periods of up to 25 days, they survive by degrowth (Frandsen and Riisgård, 1997). The jellyfish species most frequently linked with eutrophication is the globally-distributed moon jellyfish, Aurelia aurita, which during summer may make up the vast majority of the pelagic biomass in coastal waters (Möller, 1979; Arai, 2001). A. aurita mainly preys on zooplankton, and during summer it has the potential to control the zooplankton biomass in e.g. Limfjorden (Denmark) (Hansson et al., 2005; Møller and Riisgård, in press), Kertinge Nor (Denmark) (Olesen, 1995), and Kiel Bight (Germany) (Behrends and Schneider, 1995). Every year during late summer up to 40% of the bottom area in the heavily eutrophicated Limfjorden (Denmark) suffers from oxygen depletion in the nearbottom water (Jørgensen, 1980; Riisgård and Poulsen, 1981; Møhlenberg, 1999; Conley et al., 2000). In certain years, high densities of jellyfish (A. aurita) have been observed especially in Skive Fjord, an inner branch of Limfjorden. Recent studies show that the predation impact of the jellyfish on zooplankton may be particularly pronounced in Skive Fjord in July and August (Hansson et al., 2005; Møller and Riisgård, in press). Thus in August 2003, the estimated half-life of zooplankton was only 5 to 12 h, coincident with low concentrations of zooplankton and high chlorophyll a concentrations. This suggests that high densities of jellyfish may prevent the zooplankton from rapidly
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grazing down the blooming phytoplankton, thus reinforcing the effects of eutrophication and oxygen depletion. The oxygen conditions in Skive Fjord are coupled to the nitrogen-load, and thus during summer-stratification the rate of oxygen-decrease in the near-bottom water is correlated to the nitrogen-load accumulated during the preceding 10 months (Møhlenberg, 1999). Due to efforts to reduce nitrogen and phosphorus loads, decreasing trends have been observed in Skive Fjord through the period 1984–2002 (Møhlenberg et al., 2007), but the fjord still suffers from oxygen depletion every summer. The most conspicuous effect of anoxia is a mass kill of the benthic animals, particularly blue mussels (Mytilus edulis), due to release of toxic H2S accumulated in the sediment (Jørgensen, 1980; Rosenberg et al., 1992; Richardson and Jørgensen, 1996; Møhlenberg, 1999), but also sediment release of particularly phosphorous may be an important key factor for subsequent algal blooms and a possible selfsustaining “vicious circle” (Vahtera et al., 2007). The dense populations of filter-feeding mussels in Skive Fjord are likely to modify the effects of eutrophication by their grazing on the phytoplankton (Riisgård et al., 2004), thus keeping the water clear (but not clean), and by their accumulation of organic material (mainly faeces), thus enhancing oxygen depletion in the mussel bed (Jørgensen, 1980) and subsequent release of nutrients in high amounts (Asmus and Asmus, 1991). The high densities of the common jellyfish A. aurita also may influence the effects of eutrophication in Skive Fjord, where the jellyfish-predation impact on zooplankton may be particularly pronounced in July and
Fig. 1. Map showing the sampling locality in Skive Fjord, an inner branch of Limfjorden, Denmark.
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August (Hansson et al., 2005; Møller and Riisgård, in press). In order to test these ideas, we combine available data on jellyfish and blue mussels with data on oxygen, ammonia, phosphate, chlorophyll a, and zooplankton measured in Skive Fjord during the period 1996 to 2005. The present study provides an illustration of the potential links between primary production, oxygen deficiency, nutrients, mussels, and jellyfish, and highlights the value of long-term monitoring and an integrative approach in the investigation of eutrophication processes. 2. Materials and methods 2.1. Study site Skive Fjord is an inner branch of Limfjorden which is a shallow fjord-system that is open to both the North Sea (32 to 34 psu) and to the Kattegat (19 to 25 psu) (Fig. 1). Skive Fjord covers 101 km2, the mean depth is 5 m and the tidal range is 0.1 m. The mean salinity is 25 psu, and the salinity at the bottom is usually a few psu higher than at the surface. During summer a concomitant thermocline stabilizes this stratification which can only be broken by strong winds (Jørgensen, 1980; Møhlenberg, 1999). The water renewal is governed by water exchange between the North Sea (via Thyborøn Kanal) and the Kattegat: the salinity stratification in Skive Fjord often may be very pronounced due to freshwater that overlays the incoming saline water from the North Sea (Jørgensen, 1980; Møhlenberg, 1999). 2.2. Available data Skive Fjord is one of the locations in the Danish national monitoring program (Svendsen and Norup, 2005), and a fixed station in the fjord is also the site (E: 9°4.55; N: 56°37,25) for weekly sampling conducted by the Limfjord County Authorities (LCA). A considerable amount of data used in the present study (i.e. salinity, oxygen, nutrients, primary production, chlorophyll a, and zooplankton composition and concentration) have been produced by LCA in the period 1996 to 2005. Most of the data are freely available on the NERI (National Environmental Research Institute) web-data base (MADS). Monitoring of blue mussels (M. edulis) in the month of September in 1998 to 2005 formed part of LCA's environmental program in Skive Fjord. Shell length (L, mm), wet weight of total animals with shells (WW, g), and density (D, ind. m− 2) of mussels were determined for certain depth intervals. In the present study, we combine the mussel population density data with
Fig. 2. Conceptual illustration of the yearly chemical–biological cascade events in Skive Fjord.
individual filtration rate (Find) data from the literature in order to estimate the area-specific population filtration rate: Fpop = D × Find, where Find (l h− 1) = 0.0012L2.14
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(Kiørboe and Møhlenberg, 1981). The half-life time for the phytoplankton cells was estimated as: t1/2 = (V / Fpop) × ln2, where V = volume of fully mixed water above the mussels (Riisgård et al., 2004).
