Undaria pinnatifida Habitat Loss in Relation to Sea Urchin Grazing and Water Flow Conditions, and Their Restoration Effort in Ogatsu Bay, Japan

ABSTRACT This study investigated the mechanism of the loss of Undaria pinnatifida beds in Ogatsu Bay, Japan. Wave heights at the outside of the bay were 1 to 2 m over the course of study. In the outer areas of the bay with high water velocities, more than 14.5 ± 3.4 cm sec -1, U. pinnatifida grew densely and sea urchins were scarce. However, in some outer areas with lower velocities, less than 7.8 ± 2.3 cm sec -1, U. pinnatifida grew sparsely where the aggregation of sea urchin was found. In contrast, in the inner areas of the bay with calm water having velocities of 2.4 to 4.6 cm sec-1, the density of sea urchin was high and the U. pinnatifida beds disappeared. These results indicated high water velocities in the outer bay areas prevent the grazing by sea urchins. Disappearance of U. pinnatifida in the inner bay areas seemed to be caused by the high grazing pressure of sea urchins in calm water velocity conditions. We also performed a U. pinnatifida restoration effort to reduce the effects of the grazing pressure by sea urchins in the barren grounds in the inner areas of the bay. Artificial buoyed reefs were designed to prevent the migration of sea urchins by being detached from the bottom and allowed the recovery of U. pinnatifida and other non-encrusting macroalgae. Although there were some losses of transplanted U. pinnatifida partly caused by the withering after the reproductive maturation period, Saccharina japonica and other macroalgae were naturally recruited and increased due to the inhibition of migration by sea urchins using the buoyed reefs. In contrast, the formation of barren community remained at the area grounded to the bottom allowing the migration of urchin in the inner bay. Overall, our restoration efforts using the artificial buoyed reef, although not ideal, resulted in the success of the recovery of macrolagal habitats in the sea urchin - dominated barren grounds by the reduction of grazing pressure of sea urchins

Journal of Water and Environment Technology, Vol 7, No 3, 2009 Undaria pinnatifida Habitat Loss in Relation to Sea Urchin Grazing and Water Flow Conditions, and Their Restoration Effort in Ogatsu Bay, Japan Hitoshi TAMAKI*, Keisaku KUSAKA**, Minji FUKUDA***, Shogo ARAI**** and Daisuke MURAOKA***** * Ishinomaki Senshu University, Shinmito, Minamisakai, Ishinomaki, Miyagi, 986-8580, Japan ** Miyagi Prefectural Eastern Regional Promotion Office, 1-4-32, Higashinakasato, Ishinomaki, Miyagi, 986-0812, Japan *** Fukuda Ocean Research, Ltd, 166 Asahigaura, Watanoha, Ishinomaki, Miyagi, 986-2135, Japan **** Aqua Scape Research Co., Ltd, 622-1 Ushirodani, Takugi, Okinoshima, Oki, Shimane, 685-0106, Japan ***** Tohoku National Fisheries Research Institute, 3-27-5 Shinhama, Shiogama, Miyagi, 985-0001, Japan ABSTRACT This study investigated the mechanism of the loss of Undaria pinnatifida beds in Ogatsu Bay, Japan Wave heights at the outside of the bay were to m over the course of study In the outer areas of the bay with high water velocities, more than 14.5 ± 3.4 cm sec -1, U pinnatifida grew densely and sea urchins were scarce However, in some outer areas with lower velocities, less than 7.8 ± 2.3 cm sec -1, U pinnatifida grew sparsely where the aggregation of sea urchin was found In contrast, in the inner areas of the bay with calm water having velocities of 2.4 to 4.6 cm sec-1, the density of sea urchin was high and the U pinnatifida beds disappeared These results indicated high water velocities in the outer bay areas prevent the grazing by sea urchins Disappearance of U pinnatifida in the inner bay areas seemed to be caused by the high grazing pressure of sea urchins in calm water velocity conditions We also performed a U pinnatifida restoration effort to reduce the effects of the grazing