"Sea Urchin Barren": Urgent Need for Planning and Management at Xiaoliuqiu's Duzaiping Intertidal Zone

The Editor says: Did you know that the humble sea urchin is actually a vital herbivore on coral reefs? In certain ecosystems, it plays a crucial role in maintaining the balance between coral and algae, contributing enormously to reef health. A research team from National Sun Yat-sen University conducted a year-long survey on Xiaoliuqiu and discovered what may be Taiwan's very first "sea urchin barren." How did it come to this? Read on with the Editor to find out. Full article reprinted from: "Sea Urchin Barren": Urgent Need for Planning and Management at Xiaoliuqiu's Duzaiping Intertidal Zone — Conservation Management and Research Recommendations Co-submitted by National Sun Yat-sen University and Local Operators, by Zhang Shuikuai, Qiu Xunwen, Chen Yingzhu, and Liu Lilian.

In August 2020, China Times reported: "Sea urchins invade Xiaoliuqiu — the seafloor is blanketed with sea urchins, leaving almost no room to stand" (UDN, 2020; China Times, 2020). Photos showing a dense carpet of sea urchins drew widespread public attention. Coincidentally, after a year of surveys, a research team from National Sun Yat-sen University found not only that the density of marine organisms in the Duzaiping intertidal zone on Xiaoliuqiu had fallen dramatically compared to the past, but also that Taiwan's first "sea urchin barren" [1,2] may have already emerged there. Across the intertidal reef platform, all one could see were sea urchins and pockmarked rock surfaces gnawed to tatters.

The Duzaiping intertidal zone was designated as the Liuqiu Fishery Resource Conservation Area in 2000 and as a Natural and Cultural Ecological Landscape Area in 2015, owing to its rich marine life and distinctive coral reef topography. It is an important conservation site for marine benthic organisms and a popular destination where intertidal tour guides introduce visitors to intertidal life. In 2019, the zone was being considered for designation as a conservation demonstration area — a year-round no-entry seed-stock reserve [3] — but the proposal was put on hold pending the collection of scientific data to support management decisions. The Pingtung County Government subsequently secured funding through the Ocean Affairs Council to commission a National Sun Yat-sen University research team in 2020 to conduct a survey of the major intertidal benthic organisms on Xiaoliuqiu and to facilitate planning and consultation on management measures. Dr. Chao Shih-min of the National Museum of Natural Science was also invited to serve as an advisor on sea urchin issues.

Habitat Degradation in the Duzaiping Intertidal Zone on Xiaoliuqiu

According to early photographs taken by local guides and accounts from long-time residents, the reef platform at Duzaiping once had a healthy substrate supporting extensive seagrass beds of Thalassia hemprichii, teeming with marine life. Comparing photographs from July 2003 and January 2021, however, the intertidal reef environment had changed dramatically over those 17 years. The Thalassia meadows are now only seen in scattered patches, replaced by bare, jagged, uneven reef rock and vast numbers of sea urchins that continuously gnaw at the reef. The overall ecological and environmental quality has visibly declined.

潮間帶 — Changes to the ecological environment at Duzaiping: the *Thalassia hemprichii* seagrass beds have been replaced by pockmarked reef rock. July 2003, courtesy of Wang Tianzheng.

Changes to the ecological environment at Duzaiping: the *Thalassia hemprichii* seagrass beds have been replaced by pockmarked reef rock. January 2021, courtesy of the NSYSU research team.

Moreover, when the density of benthic organisms was compared to survey results from the same area five years earlier, the density of benthic invertebrates of comparable size (>2 cm) (individuals/m²) dropped from 95.5 (n=9, 2013 and 2014) to 19.4 (n=4, 2020) — a decline of nearly 80% — while the species richness index also fell by 89%. In terms of species composition, compared to research conducted a decade earlier, the dominant species in 2011 was the large Ophiocoma scolopendrina (a brittle star that hides in crevices and hollows), accounting for 68% of individuals. Today, the community is dominated by small (<2 cm) Ophiocoma brevipes. Meanwhile, sea urchins, which previously accounted for 21%, now make up 52%, with Echinometra mathaei being the most abundant, followed by Stomopneustes variolaris. Sea cucumbers also constitute a notably high proportion (39%), possibly because the increase in sea urchins generates more biodetritus, providing sea cucumbers with an ample food supply and enabling their numbers to grow.