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During the spring of 1996 to 1999, the abundance of jellyfish was monitored in Skive Fjord by Bio/consult (2001). In 2003, bell diameter and population density data on the common jellyfish, A. aurita, were obtained
Fig. 3. Skive Fjord. Chemical-biological parameters measured in the fjord during a 10 year period: A) 1996–97, B) 1998–99, C) 2000–2001, D) 2002–2003, E) 2004–05. Panels, from top and downwards: 1) oxygen and total phosphate concentration in bottom water, 2) nitrate/nitrite and ammonium concentration (bottom water), 3) primary production, 4) chl a concentration in surface and bottom water, 5) biomass of zooplankton.
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Fig. 3 (continued ).
during 5 cruises in Skive Fjord in the period February to August (Hansson et al., 2005; Møller and Riisgård, in press). From February to October in the years 2004 and 2005, LCA made weekly sampling of jellyfish in Skive Fjord in order to supplement our studies in the fjord (Møller and Riisgård, in press).
In September of every year, the Danish Institute for Fisheries Research trawls for fish in Limfjorden. The percentage of trawls that could not be made due to overloading of the fishing nets by A. aurita has recently been worked out for the period 1984 to 2004 (Hoffmann, 2005). Skive Fjord is one of the localities where the
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Fig. 3 (continued ).
highest biomass of A. aurita is found in Limfjorden (Hansson et al., 2005). As a useful, although indirect expression for the biomass of A. aurita in Skive Fjord, we have adopted an index (‘Hoffmann-index’) which expresses the percentage of standard monitoring trawls for fish that was not completed due to overloading of the fishing gear by jellyfish (Hoffmann, 2005).
3. Results 3.1. Oxygen depletion and chemical–biological cascade events A simplified graphic presentation of the yearly chemical–biological cascade events in Skive Fjord is
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Fig. 3 (continued ).
depicted in Fig. 2. High concentrations of nitrate accumulated during winter (due to run-off from the agriculture and pig farming dominated catchment area) is gradually used up by the phytoplankton in spring → algal biomass → sedimentation → oxygen demand of sediment. During summer when the water column is
stratified and re-aeration of the bottom water by windmixing is effectively prevented, the oxygen concentration gradually decreases and oxygen depletion occurs when the oxygen consumption at the bottom due to zoobenthic respiration and microbial decomposition exceeds the oxygen supply. This eventually results in
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Fig. 3 (continued ).
release of large amounts of phosphate and ammonium from the anoxic sediment. The release of nutrients now stimulates the primary production, resulting in an increase in the algal biomass which is subsequently, after a certain time lag period, grazed down by an
increasing number of zooplankton organisms (if they have not been eaten by jellyfish, see later). The measured chemical and biological parameters generally followed the above simplified presentation (Fig. 3A–E). The concentrations of oxygen in Skive
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Fig. 4. Skive Fjord. (A) “Hoffmann-index”, (B) Mean (+ or − standard deviation, n = 7) chl a concentration (surface and bottom water), (C) Mean biomass of Mytilus edulis (4 to 5 m, and 6 m depth) in September during the period 1996 to 2005. Standard deviation indicated (n = 5 for mussels on 4 to 5 m; n = 2 for mussels on 6 m).
Fjord in 1996 to 2005 showed that oxygen deficiency occurred every summer, although the degree and duration period with of lack of oxygen differed among years. Due to oxygen depletion in the near-bottom water, large amounts of nutrients (phosphate and ammonia) were usually released from the anoxic sediment, subsequently causing a peak in the primary production and chl a concentration. This phenomenon with oxygen depletion and phytoplankton bloom appeared more or less pronounced every year over the 10-year study period, and generally, the surface chl a concentrations were very high during periods with exceptionally severe oxygen depletion, and in some years peak concentrations as high as 60 to 80 μg chl a l− 1 were measured in Skive Fjord.
3.2. Jellyfish and zooplankton dynamics The Hoffmann-index suggested that the abundance of A. aurita medusae was low in Skive Fjord in the Table 1 Mytilus edulis Depth (m)
Biomass (g wet wt m− 2)
Years 0–2 2–4 4–6 6–7
2003 3974 1347 18 0
2004 2962 2148 445 366
2005 2569 2284 748 938
Area-specific biomass (wet weight, incl. shells) of mussels at different depths in Skive Fjord in September in 2003 to 2005.
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Fig. 5. Skive Fjord. Salinity profiles in autumn 2004.
period 1996 to 1998, after which their abundance increased to a maximum in 2003 before rapidly decreasing again (Fig. 4A). This pattern is supported by other more direct quantitative measurements as almost no A. aurita were observed in the springs of 1996 to 1998, whereas an increase in abundance was recorded in the spring of 1999 (Bio/consult, 2001), and further, mass occurrence of A. aurita took place during the summer of 2003 (Hansson et al., 2005; Møller and Riisgård, in press). In the early spring of both 2004 and 2005, A. aurita ephyrae were present in Skive Fjord, but they disappeared in April/May, and almost no A. aurita were present during the rest of the summer in either 2004 or 2005 (Møller and Riisgård, in press). In 2003, A. aurita had the potential to control the zooplankton from mid May to August in Skive Fjord
(half-life times between 0.8 and 6.2 d) (Hansson et al., 2005; Møller and Riisgård, in press). In agreement with this, almost no zooplankton was present in this period (Fig. 3D). A. aurita medusae were not present in Skive Fjord during the summer of 2004 and 2005 and the concentration of zooplankton was considerably higher (Møller and Riisgård, in press). Besides of these direct predation effects of A. aurita, available data also indicate some indirect effects. Thus in 2003, release of phytoplankton from zooplankton-grazing control due to zooplankton predation by A. aurita resulted in a pronounced phytoplankton bloom (with up to 60 μg chl a in the surface water) triggered by the release of nutrients from the sediment during a period with oxygen depletion (Fig. 3D). Similar algal blooms were not observed in 2004 and 2005 when no A. aurita were present, and
Fig. 6. Skive Fjord. Salinity and oxygen profiles in 2003 (11 August), 2004 (18 August), and 2005 (18 July).