pressure by sea urchins in the barren grounds in the inner areas of the bay Artificial buoyed reefs were designed to prevent the migration of sea urchins by being detached from the bottom and allowed the recovery of U pinnatifida and other non-encrusting macroalgae Although there were some losses of transplanted U pinnatifida partly caused by the withering after the reproductive maturation period, Saccharina japonica and other macroalgae were naturally recruited and increased due to the inhibition of migration by sea urchins using the buoyed reefs In contrast, the formation of barren community remained at the area grounded to the bottom allowing the migration of urchin in the inner bay Overall, our restoration efforts using the artificial buoyed reef, although not ideal, resulted in the success of the recovery of macrolagal habitats in the sea urchin - dominated barren grounds by the reduction of grazing pressure of sea urchins Keywords: sea urchin, Undaria pinnatifida, water velocity INTRDUCTION Undaria pinnatifida (Harvey) Suringar is an annual macroalga that grows in rocky coastal areas (Arasaki et al., 2002) Forests of U pinnatifida are highly productive components of estuaries and coastal ecosystems, and support diverse faunal assemblages (Ohno, 1996) They provide suitable habitats for many commercial fishes and benthic animals (Ohno, 1996; Takami et al., 2003; Tamaki et al., 2005) U pinnatifida is also a significant commercial marine food product in Japan (Akiyama et al., 1982; Ohno, 2004) Address correspondence to Hitoshi TAMAKI, Ishinomaki Senshu University, Email: thitoshi@isenshu-u.ac.jp Received 11 March 2009, Accepted 10 July 2009 - 201 - Journal of Water and Environment Technology, Vol 7, No 3, 2009 Subtidal marine macrophyte habitats around the world, including U pinnatifida, have declined due to human pollutants (Short et al., 1996; Tamaki et al., 2002), overgrazing by sea urchins (Alcoverro et al., 2002; Kawai et al., 2002; Terawaki et al., 2002) and herbivorous fishes (Nakayama et al., 2005; Tamaki et al., 2008), as well as natural disturbances (Ito, 2001) In Vestfjorden, Northern Norway, an outbreak of the green sea urchin Strongylocentrotus droebachiensis has resulted in the decrease of large kelp forests and has remained a barren community configuration dominated by crustose coralline algae (Hagen, 1995) Losses of kelp forests in Hokkaido, Japan, have been ascribed to the overgrazing pressure of sea urchin Strongylocentrotus nudus (Kawai et al., 2002) U pinnatifida had inhabited in the inner areas of Ogatsu Bay, Japan, but declined during the 1990s and resulted in the formation of barren grounds with the aggregations of sea urchin Strongylocentrotus nudus as the potential algal herbivores (Tamaki et al., 2005) However, there are many areas where U pinnatifida remains even with the high abundance of herbivorous sea urchin in the outer areas of the bay Here, we studied the biological and physical characteristics of these areas to elucidate factors responsible for the deterioration of U pinnatifida habitats in the inner areas of Ogatsu Bay, Japan We carried out a comparative study on the distribution of U pinnatifida and other macrophytes, bottom sediments, flow regime and density of sea urchin between the inner and outer areas of the Bay We also performed a U pinnatifida restoration effort to reduce the grazing pressure by sea urchins in the barren grounds in the inner areas of the bay MATERIALS AND METHODS Study site The study was carried out in the inner and outer areas of Ogatsu Bay, Pacific coast of northern Honshu, Japan, between September 2003 and August 2005 (Fig 1A) Both areas are characterized by rocky shore and the occurrence of U pinnatifida was confirmed until 1990s (Tamaki et al 2005) Inner area of the bay is protected from waves and currents, whereas the outer area is exposed to excessive levels of hydrodynamic energy We