Current status and ecological roles of Zostera marina after recovery from large-scale reclamation in the Nakdong River estuary, Korea

Estuarine, Coastal and Shelf Science 81 (2009) 38–48

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Current status and ecological roles of Zostera marina after recovery from large-scale reclamation in the Nakdong River estuary, Korea Sang Rul Park a, Jong-Hyeob Kim a, Chang-Keun Kang a, Soonmo An b, Ik Kyo Chung b, Jeong Ha Kim c, Kun-Seop Lee a, * a b c

Department of Biology, Pusan National University, Pusan 609-735, Republic of Korea Department of Marine Science, Pusan National University, Pusan 609-735, Republic of Korea Department of Biological Sciences, Sungkyunkwan University, Suwon 440-746, Republic of Korea

a r t i c l e i n f o

a b s t r a c t

Article history: Received 6 May 2008 Accepted 16 October 2008 Available online 1 November 2008

Large Zostera marina meadows (covering 13.6 km2) existed in the Nakdong River estuary on the south coast of Korea until the mid-1980s, but these Z. marina beds nearly disappeared due to reclamation of adjacent mud flats for the construction of a port and industrial complex during the late 1980s. Partial recovery of Z. marina meadows occurred recently, and Z. marina coverage of about 0.3 km2 was observed in this estuary. In this study, shoot morphology, density, biomass, productivity, and tissue nutrient content were measured to evaluate the current status of the Z. marina meadows by comparing these data to those for persistent seagrass meadows in similar geographical areas. Additionally, we examined the ecological roles of Z. marina in this estuary after recovery from the large-scale disturbance. Shoot density (151 shoots m2) and total biomass (141 g DW m2) in the estuary were similar to those reported from other Z. marina meadows in Korea. Annual leaf production (1726 g DW m2 y1) was higher than generally observed for Z. marina in other geographical areas. These results imply that the existing Z. marina meadows in this estuary have adjusted to local environmental conditions that changed after large-scale reclamation. Estimated annual whole plant carbon (C) and nitrogen (N) incorporations based on shoot production and tissue C and N content were 810.0 g C m2 y1 and 59.7 g N m2 y1, respectively. These values were equivalent to 2.4  105 kg C y1 and 1.8  104 kg N y1 for all Z. marina beds in the Nakdong River estuary. This high C and N incorporation into Z. marina tissues suggests that existing Z. marina meadows play important roles in C and N cycles in this estuary. Although the currently existing Z. marina beds in this estuary are persisting and play an important ecological role, anthropogenic factors that cause seagrass declines still affect the estuary. Thus, effective management and monitoring of Z. marina beds and environmental factors are critical to protecting and conserving this invaluable component of the Nakdong River estuary. Ó 2008 Elsevier Ltd. All rights reserved.

Keywords: growth reclamation seagrass recovery current status Nakdong River estuary

1. Introduction Estuaries have high biodiversity and primary production due to their highly variable habitat types and environmental conditions (Day et al., 1989). Estuaries also play a pivotal role as nursery habitats for various commercial fishes and invertebrates, and act as nutrient and sediment sinks (Lirman et al., 2008). However, many estuarine ecosystems have been destroyed by coastal development; consequently, submerged aquatic vegetation has seriously declined (Lotze et al., 2006). The Nakdong River estuary, which has been protected by law since the 1960s, is a representative estuary in Korea, with 32 species of vascular hydrophytes, including four

* Corresponding author. E-mail address: [email protected] (K.-S. Lee). 0272-7714/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2008.10.003

seagrass species (Kim et al., 2005). This estuary is of great value as seaweed and shellfish grounds and is a critical stopover site for migratory birds because of its location in the center of the East Asia–Australia flyway (Kim et al., 2005). Before disturbance, meadows of Zostera marina, which is a dominant primary producer in this estuary, occupied about 13.6 km2 (Chung and Choi, 1985). However, large-scale reclamation for an industrial complex, dam construction, and port development during the late 1980s resulted in the disappearance of these large Z. marina meadows from this estuary (Kim et al., 2005). Worldwide, disturbance of seagrass habitats because of dredging or filling has increased since the 1980s (Short and Wyllie-Echeverria, 1996). Dredging decreases water clarity by increasing water turbidity, levels of total suspended solids, and algal blooms, and consequently leads to seagrass declines (Cambridge et al., 1986; Goldsborough and Kemp, 1988; Onuf, 1994).

