High water temperature and feeding damage by fish vs construction of seaweed beds! Seaweed bed restoration suitable for the region

Nagasaki Prefecture, locating in the northwest Kyushu, stretches in the north-south direction and has complicated coastlines with many islands, peninsulas, bays and coves. Around the prefecture are water systems, such as Tsushima warm current, Yellow Sea cold water and Kyushu West coastal water. Thanks to them, a wide variety of seaweeds inhabit the region and there are many seaweed beds across the prefecture. Particularly, Eisenia bicyclis and Ecklonia cava beds form very good fishery areas rich in rocky shore resources. The catch of abalones used to be the largest in the country (statistics by the Ministry of Agriculture, Forestry and Fisheries). However, due to a rise in water temperature, feeding damage by herbivorous fish has increased. Since the late 1990s, the seaweed beds have been decreasing more rapidly than ever and rocky shore denudation has been spreading. Eisenia bicyclis and Ecklonia cava beds are particularly decreasing and the impact on abalones and other rocky shore resources is getting more and more serious. We interviewed Takanari Kiriyama, Director of the Shellfish and Seaweed Department, the Seed Mass-production Technology Development Center, the Nagasaki Prefectural Institute of Fisheries (hereinafter referred to as the institute), which is exploring the actual changes in seaweed beds and tackling the construction of new seaweed beds adaptable to changes in the environment due to climate change to restore lost seaweed beds.

Seaweed beds essential to biodiversity in the sea

Please talk about the role of seaweed beds and the current situation.

Seaweed beds play a role in biological production and the environment conservation. They are also essential to the maintenance of biodiversity. Seaweed beds attract fish and shellfish as places for spawning, rearing of young and feeding and serve as fisheries. Especially, Eisenia bicyclis and Ecklonia cava beds abound with rocky shore resources, such as abalones, sea urchins and turban shells, and they are the most important fisheries for inshore fishing.

Many seaweed beds are formed at the depth of around 5 m off the shores of Nagasaki Prefecture. In some areas, seaweed beds are found at the depth of 20 m.

For the past 20 years, the distribution of seaweed beds and time of their formation have greatly changed. The “four-season seaweed beds,” where large brown algae once commonly seen off the shores of Nagasaki Prefecture, such as Eisenia bicyclis, Ecklonia cava (Figure 1) and Sargassum flourish throughout the year, are decreasing and rocky shore denudation is expanding. In contrast to that, “spring seaweed beds” (flourishing only in spring and early summer) of southern Sargassum, once seen only at the southern edge of the prefecture, are now found across the prefecture.

One of the causes of those changes is (1) the feeding damage by herbivorous fish, which has posed little problem before, because of a rise in water temperature (Figure 2) due to climate change. It is considered that the balance between the browsing pressure of fish and the growth of seaweeds is disrupted, that the species of seaweeds reproducible under the current environment have survived and that unadaptable species have dwindled or died. The other cause is (2) a rise in water temperature exceeding the upper limit of the growth temperature of seaweeds. According to a report by the Fukuoka Regional Headquarters, JMA, the sea surface temperature was around 30℃ around the Kyushu area and Yamaguchi Prefecture in August 2013, which was the highest water temperature since 1985. The temperature exceeded the upper limits of the growth temperature of Eisenia bicyclis and Ecklonia kurome of 29℃ and 28℃, respectively. Because of the high water temperature, a large quantity of Eisenia bicyclis and Ecklonia cava were cut at the end of stipes and washed ashore in a broad range from Nagasaki to Fukuoka and to Yamaguchi Prefectures. That was an unprecedented phenomenon. In Nagasaki Prefecture, a similar loss of Eisenia bicyclis and Ecklonia cava due to high water temperatures occurred in August 2016. Eisenia bicyclis and Ecklonia cava that remained in the beds suffered feeding damage (1) above in autumn and early winter, which added to the damage. Eisenia bicyclis and Ecklonia cava has been rapidly dwindling or dying for the past five years.

