Directory UMM :Data Elmu:jurnal:J-a:Journal of Experimental Marine Biology and Ecology:Vol241.Issue2.Aug1999:

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L

Journal of Experimental Marine Biology and Ecology, 241 (1999) 193–205

The role of terrestrial humic substances on the shift of kelp

community to crustose coralline algae community of the

southern Hokkaido Island in the Japan Sea

a ,_* b c

Katsuhiko Matsunaga , Tomohiro Kawaguchi , Yoshihiro Suzuki ,

Goro Nigi

Department of Chemistry, Faculty of Fisheries, Hokkaido University, Hakodate 041-8611, Japan

Department of Environmental Health Sciences, School of Public Health, University of South Carolina,

Charleston, SC 29208, USA

Department of Civil and Environmental Engineering, Faculty of Engineering, Miyazaki University,

Miyazaki889-2192, Japan

Received 21 October 1998; received in revised form 8 April 1999; accepted 25 May 1999

Abstract

Crustose coralline algae dominates coastal rocky shores (crust-dominated community) in certain world coastal zones after the disappearance of kelp forest community. Local fisheries suffer greatly when this occurs. Well known ecological hypothese to explain this phenomenon such as sea urchin excessive grazing and anomalously high temperature events do not satisfactorily explain the shift in algal composition in the Japan Sea coast. Previously we have shown that coralline algae has a competitive edge over other algae under the extremely low iron levels associated with deforestation in the Japan Sea along the coast of the southern Hokkaido Island. In the present study we present direct evidence that forest-derived humic substances inhibit crustose coralline algal spore germination and also promote macroalgal oogonium formation. Our results strongly suggest that suburban development associated with deforestation in the Japan Sea coast watershed reduced the flux of humic substances into coastal water and in turn created an environment in which coralline algae dominate over other algae.  1999 Elsevier Science B.V. All rights reserved.

Keywords: Carbon isotope; Crustose coralline algae; Humic substances; Kelp forest; Macroalgal oogonium; Zoospore

*Corresponding author. Tel. / fax:181-138-40-8805.

E-mail address: [email protected] (K. Matsunaga)

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1. Introduction

In certain coastal areas of the northeastern and western United States (Mann, 1977; Pearse and Hines, 1987; Coyer et al., 1993), Canada (Watanabe and Harrold, 1991), Norway (Hagen, 1983), New Zealand (Creese, 1988), Australia (Shepherd and Turner, 1985), South America (Santelices and Ojeda, 1984), Africa (Lieberman et al., 1984) and Japan (Noro et al., 1983), changes in algal community composition have been reported in which crustose coralline algae gradually have dominated over kelp forest communities (i.e. crust-dominated community (Coyer et al., 1993). This shift in community structure has resulted in reduced production by fishes, abalones, and sea urchins dependent on the kelp habitat for food, shelter, and spawning (Mann, 1973; Nabata et al., 1992; Sanbonsuga, 1996; Kawai, 1997). This transformation has caused serious social problems and is particularly well-documented in northern Japan, specifically the Japan Sea coast of the southern part of Hokkaido Island (Nabata et al., 1992; Sanbonsuga, 1996; Kawai, 1997) (Fig. 1). Well-known ecological paradigms to explain the cause of this shift in algal composition include the ‘keystone species theory’ (Estes and Harrold, 1988), i.e. sea urchin’s excessive grazing on kelp due to the decrease of predatory pressure, and the ‘cyclic succession theory’ (Harrold and Reed, 1985), i.e. hydrographic events such as anomalously high temperatures initiate the shift from a kelp-dominated area to crust-dominated area. However, a case for the southern Hokkaido Island in Japan Sea provides a new twist for the cause of this phenomenon.