S.R. Park et al. / Estuarine, Coastal and Shelf Science 81 (2009) 38–48

Recently, Z. marina meadows have partially recovered and small meadows have been observed in the Nakdong River estuary. Although the biomass and coverage of currently existing Z. marina beds is dramatically lower than those in 1985 (Fig. 1; Table 1), the existing meadows seem persistent and have adjusted to the changed environmental conditions. The health of seagrasses is evaluated based on shoot morphology, productivity, density, and biomass (Pergent et al., 1995; Buia et al., 2004; Terrados et al., 2008). Gaeckle et al. (2006) estimated eelgrass leaf productivity by measuring sheath length and found a significant relationship between shoot morphology and plant metabolic status. Shoot density, biomass, and productivity of seagrass meadows have been compared with those of persistent meadows in similar geographical areas to assess the status of seagrass meadows (Agostini et al., 2003; Terrados et al., 2008). Seagrass meadows are among the most productive plant communities, providing food and habitats for commercially and ecologically valuable marine organisms (Holmquist et al., 1989; Montague and Ley, 1993). Because of low direct grazing pressure from herbivores, a substantial fraction of seagrass carbon enters coastal and estuarine food webs through microbial transformation of litter and particulate detritus (Duarte and Cebria´n, 1996; Cebrı´an and Duarte, 2001). Thus, organic matter produced by seagrasses is important for supporting commercial fishery production in coastal and estuarine ecosystems (Melville and Connolly, 2005). Because seagrasses have high productivity, they require high nutrient incorporation and play an important role in nutrient cycling in coastal and estuarine ecosystems (Hemminga et al., 1991; Blackburn et al., 1994). In addition, seagrasses can take up inorganic nutrients through both leaf and root tissues (Stapel et al., 1996; Pedersen et al., 1997; Lee and Dunton, 1999). Nutrient uptake through leaf tissues from the water column significantly

39

contributes to total nutrient acquisition (Lee and Dunton, 1999). Thus, seagrasses in estuarine areas might reduce levels of overenriched nutrients caused by anthropogenic loading and consequently reduce cultural eutrophication in estuarine ecosystems. In the present study, we hypothesized that the existing Z. marina beds, which partially recovered from large-scale reclamation, are persisting and play significant ecological roles in this estuary. The current status and the ecological roles of the Z. marina meadows in this estuary were evaluated based on the measurements of plant growths and nutrient uptakes by Z. marina shoots. 2. Materials and methods 2.1. Study area The study site was located in the Nakdong River estuary on the southern coast of Korea (Fig. 1). This study was conducted in a typical Z. marina meadow of the estuary at an average water depth of about 1.5 m relative to the mean sea level. This estuary has a well-developed delta and is protected by sand dunes that parallel the coastline. Commercial shellfish (mainly oysters) are cultured intensively in the vicinity of seagrass beds. The estuary has undergone significant changes in environmental conditions since the construction of a river dam in 1987. A large area of mudflat (15.5 km2) was reclaimed during the late 1980s. This estuarine area is highly dynamic, and thus many sand bars and barrier islands were newly created. Annual precipitation is about 1500 mm, with about 50% of the precipitation occurring during the summer monsoon season (Kim et al., 2005). Large freshwater inflow is associated with the summer monsoon and typhoons. The tidal regime is semi-diurnal and the system is classified as mesotidal, with a maximum tidal range of about 2.0 m during spring tides. The

Fig. 1. Study site in the Nakong River estuary, Korea, before (1985; A) and after (2005; B) large-scale reclamation.

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Table 1 Zostera marina. Distributional area, density, and biomass in May–June 1985 and May 2005 in the Nakdong River estuary. Data for 1985 were adapted from Chung and Choi (1985). Values represent Mean  SD. 1985

2005

Eelgrass coverage (km2) Total density (shoots m2)

13.6 175  46

0.3 179  11

Biomass (g DW m2) Total Above-ground Below-ground

546  288 436  250 104  64

126  14 88  20 37  8

eelgrass, Z. marina, meadows were mapped in the field with Global Positioning Systems (OziExplorer program). 2.2. Physical parameters Water temperature was measured using a YSI 85 multiparameter field meter (YSI Inc., Yellow Springs, OH, USA) once or twice a month from September 2004 to November 2004, and was then monitored using StowAway TidbitÒ temperature data loggers (Onset Computer Corp., Bourne, MA, USA) every 15 min until February 2006. Underwater irradiance at the seagrass canopy level was monitored using HOBOÒ light intensity data loggers (Onset Computer Corp.) enclosed in clear submersible polycarbonate cases every 15 min from January 2005 to March 2006. The underwater sensors were cleaned regularly to minimize fouling. Light intensity (lumens ft2) measured using the HOBO data loggers was converted to photon flux density (PFD; mmol photon m2 s1) by concurrent quantum measurements using an LI-1400 data logger and an LI-193SA spherical quantum sensor (LI-COR, Lincoln, NE, USA). A regression analysis was performed to convert the light intensity measured using the HOBO data logger to PFD. HOBO measurements and PFD exhibited a relatively strong correlation (r2 ¼ 0.84). Daily PFD (mol m2 d1) was calculated as the sum of quantum flux over each 24-h period. Salinity was measured monthly at the water surface using the Practical Salinity Scale with the YSI 85 from September 2004 to February 2006. 2.3. Water column and sediment nutrient concentrations To determine water column inorganic nutrient concentrations   3 (NHþ 4 , NO3 þ NO2 , and PO4 ), four replicate surface water samples were collected monthly from September 2004 to February 2006.  The NO 3 þ NO2 concentration was determined after running the sample through a column containing copper-coated cadmium,  which reduces NO 3 to NO2 . Sediment pore water nutrient concentrations were measured monthly from six replicate sediment samples. Samples were collected randomly to a sediment depth of about 13 cm with a syringe corer and were then frozen pending lab analyses. Sediment pore water was obtained by centrifugation (5000g for 15 min) and then diluted with low nutrient seawater (<0.1 mM) for determination of pore water dis  3 solved inorganic nitrogen (NHþ 4 and NO3 þ NO2 ) and PO4 concentrations. Water column and sediment pore water nutrient analyses were determined using standard colorimetric techniques following the methods of Parsons et al. (1984). 2.4. Biological measurements Shoot morphology, density, and biomass were measured monthly from September 2004 to February 2006. To measure shoot morphological characteristics, 10–15 mature terminal shoots were collected individually at the sampling site. Sheath length was measured from the meristem to the top of the sheath. Shoot height

