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3 Succession of Intertidal Community After the Great East Japan Earthquake

3 Succession of Intertidal Community After the Great East Japan Earthquake

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Normality of Succession of an Intertidal Community…



17



organisms on two PVC test plates (25 × 25 cm) has been investigated. The test plates

were set at 40 cm below M.S.L., kept for a month on the Sakihama jetty wall, and

then changed each month to new ones.



2.3.2



Results and Discussion



2.3.2.1



Pioneer Species into the New Habitats



At the jetty where this research was made in July 2011, the extent of the subsidence

was 1.3 m (Fig. 2.5b), which was relatively more than other adjacent land areas, due

to difference in substrata hardness and that the site stands out about 200 m apart

from the land (Fig. 2.1). The observed scale of the subsidence means that almost

two thirds of the sessile littoral organisms in this site sank into the subtidal zone.

The first settlers were the barnacle S. cariosus. They were abundant and completely covered the bare area from the mid-intertidal to about 6 m below M.S. L. not

only on the wall but also on rocky shores around the bay (Fig. 2.5e). They survived

with a high rate except loss due to detachment by their own overcrowded settlement. According to our previous study (Kado et al. 2002), this barnacle releases its

nauplii when the surface chlorophyll a concentration exceeds 1 mg/m3 at the beginning of the spring bloom. The nauplii settled on the shore 3–5 weeks later when the

chlorophyll a concentration remained at approximately the same level (Kado et al.

2002). Although the chlorophyll a concentrations were unknown during March to

June 2011, it was most likely that the concentration had been kept over 1 mg/m3 at

least for more than a month after the earthquake. This high recruitment of S. cariosus right after the earthquake might have been attributed to two reasons. One of the

reasons may be the decrease in filter feeders. Tsunamis caused by the Great East

Japan Earthquake in 2011 washed away a number of organisms including cultured

species such as oysters C. gigas, scallop Mizuhopecten yessoensis, and sea squirt

Halocynthia roretzi and the fouling organisms such as barnacles M. rosa, mussels

M. galloprovincialis, and other sedentary animals that settled on the culture rafts,

buoys, and ropes. All of these filter feeders fed on phytoplankton. Accordingly,

nauplii of S. cariosus could have sufficiently fed on phytoplankton during the algal

spring bloom and maintained a high survival rate throughout the larval stages. The

heavy settlement of this barnacle was, however, not the first case in this area. Indeed,

the same phenomenon had been observed in May 2004. However, at that time, the

abundance of the sea urchin, Strongylocentrotus nudus, reached more than ten individuals/m2 and almost all of the settled S. cariosus had been consumed by the sea

urchin within the next 3 months (Kado personal observations). This high sea urchin

abundance had been continued until February in 2011. However, the sea urchin

abundance decreased due to the tsunami. Kawamura et al. (2014) also reported that

abundance of sea decreased in Otsuchi Bay, Iwate Prefecture, by the backwash of

tsunamis caused by the earthquake. Thus, the second reason of high settlement rate

of S. cariosus right after the tsunamis was likely due to low sea urchin abundance

(<1 individual/m2) (Fig. 2.6).



18



R. Kado and N. Nanba



b



a



c



d



Chthamalus



Chthamalus



Crassostrea

old

M.S.L.



Hydroides



new

M.S.L.



Earthquake

& Subsidence



Ulva



Semibalanus



Strongylo centrotus



old

M.S.L.

Before 2010



e



March11

2011



f



July



August



g



h



Pyropia

new

M.S.L.

Megabalanus

Analipus



MyƟlus

Perforatus



Undaria



Nucella



old

M.S.L.

Oct.

2011



Dec.



May

2012



Sept.



Fig. 2.5 Diagrams showing successional changes in the intertidal communities on the wall of the

Second Jetty in Sakihama before and 1 year after the Great East Japan Earthquake. Details are

described in the text



2



19



Normality of Succession of an Intertidal Community…



i



j



k

Pyropia yezoensis

Ulva intestinalis

Analipus japonicus

new

M.S.L.



Semi balanus



Undaria

pinnatifida

Chthamalus

challengeri

Semibalanus

cariosus

Megabalanus rosa

Perforatus

perforatus

Mytilus

galloprovincialis



Perforatus



Nucella heyseana

Strongylocentrotus

nudus

old

M.S.L.