deployed 50 m × m belt transects in the outer area (Line 1, 38° 29’ 20.0” N; 140° 29’ 55.0” E) and the inner area (Line 2, 38° 30’ 07.6” N; 140° 29’ 34.3” E) of the bay Macrophyte communities at each line were confirmed to be representative vegetation in the outer or inner bay area by the previous field observations The distance between the two surveyed lines is approximately 1.5 km Composition of substratum, macrophyte flora and infauna The substratum of the bottom sediment, percentage covers of macroalgae and seagrass, and the population of infauna were quantified in the 50 m × m belt transects in the outer (Line 1) and inner (Line 2) bay areas by scuba divers in September 2003 and 2004 These belt transects were divided into six to nine surveyed sections classified by the differences in macrophyte compositions and the bottom sediments The percentage covers of macroalgae and seagrass were estimated following the method of Turner et al (2004) Bottom sediments were expressed as bedrock, isolated rock, boulder, cobble, pebble, sand and mud according to the size classification of Fujita et al (2003) - 202 - Journal of Water and Environment Technology, Vol 7, No 3, 2009 (A) (B) 141º 30’ E Mean Low Water Level 0.4 m Line Inner areas 38º 30’ N Miyagi Prefecture Artificial 2.5 m buoyed 2.5 m reef Outer areas rope Line Bottom Ogatsu Bay 1.5 m km Fig – (A) Location of the study area in Ogatsu Bay Macrophyte communities at each surveyed line were confirmed to be representative vegetation in the outer or inner bay area by the previous field observations ●: Two sets of artificial buoyed reefs were deployed to allow the recovery of U pinnatifida and other non-encrusting macroalgae (B) Diagram showing the artificial buoyed reefs at the restoration area Effect of water velocities on the distribution of sea urchins and U pinnatifida Field surveys of the water velocities at randomly selected ten U pinnatifida habitats and twenty unvegetated areas in Line and Line were conducted in September 2004 and August 2005 Each area for the measurement of water velocity was separated from the others by to m Wave heights at the outside of the bay were to m over the course of the study Water velocity was estimated to average the maximum velocity in 60 seconds (n = 3) at cm above the bottom, using a portable waterproof velocity meter (Tokyo Keisoku Co Ltd and DIV Ltd., Japan) In addition, the densities of U pinnatifida and sea urchin were recorded using 0.25 m2 quadrat in each area Restoration effort We performed a U pinnatifida restoration effort to reduce the effects of grazing pressure of sea urchins in the barren grounds adjacent to Line (Fig 1A) Two sets of artificial buoyed reefs were moored in the middle depth of water using ropes and weights in December 2004 (Fig 1B) The buoyed reefs were deployed at -0.4 m and -2.5 m depth relative to mean low water level (MLWL) The reefs were designed to prevent the migration of sea urchins by being detached from the bottom and thus, allowing the recovery of U pinnatifida and other non-encrusting macroalgae Both buoyed reefs were made of wood and their length was 1.0 m with 1.0 m width and 16 cm height We also prepared another reef grounded to the bottom to allow the migration of sea urchins, stacking blocks as the control treatment within the restoration area Control treatment was placed at -2.1 m depth (relative to MLWL) and the length was 1.0 m with 0.4 m width and 36 cm height U pinnatifida cultivated in the laboratory (Kesennuma Miyagi Prefectural Fisheries Experimental Station), with the average height of 46.7 ± 17.5 cm, were tied onto each reef (approximately 50 plants), and their coverage was monitored almost every month following the method of Turner et al (2004) In addition, the percentage covers of other macroalgae and the density of - 203 - Journal of Water and Environment Technology, Vol 7, No 3, 2009 sea urchins on the reefs were