Platax 20: 79-87, 2023
doi: 10.29926/platax.202312_18.0007

Mass mortality of the black sea cucumber Holothuria atra after
heavy rainfall at Hsiao Liouciou Island, Southern Taiwan
Shu-Yu Chao1, Li-Lian Liu2, Chen-Pan Liao3, and Shyh-Min Chao3*
1, 23

*

Department of Oceanography, National Sun Yat-sen University, Kaohsiung, Taiwan
National Museum of Natural Science, Taichung, Taiwan

Corresponding author. Email: chaosm@mail.nmns.edu.tw

Abstract
In August 2021, after 15 days of heavy rainfall, a mass mortality event of the common
black sea cucumber Holothuria atra was observed in the intertidal zone of "Duzaiping,"
Hsiao Liouciou Island, Southern Taiwan. The density of H. atra halved: from 5.60+1.42
m-2 individuals (mean±std.dev; n=20) in May of 2020 to 2.66+1.34 individuals m-2(mean±std.dev; n=5) in September of 2021. The total number dropped from 198,000 to94,000 across a 35,400 m2 study area (mortality rate=52.5%). We surmise that thecontinuous heavy rainfall, in addition to high temperatures during low tide, were the major
contributing factors that led to this sea cucumber die-off.
Keywords: Holothuria atra, marine ecology, mass mortality, rainfall, sea cucumber,
Taiwanmortality events of benthic marine species

Introductionthat had been documented across the globe

Mass mortality events have thebetween 2000 and 2013, and most of thosecapacity to drive persistent ecosystem

featuring echinoderms were reports of seachanges (Hughes, 1994). Reports of massurchins

mortalities of echinoderms have been

Strongylocentrotus

largely anecdotal, despite their worldwide

Diademaoccurrence, and such unfortunate events

Strongylocentrotus purpuratus) and sea

provide insight into the nature of thestars

impacts of both biotic and abiotic stressors

ochraceus). In this table, no large-scaleon echinoderm population biology anddeath of sea cucumbers was recorded. It

community ecology (McClintock et al.,can be seen that sea cucumbers rarely2018). Jurgens et al. (2015) tabulated mass

occur in large-scale death events. Disease79(Paracentrotus

lividus,droebachiensis,

mexicanum,(Leptasteriassp.

&&PisasterPlatax 20: 79-87, 2023
doi: 10.29926/platax.202312_18.0007

and high seawater temperatures werereproduces asexually and a large one

thought to be the major causes of many of(~>300 g) that appears to reproduce only

the documented die-offs, though low

sexually (Chao et al., 1993). Given its

salinity contributed to the decline of S.

abundance, it plays an important role inpurpuratus in Hendler (2013).

nutrient cycling on reefs and in theLawrence(1996)

reviewed

theintertidal zone (Bonham & Held, 1963).

abiotic factors that were responsible for

On August 18, 2021, after 15 days ofmass mortality of echinoderms, with nineheavy rainfall, we noticed numerous dead

identified: volcanic activity, earthquakes,

H. atra on the intertidal reef flat at Hsiao

storms (obrution, current and waves),

Liouciou Island, Southern Taiwan. In 2020,

temperature and desiccation, salinity,

we reported that this study site had thehypoxia, noxiousness from phytoplankton

highest density of H. atra in the world

toxins, ice, and pollutants. Of those driven(Chaoby low salinity, most were related toquantitatively characterize the decrease inriverine discharge, though heavy rains

both total number and density of thiswere to blame in some cases. In this review

common sea cucumber after this disaster.

etal.,2021).

Hereinwearticle, the mass deaths caused by reduced

Materials and methods

salinity are mostly sea urchins, but there

Theare also three species of sea cucumbers

locationandgeneralThyoneenvironmental characteristics of the study

aurea and Opheodesoma spectabilis).

site (Fig. 1) have been described by Chao

Decreased salinity from land runoff causes

et al. (2021). It is blocked by raisedmass

Opheodesoma

limestone rock at both ends forming aspectabilis on reef flats at Hawaii if itclosed intertidal zone with ca. 650 moccurs during low tide (Berrill, 1966).

coastline. The distance from high tide line

(Pentacucuma

spyridophora,mortalityofHolothuria atra is widely distributed

to low tide line is about 50 to 80 metersin the shallow waters of Indo-Western(Figure 1). It is a flat reef platform andPacific coral reefs and is the most common

contains many tide pools. The dominant

and abundant aspidochirotid holothurian

species are H. atra, which is mostly

on tropical reef flats (Clark & Rowe, 1971;

distributed in mid- and low-tide areas.