was measured from the meristem to the tip of the longest leaf, to the nearest 1.0 mm. Width of the longest leaf was measured to the nearest 0.1 mm. Above- and below-ground tissues inside a haphazardly thrown quadrat (0.35  0.35 m; n ¼ 4–6) were collected for shoot density and biomass measurements. Shoot density was determined by counting all shoots within a quadrat and the measurements were converted to per unit area (shoots m2). Collected tissues were thoroughly cleaned of epiphytes and sediment, separated into above- (blade þ sheath) and below-ground tissues (root þ rhizome), and dried at 60  C to constant weight. Samples were weighed and biomass was converted to per unit area estimates (g DW m2). Above- and below-ground productivities were estimated using the plastochrone method (Jacobs, 1979; Short and Duarte, 2001). Ten to 15 randomly chosen shoots were marked through the sheath bundle about 4 cm above the meristem using a hypodermic needle. After an elapsed time of 4–5 weeks, the marked shoots were harvested and rinsed in fresh water. Plastochrone intervals were calculated by dividing the marking period (days) by the number of new leaves produced after marking. The dry weights of the youngest mature leaf, which was usually the third leaf, and the rhizome/ root segments from the first to sixth youngest nodes were measured every sampling time. Above-ground and below-ground productivities of each shoot were calculated using the following equations: Above-ground productivity (mg DW shoot1 d1) ¼ dry weight of a mature leaf (mg shoot1)/plastochrone interval (d) Below-ground productivity (mg DW shoot1 d1) ¼ dry weight of a mature rhizome/root segment (mg shoot1)/plastochrone interval (d) Areal production (g DW m2 d1) was obtained by multiplying shoot production rates by the average shoot density. 2.5. Carbon and nitrogen incorporation To determine tissue carbon (C) and nitrogen (N) content, six mature terminal shoots were collected individually at each sampling date. The second and third youngest leaves and belowground tissues from the first to sixth youngest nodes were used to determine tissue C and N content. Dried tissues were ground using a mortar and pestle, and approximately 2–3 mg of ground tissues were placed in a tin boat for determination of tissue C and N content using a CHN elemental analyzer (Flash EA1112; CE Instruments, Hindley Green, UK). Carbon and N incorporations into Z. marina tissues were estimated from productivity and the C and N content of above- and below-ground tissues. Nutrient incorporation was defined as the amount of C and N allocated to newly produced tissues and was calculated using the following equation: C (or N) incorporation ¼ above- or below-ground productivity  tissue C (or N) content/100. Total C and N incorporation by the Z. marina beds in the entire estuary was estimated by multiplying C and N incorporation by total distributional area. 2.6. Statistical analyses All statistical analyses were performed using SPSS (version 12.0). Data were tested for normality and homogeneity of variance to meet the assumptions of parametric statistics. If these assumptions were not satisfied, data were log transformed. Significant differences in environmental and biological parameters among sampling times were analyzed using a one-way analysis of variance (ANOVA). Statistical significance was set at the alpha < 0.05 level. When significant differences among sampling times were observed, the means were examined using the Student–Newman–Keuls (SNK)

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test to determine where statistically significant differences among means occurred. Correlation analyses were used to examine relationships between biological parameters and environmental factors. 3. Results 3.1. Physical and chemical parameters Water temperature showed a strong seasonal pattern, ranging from 5.1  C in February to 26.9  C in August (Fig. 2A). Average daily underwater irradiance exhibited significant (p < 0.001) temporal variation (Fig. 2B). Underwater irradiance was highest in February 2005 (25.0 mol photons m2 d1) and lowest in July 2005 (1.7 mol photons m2 d1). Salinity was relatively constant (ca. 30) throughout the experimental period, except during late summer when it decreased to 20 as a result of increased precipitation (Fig. 2C). The water column NHþ 4 concentration ranged from 1.4 to 16.2 mM, but did not exhibit a clear seasonal trend (Fig. 3A). The

Water temperature (°C)

30

A

25 20 15 10 5 0 A S O N D J F M A M J J A S O N D J F M

Underwater irradiance (mol photons m-2 d-1)