quantified Small size of U pinnatifida was transplanted at the shallower buoyed reef, resulting in reduced initial coverage when compared to the other treatments Light conditions and water temperature at each reef were recorded using an underwater light sensor (LI - 193 SA, LI - COR, Inc.) and stowaway tidbit temperature loggers (Onset Computer Corporation) over the course of the study Light intensity was measured during noon ± hours Differences in the light intensity between the reefs were analyzed by Tukey’s HSD (Honestly Significant Difference) test Comparison of the macroalgal habitats between the artificial reefs and natural rocky shore We compared macroalgal biomass between the artificial reefs and natural rocky shore inhabited by U pinnatifida in Line to examine the transplant success using the buoyed reefs Samples of macroalgae were collected at both areas in August 2005 We harvested all macroalgal plants on the artificial reefs On the other hand, macroalgal biomass in rocky shore in Line was quantified using three 0.25 m2 quadrats Water depths of sampling areas in Line corresponded to the depths of each buoyed reef, i.e one of these was -0.4 m and the other was -2.5 m (relative to MLWL) In the laboratory, algal samples were sorted by species, dried in an oven for 48 h at 80 ˚C and then weighed RESULTS AND DISCUSSION Composition of substratum, macrophyte flora and infauna in the outer and inner areas of the bay A total of 16 macrophyte species in 2003 and 15 species in 2004 were observed in Line (Table 1) U pinnatifida and crustose coralline algae were the dominant species A total of sea urchin species were observed in Line between 2003 and 2004 Strongylocentrotus nudus was the most common sea urchin, and accounted for more than 95 % of the total number of sea urchins, which were 285 and 450 ind per belt transect in 2003 and 2004, respectively Among the depths distributed by U pinnatifida, more than to 10 ind m-2 of sea urchin led to the decrease in the percentage covers of U pinnatifida (Fig 2), suggesting that the grazing with a high density of herbivorous sea urchin had a negative effect on the distribution of U pinnatifida in the outer areas of the bay A total of macrophyte species in 2003 and species in 2004 were observed in Line (Table 2) The most common sea urchin species was S nudus The former U pinnatifida habitat in 1990s, which was reported by Tamaki et al (2005), had reverted to sea urchin - dominated barren grounds (Table 2) The brown alga, Dilophus okamurae, which was known to inhibit the feeding behavior of sea urchin (Taniguchi et al., 1995) had also appeared in Line The numbers of sea urchin were 212 and 365 ind per belt transect in 2003 and 2004, respectively, but both populations of sea urchin in Line were less than those in Line We also found that the absence of U pinnatifida even with the lower density of sea urchin occurred at the surveyed section with 30.0 to 40.6 m away from the shore in Line in 2003 (Table 1) Thus, in addition to the population of sea urchin as the algal herbivores, other factors might be responsible for the reduction of U pinnatifida habitat in the inner and some outer areas - 204 - Journal of Water and Environment Technology, Vol 7, No 3, 2009 of the bay Table – Compositions of substratum, macrophyte flora and infauna along Line in 2003 (A) and 2004 (B) +: percentage covers were less than % n.d.: data is not available (A) Distance from the shore（m） Depth（m relative to MLWL） Sediment composition (%) Bed rock Isolated rock Boulder and cobble Pebble Sand Mud 0.0 0.1 0.5 -0.2 100 7.7 -4.3 100 12.7 -5.7 15.1 -6.4 90 22.0 -8.3 80 + 30 60 10 100 10 30.0 -8.4 10 + + 40.6 -9.4 90 10 47.5 -9.3 + 20 60 10 + + 50.0 -10.2 40 60 + Percentage covers of algae and seagrass （%） Sargassum fusiforme Calliarthron yessoense Sargassum horneri Grateloupia turuturu Phyllospadix iwatensis Undaria pinnatifida Crustose coralline algae