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

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, 1 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 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

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,

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 × 1 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 × 1 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 classificationof Fujita et al (2003)

Fig 1 – (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 1 and Line 2 were conducted in September 2004 and August 2005 Each area for the measurement of water velocity was separated from the others by 3 to 5 m Wave heights at the outside of the bay were 1 to 2 m over the course of the study Water velocity was estimated to average the maximum velocity in

60 seconds (n = 3) at 5 cm above the bottom, using a portable waterproof velocity meter

(Tokyo Keisoku Co Ltd and DIV Ltd., Japan) In addition, the densities of U

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 2 (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

(B)

Miyagi

Prefecture

1 km

141º 30’ E

38º 30’ N

Line 1 Line 2

Ogatsu Bay

(A)

Mean Low Water Level

Bottom

Artificial buoyed reef

2.5 m

1.5 m

2.5 m 0.4 m

rope Outer areas

Inner areas

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 ± 2 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 1 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 1 was quantified using three 0.25 m2 quadrats Water depths of sampling areas in Line 1 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

1 (Table 1) U pinnatifida and crustose coralline algae were the dominant species

A total of 2 sea urchin species were observed in Line 1 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

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 6 macrophyte species in 2003 and 4 species in 2004 were observed in Line 2

(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 2 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 2 were less than those in Line 1 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 1 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

of the bay

Table 1 – Compositions of substratum, macrophyte flora and infauna along Line 1 in

2003 (A) and 2004 (B) +: percentage covers were less than 5 % n.d.: data is not available

Distance from the shore（m） 0.0 0.5 7.7 12.7 15.1 22.0 30.0 40.6 47.5 50.0

Depth（m relative to MLWL） 0.1 -0.2 -4.3 -5.7 -6.4 -8.3 -8.4 -9.4 -9.3 -10.2

Sediment composition (%)

Mud

Percentage covers of algae and seagrass （%）

Distance from the shore（m） 0.0 3.4 12.0 12.5 13.7 25.5 37.6 50.0

Depth（m relative to MLWL） +0.6 -1.9 -5.1 -5.0 -6.2 -7.4 -9.1 -9.2

Sediment composition (%)

Percentage covers of algae and seagrass （%）

Calliarthron yessoense 10

Serraticardia maxima 10

Corallina pilulifera 10

Gigartinales +

Phyllospadix iwatensis 10

(A)

(B)

Table 2 – Compositions of substratum, macrophyte flora and infauna along Line 2 in

2003 (A) and 2004 (B) +: percentage covers were less than 5 %

Distance from the shore（m） 0.0 4.2 11.5 17.0 20.7 31.7 43.0 50.0

Depth（m relative to MLWL） 0.3 -0.9 -1.4 -1.8 -2.5 -5.1 -9.3 -12.0

Sediment composition (%)

Bed rock

Isolated rock

Percentage covers of algae and seagrass （%）

Distance from the shore（m） 0.0 8.9 14.3 16.6 35.6 40.0 50.0

Depth（m relative to MLWL） +1.6 -0.6 -2.0 -2.1 -7.9 -9.3 -11.7

Sediment composition (%)

Bed rock

Percentage covers of algae and seagrass （%）

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 3 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 8 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 (A)

(B)

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

0 10 20 30 40 50 60 70 80

Density of sea urchin (ind m -2 )

2003 2004

Fig 2 – 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

0 10 20 30 40 50

0 10 20 30 40 50 60 70

-2 )

-2 )

Water velocity (cm sec -1 )

U pinnatifida

U pinnatifida

Sea urchin (Line 1) Sea urchin (Line 2)

Fig 3 – 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 1 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

(Line 1) (Line 2)

Ohno (2004) reported that U pinnatifida survived between 5 ˚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

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)

Fig 4 – 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 5 shows the percentage covers of macroalgae and the density of sea urchins

between the artificial buoyed reefs and the control After 3 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 6 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 5 % 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 1 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

(A) (B)

Days after transplanting Days after transplanting

Dec

2004

Feb

2005

Apr

2005

Jun

2005

0 200 400 600 800 1000 1200 1400

0 50 100 150 200 250

-2 se

-1 )

Shallower buoyed reef Deeper buoyed reef Control

Dec

2004

Feb

2005

Apr

2005

Jun

2005

0

2

4

6

8

10

12

14

16

18

0 50 100 150 200

0

10

20

30

40

50

60

0 20 40 60 80 100

-2 )

U pinnatifida

Others Sea urchin

Fig 5 – 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%

Dec

2004

Feb

2005

Apr

2005

Jun

2005

(A)

0 10 20 30 40 50 60

0 20

40

60

80

100

-2 )

) U pinnatifida

Diatoms

S lomentaria

S japonica

Others Sea urchin

0 10 20 30 40 50 60

0 20

40

60

80

100

-2 )

U pinnatifida

S japonica

Others Sea urchin

(B)

(C)

Days after transplanting

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 6 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

0 250 500 750 1000

Shallower buoyed reef

Line 1(-0.4 m relative to MLWL)

Deeper buoyed reef

Line 1(-2.5 m relative to MLWL)

-2 )

U pinnatifida

S japonica

Others

Fig 6 – Algal biomass between the artificial buoyed reefs and natural rocky shore

inhabited by U pinnatifida in Line 1 Others indicate the biomass of Ulva sp and

Sargassum horneri

Fig 6 shows the algal biomass between the artificial buoyed reefs and natural rocky

shore inhabited by U pinnatifida in Line 1 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 1 Overall, our restoration efforts

using the artificial buoyed reef, although not ideal, resulted in the establishment of