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although the primary production was equally high (Fig. 3). This is in agreement with the observation that very high chl a concentrations in the surface water only occurred in years with high densities of A. aurita and
reduced grazing impact by zooplankton, whereas the chl a concentration in years with few A. aurita was relatively low (10 to 20 μg l− 1) due to a pronounced zooplankton-grazing impact. The large variation in the
Fig. 7. Skive Fjord. Density-driven volume flow (m− 3 s− 1) of surface and bottom water during early spring of 2003, 2004 and 2005. Positive values indicate flow of usually lighter (less saline) surface water out of the fjord; negative values indicate inflow of usually high-density saline bottom water.
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mass occurrence of jellyfish in Skive Fjord may be explained by irregular hydrographical incidents where incoming North Sea water replaces the old water and thus at the same time partly or completely (as seen in 2004 and 2005) wash the jellyfish out of the fjord (see later).
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feeding behaviour and a diet not including copepods (Riisgård, 2007). Thus, infrequent intrusions of large volumes of high-salinity seawater from the North Sea, may radically change the hydrographic situation and thereby strongly influence the chemical–biological cascade events as well as the distribution and abundance of jellyfish in Skive Fjord.
3.3. Oxygen depletion and mussels 4. Discussion The biomass of mussels (M. edulis) recorded in Skive Fjord in September seems to be inversely correlated with both the abundance of A. aurita and the nearbottom chl a concentration (Fig. 4). The highest biomass of mussels were found in 1998, 2004, and 2005, but due to severe oxygen depletion in 1999 and 2001 to 2003, almost no mussels were found at water depths below 4 m. In the years 2003 to 2005 M. edulis thrived well at depths down to 4 m, but below 4 m it was seriously affected by oxygen depletion (Table 1), the extent of which was strongly correlated with the salinity stratification that prevented mixing of oxygen down to the bottom 13(Fig. 5). The area-specific population filtration rate of M. edulis was calculated to be Fpop = 0.2 m3 m− 2 d− 1 at 4 to 5 m depth in September of 2003 and Fpop = 6 m3 m− 2 d− 1 at 4 to 7 m in September of 2004. The thickness of the water layer below the halocline was about 2 m at 5 m depth (Fig. 5). Therefore, assuming full mixing in this layer, the estimated phytoplankton halflife times were 7 and 0.2 d in 2003 and 2004, respectively. The systematically lower chl a concentrations in the near-bottom water (Fig. 4B) may thus be explained by the grazing impact of mussels. 3.4. Hydrography and jellyfish The mean salinity in Skive Fjord is about 25 psu and the salinity at the bottom it is usually a few psu higher than at the surface (Fig. 5). Occasionally, persistent, strong westerly winds push high saline North Sea water into the fjord-system through the Thyborøn Kanal, which may cause large variations in the vertical salinity profiles, as seen in August–September 2004 in Skive Fjord (Fig. 6). Here, the vertical variations in salinity are generally caused by the interplay between input of light freshwater from the catchment area and near-bottom inflow of high-density saline water. In early spring of both 2004 and 2005, dramatic changes in the salinity vertical profiles and subsequent density-driven water exchange (Fig. 7) coincided with the disappearance of A. aurita (Møller and Riisgård, in press) and the introduction of a new species of jellyfish in the fjord, the hydromedusa, Aequorea vitrina, which has a different
Comparable effects of A. aurita as reported here for Skive Fjord has previously been suggested by Schneider and Behrends (1998) who observed a linear correlation between chl a (in upper 10 m water column) and A. aurita abundance in Kiel Bight in the period 1990 to 1994. Likewise, a tendency of algal blooms related to high abundances of jellyfish was noticed by Huntley and Hobson (1978) who suggested that a second “spring” bloom in a Canadian fjord was due to reduced herbivore grazing caused by a high zooplankton-predation impact exerted by medusae (Phialidium gregarium). Further, in Gullmar Fjord (Sweden) heavy phytoplankton blooms occurred in 1978 and 1981 during spring and autumn and coincidently low zooplankton and high scyphomedusae abundances were observed. This lead to increased sedimentation of organic matter and oxygen deficiency occurred in absence of adequate water exchange (Lindahl and Hernroth, 1983). Similar cascading effects have been demonstrated for predation by the ctenophore, Mnemiopsis leidyi, on zooplankton in the Black Sea and in Chesapeake Bay (e.g. Oguz, 2005; Purcell and Decker, 2005). By examining 19 years of monitoring data from Skive Fjord, Møhlenberg et al. (2007) found that high biomass of blue mussels cause reduced chl a and increased transparency (Secchi depth), while short-term variability in water-column mixing cause changes in chl a due to nutrient entrainment and coupling to benthic mussels. The present work moderates the above statement by specifically suggesting that variations in near-bottom water chl a may be explained by grazing mussels (Fig. 4B) (see also Dolmer, 2000a,b; Nielsen and Maar, 2007) whereas variations of chl a in the surface water are more likely to be due to the grazing impact of zooplankton, which may be controlled by jellyfish in certain years. It is well known that the first effects of oxygendepleted bottom water in Limfjorden are likely to appear in the dense mussel beds where the rate of oxygen uptake may be 10 times higher than on the surrounding bottom (Jørgensen, 1980). This explains why the stagnant water below a stable halocline can be rapidly