Nagasaki boasts the second largest catches among the prefectures. How important are seaweed beds to fisheries production?

As to the role of seaweed beds, the revised Guidelines on Rocky Shore Denudation Prevention (Fisheries Agency in 2015) state its importance. The guidelines say that a seaweed bed “serves as a place of primary production in coastal waters, has ecologically important functions as a place of the environment conservation and provides a habitat for fish and shellfish useful for the fisheries industry and other various life.”

The output of the marine fisheries of Nagasaki Prefecture was the second largest in the country in 2015. It was about 300,000 tons and fishes, such as sardines, Japanese horse mackerel and mackerel, accounted for more than 90% (statistics by the Ministry of Agriculture, Forestry and Fisheries). The catches of rocky shore resources closely related to seaweed beds are very small compared with those of fish but Nagasaki Prefecture is one of Japan’s major producers of abalones, sea urchins and turban shells. Their catches are the fifth, fourth and first largest in the country, respectively. That suggests the importance of seaweed beds, especially those of Eisenia bicyclis and Ecklonia cava. Seaweed beds are playing a key role in our prefecture’s fisheries industry. A decrease in the seaweed beds is considered to impair their functions and directly and indirectly affect the fisheries production in the short term and the long term.

In 1998, unprecedented changes happened in the sea.

When was climate change impact on seaweed beds observed first in Nagasaki Prefecture?

In 1998, various abnormal phenomena in large brown seaweeds that had been never seen before were observed.

In Nagasaki Prefecture, hijiki seaweeds (Hizikia fusiformis) inhabit the coastal areas across the prefecture. Nagasaki used to be the largest hijiki producer in the country (statistics by the Ministry of Agriculture, Forestry and Fisheries). In 1998, the growth of hijiki was slow in season in spring. In the worst case, a “stunting” phenomenon occurred. Hijiki was stunted and too short to harvest. In autumn and early winter, a phenomenon called “missing blades” happened. Eisenia bicyclis and Ecklonia cava lacked blades. In some cases, only the stipes stood. From that appearance, the phenomenon was also called “standing dead.” As to farmed wakame seaweeds, young wakame did not grow properly all along the coast of the Shimabara peninsula in the Ariake Sea, the prefecture’s major place of production, in autumn and early winter when farming was started. In the worst case, a “stunting” phenomenon occurred and wakame seaweeds were not left to harvest in the farms.

Those abnormal phenomena of large brown seaweeds have never been reported and became a problem. The institute conducted studies to grasp the situation and identify the cause. As a result, we found that the cause was feeding damage by herbivorous fishes, such as mottled spinefoot, brown chub and Japanese parrotfish (Figure 3), which had not been seen as a problem before. According to a report by the Japan Meteorological Agency, the largest-scale El Nino phenomenon occurred in 1997 and 1998. The annual average sea surface temperatures in the Kyushu and Okinawa waters were record highs. Mottled spinefoot, brown chub and Japanese parrotfish had inhabited the coastal waters of Nagasaki Prefecture from a long time ago. As the water temperature falls from autumn to winter, they are feeding less and less and they hardly feed in winter. The unusually high water temperature was considered to delay a temperature fall, make their feeding activity long and active and lead to the abnormal phenomena of the large brown seaweeds. Since then, the water temperatures have remained high. Those phenomena due to feeding damage by fish now occur every year.

I see. The decrease in Eisenia bicyclis and Ecklonia cava in and after 1998 was caused by an increasing browsing pressure of herbivorous fish due to a rise in seawater temperature. What measures did the institute take against the effect?