Four decades ago, this area was dominated by kelp forests that extended at depth 0–20 m, 1 km seaward. In the1930s, crustose coralline algae (Lithophyllum spp.) started to cover this area. Since the1960s the area has been completely covered by coralline algae, with no sign of kelp forest recovery (Kawai, 1997; Noro et al., 1983; Nabata et al., 1992) (shaded area of the Japan Sea coast in Fig. 1). The southern Hokkaido Island coast neighboring the Japan Sea waters where kelp are lacking is marked by the development of roads and small agricultural areas (Matsunaga, 1993). Due to this coastal development, many streams feeding into the coastal waters have been eliminated and / or blocked by concrete impervious surfaces (Matsunaga, 1993). Occasionally, thick kelp forests are observed among crust-dominated communities in areas influenced by riverine inputs, which drain the forested and agricultural areas (Kawai, 1997; Kuwahara et al., 1997) (B–D in Fig. 1). In contrast to the Japan Sea coast, the Pacific Ocean coast of the southern Hokkaido Island is characterized by many forested coastal streams (150–200 m apart) feeding into coastal waters that contain a rich kelp forest community (Laminaria japonica, Laminaria religiosa and Undaria pinnatifida) (E and F in Fig. 1). Hypotheses which have been applied to explain the shift in algal community structure off Hokkaido Island and other coastal areas include the possibilities that excessive sea urchin grazing of kelp (Fujita, 1997) or changes in hydrological conditions (e.g. increased water temperature, especially in February and March which is a critical time for macroalgal reproduction and growth) have initiated this transformation (‘cyclic succession theory’) (Iizumi, 1997; Taniguchi, 1997). Although sea urchin (Strongylocentrous nudus and Strongylocentrous intermedius) catch in the Japan Sea coast off Hokkaido Island have declined considerably since 1960 due to commercial over harvesting, the kelp population has not recovered and continuously decreased

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Fig. 1. Sampling locations of the southern Hokkaido Island, Japan. Each station is located 50–100 m off, except for B, depth 3–5 m. Crust-dominated community (A), kelp forest community (B–F). (B, rocky shore) is located 1 km off. Tsushima warm current flows through both sides of the southern Hokkaido Island. (Light shaded area): crust-dominated community; (dark shaded area): kelp forest community.

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(JMAF, 1960–1984) (Fig. 2). Also, within recent years the sea urchin population density

(.100 individuals m ) in the Pacific Ocean is much higher than that (3–20

individuals m ) in the crust dominated area of the Japan Sea coast (unpublished data).

Fig. 2. Relationship between commercial harvesting of sea urchins (Strongylocentrotus nudus and

Strongylocentrotus intermedius) and kelp (Laminaria sp.) production in Japan Sea coast and Pacific Ocean

coast during 1960–1984. Source: Annual Record of Fishery and Aquaculture (JMAF, 1960–1984). Sea urchins were over harvested at the Japan Sea coast due to the development of freezing technology for transportation since 1960. Commercial harvesting of sea urchin shows a slight increase from 1984 at the Japan Sea coast due to the aquaculture efforts in the scattered kelp forest communities (B–D in Fig. 1) in the crust-dominated community (A in Fig. 1). Therefore, data was not shown after 1984. In contrast, kelp community and sea urchins have maintained the population balance in Pacific Ocean coast in contrast to the Japan Sea coast. (s) Sea urchin; (d) Laminaria spp.

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Therefore, excessive sea urchin grazing of kelp may partially explain the cause of the decline of kelp forests, yet does not explain why kelp communities do not recover despite the few number of sea urchins in the coast of Japan Sea. Also, temperature increases cannot fully explain this phenomenon because the Tsushima warm current flows along both sides of this island, and historical data show that the temperature has stayed nearly constant, between 10 and 138C, in the Japan Sea coast (JMA, 1941–1984) (Fig. 3). Low water temperature (5–108C) in late winter to early spring is reported to be critical for the macroalgal reproductive success (i.e. gametophytes growth and oogonium formation) (Kihara, 1997). Anomalously high temperatures in February and March, in which gametophytes or oogoniums of L. japonica grow, in the Japan Sea along the coast of the southern Hokkaido Island have not been recorded in the past three decades (JMA, 1941–1984) (Fig. 3). Thus, neither hypothesis satisfactorily explains the shift in algal composition in the Japan Sea coast.

The appearance of kelp forests in the crust-dominated community (Kawai, 1997; Kuwahara et al., 1997) in the Japan Sea where riverine influence prevails (B–D in Fig. 1) led us to believe that chemical elements in the river water may be responsible for the kelp forest predominance and inhibition of the growth of coralline algae. We have previously shown that reduced iron levels associated with deforestation due to the suburban development play an important role in the decline of brown macroalgal populations and the subsequent replacement by coralline algae in this area (Suzuki et al., 1995). Supporting evidence includes the following: (1) iron levels in those crust-dominated community in the Japan Sea coast were extremely low (,1 nM) compared

Fig. 3. Water temperature trend in the Japan Sea along the coast of the southern Hokkaido Island during 1941–1984. Source: Annual Record of monthly mean water temperature and density in the coastal zone (JMA, 1941–1984).