The sandy fecal pellets left by sea urchins after feeding still contain abundant organic matter, making them an important food resource for sea cucumbers. The black sea cucumber pictured here is using its tentacles to gather organic particles from the substrate. Photo courtesy of the NSYSU research team, taken January 2021.

A Sea Urchin Barren Blanketed by Sea Urchins

Just how many sea urchins are there at Duzaiping? By combining field surveys with sea urchin distribution data provided by local tour operators, the research team first calculated the area of the mid-tidal zone where sea urchins were densely concentrated, then used drone imagery to analyze and calculate sea urchin numbers per unit area. Based on this, the team estimates that the number of sea urchins in the mid-tidal zone is approximately 800,000 to 1,000,000 — or possibly even more.

In coral reef ecosystems, algae and coral populations compete for habitat, while sea urchins play the role of herbivores. By grazing on algae, sea urchins free up space for coral growth, so a moderate sea urchin population can help promote the development of coral reef ecosystems. However, once the sea urchin population expands out of control, the original seagrass/macro-algae habitat is destroyed by high-density grazing. Seagrass and macroalgae are important primary producers in tropical and temperate waters, and these habitats also serve as natural nurseries, feeding grounds, and refuges from predators for many marine fish and invertebrates. When the primary producers and habitat of an ecosystem disappear, the marine life that depends on them vanishes as well, leaving behind nothing but reef rock and sea urchins. This state is known in the scientific community as a "sea urchin barren" [4,5]. Without timely intervention, the habitat will continue to degrade under relentless sea urchin grazing until only lifeless bare rock remains.

Today, Duzaiping has already reached the state of a sea urchin barren, with enormous numbers of sea urchins in the mid- and low-tidal zones. The most abundant species, Echinometra mathaei, uses its mouthparts and spines to bore holes in the reef, sheltering inside to evade predators while feeding on algal fragments and organic detritus carried in by waves, as well as scraping epilithic algae from the walls of its burrow. This continuous, year-round boring and scraping is the primary cause of the rough, jagged, pockmarked appearance of the reef rock. Although the pits and holes do provide hiding places for small animals, rock that has been excessively eroded by sea urchins becomes structurally weakened and far more susceptible to fragmentation from wave action and human trampling — leaving the sea urchins themselves without adequate shelter and resulting in vast numbers of sea urchins exposed on the open reef surface.

In today's Duzaiping intertidal zone, enormous numbers of *Echinometra mathaei* can be observed in the mid- and low-tidal zones. Photo courtesy of the NSYSU research team, taken January 2021.

A sea urchin barren blanketed by sea urchins. The dark spots in the photograph are all sea urchins; some are also hidden inside reef cavities. Photo credit: Cai Zhengnan (drone photograph taken November 2020).

Possible Causes of the Sea Urchin Barren

Because ecological survey data for Duzaiping from the past is scarce and incomplete, it is difficult to pinpoint the causes of the current situation with certainty. After reviewing international literature and consulting with sea urchin specialists and local operators, the research team identified a combination of possible natural factors — including typhoons and climate change — as well as the following human-induced factors.

Uncontrolled sea urchin population growth has been documented in numerous locations around the world. Scientists consider the primary drivers of sea urchin barrens to be overfishing leading to the disappearance of sea urchin predators, and excess organic nutrients stimulating the growth of sea urchin food sources. Sea urchins have numerous natural predators, including certain species of lobster, crab, fish (such as various balistid triggerfishes, some filefish, and wrasse), and gastropods (such as triton shells and frog shells). Long-time residents of Xiaoliuqiu, who have historically relied on the sea for their livelihoods, continue to do so today — some residents still go to the intertidal zone at low tide to collect shellfish and gastropods, or fish and catch marine animals along the shore. These activities have not only gradually depleted Xiaoliuqiu's marine biodiversity, but have also eliminated the sea urchin's natural predators, allowing Echinometra mathaei — which has no commercial value — to proliferate unchecked and devastate the reef platform.

Before 2008, when tourism was not yet widespread, the number of passengers taking ferries to Xiaoliuqiu from Donggang was under 500,000 per year. In recent years, with the boom in tourism, the number of passengers arriving by ferry in 2019 reached approximately 1,500,000 (Tourism Bureau website), from which the actual number of tourists is estimated at around 1,000,000. The volume of domestic wastewater generated on the island by this tourist influx is not to be underestimated. Although wastewater treatment facilities exist, they cannot accommodate all the rapidly proliferating guesthouses, and a large amount of domestic wastewater still flows directly into the sea or the intertidal zone. This causes eutrophication of coastal waters, excessive algal growth, and ocean acidification — altering the biological composition of surrounding waters while simultaneously accelerating the rate at which sea urchins erode the coral reef. Additionally, in 2019, the total number of tourists entering the intertidal zones at Shanfu, Yucheng Wei, and Duzaiping on Xiaoliuqiu was approximately 152,000 (Pingtung County Government statistics). The trampling and handling of organisms by excessive numbers of tourists in the intertidal zone is also accelerating the disappearance of marine life and the destruction of the fragile reef platform.