The most seaweed beds developed in Nagasaki Prefecture have been Eisenia bicyclis and Ecklonia cava beds abalones and other creatures feed on. In the conventional method, a seaweed bed was developed by removing a large quantity of sea urchins and sea snails that would hinder the recovery of the bed and placing the mother algae of Eisenia bicyclis and Ecklonia cava to supply seeds artificially. In addition to the conventional method of seaweed bed construction, the necessity of feeding damage prevention arose. We worked on the development of technology to protect seaweeds from feeding damage by fish, capture technology to eliminate fish and technology to make the most of the fish for promotion of their capture. Unfortunately, developed technologies have never been put into practice. There are no effective measures against feeding damage by fish. A measure taken at the moment is to cover seaweeds with a net for protection. This measure needs a lot of improvements. For instance, the net is not durable enough, it is easily covered with deposits and it only protects a small area.

We also identified trends of change in seaweed beds and grouped the inhabitant seaweeds based on the past research. We have divided them into three groups, species that dwindled or died (lost species), species without any change (maintained species) and species with their habitat expanding (new species). Eisenia bicyclis and Ecklonia cava are lost species. Sargassum species, particularly southern Sargassum, are more likely to survive than Eisenia bicyclis and Ecklonia cava.

We thought, if we grasped the extent of browsing pressure of fish in each fishery and used “maintained species” and “new species” of each fishery as the target species according to the extent, we would be able to develop a seaweed bed simply by removing sea urchins and snails and supplying seaweed seeds as before without any measure against feeding damage. In other words, we launched “new seaweed bed construction adaptable to changing environment” to change the conventional target species of Eisenia bicyclis and Ecklonia cava to Sargassum (native species) or to southern Sargassum species according to the extent of browsing pressure of fish. After a small-scale verification test in 2008 to 2010, we verified practical development of a 1-ha seaweed bed in 2011 to 2015. Those studies have confirmed that seaweed beds can be developed in the current environment.

Why are Sargassum species more resilient than Eisenia bicyclis and Ecklonia cava?

Even if Eisenia bicyclis, Ecklonia cava and Sargassum species sustain feeding damage by fish and the alga bodies are partly bitten off, they can regenerate provided the meristems are left intact. The meristems of Eisenia bicyclis and Ecklonia cava are located at blade bases on branches. If only stipes and roots (holdfasts) are left, the seaweed will die. The seaweed cannot be reproduced unless seeds are released and the next generation young seaweeds grow and mature. Feeding damage by fish increases in autumn and early winter when Eisenia bicyclis and Ecklonia cava mature. That hinders supply of seeds and leads to a decline in the next generations. As this cycle is repeated every year, the seaweed can no longer reproduce and it is lost eventually. The process of dwindling and dying have been confirmed by the monitoring of Ecklonia kurome communities. Adult Ecklonia kurome dwindled or died due to feeding damage in autumn and early winter. In winter to spring, new year-classes grew. At first, they grew to three to five year-classes. They gradually got younger and younger to one to two year-classes, to zero to one year-classes and eventually gone.

Sargassum species grows many branches from the main branch. Even if a branch is shortened due to feeding damage, it regenerates from the tip. Some species can regenerate even if only the root (holdfast) is left. Especially, in the case of southern species, after the seaweed grows to the largest in summer, all the main branches die and flow away. In the case of other Sargassum species, some main branches die after maturity but not all of them flow away and new main branches are already growing. Southern Sargassum species survive as the holdfasts only in late summer to early winter when the browsing pressure of fish is strong. They start to grow in winter when the browsing pressure is reduced. These ecological characteristics make their reproduction possible even in a place where the browsing pressure of fish is strong. Sargassum species can also travel in a broad range of area by drifting on the sea surface after they have grown and matured and therefore they can supply seeds in a wider range than Eisenia bicyclis and Ecklonia cava. In addition, they have many advantages in reproduction, for instance, they greatly vary in species and the time of maturity.

Selecting suitable seaweeds for each area to increase them

Southern species grow when fish becomes less active to preserve seeds. How are you utilizing that?