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to those in the Pacific Ocean coast (Suzuki et al., 1995) although coastal waters in both coasts had similar major nutrient (e.g. phosphate, nitrate) concentrations; (2) the coralline algae grew well at low iron levels found in Japan Sea coast (Suzuki et al., 1995); (3) iron bioavailability under sufficient major nutrient (e.g. phosphate, nitrate) condition plays an important role to promote oogonium formation, growth rate and pigment synthesis of the kelp (Suzuki et al., 1994); (4) organically-complexed iron in forested stream and river water promoted far more microalgal growth than iron oxides which are predominantly found in the Japan Sea coastal water (Matsunaga et al., 1998); (5) iron enrichment by placing iron frames in crust-dominated community stimulated macroalgal growth (Matsunaga et al., 1994). Interestingly, however, three years after the placement of iron frames, coralline algal growth recovered and replaced macroalgal growth on the frames (unpublished observation). This suggested that reduced iron bio-availability may not be the only factor involved in the selection of crustose coralline alga over kelp growth.

We hypothesized that, besides decreasing the potential for organic iron complexation, the reduction of humic substances associated with deforestation had another direct effect leading to the selection of crustose coralline alga over kelp communities. That is, forest-or river-derived humic compounds may act as inhibitforest-ors of crustose cforest-oralline algal spforest-ore germination. In this paper, the effects of humic substances on the tetraspore growth of crustose coralline algae and macroalga were investigated.

2. Materials and methods

2.1. Effect of humic substances on the tetraspores growth of crustose coralline algae (Lithophyllum spp.)

Humic soils was extracted with 0.1 N NaOH, centrifuged, and pH adjusted to 2. After centrifugation, pH of the supernatant was adjusted to 7 with 0.1 N NaOH, and the supernatant was filtered through a 0.45-mm HA filter membrane. Filtrate and precipitated humic acid (after dissolving in NaOH and neutralizing) were used for the culture experiments. Triplicate tissue culture flasks containing 30 ml of filtered seawater (34 p.s.u.) were prepared for the experiment. Tetraspores were obtained from mature coralline alga, Lithophyllum spp. collected at the coastal region in the northern Japan Sea, in August and September, 1993. Tetraspores were adhered onto a glass plate (2.532.5 cm) in filtered seawater (0.45 mm). Number of tetraspores on the plate was counted by a light microscopy (initial number: N0¯100). The tetraspores on the plate

were immediately transferred to 30 ml of medium. The test media were prepared by the addition of 100ml of each fulvic and humic acid to make a final concentration of 2 and 1

mg l , respectively, to filtered seawater containing nitrate (500mM) and phosphate(5

mM). The culture experiment of tetraspores was carried out under the following

22 21

conditions; 80mE cm s , 12-h light / dark cycle and 108C. After 10 days, the number of germinate alga (grown with doubling cell) was counted (survival number: N ). Thet

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the following equations: R5 (%)5N /Nt 03100 and Normality (%)5(each survival ratio / mean survival ratio)3100. Error bar shows S.D. (n55).

The culture experiment of the spores with and without 5 mg l of fulvic acid or humic acid was also carried out. After 3 or 10 days, the photographs of the spores in both media were taken by a light microscope. The range of humic or fulvic acid used for this experiment was decided by their ambient concentration measured in the study sites. The concentration of aggregated humic substances in surface seawater at the four river

mouths (10–300 m off the coast) was found to be a range between 1–10 mg C l by a fluorescence spectrophotometric method mentioned below. The fluorescence spectrum of humic substances used for these experiments matched the fluorescence spectrum of organic substances from Pacific Ocean and Japan Sea coasts with riverine influence. 2.2. Effect of different iron species on oogonium formation of Laminaria religiosa

Zoospores were obtained from mature sporophytes of Laminaria religiosa which were harvested at a coastal region in the northern Japan Sea, Hokkaido, in November 1996. The zoospores were adhered onto glass plates (2.532.5 cm) in 30 ml of the sterilized filtrate (0.45mm) sea water. The number of zoospores (male and female) on each plate was about 150 cells. The iron enrichment media were prepared by the addition of

amorphous Fe, fulvic acid–Fe (the concentration was adjusted to 1 mg C l ), and nitrate and phosphate. The final concentrations of iron, nitrate and phosphate were 0.2

mM, 500 and 30mM in all media, respectively. Filtered (0.45 mm), autoclaved natural sea water (,10 nM Fe, 500mM nitrate, and 30mM phosphate) was used for the control.