30

B

25 20 15 10 5 0 A S O N D J F M A M J J A S O N D J F M 40

C

Salinity

30

20

41

NHþ 4 concentration in the water column was usually about 5 mM,  except in July and August 2005. The NO 3 þ NO2 concentration in the water column fluctuated greatly, but did not exhibit a clear  seasonal trend (Fig. 3B). The average NO 3 þ NO2 concentration over the experimental period was 10.4 mM. The water column PO3 4 concentration exhibited a clear seasonal trend (p < 0.001), increasing during fall and decreasing during spring (Fig. 3C). The sediment pore water NHþ 4 concentration ranged from 39.8 mM in November 2004 to 167.7 mM in April 2005 (Fig. 3D). The average sediment pore water NHþ 4 concentration was  98.1 mM. The sediment NO 3 þ NO2 concentration was significantly (p < 0.001) higher during winter and spring than during  summer and fall (Fig. 3E). The mean NO 3 þ NO2 concentration in sediment pore water was about 2.5 mM. The sediment PO3 4 concentration, however, was significantly (p < 0.001) higher during summer and fall than during winter and spring (Fig. 3F). 3.2. Biological measurements Shoot density was highest (269 shoots m2) in June 2005 and lowest (71 shoots m2) in late August 2004 (Fig. 4A). Total biomass showed significant seasonal differences (p < 0.001), ranging from 59 g DW m2 d1 in February 2005 to 384 g DW m2 d1 in June 2005 (Fig. 4B). Above- and below-ground biomass also showed strong seasonal variation (Fig. 4B). Above- and below-ground biomass were highest in summer (259 and 125 g DW m2, respectively) and lowest in winter (41 and 14 g DW m2, respectively). The average above- and below-ground biomass were 96 and 45 g DW m2, respectively. Individual plant part and total productivities exhibited clear seasonal variation, increasing during spring and decreasing during late summer (Fig. 4C). Total, above- and below-ground productivities per shoot were highest (81, 66, and 15 mg DW shoot1 d1, respectively) in June 2005 and lowest (8, 5, and 3 mg DW shoot1 d1, respectively) in early February 2005. The seasonal change in total productivity per shoot was closely correlated with that in above-ground productivity. The seasonal pattern of areal productivity was similar to that of productivity per shoot (Fig. 4D). Above-ground productivity per unit area ranged from 0.7 g DW m2 d1 in February 2005 to 14.0 g DW m2 d1 in July 2005, while below-ground productivity per unit area ranged from 0.3 g DW m2 d1 in February 2005 to 3.1 g DW m2 d1 in July 2005 (Fig. 4D). Total productivity per unit area was highest (17.1 g DW m2 d1) in June 2005 and lowest (1.0 g DW m2 d1) in early February 2005 (Fig. 4D). Annual Z. marina production in 2005 was 2153 g DW m2 y1. Above-ground production accounted for about 80% of total production. Shoot height showed clear seasonal variation; shoots were tallest (167.0 cm) in May 2005 and shortest (40.9 cm) in February (Fig. 5A). Sheath length also varied seasonally, increasing during spring and decreasing during late summer (Fig. 5B). Annual average sheath length was 20.6 cm. Leaf blades were widest during spring and summer, and narrowest during fall (Fig. 5C). Leaf blade width ranged from 8.6 to 11.8 mm, with a mean of 10.0 mm. 3.3. Tissue C and N content and incorporation

10

0 A S O N D J F M A M J J A S O N D J F M

2004

2005

2006

Fig. 2. Water temperature (A), average daily underwater photon flux density (PFD) at the eelgrass canopy level (B), and salinity (C) at the study site in the Nakdong River estuary from September 2004 to March 2006.

Leaf C content varied significantly with sampling time (p < 0.001), but exhibited no obvious seasonal pattern (Fig. 6A). Leaf C content ranged from 35.0 to 38.8%, averaging 36.5%. However, the N content and C:N ratio of leaf tissues exhibited clear seasonal variations (Fig. 6B, C). Leaf N content was highest during winter and lowest during summer, whereas the leaf C:N ratio was highest during late summer and lowest during winter.

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Sediment pore water

Water column

NH4+ (µM)

20

200

A

15

150

10

100

5

50

0

0 A S O N D J F M A M J J A S O N D J F

25

NO3- + NO2- (µM)

A S O N D J F M A M J J A S O N D J F 8

B

20

E

6

15 4 10 2

5

0

0 A S O N D J F M A M J J A S O N D J F

3

PO43- (µM)

D

A S O N D J F M A M J J A S O N D J F 30

C

2

20

1

10

0

F

0 A S O N D J F M A M J J A S O N D J F

2004

2005 NHþ 4

 NO 3 þ NO2

2006 PO3 4

A S O N D J F M A M J J A S O N D J F

2004

Fig. 3. Seasonal changes in water column (A), (B), and (C) concentrations, and sediment pore water the Nakdong River estuary from September 2004 to February 2006. Values represent mean  SE (n ¼ 4–6).