Crassostrea gigas

Hydroides ezoensis



May

2013



May

2014



April

2015



Fig. 2.5 (continued)



2.3.2.2



Formation of Littoral Communities



2011

Soon after the heavy settlement of S. cariosus, several organisms were initiated to

form a new community over the barnacles as substrates. For example, the green alga

Ulva (Enteromorpha) intestinalis initially settled on the shells of S. cariosus growing over the mid-littoral in August (Fig. 2.5d). During the same period, surf barnacle

C. challengeri recruited in the high littoral zone with a high density. Then, the mussel M. galloprovincialis followed to settle on the shells of the barnacles from the

mid-littoral to the upper sublittoral zone from summer to fall in 2011 (Fig. 2.5e).

During the summer of 2011, oysters also settled over the shells of barnacles in the

mid-littoral zone. Oysters C. gigas and serpulids H. ezoensis which had colonized

in the mid-littoral zone before the tsunamis were taken to the sublittoral zone due to

the subsidence of substrate jetty by the earthquake. However, these animals lived

there even after the earthquake.



25



25



20



20



15



15



10



10



5

0



5



Temperature

Sea urchin denisity



A N F M A N F M A N F M A

2011 2012

2013

2014



N F M

2015



Sea surface

temperature (°C)



R. Kado and N. Nanba



Density (ind/m2)



20



0



Fig. 2.6 Changes in average abundance of sea urchin Strongylocentrotus nudus (red line) on the

wall of the Second Jetty in Sakihama and surface seawater temperature (blue line) in front of the

wall at Sakihama fishing port in Iwate Prefecture. Error bars indicate standard deviation



2012

In winter 2012, S. cariosus grew to more than 10 mm in shell diameter (Fig. 2.5f).

Abundance of the sea urchin had increased to about five individuals/m2 by the

summer of 2012 (Fig. 2.6), and the abundance of S. cariosus in the sublittoral zone

decreased to about 3 × 103 individuals/m2. M. galloprovincialis in the mid- to lower

littoral zones grew larger, resulting in forming a black mussel bed (about 15 × 102

individuals/m2) over the barnacles.

In spring 2012, the brown alga Undaria pinnatifida and red alga Analipus japonicus grew on the barnacles in the sublittoral zone and on the mussels in the midlittoral zone, respectively (Fig. 2.5g). S. cariosus usually settled in spring but had

a poor recruitment in this year. In the summer and fall of this year, C. challengeri,

S. cariosus, and M. galloprovincialis that were sessile animals were abundantly found

in the upper, the middle to the lower, and the lower intertidal zones, respectively

(Fig. 2.5h). The mussels anchored by the byssus matrix on the barnacles. Such a

community structure was found before 1998 (Kado personal observation) and

accorded well with those in the experiment done before the earthquake in which

predation pressure of sea urchin was artificially decreased (see above). This concordance implies that biological succession observed in the littoral zone after the

earthquake was not an ecologically rare event.

However, we found some rare phenomena. In the summer 2012, the reddish

barnacle Megabalanus rosa settled on the mussel shells (Fig. 2.5h). This barnacle

was common in this area on the culture buoys and ropes before the earthquake but

was not observed to occur on the shells of mussels. This rare event was also observed

in the experiment done before the earthquake in which predation pressure of sea

urchin was artificially decreased (see above). In addition to this, a new alien barnacle Perforatus perforatus appeared and settled on the mussel shells.



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Normality of Succession of an Intertidal Community…



21



P. perforatus is a barnacle distributed in a range from the English Channel to the

Mediterranean (Herbert et al. 2003) and is reported to have been introduced along

the east coast of Korea in 2004 (Choi et al. 2013). In Japan, this barnacle was noted

in 2012 for the first time at Toga Bay in Akita Prefecture, northern Honshu along the

Japan Sea (Nogata et al. 2015). According to Nogata et al. (2015), this alien barnacle settled on culture buoys and ropes abundantly. In some cases, more than two

thirds of the settled barnacles on these culture buoys and ropes were P. perforatus.