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depleted of oxygen (Fig. 5) and eventually kills the mussels when toxic H2S produced in the anoxic sediment penetrates up into the bottom water (Table 1). The present work has demonstrated the strength of long and thorough time series of traditional environmental monitoring parameters (oxygen, nutrients, chl a, phytoand zooplankton), but it also emphasizes that available data on the abundance of jellyfish is unsystematically collected, although of obvious importance for correct interpretation of the often conspicuous variations in the traditional environmental parameters. Clearly, knowledge about the zooplankton-predatory impact exerted by jellyfish may explain otherwise unaccountable large variations in both zoo- and phytoplankton biomasses. Such insight, along with knowledge about the grazing impact of filter-feeding zoobenthos, is of great importance, not only for a basic understanding of the plankton dynamics in fjords and coastal ecosystems, but also for marine monitoring programmes that routinely use traditional chemical–biological parameters as the only tools in assessment of the environmental conditions. The present case study provides a framework for future experimentally oriented environmental studies based on a holistic ecological approach. Acknowledgements Thanks are due to the Limfjord County Authorities (Limfjordsamterne) for excellent co-operation, especially J. Gross, J. Deding, G. Pedersen, and B. Jensen for supplying data. Unpublished data on jellyfish were kindly supplied by E. Hoffmann. Critical comments and constructive suggestions made by J. E. Purcell and an anonymous referee are highly appreciated. [SS] References Arai, M.N., 2001. Pelagic coelenterates and eutrophication: a review. Hydrobiologia 451, 69–87. Asmus, R., Asmus, H., 1991. Mussel beds: limiting or promoting phytoplankton? J. Exp. Mar. Biol. Ecol. 148, 215–232. Behrends, G., Schneider, G., 1995. Impact of Aurelia aurita medusae (Cnidaria, Schyphozoa) on the standing stock and community composition of mezozooplankton in the Kiel Bight (western Baltic Sea). Mar. Ecol. Prog. Ser. 127, 39–45. Bio/consult, 2001. Fiskelarver og gopler i Limfjorden, foråret 1996–1999. Report in Danish Produced for Limfjordssamarbejdet. v/Nordjyllandsamt, Ålborg, Denmark. Conley, D.J., Kaas, H., Møhlenberg, F., Rasmussen, B., Windolf, J., 2000. Characteristics of Danish estuaries. Estuaries 23, 820–837. Diaz, R.J., 2001. Overview of hypoxia around the world. J. Environ. Qual. 30, 275–281. Dolmer, P., 2000a. Algal concentration profiles above mussel beds. J. Sea Res. 43, 113–119.
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L.F. Møller, H.U. Riisgård / Journal of Experimental Marine Biology and Ecology 351 (2007) 92–105 Purcell, J.E., Breitburg, D.L., Decker, M.B., Graham, W.M., Youngbluth, M.J., Raskoff, K.A., 2001. Pelagic cnidarians and ctenophores in low dissolved oxygen environments: a review. In: Rabalais, N.N., Turner, R.E. (Eds.), Coastal Hypoxia: Consequences for Living Resources and Ecosystems. Coastal and Estuarine Studies, vol. 58. American Geophysical Union, Washington, D.C., pp. 77–100. Richardson, K., Jørgensen, B.B., 1996. Eutrophication: definition, history and effects. In: Jørgensen, B.B., Richardson, K. (Eds.), Eutrophication in Coastal Marine Ecosystems. Coastal and Estuarine Studies, vol. 52. American Geophysical Union, Washington, D.C., pp. 1–19. Riisgård, H.U., 2007. Feeding behaviour of the hydromedusa Aequorea vitrina. Sci. Mar. 71, 395–404. Riisgård, H.U., Poulsen, E., 1981. Growth of Mytilus edulis in net bags transferred to different localities in a eutrophicated Danish fjord. Mar. Pollut. Bull. 12, 272–276. Riisgård, H.U., Seerup, D.F., Hjort, M.H., Glob, E., Larsen, P.S., 2004. Grazing impact of filter-feeding zoobenthos in a Danish fjord. J. Exp. Mar. Biol. Ecol. 307, 171–261.
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Rosenberg, R., Loo, L.-O., Möller, P., 1992. Hypoxia, salinity and temperature as structuring factors for marine benthic communities in a eutrophic area. Neth. J. Sea Res. 30, 121–129. Rutherford Jr., L.D., Thuesen, E.V., 2005. Metabolic performance and survival of medusae in estuarine hypoxia. Mar. Ecol. Prog. Ser. 294, 189–200. Schneider, G., Behrends, G., 1998. Top-down control in a neritic plankton system by Aurelia aurita medusae — a summary. Ophelia 48, 71–82. Svendsen, L.M., Norup, B., 2005. NOVANA. Nationwide Monitoring and Assessment Programme for the Aquatic and Terrestrial Environments. Programme Description — Part 1. National Environmental Research Institute, Denmark, pp. 1–53. Vahtera, E., Conley, D.J., Gustafson, B.G., Kuosa, H., Pitkänen, H., Savchuck, O.P., Tamminen, T., Viitasalo, M., Voss, M., Wasmund, N., Wulff, F., 2007. Internal ecosystem feedbacks enhance nitrogenfixing cyanobacteria blooms and complicate management in the Baltic Sea. Ambio 36, 186–194.