The average leaf N content and C:N ratio were 2.76% and 16.8, respectively. In contrast to leaf C content, the C content of below-ground tissues showed clear seasonal variation, increasing during spring and summer and decreasing during fall and winter (Fig. 6D). Average below-ground tissue C content was 37.8%. The N content of below-ground tissues also exhibited clear seasonal variation, ranging from 1.3% in December 2004 to 3.7% in August 2005 (Fig. 6E). The C:N ratio of below-ground tissues was highest (30.9) in December 2004 and lowest (13.2) in August 2005, with an average of 20.3 (Fig. 6F). Daily and monthly C and N incorporations into plant tissues were highest in summer and lowest in winter (Fig. 7). Carbon incorporation into above-ground tissues ranged from 9.7 g C m2 month1 in February and 145.4 g C m2 month1 in June, whereas carbon incorporation into below-ground tissues ranged from 4.1 g C m2 month1

2005 NHþ 4

(D),

 NO 3 þ NO2

2006 (E), and PO3 4 (F) concentrations in

in February to 36.3 g C m2 month1 in June (Fig. 7C). Carbon incorporation into leaf tissues accounted for about 78% of the total C incorporation. The calculated annual C incorporation into the whole plant was 810.0 g C m2 y1 (Fig. 7C). Nitrogen incorporation into above- and below-ground tissues was lowest (0.9 and 0.2 g N m2 month1, respectively) in January and highest (10.4 and 2.9 g N m2 month1, respectively) in June (Fig. 7D). Nitrogen incorporation into above-ground tissues was four-fold higher than that into below-ground tissues. The calculated annual N incorporation into the whole plant was 59.7 g N m2 y1 (Fig. 7D). 3.4. Relationships between environmental factors and eelgrass growth Water temperature was significantly correlated with total biomass and leaf productivity (Table 2). Underwater irradiance and

300

200

A

240

Shoot height (cm)

Total shoot density (shoots m-2)

S.R. Park et al. / Estuarine, Coastal and Shelf Science 81 (2009) 38–48

180 120 60

A S O N D J F M A M J

50

40 Total Above-ground Below-ground

Sheath length (cm)

Biomass (g DW m-2)

100

A S O N D J F M A M J

200

100

A S O N D J F M A M J

B

30

20

A S O N D J F M A M J

J A S O N D J F 14

C Leaf width (mm)

80 60 40

J A S O N D J F

C

12

10

20 8

0 A S O N D J F M A M J

J A S O N D J F

A S O N D J F M A M J

2004 Areal productivity (g DW m-2 d-1)

J A S O N D J F

10

0

Productivity (mg DW sht-1 d-1)

150

J A S O N D J F

B

300

100

A

0

0

400

43

20

D

J A S O N D J F

2005

2006

Fig. 5. Zostera marina. Seasonal variations in shoot height (A), sheath length (B), and blade width (C) from September 2004 to February 2006 in the Nakdong River estuary. Values represent mean  SE (n ¼ 10–15).

15

4. Discussion

10

4.1. The current status of Z. marina meadows 5

0 A S O N D J F M A M J

2004

J A S O N D J F

2005

2006

Fig. 4. Zostera marina. Seasonal variations in total shoot density (A), biomass (B), productivity per shoot (C), and areal productivity (D) in the Nakdong River estuary from September 2004 to February 2006. Values represent mean  SE.

salinity were not significantly correlated with eelgrass growth  (Table 2). The water column NO 3 þ NO2 concentration was negatively correlated with total biomass and the sediment PO3 4 concentration was positively correlated with leaf productivity (Table 2). Shoot height and density were not significantly correlated with any environmental factors (Table 2).

Zostera marina beds in the Nakdong River estuary were almost completely eliminated due to anthropogenic activities, mainly reclamation and dam construction, during the last 20 years (Kim et al., 2005). However, many small Z. marina beds have been observed in the estuary recently. Recovery of seagrass beds following destruction by anthropogenic disturbances has been reported in many geographical areas (Frederiksen et al., 2004; Orth et al., 2006). Shoot density of existing beds in this estuary ranged from 71 to 269 shoots m2, with an average of 151 shoots m2. These densities are similar to those reported for persistent Z. marina meadows in Korea, which range from 16 to 276 shoots m2 (Kim and Choi, 2004; Lee et al., 2005; Kaldy and Lee, 2007). Biomass at the study site was also similar to that reported from Z. marina beds in Korea and other areas (Robertson and Mann, 1984; Pedersen and Borum, 1993; Duarte et al., 2002; Kim and Choi, 2004; Lee et al., 2005; Kaldy and Lee, 2007). The maximum seasonal biomass of above- and

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Leaf

C content (%)

44

Rhizome 44

A

42

42

40

40

38

38

36

36

34

34

32

32

30

30 A S O N D J F M A M J J A S O N D J F

N content (%)

5

A S O N D J F M A M J J A S O N D J F 5

B

4

4

3

3

2

2

1

E

1 A S O N D J F M A M J J A S O N D J F

25

D

A S O N D J F M A M J J A S O N D J F 35

C

F

30

C:N ratio

20 25

20 15 15

10

10 A S O N D J F M A M J J A S O N D J F

2004

2005

2006

A S O N D J F M A M J J A S O N D J F

2004

2005

2006

Fig. 6. Zostera marina. Seasonal variations in carbon (A) and nitrogen (B) content and the C:N ratio (C) of above-ground tissues, and carbon (D) and nitrogen (E) content and C:N ratios (F) of below-ground tissues in the Nakdong River estuary from September 2004 to February 2006. Values represent mean  SE (n ¼ 4–6).