A field survey along the coast of the Japan Sea revealed that this barnacle settled on

piers and tetrapods with a large abundance and on shells of various mollusks such

as turbo shell Turbo cornutus, rock shell Thais clavigera, and oyster Crassostrea

nippona (Kado, unpublished data). According to the monthly monitoring data on

sedentary organisms on the Sakihama jetty wall, P. perforatus appeared for the first

time on the plates in September 2012 (Kado unpublished data).



2013

From late 2012 to 2013, abundance of the sea urchin on the jetty wall further

increased and reached to be more than ten individuals/m2 (Fig. 2.6). As a result,

barnacles that settled below the lower littoral zone almost disappeared, and the ecological situation returned to a sea urchin-dominated barren that was similar to that

before the earthquake.

In February 2013 when the seawater temperature was 1.5–2.0 °C higher than that

of an average year, only a small number of macroalgae recruited (Fig. 2.5i).

Although S. cariosus recruited on the mussels, abundance of the mussels decreased

from 10.7 × 102 individuals/m2 in June 2012 to 1.3 × 102 individuals/m2 in April

2013. In the summer of 2013, the reddish barnacle M. rosa that had settled in the

previous year on the mussels almost disappeared with the decrease in abundance of

mussels. P. perforatus that had settled the previous summer survived and overwintered with a low mortality. They reached to about 10 mm in shell diameter in the

summer of 2013. In addition, their newly settled individuals were observed on the

mussels and on the walls.



2014

In the spring of 2014, we found S. cariosus individuals only in the tidal level higher

than 60 cm M.S.L. In this zone, sea urchins could not remain for a long time. The S.

cariosus individuals grew to about 20 mm in size. Some individuals of this species

were fed on even in this zone by predatory gastropods such as Nucella heyseana and

Ceratostoma burnetti (Fig. 2.5j). A number of recruited individuals of this barnacle

were observed in the spring of 2014 as in 2011. However, S. cariosus individuals

that had settled below the lower littoral zone disappeared before the late autumn.

During this period, abundance of the mussels also decreased, and their recruitment

was very limited probably due to the lack of S. cariosus as an appropriate substrate.



22



R. Kado and N. Nanba



2015

In the spring of 2015, abundances of S. cariosus and M. galloprovincialis were

highly limited in the tide level between 15 and 30 cm below M.S.L. In contrast,

carnivorous rock snails accumulated at the wall of the jetty in this experimental site

(Fig. 2.5k). Besides, few oysters Crassostrea gigas settled on the jetty wall after the

earthquake. Even when the number of barnacle individuals was reduced by the sea

urchins in 2015, the oyster never dominated in the mid-littoral zone.



2.4



Conclusion



A variety of benthic organisms occurred on the jetty wall of Sakihama at the Sanriku

coast after the ground subsidence caused by the Great East Japan Earthquake in

March 2011. The increase in abundance of some species such as S. cariosus was

attributable to two reasons. One reason was reduction of the sea urchin abundance

due to the tsunamis. The other reason was the temporal decrease in abundance of

filter feeders that enabled a rapid colonization of S. cariosus which, in turn, provided a hard uneven substrate for other sedentary settlers. Accordingly, the community with diverse organisms was developed on the jetty wall in 2012, a year after

the earthquake. However, the community with various organisms did not last for a

long time. In 2013, with an increasing abundance of the common sea urchin S.

nudus, the community on the jetty wall has returned to be a poor species composition. In the sublittoral zone on the wall, the community with a very poor biodiversity like “rocky shore denudation” was commonly observed from the third to fourth

years after the Great East Japan Earthquake. Thus, the community structure in the

intertidal zone of Sakihama area has been gradually approaching that found before

the earthquake. In addition to the common sea urchin, increase in the number of

gastropods has accelerated this succession by predating on the barnacles and mussels left on the jetty wall.