Impact of jellyfish and mussels on algal blooms caused by seasonal oxygen depletion and nutrient release from the sediment in a Danish fjord Lene Friis Møller, Hans Ulrik Riisgård ⁎ Marine Biological Research Centre, University of Southern Denmark, Hindsholmvej 11, DK-5300 Kerteminde, Denmark Received 1 May 2007; received in revised form 1 June 2007; accepted 11 June 2007
Abstract The present case study in the heavily eutrophicated Skive Fjord (Denmark) provides an illustration of the potential links between primary production, oxygen deficiency, nutrients, mussels and jellyfish, and highlights the value of long-term monitoring and an experimental, integrative approach in the investigation of eutrophication processes. Skive Fjord suffers every summer from oxygen depletion in the near-bottom water causing large amounts of nutrients (phosphate and ammonia) to be released from the anoxic sediment. This subsequently stimulates a phytoplankton bloom, followed later on by an increase in the zooplankton. The surface chlorophyll a concentrations may become very high during periods with exceptionally severe oxygen depletion, and in certain years with mass occurrence of jellyfish (Aurelia aurita) peak concentrations as high as 60 to 80 μg chl a l− 1 have be measured in Skive Fjord because the jellyfish effectively eliminate the zooplankton-grazing impact on the phytoplankton bloom. Likewise, the grazing impact by dense populations of mussels (Mytilus edulis) can modify the phytoplankton biomass, especially in the near-bottom water. Here we combine available data on jellyfish and mussels with data on oxygen, nutrients, chlorophyll a, zooplankton, and other data from different studies conducted in Skive Fjord during the period 1996–2005. The study indicates that especially severe cases of oxygen depletion take place in years with mass occurrence of jellyfish because the blooming algae are not efficiently grazed, but settle to the bottom to be subsequently decomposed, leading to more severe oxygen depletion and killing of filter-feeding mussels, further escalation of the issue and severely impact of ecosystem services proved by the mussels. © 2007 Elsevier B.V. All rights reserved. Keywords: Aurelia aurita; Eutrophication; Grazing impact; Mytilus edulis; Oxygen depletion; Phytoplankton blooms; Zooplankton control
1. Introduction Eutrophication and subsequent near-bottom oxygen depletion in near shore and estuarine areas is an increasing environmental problem worldwide (Jørgensen and Richardson, 1996; Diaz, 2001). Eutro⁎ Corresponding author. Tel./fax: +45 6532 1433. E-mail address: [email protected] (H.U. Riisgård). 0022-0981/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2007.06.026
phication has been suggested to be an important environmental factor for increasing mass occurrence of jellyfish, possibly accelerated in combination with overfishing (Mills, 2001). Jellyfish are tolerant to low dissolved oxygen concentrations (Purcell et al., 2001; Rutherford and Thuesen, 2005) and they are therefore likely to take over oxygen depleted waters previously inhabited by zooplanktivorous fish. A new dominance of jellyfish alters the pathway of energy (Matsakis and
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Conover, 1991), and jellyfish respond quickly to changes in patches of food by exploiting their high feeding and growth rate potentials (Olesen et al., 1994; Olesen, 1995): during starvation periods of up to 25 days, they survive by degrowth (Frandsen and Riisgård, 1997). The jellyfish species most frequently linked with eutrophication is the globally-distributed moon jellyfish, Aurelia aurita, which during summer may make up the vast majority of the pelagic biomass in coastal waters (Möller, 1979; Arai, 2001). A. aurita mainly preys on zooplankton, and during summer it has the potential to control the zooplankton biomass in e.g. Limfjorden (Denmark) (Hansson et al., 2005; Møller and Riisgård, in press), Kertinge Nor (Denmark) (Olesen, 1995), and Kiel Bight (Germany) (Behrends and Schneider, 1995). Every year during late summer up to 40% of the bottom area in the heavily eutrophicated Limfjorden (Denmark) suffers from oxygen depletion in the nearbottom water (Jørgensen, 1980; Riisgård and Poulsen, 1981; Møhlenberg, 1999; Conley et al., 2000). In certain years, high densities of jellyfish (A. aurita) have been observed especially in Skive Fjord, an inner branch of Limfjorden. Recent studies show that the predation impact of the jellyfish on zooplankton may be particularly pronounced in Skive Fjord in July and August (Hansson et al., 2005; Møller and Riisgård, in press). Thus in August 2003, the estimated half-life of zooplankton was only 5 to 12 h, coincident with low concentrations of zooplankton and high chlorophyll a concentrations. This suggests that high densities of jellyfish may prevent the zooplankton from rapidly
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grazing down the blooming phytoplankton, thus reinforcing the effects of eutrophication and oxygen depletion. The oxygen conditions in Skive Fjord are coupled to the nitrogen-load, and thus during summer-stratification the rate of oxygen-decrease in the near-bottom water is correlated to the nitrogen-load accumulated during the preceding 10 months (Møhlenberg, 1999). Due to efforts to reduce nitrogen and phosphorus loads, decreasing trends have been observed in Skive Fjord through the period 1984–2002 (Møhlenberg et al., 2007), but the fjord still suffers from oxygen depletion every summer. The most conspicuous effect of anoxia is a mass kill of the benthic animals, particularly blue mussels (Mytilus edulis), due to release of toxic H2S accumulated in the sediment (Jørgensen, 1980; Rosenberg et al., 1992; Richardson and Jørgensen, 1996; Møhlenberg, 1999), but also sediment release of particularly phosphorous may be an important key factor for subsequent algal blooms and a possible selfsustaining “vicious circle” (Vahtera et al., 2007). The dense populations of filter-feeding mussels in Skive Fjord are likely to modify the effects of eutrophication by their grazing on the phytoplankton (Riisgård et al., 2004), thus keeping the water clear (but not clean), and by their accumulation of organic material (mainly faeces), thus enhancing oxygen depletion in the mussel bed (Jørgensen, 1980) and subsequent release of nutrients in high amounts (Asmus and Asmus, 1991). The high densities of the common jellyfish A. aurita also may influence the effects of eutrophication in Skive Fjord, where the jellyfish-predation impact on zooplankton may be particularly pronounced in July and
Fig. 1. Map showing the sampling locality in Skive Fjord, an inner branch of Limfjorden, Denmark.