Harriott, 1982; Conand & De Ridder,

Other common species of echinoderms1990). It is amongst the most conspicuous

include sea urchins (Echinometra mathaei,

fissiparous species and presents one of two

Stomopneustes variolaris) and brittle starphenotypes: a small form (~<200 g) that(Ophiocoma scolopendrina).
80

Platax 20: 79-87, 2023
doi: 10.29926/platax.202312_18.0007

A125O23'

B●4●1●223O23'●3Fig. 1. Study area. A: Map showing Hsiao Liouciou Island. 1=Yuchengwei, 2=LobsterCave, 3=Haizikuo, 4=Beauty Cave. Salinity was measured at each, and surveys
were carried out Duzaiping. B: Aerial photograph of the 35,400 m2 intertidal reef
platform at Duzaiping. Scale bar=100 m. These "snapshots" were from Google
Earth (accessed in 2021).
Heavy rain started from July 28 to

we used quadrats and belt transects toAugust 14. After four days, on August 18

estimateand 19, 2021, mass mortality of black sea

abundance at Duzaiping. As higher sea

cucumbers was observed. Pictures were

cucumber densities on this shallow

taken,andplatform occurred in tidal pools (low- to

temperature were measured. We use a

mid-tide range), we deployed ten 0.5 m x

refractometer to measure the surface water

0.5 m quadrats during low tide to estimate

temperature and salinity in tide pools (n=3)

density. To additionally estimate the total

in the mid-tide area during low tide. The

number and average density, we deployeddepth of the tide pool is 10 to 15

five belt transects (1 m x 80 m from thecentimeters. In addition to the study site,high tide to the low tide line). Transects

we measured salinity at four other sites inwere 50-m apart, and we counted thethe vicinity from 12 to 21 August during or

number of H. atra in each belt transect

after the heavy rainfall (Fig. 1A).

(thereby covering an area totaling 400 m2).

Precipitation data were acquired from theThe positions of the transect lines andCentral Weather Bureau of Taiwan via

quadrats were as similar to those of ourtheir website.

2020 surveys as possible (Chao et al.,andseawatersalinity

On September 18, 2021 (one2021).

mother after mass mortality was observed),81

sea

cucumberdensityandPlatax 20: 79-87, 2023
doi: 10.29926/platax.202312_18.0007

Results and Discussion

highlighting the immense degree ofFig. 2 shows the daily rainfall

salinity stress experienced by local marine

between July and August of 2021 at Hsiao

organisms after this particularly rainy

Liouciou Island. From July 28 to Augustperiod.

14, except for three days, over 50 mm ofThe next day (19 August), many deadrain fell on each of 15 days, with asea cucumbers washed up on the beachparticularly intense rainfall on Aug. 1 (275(Fig. 5), and a strong, rotten smell

mm of rain over the course of the day). The

permeated the air. On Sept. 18, 2021, one

salinity was 15+0 ‰ (mean±std.dev; n=3)month after this mass mortality, the density

oand the temperature was 37-39 C (n=3) inin the formerly densest areas (lower inner

the tide pools at Duzaiping, wheretidal area) dropped from 80.75+11.94

hundreds of dead sea cucumbers were(mean±std.dev; n=20) individuals m-2

observed on August 18, 2021 (Fig. 3). At(May 2020, Chao et al. 2021) tothe other four study sites off the coast (Fig.

49.40+11.82

1 & Tab. 2), salinity ranged from 0 to 16,(mean±std.dev;n=10)-2

individuals m . The average density ofFig. 2. Precipitation through July and August 2021 at Hsiao Liouciou Island. Blackbars depict the total daily precipitation. The red dashed line indicates thedate of the mass mortality event (18 Aug.). The rainfall data were from theCentralWeatherBureauofTaiwan’swebsite(//https://www.cwa.gov.tw/V8/C/).

82

Platax 20: 79-87, 2023
doi: 10.29926/platax.202312_18.0007

fivebelts

dropfrom

5.6+1.42

52.5% decrease is primarily attributed to(mean±std.dev; n=20) individuals m-2

this mass mortality event. In fact, we(May 2020) to 2.66+1.34 (mean±std.dev;

almost did not find a single living H. atra-2n=5) individuals m . The total numberin the mid- and high-tide areas (i.e., fromestimated by belt transects dropped fromthe high tide line to 45-m seaward). Most198,000 (May 2020) to 94,000 individuals

live individuals were found in the tidal

2

across this 35,400 m study area. Thispools near the low tide area.