Cladophora sakaii Rhodymenia sp Herpochondria elegans Delesseriaceae Dictyopteris prolifera Corallinaceae Codium latum Costaria costata Ceramiaceae 70 10 + + + + 50 50 + 10 40 + + + 70 10 + 70 30 70 + + + + 50 + + + 20 70 50 + 10 + + 20 6.4 0.0 0.1 2.8 0.0 0.0 -2 Dencity of infauna （ind.m ） Strongylocentrotus nudus Hemicentrotus pulcherrimus Nordotis discus hannai 0.0 0.0 0.0 1.1 1.0 1.7 12.6 1.0 5.2 3.3 0.0 6.3 6.7 0.1 0.1 9.3 0.0 1.1 2.1 0.0 0.1 (B) Distance from the shore（m） Depth（m relative to MLWL） Sediment composition (%) Bed rock Isolated rock Boulder Cobble Pebble Sand Sediment deposition 0.0 +0.6 3.4 -1.9 100 12.0 -5.1 12.5 -5.0 13.7 -6.2 100 100 100 30 10 + 50 25.5 -7.4 80 20 30 37.6 -9.1 50.0 -9.2 60 30 10 + + + + 10 + 30 + 50 + 10 20 + + + + + Percentage covers of algae and seagrass （%） Sargassum fusiforme Calliarthron yessoense Serraticardia maxima Corallina pilulifera Gigartinales Codium fragile Phyllospadix iwatensis Undaria pinnatifida Crustose coralline algae Laurencia sp Bossiella cretacea Congregatocarpus sp Dictyopteris divaricata Neoholmesia japonica Ceramiaceae + 10 10 10 + + 10 20 + + 70 + 10 + + + -2 Dencity of infauna （ind m ） Strongylocentrotus nudus Nordotis discus hannai 0.0 n.d 10.1 0.3 0.0 n.d 44.2 4.2 - 205 - 9.1 0.3 10.5 0.7 6.1 0.1 Journal of Water and Environment Technology, Vol 7, No 3, 2009 Table – Compositions of substratum, macrophyte flora and infauna along Line in 2003 (A) and 2004 (B) +: percentage covers were less than % (A) 0.0 0.3 Distance from the shore（m） Depth（m relative to MLWL） Sediment composition (%) Bed rock Isolated rock Boulder and cobble Pebble Sand Mud 4.2 -0.9 11.5 -1.4 17.0 -1.8 20.7 -2.5 31.7 -5.1 43.0 -9.3 50.0 -12.0 100 10 90 10 90 100 + + 90 10 + 90 10 + + 30 70 + 50 40 30 + 10 80 80 10 50 70 10 + + 5.8 0.0 0.1 3.1 0.0 0.0 Percentage covers of algae and seagrass （%） Crustose coralline algae Dilophus okamurae Lithophyllum okamurae Corallinaceae Grateloupia turuturu Laurencia sp + + + Dencity of infauna （ind.m -2） Strongylocentrotus nudus Hemicentrotus pulcherrimus Nordotis discus hannai 0.2 0.2 0.0 1.5 0.1 0.3 0.4 0.0 0.0 12.4 0.3 0.0 5.3 0.3 0.0 (B) Distance from the shore（m） Depth（m relative to MLWL） Sediment composition (%) Bed rock Isolated rock Boulder Cobble Pebble Sand Mud 0.0 +1.6 8.9 -0.6 14.3 -2.0 16.6 -2.1 + 100 + + + 20 70 10 10 40 40 10 80 10 35.6 -7.9 + 80 10 + 40.0 -9.3 50.0 -11.7 30 10 + 60 + 70 10 + + + 10 70 Percentage covers of algae and seagrass （%） Crustose coralline algae Dilophus okamurae Laurencia sp Bossiella cretacea Diatom + 90 + + + + + + Density of infauna （ind m-2 ） Strongylocentrotus nudus Nordotis discus hannai 0.9 0.0 10.4 0.2 19.1 0.0 8.2 0.1 6.4 0.0 7.3 0.0 Effect of water flow on the feeding behavior of sea urchin Evidence has led investigators to suggest that grazing pressure of sea urchins might vary among their populations and hydrodynamic conditions that would allow the migration and feeding behavior of sea urchins (Deny, 1988; Kawamata, 1998; Kuwahara et al., 2002) Fig shows the effects of water velocities on the density of U pinnatifida and sea urchins in the outer and inner areas of the bay In the outer areas (Line 1) with high water velocities, more than 14.5 ± 3.4 cm sec -1, U pinnatifida grew densely and sea urchins were scarce In some outer areas with lower velocities, less than 7.8 ± 2.3 cm sec -1, U pinnatifida grew sparsely where the aggregation of sea urchin was found SCUBA observations also revealed that sea urchins actively grazed plants at the areas with calm water These results indicated that there were areas under high water flow conditions preventing the migration and/or grazing by sea urchin even with their high abundance in the outer bay In contrast, in the inner areas (Line 2) where U pinnatifida no longer occurred, the density of sea urchins and water velocities ranged from to 20 ind m-2 and from 2.4 to 4.6 cm sec-1, respectively The