We found an alien barnacle P. perforatus for the first time in 2012 in Sakihama

area. This barnacle survived in the following winter seasons and colonized successfully at the mid-littoral to upper sublittoral zone, although the mean sea surface

temperature (SST) in winter in this area (6.8 °C in Kamaishi near Sakihama) was

much lower than that (8.2 °C in Brighton in the eastern English Channel) which is

the most northeastern native locality in Europe (Herbert et al. 2003; World Sea

Temperatures a, b). One may suppose that the appearance of P. perforatus in

Sakihama area was a result of natural range expansion by the larval dispersion from

Japan Sea to the Pacific Ocean by means of the Tsugaru Warm Current. However,

although we examined their distribution range along the coasts of northeast Japan,

we did not find this species at least in coastal areas of the Pacific side of Aomori

Prefecture (Kado unpublished data). This implies that there is a large gap in their

distribution range between coasts of Japan seaside and Pacific Ocean seaside.

Rather, P. perforatus may have been introduced by anthropogenic activities. It is



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Normality of Succession of an Intertidal Community…



23



reported that plastic flotsam provided a means of range expansion of various sessile

organisms in North Wales (Rees and Southward 2009). Considering that plastic

debris with Korean alphabet is occasionally found close to the Pacific coast in Iwate

Prefecture, floating objects such as aquaculture buoys may act as a vector for this

barnacle from the Japan Sea side to the Pacific side. However, it has never reported

that this species had settled on such plastic debris to the present. Thus, another

human-mediated introduction of P. perforatus seems to be much more probable.

Many barges and tugboats came into Iwate Prefecture from various localities in

Japan from Hokkaido in the north to Kagoshima in the south for reconstruction of

harbors and shore areas that were damaged heavily by the earthquake and tsunami

in 2011. Furthermore, in 2013, we found several individual P. perforatus (about

10 mm diameter) on the hull and fenders of a barge that was registered in Niigata, a

city faced to Japan Sea, and anchored at Ofunato near Sakihama (Kado personal

observation). These results may indicate that the barges and tugboats with home

ports on the Japan Sea may have aided the range expansion of this barnacle.

Although the possibility should be examined by genetic analysis like as the case of

Balanus glandula (Geller et al. 2008; Kado 2003b; Kado and Nanba 2006), we need

to consider that these boats may have already accelerated further expansion of this

barnacle in various localities in Japan when they terminate their mission and return

to the home harbors where Balanus glandula were not distributed.

Acknowledgements We express our appreciation to the following graduate and undergraduate

students for their assistance to this research: H. Hamaguchi, T. Kimura, A. Sakai, H. Ozasa,

F. Yoshida, S. Nagano, T. Tsuji, Y. Abe, and H. Arai. We also express our thanks to the two editors

and Dr. C. Norman who checks English text and gave some valuable comments. This research was

supported by Grant-in-Aid for Scientific Research (C) (Grant No. 16580276, 24580279) and

Tohoku Ecosystem-Associated Marine Sciences (TEAMS) of the Ministry of Education, Culture,

Sports, Science and Technology Japan.



References

Choi KH, Choi HW, Kim IH, Hong JS (2013) Predicting the invasion pathway of Balanus perforatus in Korean seawaters. Ocean Polar Res 35:63–68

Fujiwara T (2008) 3.4 Sanriku coast/ Iwate Prefecture, chapter 3. Sea urchin barren in Japan. In:

Fujita D, Machiguchi Y, Kuwahara H (eds) Recovery from urchin barrens – ecology, fishery

and utilization of sea urchins. Seizando-Shoten, Tokyo, pp 39–43 (in Japanese)

Geller J, Sotka EE, Kado R, Palumbi SR, Schwindt E (2008) Sources of invasions of a northeastern

Pacific acorn barnacle, Balanus glandula Darwin 1854 in Japan and Argentina. Mar Ecol Prog

Ser 358:211–218

Herbert RJH, Hawkins SJ, Sheader M, Southward AJ (2003) Range expansion and reproduction of

the barnacle Balanus perforatus in the eastern English Channel. J Mar Biol Ass UK 83:73–82

Kado R (2003a) Recruitment of thatched barnacle Semibalanus cariosus and concerning environmental factors. Sessile Org 20:63–68 (in Japanese)

Kado R (2003b) Invasion of Japanese shores by the NE Pacific barnacle Balanus glandula and its

ecological impacts. Mar Ecol Prog Ser 249:199–206



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Kado R (2006) Life cycle of barnacles and ecology of its early stage – how they live and how to

reach appropriate site for settlement. In: Sessile Organisms Society of Japan (ed) Newest studies of Cirripedia – the relationship between barnacles and human. Koseisha Kouseikakku,