below-ground tissues in the existing Z. marina beds in this estuary was 259.1 and 124.8 g DW m2, respectively, whereas the average maximum seasonal biomass of Z. marina beds worldwide was 298.4 g DW m2 and 149.7 g DW m2, respectively (Duarte and Chiscano, 1999). Additionally, the below-ground biomass at the study site was much higher than values reported for other Z. marina meadows in Korea (Kim and Choi, 2004; Lee et al., 2005; Kaldy and Lee, 2007). These results imply that the existing Z. marina in the Nakdong River estuary have adjusted to local environmental conditions that were altered by large-scale reclamation. The shoot morphology of existing plants in the Nakdong River estuary was similar to that previously reported from persistent Z. marina meadows in Korea (Kim and Choi, 2004; Lee et al., 2005). Annual leaf production of Z. marina in the Nakong River estuary was 1726 g DW m2 y1, which is two to five times higher than that of other Z. marina meadows in Korea (Lee et al., 2005; Kaldy and Lee,

2007). Additionally, annual leaf production in this estuary was usually higher than that reported from other areas (Table 3). Thus, the existing Z. marina meadows in the Nakdong River estuary are probably healthy and will persist. In the present study, seasonal patterns of biomass and productivity reflected seasonal changes in water temperature (Table 2). Biomass and productivity increased during spring and early summer and decreased during fall and winter. This seasonal pattern is identical to that observed for other Z. marina meadows in Korea (Kim and Choi, 2004; Lee et al., 2005; Kaldy and Lee, 2007). Therefore, seasonal Z. marina growth in this estuary might also be controlled by water temperature, as in other Z. marina beds in Korea. However, Z. marina growth in this estuary was not significantly correlated with underwater irradiance (Table 2). Light saturation at 100–200 mmol photons m2 s1 has been reported for photosynthesis of Z. marina (Dennison, 1987). Daily maximum

Daily C incorporation (g C m-2 d-1)

S.R. Park et al. / Estuarine, Coastal and Shelf Science 81 (2009) 38–48

6

Table 2 Correlations between environmental variables and eelgrass growth in the Nakdong River estuary. All parameters were subjected to a 1-month lag. Values in each cell, from top to bottom, are the correlation coefficient, P value, and sample size for each correlation. Cells in bold were statistically significant (p < 0.05).

A

5

Below-ground Above-ground

4

Shoot height

Shoot density

Total biomass

Leaf productivity

Areal leaf productivity

Water temperature

0.383 0.129 17

0.279 0.314 15

0.587 0.045 12

0.681 0.005 15

0.500 0.05 15

Underwater irradiance

0.392 0.185 13

0.247 0.464 11

0.447 0.195 10

0.494 0.122 11

0.353 0.288 11

Salinity

0.095 0.718 17

0.176 0.547 14

0.180 0.575 12

0.032 0.913 14

0.019 0.950 14

Water column NHþ 4

0.260 0.330 16

0.092 0.765 13

0.478 0.137 11

0.493 0.087 13

0.518 0.070 13

Water column  NO 3 þ NO2

0.219 0.415 16

0.016 0.960 13

0.646 0.032 11

0.537 0.058 13

0.390 0.188 13

Water column PO3 4

0.192 0.477 16

0.539 0.057 13

0.480 0.135 11

0.166 0.588 13

0.434 0.138 13

Sediment NHþ 4

0.212 0.430 16

0.180 0.557 13

0.357 0.281 11

0.112 0.715 13

0.237 0.435 13

Sediment  NO 3 þ NO2

0.166 0.539 16

0.313 0.297 13

0.003 0.994 11

0.210 0.490 13

0.028 0.927 13

Sediment PO3 4

0.312 0.240 16

0.019 0.950 13

0.479 0.136 11

0.701 0.008 13

0.586 0.035 13

3 2 1 0 A S O N D J F M A M J J A S O N D J F

Daily N incorporation (g N m-2 d-1)

0.4

B

0.3

0.2

0.1

0.0 A S O N D J F M A M J J A S O N D J F

2004

2006

Below-ground Above-ground

150

600 100 400 50

200 0

0 J 15

Monthly N incorporation (g N m-2 mo-1)

800

Annual C incorporation (g C m-2 y-1)

1000

C

F M A M J

J

A S O N D

Annaul 80

D

12

60

9 40 6 20

3

Annual N incorporation (g N m-2 y-1)

Monthly C incorporation (g C m-2 mo-1)

200

2005

0

0 J

F M A M J

J

A S O N D

45

Annaul

2005 Fig. 7. Daily, monthly, and annual estimate of carbon (A, C) and nitrogen (B, D) incorporation into above- and below-ground tissues of Zostera marina in the Nakdong River estuary, Korea.

underwater PFD at the study site was usually much higher than the light saturation point of Z. marina. Thus, underwater irradiance at the study site was probably sufficient for persistent Z. marina growth in this estuary. 4.2. Ecological roles of Z. marina in the Nakdong River estuary Seagrass communities support rich and diverse populations of both autotrophic and heterotrophic organisms by providing habitat, protection, and food (Holmquist et al., 1989; Montague and