Fig. 3. Numerous dead H. atra, one H. cinerascens (the brown individual), and two sea
urchin tests in a tide pool at Duzaiping. Scale bar=10 cm.

Fig. 4. One large (476 g) and several small, dead H. atra in a tide pool at Duzaiping.
Scale bar=10 cm.

83

Platax 20: 79-87, 2023
doi: 10.29926/platax.202312_18.0007

Fig. 5. Many dead H. atra that had washed onto the shore after heavy rainfall on August19, 2021 at the main study site of Duzaiping (Fig. 1). Scale bar=10 cm.
Both small (<50 g) and large sea

sea cucumber Holothuria scabra (sandfish)

cucumbers (>400 g) were affected by thisduring the rainy season; indeed, they

event (Figs. 3-5). We deduce that thissuggested that, for cultivation in coastal

catastrophe was caused by heavy rainfall

ponds, salinity should not be allowed toaccompanied with high temperatures

fall below 18 ‰. Although Apostichopus

during low tides in the summer. Tab. 1 lists

japonica can tolerate a range of salinity

several other sea cucumber mass mortality

from 22 to 36 ‰, most sea cucumbers

events from the literature. Most involved acannot survive at salinities <16 ‰ (Yuansudden increase in river discharge, but aet al., 2006). Salinity measured from ourfew were due to heavy rains in restrictedfive study sites of Hsiao Liouciou Island inareas (Lawrence, 1996). Mass mortality ofAugust ranged from 0 to 16 (Tab. 2) during

Opheodesma spectabilis on reef flats ofand after the heavy rainfall. Additionally,

Hawaii was triggered by decreased salinity

low spring tides during summer normallyfrom land-based runoff caused by heavy

occur around noon in Southern Taiwan

rainfall in Berrill (1966). This study is very

(Chao et al., 1994), the period at whichsimilar to ours. Heavy rainfall on thetemperatures are highest. Such extreme

island flowed into inshore areas caused

temperatures could have exacerbated thethis mass mortality could be the cause.

low-salinity stress experienced by H. atra

Echinoderms are generally considered toat Hsiao Liouciou. As temperatures

be stenohaline (Russell, 2013), and Tuwo

continue

et al. (2020) noticed an increase ofanthropogenic climate change (IPCC,mortality of the commercially important2013), it will be critical to continue to84

toclimbonaccountof

Platax 20: 79-87, 2023
doi: 10.29926/platax.202312_18.0007

Tab. 1. Mass mortality events of holothurians.
Location

Causes

EffectReference

Cucumaria saxicolo

North Wales,
Britain

Severe wintry
weatherMassmortality

Crisp, 1964

Opheodesma spectabilis

Reef flats ofHawaii

Massmortality

Berrill, 1966Cucummaria planci
Holothuria tubulosa
Thyone fusus

Gulf ofTrieste,
Slovenia

Massmortality

Stachowitsch,
1984

Pentacucuma spyridophora
Thyone aurea

Off the coastof South
Africa100%
mortality

Branch et al.,
1990

Holothuria princeps

FloridaPanhandle

Massmortality

McClintock etal., 2018

Holothuria atra

Reef flats of
Hsiao
LiouciouIsland,TaiwanDecreasedsalinity fromland-based
runoffHypoxia
attributed to astrong
thermocline
Reducedsalinities
resulting fromriverine floods
Lowtemperatureinduced stress
Decreasedsalinity fromland-based
runoff caused byheavy rainfall

Massmortality(52.5%)

HereinSpeciesestablish

notonlybaselinemarinestorm events driven by climate change, inecosystem data, but also more thoroughly

addition to the associated higher seawater

document mass mortality events such astemperatures, will lead to an increasingthese as a means of evaluating future

number of mass mortality events of marine

climate impacts (McClintock et al., 2018).

organisms in both Southern Taiwan and

We expect that more frequent and extreme

elsewhere.
85

Platax 20: 79-87, 2023
doi: 10.29926/platax.202312_18.0007

Tab. 2. Mass Salinity from 10 to 20 August 2021 at five localities on Hsiao Liouciou
Island (Fig. 1).
Location

Beauty Cave Lobster Cave Duozaiping Yuchengwei

Haizikou

Date (August 2021)

101218

1920

Salinity

0 - 16615

107

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