Tokyo, pp 93–111 (in Japanese)

Kado R, Hayakawa Y, Hayashizaki K, Nanba N, Ogawa H, Okano K (2002) Spatial distribution

and abundance of barnacle larvae in Okkirai Bay, northeast Honshu, Japan, a case study of

Semibalanus cariosus (Pallas). Fish Sci 68(1):405–408

Kado R, Nanba N (2006) Balanus glandula: a new alien species from the west coast of North

America, established on the northeast coast of Japan. In: Koike F, Clout MN, Kawamichi M,

De Poorter M, Iwatsuki K (eds) Assessment and control of biological invasion risks, Shoukadoh

Book Sellers, /World Conservation Union. IUCNa9, Kyoto/Gland, pp 210–211

Kawamura T, Tamaki H, Hayakawa J, Won NI, Muraoka D, Kurita Y (2014) Changes in abalone

and sea urchin populations in rocky reef ecosystems on the Sanriku coast damaged by the massive tsunami and other environmental changes associated with the Great East Japan Earthquake

in 2011. Glob Environ Res 18:47–56

Newman WA, Abbott DP (1980) Cirripedia: the barnacles. In: Morris RH, Abbott DP, Haderlie EC

(eds) Intertidal invertebrates of California. Stanford University Press, Stanford, pp 504–535

Nogata Y, Yoshimura E, Sato K, Kado R, Okano K (2015) The first find of invasive alien barnacle

Perforatus perforatus in Japan and the development of a detection method using real-time

PCR. Sessile Org 32:1–6 (in Japanese with English abstract)

Raffaelli D, Hawkins SJ (1996) Intertidal ecology. Kluwer Academic Publishers, Dordrecht/

Boston/London

Rees EIS, Southward AJ (2009) Plastic flotsam as an agent for dispersal of Perforatus perforatus

(Cirripedia: Balanidae). Mar Biodivers Rec 2:1–3

World Sea Temperatures (a) http://www.seatemperature.org/asia/japan/kamaishi-october.htm

World Sea Temperatures (b) http://www.seatemperature.org/europe/united-kingdom/brightonoctober.htm



Chapter 3



Rocky Intertidal Zonation: Impacts

and Recovery from the Great East Japan

Earthquake

Takashi Noda, Aiko Iwasaki, and Keiichi Fukaya



Abstract We assessed the course and status of the recovery of rocky intertidal

zonation after the Great East Japan Earthquake by conducting a census of the vertical distribution of 11 dominant macrobenthos (7 sessile and 4 mobile species)

around the mid-tidal elevation at 23 sites along the Sanriku Coast, 150–160 km

north-northwest of the epicenter of the earthquake. Sites were observed from 2011

to 2013, and the vertical distributions of each species were compared with those

from the pre-earthquake period. Our results show that the earthquake considerably

altered rocky intertidal zonation, mainly through coseismic subsidence rather than

by the subsequent tsunami. By 28 months after the earthquake, the zonation of latesuccessional sessile taxa had not recovered, suggesting that the rocky intertidal

community will experience a long delay before recovering from the influence of the

earthquake. The dynamics of rocky intertidal zonation after the earthquake and

accompanying subsidence includes two unique features: a delayed negative impact

and an occasional increase in population sizes of several taxa. Neither of which has

been reported following earthquakes of similar magnitude with accompanying

uplift, in which there were mass mortalities of zone-forming species within 1 year

after the event, preceding downward shifts in their zonations.

Keywords Benthos • Distribution • Disturbance • Earthquake • Rocky intertidal •

Seaweed • Subsidence • Succession • Tsunami • Zonation



T. Noda (*) • A. Iwasaki

Faculty of Environmental Earth Science, Hokkaido University, Sapporo, Hokkaido, Japan

e-mail: noda@ees.hokudai.ac.jp

K. Fukaya

The Institute of Statistical Mathematics, Tachikawa, Tokyo, Japan

© Springer Japan 2016

J. Urabe, T. Nakashizuka (eds.), Ecological Impacts of Tsunamis on Coastal

Ecosystems, Ecological Research Monographs,

DOI 10.1007/978-4-431-56448-5_3



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26



3.1



T. Noda et al.



Introduction



The Great East Japan Earthquake (Mw 9.0) caused a large tsunami, with run-up

heights exceeding 30 m and subsidence of 35–70 cm throughout the Tohoku region

(Lay and Kanamori 2011; Tajima et al. 2013). There is no doubt that the tsunami

had great potential to affect a variety of marine benthos. This is because tsunami

waves can transport benthos away from their original habitats (Castilla 1988;

Castilla et al. 2010; Whanpetch et al. 2010; Lomovasky et al. 2011; Takami et al.