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August (Hansson et al., 2005; Møller and Riisgård, in press). In order to test these ideas, we combine available data on jellyfish and blue mussels with data on oxygen, ammonia, phosphate, chlorophyll a, and zooplankton measured in Skive Fjord during the period 1996 to 2005. The present study provides an illustration of the potential links between primary production, oxygen deficiency, nutrients, mussels, and jellyfish, and highlights the value of long-term monitoring and an integrative approach in the investigation of eutrophication processes. 2. Materials and methods 2.1. Study site Skive Fjord is an inner branch of Limfjorden which is a shallow fjord-system that is open to both the North Sea (32 to 34 psu) and to the Kattegat (19 to 25 psu) (Fig. 1). Skive Fjord covers 101 km2, the mean depth is 5 m and the tidal range is 0.1 m. The mean salinity is 25 psu, and the salinity at the bottom is usually a few psu higher than at the surface. During summer a concomitant thermocline stabilizes this stratification which can only be broken by strong winds (Jørgensen, 1980; Møhlenberg, 1999). The water renewal is governed by water exchange between the North Sea (via Thyborøn Kanal) and the Kattegat: the salinity stratification in Skive Fjord often may be very pronounced due to freshwater that overlays the incoming saline water from the North Sea (Jørgensen, 1980; Møhlenberg, 1999). 2.2. Available data Skive Fjord is one of the locations in the Danish national monitoring program (Svendsen and Norup, 2005), and a fixed station in the fjord is also the site (E: 9°4.55; N: 56°37,25) for weekly sampling conducted by the Limfjord County Authorities (LCA). A considerable amount of data used in the present study (i.e. salinity, oxygen, nutrients, primary production, chlorophyll a, and zooplankton composition and concentration) have been produced by LCA in the period 1996 to 2005. Most of the data are freely available on the NERI (National Environmental Research Institute) web-data base (MADS). Monitoring of blue mussels (M. edulis) in the month of September in 1998 to 2005 formed part of LCA's environmental program in Skive Fjord. Shell length (L, mm), wet weight of total animals with shells (WW, g), and density (D, ind. m− 2) of mussels were determined for certain depth intervals. In the present study, we combine the mussel population density data with
Fig. 2. Conceptual illustration of the yearly chemical–biological cascade events in Skive Fjord.
individual filtration rate (Find) data from the literature in order to estimate the area-specific population filtration rate: Fpop = D × Find, where Find (l h− 1) = 0.0012L2.14
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(Kiørboe and Møhlenberg, 1981). The half-life time for the phytoplankton cells was estimated as: t1/2 = (V / Fpop) × ln2, where V = volume of fully mixed water above the mussels (Riisgård et al., 2004).
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During the spring of 1996 to 1999, the abundance of jellyfish was monitored in Skive Fjord by Bio/consult (2001). In 2003, bell diameter and population density data on the common jellyfish, A. aurita, were obtained
Fig. 3. Skive Fjord. Chemical-biological parameters measured in the fjord during a 10 year period: A) 1996–97, B) 1998–99, C) 2000–2001, D) 2002–2003, E) 2004–05. Panels, from top and downwards: 1) oxygen and total phosphate concentration in bottom water, 2) nitrate/nitrite and ammonium concentration (bottom water), 3) primary production, 4) chl a concentration in surface and bottom water, 5) biomass of zooplankton.
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Fig. 3 (continued ).
during 5 cruises in Skive Fjord in the period February to August (Hansson et al., 2005; Møller and Riisgård, in press). From February to October in the years 2004 and 2005, LCA made weekly sampling of jellyfish in Skive Fjord in order to supplement our studies in the fjord (Møller and Riisgård, in press).
In September of every year, the Danish Institute for Fisheries Research trawls for fish in Limfjorden. The percentage of trawls that could not be made due to overloading of the fishing nets by A. aurita has recently been worked out for the period 1984 to 2004 (Hoffmann, 2005). Skive Fjord is one of the localities where the
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Fig. 3 (continued ).
highest biomass of A. aurita is found in Limfjorden (Hansson et al., 2005). As a useful, although indirect expression for the biomass of A. aurita in Skive Fjord, we have adopted an index (‘Hoffmann-index’) which expresses the percentage of standard monitoring trawls for fish that was not completed due to overloading of the fishing gear by jellyfish (Hoffmann, 2005).
3. Results 3.1. Oxygen depletion and chemical–biological cascade events A simplified graphic presentation of the yearly chemical–biological cascade events in Skive Fjord is
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Fig. 3 (continued ).
depicted in Fig. 2. High concentrations of nitrate accumulated during winter (due to run-off from the agriculture and pig farming dominated catchment area) is gradually used up by the phytoplankton in spring → algal biomass → sedimentation → oxygen demand of sediment. During summer when the water column is
stratified and re-aeration of the bottom water by windmixing is effectively prevented, the oxygen concentration gradually decreases and oxygen depletion occurs when the oxygen consumption at the bottom due to zoobenthic respiration and microbial decomposition exceeds the oxygen supply. This eventually results in
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Fig. 3 (continued ).
release of large amounts of phosphate and ammonium from the anoxic sediment. The release of nutrients now stimulates the primary production, resulting in an increase in the algal biomass which is subsequently, after a certain time lag period, grazed down by an
increasing number of zooplankton organisms (if they have not been eaten by jellyfish, see later). The measured chemical and biological parameters generally followed the above simplified presentation (Fig. 3A–E). The concentrations of oxygen in Skive
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Fig. 4. Skive Fjord. (A) “Hoffmann-index”, (B) Mean (+ or − standard deviation, n = 7) chl a concentration (surface and bottom water), (C) Mean biomass of Mytilus edulis (4 to 5 m, and 6 m depth) in September during the period 1996 to 2005. Standard deviation indicated (n = 5 for mussels on 4 to 5 m; n = 2 for mussels on 6 m).