22 21

After 10 days cultivation under the following conditions (108C; 40mE m s ; 12-h light / dark cycle), the number of female gametophytes of L. religiosa on the glass plates was counted by an optical microscope. The percentages of oogonium formation after 25, 30 and 35 culture days were calculated by the following equation:

Oogonium formation rate

5(Number of oogoniums at 25, 30 and 35 days / Number of female gametophytes at 10 days)3100

2.3. Organic substances flux measurement at the Japan Sea and the Pacific Ocean

coast andd C in the organic substances

Organic substances were captured with a sediment trap (8Ø350 cm) which was settled at 2-m depth from the sea surface for 2–4 h at the four stations (A–D in Fig. 1) at the Japan Sea side and two locations (E and F in Fig. 1) at the Pacific Ocean coast during summer 1996–1998, water depth was 5 m, 50–100 m away from the land. Water in the sediment trap was filtered through a 0.45-mm GF / F filter to collect organic matter. Collected organic matter was dissolved in 10 ml of 0.1 N NaOH for 5 h, followed by neutralization with HCl total organic carbon was analyzed by a total organic carbon analyzer. The fluorescence spectrum of isolated organic matter was analyzed by a fluorescence spectrophotometer.

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Isotope ratios in the organic matter collected in 1998 were also measured by a Finnigan Mat Delta plus mass spectrometer, and expressed in per millilitre deviations from a standard as defined by the following equation:

d C5(Rsample/Rstandard21)31000

13 12

where R means C / C and Peedee belemnite (PDB) was used as a standard. The standard deviation was60.2‰.

3. Results and discussion

As Berner et al. (1978) showed that humic substances can inhibit inorganic precipitation of calcium carbonate, we demonstrated that fulvic and humic acids isolated from forest soils inhibited germination of crustose coralline algal spores (Fig. 4). Fulvic

acid completely destroyed tetraspores of Lithophyllum spp. at 5 mg C l after 3 days incubation (Fig. 5). This concentration is similar to ambient levels measured in the Pacific Ocean coast of Hokkaido Island. In contrast, the forest-derived fulvic acid–iron complex found in the Pacific Ocean coast promoted the highest formation rate (79%) of macroalgal oogonium compared to other forms of iron (41%) (e.g. less bioavailable ferric oxides) that are predominantly found in the Japan Sea coast (Fig. 6).

Comparisons of ambient dissolved organic substance composition on two sides of the

Fig. 4. Effect of humic substances on the tetraspores growth of crustose coralline algae (Lithophyllum spp.). FA, fulvic acid; HA, humic acid.

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Fig. 5. Effect of humic substances on Lithophyllum spp. Tetraspores of Lithophyllum spp. were destroyed at 5

mg C l of isolated humic substances and fulvic acid (3 days). (A) Humic substances (after 3 days), (B) fulvic acid (after 3 days), and (C) control (10 days). After 3 days, the color of spores turned from pink to black and the spores started to be destroyed. At 10 days, all spores were destroyed completely.

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Fig. 6. Effect of different iron species on oogonium formation of Laminaria religiosa. Fulvic–iron complex promoted the best oogonium formation rate (79%) of L. religiosa at 35 days compared to amorphous Fe (41%) and control (3%) (n52).

southern Hokkaido Island further supported the effect of terrestrial humic substance on coastal ecosystem. Field surveys indicate that the organic substance flux in coastal water with riverine influence on both sides of Hokkaido Island is much higher (25–83 mg C

22 21 22 21

m h ) than that in the crust-dominated Japan Sea coast (1 mg C m h ) (Table 1). Also, organic substances collected from Pacific Ocean and Japan Sea coasts with riverine influence were found to have originated from forest-derived humic substances, and the fluorescence spectrum of organic substances in these waters matched the pattern of fulvic acids from terrestrial origin (Fig. 7). In contrast, the fluorescence spectrum of organic substances from the crust-dominated Japan Sea resembled that from phyto-plankton exudates, and not fulvic acid (Fig. 7).