2013) and often severely damage benthic habitats, such as seagrass beds (Whanpetch

et al. 2010) and coral reefs (Chavanich et al. 2005; Campbell et al. 2007), by removing and redepositing coastal substrata at large spatial scales (Lomovasky et al.

2011). In contrast to the widespread impact of a tsunami on various organisms living in diverse habitats, a subsidence of several tens centimeters should affect relatively few species living in specific habitats, such as the intertidal rocky shore. In

particular, sessile species living in this habitat, whose distributions are often

restricted to within a narrow vertical range of several tens of centimeters (Stephenson

and Stephenson 1972), might be quite sensitive to land-level changes caused by an

earthquake. Indeed, previous studies have demonstrated that earthquake-related

uplifts caused mass mortalities of various sessile species and consequently altered

rocky intertidal communities at regional scales (Haven 1972; Johansen 1972; Bodin

and Klinger 1986; Castilla 1988; Castilla et al. 2010).

In rocky intertidal habitats, zonation (Fig. 3.1) is the most general spatial distribution pattern of organisms (Stephenson and Stephenson 1972). A mega-earthquake

would immediately alter the zonation of each species through the direct effect of the

tsunami and subsidence; thereafter, there could be additional changes in zonation

via modification of population processes after the earthquake, such as mortality and

recruitment. In addition, the immediate impacts of the earthquake and subsequent

changes in zonation should vary among species. Although Castilla (1988) described

the impact and recovery of rocky intertidal zonation from the uplift associated with

a megaquake for a single sessile species, there are no studies yet concerning the

impact and recovery from an earthquake and associated subsidence except for several qualitative evaluations of changes in vertical position of zones (Haven 1972;

Johansen 1972).

Long-term community census data from before the event provide a unique

opportunity to evaluate the community impacts and recovery from the rare disturbance event (Parker and Wiens 2005). For 8 years before the 2011 Tohoku earthquake, we regularly carried out censuses of the distribution and abundance of rocky

intertidal organisms at 23 sites on five shores close to the epicenter (Okuda et al.

2004; Nakaoka et al. 2006; Fukaya et al. 2010; Munroe and Noda 2010). To assess

the impacts and recovery from the earthquake, we have been continuing the surveys

using the same methods at the same places after the earthquake, so as to compare

the post-earthquake results with the data collected before the event. To our knowledge this is a unique example of research on the zonation dynamics of rocky intertidal organisms encompassing periods before and after a megaquake. Here we report



3



Rocky Intertidal Zonation: Impacts and Recovery from the Great East Japan…



27



Fig. 3.1 Photograph of rocky intertidal zonation in a study site (Myojin). Horizontal bands with

different color are dominated by different sessile organisms



the course and status of recovery of the vertical distribution of 11 dominant rocky

intertidal macrobenthos (seven sessile and four mobile species) in the mid-shore of

23 sites located 150–160 km north-northwest of the epicenter of the 2011 Tohoku

earthquake. We compare the vertical gradients of abundance of each species 4, 16,

and 28 months after the megaquake with those obtained before the earthquake

(2003–2010).



3.2

3.2.1



Materials and Methods

Census Design



Rocky intertidal zonation was monitored at 23 sites along five shores located 150–

160 km north-northwest of the epicenter (38°06′12.0″N, 142°51′36.0″E) of the

2011 Tohoku earthquake (Fig. 3.2). For each shore, four or five sites were haphazardly chosen from semi-exposed locations. At each site a permanent plot (50 cm

horizontally by 100 cm vertically, centered at mid-tide) was marked with plastic

anchors drilled into roughly vertical rock delimiting the study area. The vertical

extent of the permanent plots covered 72.4 % of the tidal range. In March 2011,



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