Fjord in 1996 to 2005 showed that oxygen deficiency occurred every summer, although the degree and duration period with of lack of oxygen differed among years. Due to oxygen depletion in the near-bottom water, large amounts of nutrients (phosphate and ammonia) were usually released from the anoxic sediment, subsequently causing a peak in the primary production and chl a concentration. This phenomenon with oxygen depletion and phytoplankton bloom appeared more or less pronounced every year over the 10-year study period, and generally, the surface chl a concentrations were very high during periods with exceptionally severe oxygen depletion, and in some years peak concentrations as high as 60 to 80 μg chl a l− 1 were measured in Skive Fjord.
3.2. Jellyfish and zooplankton dynamics The Hoffmann-index suggested that the abundance of A. aurita medusae was low in Skive Fjord in the Table 1 Mytilus edulis Depth (m)
Biomass (g wet wt m− 2)
Years 0–2 2–4 4–6 6–7
2003 3974 1347 18 0
2004 2962 2148 445 366
2005 2569 2284 748 938
Area-specific biomass (wet weight, incl. shells) of mussels at different depths in Skive Fjord in September in 2003 to 2005.
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Fig. 5. Skive Fjord. Salinity profiles in autumn 2004.
period 1996 to 1998, after which their abundance increased to a maximum in 2003 before rapidly decreasing again (Fig. 4A). This pattern is supported by other more direct quantitative measurements as almost no A. aurita were observed in the springs of 1996 to 1998, whereas an increase in abundance was recorded in the spring of 1999 (Bio/consult, 2001), and further, mass occurrence of A. aurita took place during the summer of 2003 (Hansson et al., 2005; Møller and Riisgård, in press). In the early spring of both 2004 and 2005, A. aurita ephyrae were present in Skive Fjord, but they disappeared in April/May, and almost no A. aurita were present during the rest of the summer in either 2004 or 2005 (Møller and Riisgård, in press). In 2003, A. aurita had the potential to control the zooplankton from mid May to August in Skive Fjord
(half-life times between 0.8 and 6.2 d) (Hansson et al., 2005; Møller and Riisgård, in press). In agreement with this, almost no zooplankton was present in this period (Fig. 3D). A. aurita medusae were not present in Skive Fjord during the summer of 2004 and 2005 and the concentration of zooplankton was considerably higher (Møller and Riisgård, in press). Besides of these direct predation effects of A. aurita, available data also indicate some indirect effects. Thus in 2003, release of phytoplankton from zooplankton-grazing control due to zooplankton predation by A. aurita resulted in a pronounced phytoplankton bloom (with up to 60 μg chl a in the surface water) triggered by the release of nutrients from the sediment during a period with oxygen depletion (Fig. 3D). Similar algal blooms were not observed in 2004 and 2005 when no A. aurita were present, and
Fig. 6. Skive Fjord. Salinity and oxygen profiles in 2003 (11 August), 2004 (18 August), and 2005 (18 July).
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although the primary production was equally high (Fig. 3). This is in agreement with the observation that very high chl a concentrations in the surface water only occurred in years with high densities of A. aurita and
reduced grazing impact by zooplankton, whereas the chl a concentration in years with few A. aurita was relatively low (10 to 20 μg l− 1) due to a pronounced zooplankton-grazing impact. The large variation in the
Fig. 7. Skive Fjord. Density-driven volume flow (m− 3 s− 1) of surface and bottom water during early spring of 2003, 2004 and 2005. Positive values indicate flow of usually lighter (less saline) surface water out of the fjord; negative values indicate inflow of usually high-density saline bottom water.
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mass occurrence of jellyfish in Skive Fjord may be explained by irregular hydrographical incidents where incoming North Sea water replaces the old water and thus at the same time partly or completely (as seen in 2004 and 2005) wash the jellyfish out of the fjord (see later).
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feeding behaviour and a diet not including copepods (Riisgård, 2007). Thus, infrequent intrusions of large volumes of high-salinity seawater from the North Sea, may radically change the hydrographic situation and thereby strongly influence the chemical–biological cascade events as well as the distribution and abundance of jellyfish in Skive Fjord.