similarity in water flow conditions between the inner - 206 - Journal of Water and Environment Technology, Vol 7, No 3, 2009 Percentage covers of U pinnatifida (%) bay areas and unvegetated areas with aggregations of sea urchins in the outer bay indicated that water velocities in the inner bay were not high enough to prevent the grazing pressure of sea urchin 80 70 60 50 40 2003 30 2004 20 10 0 10 20 30 40 50 Density of sea urchin (ind m-2) 70 50 60 U pinnatifida (Line 1) U pinnatifida (Line 2) Sea urchin (Line 1) Sea urchin (Line 2) 50 40 30 40 30 20 20 10 10 0 10 12 14 16 18 Density of sea urchin (ind m-2) Density of U pinnatifida (ind m-2) Fig – Relationship between the percentage covers of Undaria pinnatifida and density of sea urchins in 2003 and 2004 Depth distribution of U pinnatifida: -0.2 to -9.3 m relative to MLWL in 2003 +0.6 to -6.2 m relative to MLWL in 2004 20 Water velocity (cm sec-1) Fig – Effect of water velocity on the density of Undaria pinnatifida and sea urchins Mine et al (2000) reported that the movement of sea urchin was inhibited in the sandy bottom sediment In this study, although there were some sandy areas, substratum at both areas of the bay was mainly composed by bed rock, isolated rock, boulder, cobble and pebble (Table and 2) Thus, the bottom sediment was not a major factor leading to the different distribution of sea urchin in the outer and inner areas of the bay Restoration effort Water temperature and light intensity Fig 4A shows the change in water temperature from December 2004 to June 2005 Water temperature decreased to 6.5 ˚C in March and increased to 14.9 ˚C in June - 207 - Journal of Water and Environment Technology, Vol 7, No 3, 2009 Ohno (2004) reported that U pinnatifida survived between ˚C and 20 ˚C This result suggested that the condition of water temperature at the restoration area was enough for the survival of transplanted U pinnatifida 18 16 14 12 10 (A) (B) Light intensity (µmol m -2 sec-1) Water temperature ( ˚C) Light intensity has been documented as an important factor affecting the survival of U pinnatifida (Ohno, 2004; Tokuda, et al., 1987) Fig 4B shows the change in photosynthetic photon flux density (PPFD) at each reef PPFD values at the shallower buoyed reef were slightly higher than those at other reefs Light intensities between the deeper buoyed reef and the control showed no significant differences (p = 0.96) 50 100 150 200 Days after transplanting Dec 2004 Feb 2005 Apr 2005 1400 Shallower buoyed reef 1200 Deeper buoyed reef 1000 Control 800 600 400 200 0 50 100 150 200 250 Days after transplanting Jun 2005 Dec 2004 Feb 2005 Apr 2005 Jun 2005 Fig – Changes in (A) water temperature and (B) light intensity at the restoration area Water temperature is shown as the mean ± standard deviation Survival of macroalgae Fig shows the percentage covers of macroalgae and the density of sea urchins between the artificial buoyed reefs and the control After days, almost all transplants of U pinnatifida at the control disappeared, while the density of sea urchins had increased to 54 ind m-2 (Fig 5A) The control treatment of transplanted U pinnatifida bed reverted to the sea urchin - dominated barren grounds after days Even though the initial coverage of transplants at the shallower buoyed reef was low, distinct difference in macroalgal community was found when compared to the control treatment (Fig 5B) The percentage covers of transplanted U pinnatifida at the shallower buoyed reef decreased to % after 11 days At that time, we observed the feeding behavior of sea hare on the buoyed reef, although there was no distribution data of sea hare during the investigation period at two surveyed lines (Table and 2) Sea hare is also known to be a potential algal herbivore (Utsumi et al., 1996), which suggested that loss of transplanted U pinnatifida on the reef may have been affected by the feeding behavior of sea hare