Ley, 1993). Production of economically important finfish and shellfish is significantly associated with seagrasses (Heck et al., 1995; Kwak and Klumpp, 2004). Vizzini et al. (2002) demonstrated using stable isotope analysis that seagrass plays a critical role as a food source for secondary consumers. Based on Hoshika et al. (2006), the carbon isotope ratios of primary and secondary consumers in seagrass meadows reflect those of the seagrass and its epiphytes. Zostera marina in the present study area produced 810.0 g C m2 of new organic material annually, equivalent to production of 2.4  105 kg C y1 for all the Z. marina beds in the Nakdong River estuary. Organic C production in all the Z. marina beds in this estuary is higher than that in Funakoshi Bay, Japan (9.5  104 kg C y1 in 0.5 km2 of Zostera caulescens beds; Nakaoka et al., 2003) and Yaquina Bay, OR, USA (1.8  105 kg C y1 in 1 km2 of Z. marina beds; Kaldy, 2006), which have similar seagrass coverage. Because of their high productivity, seagrasses require high nutrient incorporation and play an important role in nutrient cycling of shallow estuarine ecosystems (Hemminga et al., 1991; Blackburn et al., 1994). In addition, remineralization of dissolved organic matter released from seagrass detritus is a major source of water column inorganic nutrients, and thus influences nutrient cycling in the overlying water column (Ziegler and Benner, 1999). In this study, total N acquisition by Z. marina shoots was 59.7 g N m2 y1. Therefore, all the Z. marina beds in the Nakdong River estuary should incorporate 1.8  104 kg of N annually. The large amount of N incorporated by the Z. marina beds in this estuary suggests that Z. marina beds play an important role in the N cycle in this estuary. In addition, because seagrasses take up large amounts of N and phosphorus, and contain high levels of nutrients in their tissues, they act as a bio-sink for nutrients in coastal and estuarine ecosystems (Duarte and Cebria´n, 1996). The high level of nutrient

46

S.R. Park et al. / Estuarine, Coastal and Shelf Science 81 (2009) 38–48

Table 3 Above- and below-ground productivities of Zostera marina at various geographical locations. Location

Latitude

Time period Method

Tissue

Productivity

Source

mg DW shoot1 d1 g DW m2 d1 g DW m2 y1 Limfjorden, Denmark

56 N

Seasonal

Biomass change

Above-ground

654–995

Limfjorden, Denmark

56 N

Seasonal

Rhizome tagging Below-ground

177–326

Øresund, Denmark

55 N

Seasonal

Leaf marking

Above-ground

937

Øresund, Denmark

55 N

Seasonal

Rhizome marking Below-ground

313

Øresund, Denmark



55 N

Seasonal

Short method

Above-ground

1576

Øresund, Denmark

55 N

Seasonal

Short method

Below-ground

812

Vellerup Vig, Denmark Vellerup Vig, Denmark

55 N 55 N

Apr.–Oct. Apr.–Oct.

Above-ground Below-ground

2.3–7.9 1.27

856 241

Zandkreek, The Netherlands

51450 N

Seasonal

Short method Plastochrone method Short method

Above-ground

1.7–3.6a

303a

Zandkreek, The Netherlands

51450 N

Seasonal

Below-ground

0.2–2.2a

132a

Veerse Meer, The Netherlands

51450 N

Seasonal

Above-ground

4.8–5.1a

412a

Veerse Meer, The Netherlands

51450 N

Seasonal

Below-ground

0.3–1.8a

119a

Grevelingen, The Netherlands

51450 N

Seasonal

Above-ground

1.3–1.7a

160a

Grevelingen, The Netherlands

51450 N

Seasonal

Grevelingen, The Netherlands

51450 N

Seasonal

Grevelingen, The Netherlands

51450 N

Seasonal

Lake Grevelingen, The Netherlands

51 N

Lake Grevelingen, The Netherlands

Olesen and Sand-Jensen (1994) Olesen and Sand-Jensen (1994) Wium-Anderson and Borum (1980) Wium-Anderson and Borum (1980) Pedersen and Borum (1993) Pedersen and Borum (1993) Sand-Jensen (1975) Sand-Jensen (1975)

Below-ground

0.5–0.8a

111a

Feb.–Oct.

Plastochrone method Biomass change

Above-ground

1.2–12.9a

478.9a

51 N

Feb.–Oct.

Biomass change

Below-ground

0.9–1.9a

82.7a

Roscoff, France

48 440 N

Seasonal

Above-ground

1116

Roscoff, France

48 440 N

Seasonal

Below-ground

492

Jacobs (1979)

Chezzetcook Inlet, Nova Scotia, USA

44 410 N

Seasonal

Chezzetcook Inlet, Nova Scotia, USA

44 410 N

Mar.–Aug.