The isotope ratio collected in C, D and F in 1998 was 226.160.4‰ (n53) which corresponds to the ratio in the aggregated organic matter (suspended matter) in the river

Table 1

Organic substances flux measurement at the Japan Sea coast and the Pacific Ocean coast (n51)

Japan Sea coast Pacific Ocean coast

22 21 22 21

Location mg C m h Location mg C m h

A 1 E 29

B 83 F 42

C 25

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Fig. 7. Fluorescence spectra of organic substances (2 mg l as carbon) collected by the sediment traps at various sampling locations (The emission wavelength is 460 nm). (A) Pattern of organic substances collected at stations B–F in Fig. 1 (kelp forest community) matched the patterns of fulvic acid and humic acid. (B) Pattern of organic substances collected at station A in Fig. 1 (crust-dominated community) matched the patterns of phytoplankton, Chaetoceros spp. and kelp, Laminaria spp. Both dashed lines show the trap samples.

mouths at about 10 p.s.u. salinity (226.060.3‰, n59). The ratio in mountain soil was

226.460.4 (n56). The ratios collected in E and A were 225.260.6 (n53) and

221.060.5 (n52), respectively. The former means that the organic matter collected in the traps contained small amounts of phytoplankton. The latter was close to the ratio (220.860.5, n510) in phytoplankton collected in both the Japan Sea and Pacific Ocean sides. These compositional difference are consistent with the predominant influence of terrestrially-derived humic substances in the Pacific Ocean coastal waters, but a

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negligible influence in the crust-dominated community in the southern Hokkaido of Japan Sea waters. Forested watershed changes associated with coastal development are reported to significantly alter the quality, quantity, and timing of organic substances in streams draining into coastal water by increasing impervious surfaces (Wahl et al., 1996). Therefore, evidence is strong that selection for crustose coralline algae is related to the reduction in the supply of forest derived humic substances. It is apparent that the replacement of kelp community by crustose coralline algal communities in the southern Hokkaido Island in the Japan Sea is linked to deforestation associated suburban coastal development.

4. Conclusion

With increasing riverine and coastal water degradation by human activity worldwide (Dynesius and Nilsson, 1994; Nixon, 1995), this finding has significant global implications for coastal management, in that humic substances of terrestrial origin play highly significant roles in maintaining the integrity of the coastal ecosystem (McKnight, 1991; Kawaguchi et al., 1997).

Acknowledgements

We would like to thank Drs. Norimitsu Watabe and Alan J. Lewitus for their valuable suggestions.

References

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Creese, R.G., 1988. Ecology of molluscan grazers and their interactions with marine algae in northern-eastern New Zealand: a review. NZ J. Mar. Freshwat. Res. 22, 427–444.

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JMAF, 1960–1984. Annual Record of Fishery and Aquaculture (1960–1984, Japanese Minister of Agriculture and Forestry.

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Kihara, S., 1997. Relationship between kelp (Laminaria sp.) and water temperature. In: The mechanism of crust-dominated community and the development of its forecasts, Jpn. Agric. Fish. Tech. Assoc, pp. 16–33. Kuwahara, H., Akaike, S., Hayashi, H., Yamashita, T., 1997. Investigation on the growth factors for macroalgal

community in the Isoyake area. Coast. Eng. Ser. 44, 1181–1185.

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200 K. Matsunaga et al. / J. Exp. Mar. Biol. Ecol. 241 (1999) 193 –205

Isotope ratios in the organic matter collected in 1998 were also measured by a

Finnigan Mat Delta plus mass spectrometer, and expressed in per millilitre deviations

from a standard as defined by the following equation:

d

C

5 (R

sample

/R

standard

2 1)

3 1000

13 12

where R means

C / C and Peedee belemnite (PDB) was used as a standard. The

standard deviation was

6 0.2‰.