After some loss of macroalgae on the reef, however, Scytosiphon lomentaria and Saccharina japonica were naturally recruited due to the reduction of migration by sea urchin, 0.8 ± 1.8 ind m-2, using the buoyed reef (Fig 5B), while the formation of barren ground remained around the inner areas of the bay (data not shown) After 186 days, kelp forests became well established and persistent - 208 - 80 Percentage covers of macroalgae (%) 50 40 60 30 40 20 20 10 0 50 U pinnatifida Diatoms S lomentaria S japonica Others Sea urchin 100 80 100 150 200 60 (B) 50 40 60 30 40 20 20 10 0 Percentage covers of macroalgae (%) 60 U pinnatifida Others Sea urchin Density of sea urchin (ind m-2) (A) Density of sea urchin (ind m-2 ) 100 100 50 100 150 200 60 (C) 50 80 40 60 U pinnatifida 30 S japonica 40 Others 20 Sea urchin 20 10 Density of sea urchin (ind m-2 ) Percentage covers of macroalgae (%) Journal of Water and Environment Technology, Vol 7, No 3, 2009 0 Dec 2004 50 Feb 2005 100 150 200 Days after transplanting Apr Jun 2005 2005 Fig – Macroalgal habitats and population of sea urchin at the artificial buoyed reefs (A) Control, (B) Shallower buoyed reef, (C) Deeper buoyed reef Others indicate the percentage cover of macroalgal species which were less than 20% - 209 - Journal of Water and Environment Technology, Vol 7, No 3, 2009 Transplanted U pinnatifida at the deeper buoyed reef increased and persisted by 110 days (Fig 5C), although there was no significant difference in light intensity between the deeper buoyed reef and control where U pinnatifida had been eliminated within days Withering of U pinnatifida after the reproductive maturation period in spring led to a decrease in the percentage cover of U pinnatifida, while S japonica was recruited and kelp forests became well established after 186 days Migrated sea urchin on the buoyed reef was lower than those of the control over the course of the study, and the densities were 1.2 ± 1.8 ind m-2 Thus, inhibition of migration by sea urchin using the buoyed reef seemed to be a factor responsible for the recovery of macroalgal habitats at the restoration area Furthermore, the loss of transplanted U pinnatifida that we observed at the control treatment also indicated that disappearance of U pinnatifida in the inner areas of the bay may have been accelerated by the grazing pressure of sea urchin Biomass (g D.W m-2) 1000 750 U pinnatifida S japonica Others 500 250 Shallower buoyed reef Line 1(-0.4 m relative to MLWL) Deeper buoyed reef Line 1(-2.5 m relative to MLWL) Fig – Algal biomass between the artificial buoyed reefs and natural rocky shore inhabited by U pinnatifida in Line Others indicate the biomass of Ulva sp and Sargassum horneri Fig shows the algal biomass between the artificial buoyed reefs and natural rocky shore inhabited by U pinnatifida in Line Although the algal compositions were different, the biomass at each depth between the artificial reefs and natural rocky shore was almost the same The distinct difference in algal compositions between the buoyed reefs and natural habitat related to the reduction of cultivated U pinnatifida transplants Except for the possibility of the feeding behavior of sea hare, cultivated U pinnatifida transplants at both buoyed reefs were reduced by the withering after the reproductive maturation period However, we could not find significantly withering plants for the natural U pinnatifida habitat The reproductive maturation and withering periods of cultivated U pinnatifida occurred between January and March, while natural U pinnatifida plants maturated after spring (Taniguchi et al., 1981; Akiyama et al., 1982; Tokuda et al., 1987; Saitoh et al., 1999) Thus, prematurity and withering of the cultivated U pinnatifida transplants seemed to be a factor responsible for the difference in algal compositions between the artificial buoyed reefs and natural rocky shore inhabited by U pinnatifida