Plastochrone method Plastochrone method Plastochrone method Plastochrone method Leaf marking

Van Lent and Verschuure (1994) Van Lent and Verschuure (1994) Van Lent and Verschuure (1994) Van Lent and Verschuure (1994) Van Lent and Verschuure (1994) Van Lent and Verschuure (1994) Van Lent and Verschuure (1994) Van Lent and Verschuure (1994) Nienhuis and de Bree (1980) Nienhuis and de Bree (1980) Jacobs (1979)

Robertson and Mann (1984) Robertson and Mann (1984) Kaldy (2006), Kaldy and Lee (2007) Kaldy (2006) Cebrı´an et al. (1997)



0

Yaquina Bay, Oregon, USA

43 37 N

Seasonal

Yaquina Bay, Oregon, USA Cala Jonquet, Spain

Seasonal 43 370 N 42 18.260 N Seasonal

Cala Jonquet, Spain

42 18.260 N Seasonal

Plastochrone method Short method Plastochrone method Short method Plastochrone method Short method

53a

Below-ground Above-ground

2.6–3.2a

403a

Above-ground

1.46

534

Below-ground

0.24–2.47

395

Above-ground

0.5–3.5

353

Below-ground Above-ground

0.25–0.5

Above-ground

0.7–11.1

535  92

0.3–3.2

219

Ninigret Pond, Rhode Island, USA



41 N

Seasonal

Rhizome tagging Reconstruction technique Reconstruction technique Biomass change

Ninigret Pond, Rhode Island, USA

41 N

Seasonal

Biomass change

Below-ground

Jehu Pond, Waquoit Bay, MA, USA Jehu Pond, Waquoit Bay, MA, USA

41 N 41 N

Seasonal Seasonal

Above-ground 3.20  0.16 Below-ground 1.23

203  7 84

Hamblin Pond, Waquoit Bay, MA, USA 41 N Hamblin Pond, Waquoit Bay, MA, USA 41 N

Seasonal Seasonal

Above-ground 2.38  0.16 Below-ground 1.1

49  6 25

Hauxwell et al. (2003) Hauxwell et al. (2003)

Sage Lot Pond, Waquoit Bay, MA, USA 41 N Sage Lot Pond, Waquoit Bay, MA, USA 41 N

Seasonal Seasonal

Above-ground 3.51  0.22 Below-ground 1.12

395  29 120

Hauxwell et al. (2003) Hauxwell et al. (2003)

Timms Pond, Waquoit Bay, MA, USA Timms Pond, Waquoit Bay, MA, USA

41 N 41 N

Seasonal Seasonal

Above-ground 1.89  0.08 Below-ground 0.88

159  9 66

Hauxwell et al. (2003) Hauxwell et al. (2003)

Nakdong River estuary, Korea

35 N

Seasonal

Nakdong River estuary, Korea

35 N

Seasonal

Leaf marking Plastochrone method Leaf marking Plastochrone method Leaf marking Plastochrone method Leaf marking Plastochrone method Plastochrone method Plastochrone method

Thorne-Miller and Harlin (1984) Thorne-Miller and Harlin (1984) Hauxwell et al. (2003) Hauxwell et al. (2003)

a

Ash free dry weight.

1020.9

404.6  152.1 Cebrı´an et al. (1997)

Below-ground

Above-ground 5.04–66.76

0.67–14.02

1726

This study

Below-ground 2.89–14.62

0.34–3.07

427

This study

S.R. Park et al. / Estuarine, Coastal and Shelf Science 81 (2009) 38–48

incorporation by Z. marina beds in the Nakdong River estuary implies that Z. marina helps maintain and improve water quality in this estuary by removing nutrients from the water column. Unfortunately, Z. marina beds in this estuary are still exposed to anthropogenic disturbances that cause seagrass declines. Reclamation for port and industrial complex construction continues, consequently increasing water turbidity and water velocity, which results in seagrass loss. Commercial oyster culture can cause significant decreases in seagrass abundance because of the associated increase in sedimentation and direct physical disturbance during placement and harvest (Everett et al., 1995). In the present study area, oysters are being cultured extensively and many oyster cultivation areas overlap with Z. marina beds. Thus, commercial oyster cultivation may have a detrimental affect on the persistence of Z. marina in the Nakdong River estuary. There is also heavy boat traffic for fisheries, which can physically damage Z. marina beds. In conclusion, the coverage of Z. marina beds in the Nakdong River estuary significantly declined after large-scale reclamation during the late 1980s. However, Z. marina has partially recovered recently, and the currently existing beds are performing within the productivity range of other Z. marina meadows elsewhere in the world and to play important ecological roles in the estuary. However, many anthropogenic factors that can cause seagrass declines remain in the area. Thus, effective management and continuing long-term monitoring of Z. marina beds are necessary to protect and conserve this invaluable estuarine component.

Acknowledgments We thank J.I. Park, Y.K. Kim, T.H. Kim, W. Li, and S.H. Kim for field assistance and laboratory support. Two anonymous reviewers and an editor provided useful comments on earlier version of the manuscript. This work was supported by the Ministry of Environment (Eco-technopia 21 project #050010013) and the Ministry of Land, Transport and Maritime Affairs of Korea (Program of Greenhouse Gas Emissions Reduction Using Seaweeds).

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