At the moment, there are no effective measures against feeding damage by fish for the construction of seaweed beds. I have explained that selecting more potential species as the target to grow according to the extent of feeding damage of each area is an indirect but effective measure against feeding damage.

When it is difficult to grow Eisenia bicyclis, Ecklonia cava and many native Sargassum species without direct measures against feeding damage due to severe feeding damage, we use southern Sargassum as one of effective target species for the fishery area.

In Nagasaki Prefecture, eight southern Sargassum species are confirmed to inhabit the coastal waters. Those species differ in habitat (inner bay or open sea and depth), bottom sediment and other ecological characteristics. We choose among those southern Sargassum species the most suitable species for the conditions of a fishery area to develop.

Why do you use southern species not developing a new species?

In developing a seaweed bed, the target species to grow must be the most suitable species for the environment of the fishery area to develop. We use southern species because it is confirmed that the habitat range has naturally expanded with changes in the fishery environment and settled. That means the species is adaptable to the current environment change. In some areas of the prefecture, including Omura Bay, the inhabitation of southern Sargassum has not been confirmed yet. We do not introduce southern Sargassum to such areas. Introducing a new species from another area or using an improved species by selective breeding means human intervention on the natural environment. That can affect the ecological balance and biodiversity. Unless there is evidence to deny the possibility, we believe we must try to use the existing species for the construction of seaweed beds.

Cooperation with the local fisheries operators and a shift to new businesses adaptable to climate change

I imagine you have had a hard time increasing abalone producers’ understanding about ocean environment change. What did they think about it?

After 1998 when the stunting of hijiki, the missing blades of Eisenia bicyclis and Ecklonia cava and the stunting of farmed wakame occurred, those phenomena happened every year to a greater or lesser degree. There were growing concern and sense of crisis about the maintenance of seaweed beds and management of seaweed farming among fisheries operators. Still, they would not accept that the phenomena were caused by feeding damage by fish. To prove the feeding damage, we conducted an on-site experiment of seaweed protection with nets, a feeding test of Eisenia bicyclis and Sargassum in a tank and a survey of digestive tract contents of fish, and revealed the true situation. We compiled the “Guidelines on Rocky Shore Denudation Prevention in Nagasaki Prefecture” from the findings and tried to convey the information through study meetings and other occasions. Thanks to the accumulation of efforts, the fisheries operators accepted the fact of feeding damage by fish and began to adopt the capture by gillnetting and protection with nets as techniques for seaweed bed construction. We have also tried to develop measures against feeding damage by fish but effective and efficient technologies for protection and capture are yet to be developed. Although it was an indirect measure, a new seaweed bed construction technique to select the target species more likely to survive according to the extent of feeding damage gradually came to be implemented across the prefecture. The main target species have changed from Eisenia bicyclis and Ecklonia cava to Sargassum. It’s true that many fisheries operators are hoping for the recovery or an increase in the catches of abalones and thus there is a great demand for an increase in Eisenia bicyclis and Ecklonia cava. We are often asked about the feed efficiency of southern Sargassum for abalones. That demonstrates a keen interest.

Nagasaki Prefecture is long in a north-south direction and varies in sea area characteristics. In its coastal waters, Eisenia bicyclis and Ecklonia cava beds are still maintained in some areas. In the fishery areas dramatically changed as affected by feeding damage by fish due to climate change, Eisenia bicyclis and Ecklonia cava beds have changed to those with southern Sargassum flourishing only in spring to early summer, that is, the spring seaweed beds. These fishery areas can no longer provide abalones with sufficient feed throughout the year. In such areas, it is impossible to develop Eisenia bicyclis and Ecklonia cava beds without measures against feeding damage, including net covering to protect a wide area and therefore it is difficult to continue abalone fishery. The change in seaweed beds due to climate change is in a transition phase and we cannot tell how it will be in the future. We will continue to explore the actual situation of the seaweed beds and would like to think about the use of profitable rocky shore resource alternatives for abalones in the current fishery areas together with the fisheries operators.