in Line Overall, our restoration efforts using the artificial buoyed reef, although not ideal, resulted in the establishment of - 210 - Journal of Water and Environment Technology, Vol 7, No 3, 2009 functional macrolagal habitats in the sea urchin - dominated barren grounds by the reduction of grazing pressure of sea urchins CONCLUSIONS U pinnatifida habitats in the inner areas of Ogatsu Bay, Japan, declined during the 1990s and resulted in the formation of barren grounds with the aggregations of sea urchin S nudus as the potential algal herbivores (Tamaki et al., 2005) However, there are many areas where U pinnatifida inhabited even with a high abundance of herbivorous sea urchins in the outer areas of the bay Here, we carried out a comparative study on the biological and physical characteristics of these areas to elucidate factors responsible for the deterioration of U pinnatifida habitats in the inner areas of Ogatsu Bay, Japan We also performed U pinnatifida restoration effort to reduce the effect of grazing pressure by sea urchins in the barren grounds in the inner areas of the bay Specific conclusions derived from this study are as follows In the outer areas of the bay with high water velocities, more than 14.5 ± 3.4 cm sec -1, U pinnatifida grew densely and sea urchins were scarce However, in some outer areas with lower velocities, less than 7.8 ± 2.3 cm sec -1, U pinnatifida grew sparsely where the aggregation of sea urchin was found In contrast, in the inner areas of the bay with calm water having velocities of 2.4 to 4.6 cm sec-1, the density of sea urchin was high and the U pinnatifida beds disappeared These results indicated that high water velocities in the outer bay areas prevent the grazing by sea urchins Disappearance of U pinnatifida in the inner bay areas seemed to be caused by the high grazing pressure of sea urchins in calm water velocity conditions Considering the restoration efforts, artificial buoyed reefs were designed to prevent the migration of sea urchins by being detached from the bottom and allowed the recovery of U pinnatifida and other non-encrusting macroalgae Two sets of the buoyed reefs were deployed at the barren ground in the inner bay areas Although there were some losses of transplanted U pinnatifida partly caused by the withering after the reproductive maturation period, S japonica and other macroalgae were naturally recruited and increased due to the inhibition of migration by sea urchins using the buoyed reefs In contrast, the formation of barren community remained at the area grounded to the bottom in the inner bay Overall, our restoration efforts using the artificial buoyed reef, although not ideal, resulted in the success of the recovery of macrolagal habitats in the sea urchin - dominated barren grounds by the reduction of grazing pressure of sea urchins ACKNOWLEDGEMENTS This research was supported by the Showa Shell Sekiyu foundation We especially thank Hiroyuki Takahashi and Atsushi Fukaya for the field assistance Professor Dr Mitsuru Takasaki is acknowledged for giving us the opportunity to this research This work would not have been possible without the assistance of Yasuhiko Nakayama so his contribution is appreciated We also thank the Fisherman’s Association of Ogastu in Miyagi Prefecture - 211 - Journal of Water and Environment Technology, Vol 7, No 3, 2009 REFERENCES Akiyama, K and Kurogi, M (1982) Cultivation of Undaria pinnatifida (Harvey) Suringar The decrease in crops from natural plants following crop increase from cultivation., Bull Tohoku Reg Res Lab., No.44, 91 - 100 Alcoverro, T and Mariani, S (2002) Effects of sea urchin grazing on seagrass (Thalassodendron ciliatum) beds of a Kenyan lagoon., Mar Ecol Prog Ser., Vol.226, 255 - 263 Arasaki, S and Tokuda, H (2002) Keys to the seaweeds of Japan and its vicinity Hokuryukan Press, Tokyo, pp 52 - 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