3.3. Oxygen depletion and mussels 4. Discussion The biomass of mussels (M. edulis) recorded in Skive Fjord in September seems to be inversely correlated with both the abundance of A. aurita and the nearbottom chl a concentration (Fig. 4). The highest biomass of mussels were found in 1998, 2004, and 2005, but due to severe oxygen depletion in 1999 and 2001 to 2003, almost no mussels were found at water depths below 4 m. In the years 2003 to 2005 M. edulis thrived well at depths down to 4 m, but below 4 m it was seriously affected by oxygen depletion (Table 1), the extent of which was strongly correlated with the salinity stratification that prevented mixing of oxygen down to the bottom 13(Fig. 5). The area-specific population filtration rate of M. edulis was calculated to be Fpop = 0.2 m3 m− 2 d− 1 at 4 to 5 m depth in September of 2003 and Fpop = 6 m3 m− 2 d− 1 at 4 to 7 m in September of 2004. The thickness of the water layer below the halocline was about 2 m at 5 m depth (Fig. 5). Therefore, assuming full mixing in this layer, the estimated phytoplankton halflife times were 7 and 0.2 d in 2003 and 2004, respectively. The systematically lower chl a concentrations in the near-bottom water (Fig. 4B) may thus be explained by the grazing impact of mussels. 3.4. Hydrography and jellyfish The mean salinity in Skive Fjord is about 25 psu and the salinity at the bottom it is usually a few psu higher than at the surface (Fig. 5). Occasionally, persistent, strong westerly winds push high saline North Sea water into the fjord-system through the Thyborøn Kanal, which may cause large variations in the vertical salinity profiles, as seen in August–September 2004 in Skive Fjord (Fig. 6). Here, the vertical variations in salinity are generally caused by the interplay between input of light freshwater from the catchment area and near-bottom inflow of high-density saline water. In early spring of both 2004 and 2005, dramatic changes in the salinity vertical profiles and subsequent density-driven water exchange (Fig. 7) coincided with the disappearance of A. aurita (Møller and Riisgård, in press) and the introduction of a new species of jellyfish in the fjord, the hydromedusa, Aequorea vitrina, which has a different
Comparable effects of A. aurita as reported here for Skive Fjord has previously been suggested by Schneider and Behrends (1998) who observed a linear correlation between chl a (in upper 10 m water column) and A. aurita abundance in Kiel Bight in the period 1990 to 1994. Likewise, a tendency of algal blooms related to high abundances of jellyfish was noticed by Huntley and Hobson (1978) who suggested that a second “spring” bloom in a Canadian fjord was due to reduced herbivore grazing caused by a high zooplankton-predation impact exerted by medusae (Phialidium gregarium). Further, in Gullmar Fjord (Sweden) heavy phytoplankton blooms occurred in 1978 and 1981 during spring and autumn and coincidently low zooplankton and high scyphomedusae abundances were observed. This lead to increased sedimentation of organic matter and oxygen deficiency occurred in absence of adequate water exchange (Lindahl and Hernroth, 1983). Similar cascading effects have been demonstrated for predation by the ctenophore, Mnemiopsis leidyi, on zooplankton in the Black Sea and in Chesapeake Bay (e.g. Oguz, 2005; Purcell and Decker, 2005). By examining 19 years of monitoring data from Skive Fjord, Møhlenberg et al. (2007) found that high biomass of blue mussels cause reduced chl a and increased transparency (Secchi depth), while short-term variability in water-column mixing cause changes in chl a due to nutrient entrainment and coupling to benthic mussels. The present work moderates the above statement by specifically suggesting that variations in near-bottom water chl a may be explained by grazing mussels (Fig. 4B) (see also Dolmer, 2000a,b; Nielsen and Maar, 2007) whereas variations of chl a in the surface water are more likely to be due to the grazing impact of zooplankton, which may be controlled by jellyfish in certain years. It is well known that the first effects of oxygendepleted bottom water in Limfjorden are likely to appear in the dense mussel beds where the rate of oxygen uptake may be 10 times higher than on the surrounding bottom (Jørgensen, 1980). This explains why the stagnant water below a stable halocline can be rapidly
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depleted of oxygen (Fig. 5) and eventually kills the mussels when toxic H2S produced in the anoxic sediment penetrates up into the bottom water (Table 1). The present work has demonstrated the strength of long and thorough time series of traditional environmental monitoring parameters (oxygen, nutrients, chl a, phytoand zooplankton), but it also emphasizes that available data on the abundance of jellyfish is unsystematically collected, although of obvious importance for correct interpretation of the often conspicuous variations in the traditional environmental parameters. Clearly, knowledge about the zooplankton-predatory impact exerted by jellyfish may explain otherwise unaccountable large variations in both zoo- and phytoplankton biomasses. Such insight, along with knowledge about the grazing impact of filter-feeding zoobenthos, is of great importance, not only for a basic understanding of the plankton dynamics in fjords and coastal ecosystems, but also for marine monitoring programmes that routinely use traditional chemical–biological parameters as the only tools in assessment of the environmental conditions. The present case study provides a framework for future experimentally oriented environmental studies based on a holistic ecological approach. Acknowledgements Thanks are due to the Limfjord County Authorities (Limfjordsamterne) for excellent co-operation, especially J. Gross, J. Deding, G. Pedersen, and B. Jensen for supplying data. Unpublished data on jellyfish were kindly supplied by E. Hoffmann. Critical comments and constructive suggestions made by J. E. Purcell and an anonymous referee are highly appreciated. [SS] References Arai, M.N., 2001. Pelagic coelenterates and eutrophication: a review. Hydrobiologia 451, 69–87. Asmus, R., Asmus, H., 1991. Mussel beds: limiting or promoting phytoplankton? J. Exp. Mar. Biol. Ecol. 148, 215–232. Behrends, G., Schneider, G., 1995. Impact of Aurelia aurita medusae (Cnidaria, Schyphozoa) on the standing stock and community composition of mezozooplankton in the Kiel Bight (western Baltic Sea). Mar. Ecol. Prog. Ser. 127, 39–45. Bio/consult, 2001. Fiskelarver og gopler i Limfjorden, foråret 1996–1999. Report in Danish Produced for Limfjordssamarbejdet. v/Nordjyllandsamt, Ålborg, Denmark. Conley, D.J., Kaas, H., Møhlenberg, F., Rasmussen, B., Windolf, J., 2000. Characteristics of Danish estuaries. Estuaries 23, 820–837. Diaz, R.J., 2001. Overview of hypoxia around the world. J. Environ. Qual. 30, 275–281. Dolmer, P., 2000a. Algal concentration profiles above mussel beds. J. Sea Res. 43, 113–119.
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