What specific efforts were made in the field?

Nagasaki Prefecture is strengthening “seaweed bed monitoring team” of each fisheries cooperative as an organization and supporting their activities to tackle the construction of seaweed beds proactively together with public projects. The institute is organizing study meetings on seaweed bed construction and on-site technical training on the activities for the construction.

As a research topic, we are working on technology development for greater efficiency in seaweed bed construction and effective use as a fishery of the “spring seaweed beds” newly created due to climate change impacts. About southern Sargassum mainly constituting the spring seaweed beds, we have found out their distribution in the prefecture, their growth and maturity and obtained basic findings for using them as the target species to grow. We paid attention to small seaweeds distributed across the prefecture even under the current environment, we are examining them to find new target species and their effectiveness as feed for sea urchins. We are trying to develop the technology for utilizing purple sea urchins, which can be made meaty in a short time by the construction of spring seaweed beds and growth of small seaweeds, to balance an increase in income by capture of sea urchins with maintenance and management of seaweed beds.

Future challenges and outlooks after 20 years of monitoring of seawater temperature rises

How do you see medium- to long-term predictions of future impacts in relationship to future construction of seaweed beds?

It is difficult to predict how climate change impacts are going to change because of the complicated interaction with the environment and living things surrounding seaweed beds. If accurate medium- to long-term predictions of impacts are possible, the national and local governments can set out their strategies, goals to achieve will be clarified and well-planned efficient measures are expected to be developed, based on shared awareness of changing phenomena. It is desirable that the monitoring, essential to impact prediction, should be continued for a long time with more stationary observation points. In reality, the institute can barely continue even minimum monitoring because of a limited budget and manpower. The coasts of Nagasaki Prefecture consist of eight sea areas with different fishery environments particular to each area. To ensure accuracy, all the sea areas need to be monitored. The truth is, we haven’t been able to do that. I hope monitoring technology will be advanced and enhanced in efficiency in the future. Using the technology, I hope, a monitoring system covering various fishery environments not only in our prefecture but also in the entire country will be established and the information will be shared.

Climate change impacts on living things will influence the fisheries production and a situation might demand a shift from one target species to catch or way of doing a job to another. There is concern how many people can respond to the demand when the fisheries management base has weakened due to a number of problems, such as aging society, a shortage of successors and a decline in the catches. I hope medium- to long-term predictions of climate change impacts will include assessments of the distribution of marine life and impacts on the fisheries industry besides changes in climate and sea state. By doing that, I believe, the predictions will serve as a wake-up call to fisheries operators, heighten their awareness of the impacts on fisheries and a sense of urgency, and encourage development of far-sighted measures and well-planned adaptation.

I understand it is important to examine not only future impacts but also the consequent social changes. Please tell me what you find it rewarding to tackle the seaweed bed construction with the local fisheries operators and what you think the future outlooks will be?

I have been engaged in surveys and research on the construction of seaweed beds and I have worked with the fisheries operators most of the time. I worked by trial and error while listening to them. We shared good times and hard times together and built up trust between us. That is what I feel greatest joy. The bond is still liking us after the project has finished. It is a big asset to me working as prefectural government employee. I will continue to tackle the “development of seaweed bed construction technology as an adaptation measure against climate change” to help the effective use of spring seaweed beds as fishing grounds. I believe this research will contribute to the promotion of coastal fisheries.

Aging of fisheries operators and a shortage of successors are posing a serious problem on the construction, maintenance and management of seaweed beds. It is certain that the problem cannot be solved by fisheries operators alone. Seaweed beds are also used by the public for recreation and refreshing. To use seaweed beds for a long time, it is necessary to raise renewed public awareness of the importance of seaweed beds besides development of their construction technology. To that end, a public-participation activity for the construction and efforts to establish a management system will be needed.

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