3. Results and discussion

As Berner et al. (1978) showed that humic substances can inhibit inorganic

precipitation of calcium carbonate, we demonstrated that fulvic and humic acids isolated

from forest soils inhibited germination of crustose coralline algal spores (Fig. 4). Fulvic

acid completely destroyed tetraspores of Lithophyllum spp. at 5 mg C l

after 3 days

incubation (Fig. 5). This concentration is similar to ambient levels measured in the

Pacific Ocean coast of Hokkaido Island. In contrast, the forest-derived fulvic acid–iron

complex found in the Pacific Ocean coast promoted the highest formation rate (79%) of

macroalgal oogonium compared to other forms of iron (41%) (e.g. less bioavailable

ferric oxides) that are predominantly found in the Japan Sea coast (Fig. 6).

Comparisons of ambient dissolved organic substance composition on two sides of the

Fig. 4. Effect of humic substances on the tetraspores growth of crustose coralline algae (Lithophyllum spp.). FA, fulvic acid; HA, humic acid.

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Fig. 5. Effect of humic substances on Lithophyllum spp. Tetraspores of Lithophyllum spp. were destroyed at 5 21

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202 K. Matsunaga et al. / J. Exp. Mar. Biol. Ecol. 241 (1999) 193 –205

southern Hokkaido Island further supported the effect of terrestrial humic substance on

coastal ecosystem. Field surveys indicate that the organic substance flux in coastal water

with riverine influence on both sides of Hokkaido Island is much higher (25–83 mg C

22 21 22 21

m

h

) than that in the crust-dominated Japan Sea coast (1 mg C m

h

) (Table 1).

Also, organic substances collected from Pacific Ocean and Japan Sea coasts with

riverine influence were found to have originated from forest-derived humic substances,

and the fluorescence spectrum of organic substances in these waters matched the pattern

of fulvic acids from terrestrial origin (Fig. 7). In contrast, the fluorescence spectrum of

organic substances from the crust-dominated Japan Sea resembled that from

phyto-plankton exudates, and not fulvic acid (Fig. 7).

The isotope ratio collected in C, D and F in 1998 was

2

26.1

6 0.4‰ (n

5 3) which

corresponds to the ratio in the aggregated organic matter (suspended matter) in the river

Table 1

Organic substances flux measurement at the Japan Sea coast and the Pacific Ocean coast (n51)

Japan Sea coast Pacific Ocean coast

22 21 22 21

Location mg C m h Location mg C m h

A 1 E 29

B 83 F 42

C 25

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mouths at about 10 p.s.u. salinity (

2

26.0

6 0.3‰, n

5 9). The ratio in mountain soil was

2

26.4

6 0.4 (n

5 6). The ratios collected in E and A were

2

25.2

6 0.6 (n

5 3) and

2

21.0

6 0.5 (n

5 2), respectively. The former means that the organic matter collected in

the traps contained small amounts of phytoplankton. The latter was close to the ratio

(

2

20.8

6 0.5, n

5 10) in phytoplankton collected in both the Japan Sea and Pacific Ocean

sides. These compositional difference are consistent with the predominant influence of

terrestrially-derived humic substances in the Pacific Ocean coastal waters, but a

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204 K. Matsunaga et al. / J. Exp. Mar. Biol. Ecol. 241 (1999) 193 –205

negligible influence in the crust-dominated community in the southern Hokkaido of

Japan Sea waters. Forested watershed changes associated with coastal development are

reported to significantly alter the quality, quantity, and timing of organic substances in

streams draining into coastal water by increasing impervious surfaces (Wahl et al.,

1996). Therefore, evidence is strong that selection for crustose coralline algae is related

to the reduction in the supply of forest derived humic substances. It is apparent that the

replacement of kelp community by crustose coralline algal communities in the southern

Hokkaido Island in the Japan Sea is linked to deforestation associated suburban coastal

development.

4. Conclusion

With increasing riverine and coastal water degradation by human activity worldwide

(Dynesius and Nilsson, 1994; Nixon, 1995), this finding has significant global

implications for coastal management, in that humic substances of terrestrial origin play

highly significant roles in maintaining the integrity of the coastal ecosystem (McKnight,

1991; Kawaguchi et al., 1997).

Acknowledgements

We would like to thank Drs. Norimitsu Watabe and Alan J. Lewitus for their valuable

suggestions.

References