The number of visitors to Xiaoliuqiu has been rising year on year, placing excessive strain on the marine ecological environment. The upper photos show a bag of trochus and turban shell remains discarded in the intertidal zone by visitors in 2020; the lower photos show wastewater pools near the Shanfu and Duzaiping intertidal zones. Courtesy of Liu Lilian.

Industry, Government, and Academia Join Hands to Reverse the "Sea Urchin Barren"

Based on the current survey findings, it is clear that the coral reef ecosystem of the Duzaiping intertidal zone has been gradually losing its functional integrity and is no longer fulfilling the original intent of the "Fishery Resource Conservation Area" and "Natural and Cultural Ecological Landscape Area" designations — namely, to protect natural landscapes and conserve biodiversity. Because the sea urchin surplus is not entirely the result of natural ecosystem fluctuations, but is largely linked to excessive human disturbance — including overharvesting of sea urchin predators, eutrophication caused by wastewater discharge, and physical damage from excessive tourist trampling — action must be taken to change the current situation.

The research team and local tour operators jointly discussed how to reverse the "sea urchin barren." The following management recommendations are offered for reference by relevant authorities:

The decline in sea urchin predators: It is recommended that residents and anglers be educated about restrictions on harvesting the primary predators of sea urchins; consideration should also be given to listing these species as protected organisms prohibited from capture under relevant legislation.
Wastewater discharge: It is recommended that the sewage system and wastewater treatment facilities be reviewed to ensure that all wastewater is properly treated before being discharged into the ocean.
Human trampling: It is recommended that the number of visitors entering the intertidal zone at any given time be limited (e.g., a cap of 300 people), and that a "core conservation zone" be designated within the Duzaiping intertidal zone to protect organisms in that area from disturbance and to facilitate ecological restoration. An eco-tour route should also be established within the zone to restrict the area over which visitors can walk.
Sea urchin overabundance: It is recommended that sea urchin removal be carried out by human intervention, following practices adopted overseas. As no relevant research has been conducted domestically, the required removal quantity and methods needed to effectively reverse the sea urchin barren phenomenon are not yet established. It is therefore recommended to first conduct a literature review and a small-scale removal trial, monitoring biodiversity and the rate of ecosystem recovery within the removal area to assess effectiveness, which will then serve as the evidence base for action to reverse the "sea urchin barren." The Pingtung County Government has agreed to take these recommendations into consideration in promoting ecological restoration of the Duzaiping intertidal zone.

References:

[1] K. Filbee-Dexter, R.E. Scheibling, Sea urchin barrens as alternative stable states of collapsed kelp ecosystems, Mar. Ecol. Prog. Ser. 495 (2014) 1–25. https://doi.org/10.3354/meps10573.
[2] D.R. Bellwood, T.P. Hughes, C. Folke, M. Nyström, Confronting the coral reef crisis, Nature. 429 (2004) 827–833. https://doi.org/10.1038/nature02691.
[3] Zhang Shuikuai, Chen Yingzhu, Xiaoliuqiu's Intertidal Zone "Trampled" by Tourism — Conservation Area Management Framework Needs Strengthening, Taiwan Environmental Information Association — Environmental Information Center. (2020). https://e-info.org.tw/node/223328 (accessed March 29, 2020).
[4] J. Pearse, C. M.E., D. Leighton, M. C.T., N. W.J., Marine waste disposal and sea urchin ecology, in: W.J. North (Ed.), Kelp Habitat Improvement Project, California Annual Report, 1969 to 1970., California Institute of Technology, Pasadena, CA, 1970: pp. 1–93.
[5] C. Birkeland, The influence of echinoderms on coral-reef communities, Echinoderm Studies. 3 (1989) 1–79.
Zhang Shuikuai, Qiu Xunwen, Chen Yingzhu, Liu Lilian. 2021. Duzaiping Intertidal Zone on Xiaoliuqiu Has Become Taiwan's First "Sea Urchin Barren". Environmental Information Center, 2021/2/18.

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