Platax 14: 62-81, 2017

Spatial variation in the benthic community structure ofcoral reefs of Hsiaoliuchiu, Taiwan
Tung-Lin Yang1,2, Sonny Tuan Meng Lee3,4*, Pei-Yun Tsai,
Chih-Jui Tan1,5, Tung-Yung Fan1,2*1National Museum of Marine Biology and Aquarium, Checheng, Pingtung 944, Taiwan, R.O.C.

2

Institute of Marine Biology, National Dong Hwa University, Checheng, Pingtung 944, Taiwan, R.O.C.

3

School of Environment, The University of Auckland, Auckland, 1142, New Zealand4

Department of Medicine, The University of Chicago, Chicago, IL, United States

5

Department of Oceanography, National Sun Yat-Sen University, Kaohsiung 80424, Taiwan, R.O.C.

* Corresponding authors. E-mail address: leet1@uchicago.edu (Sonny T.M. Lee);tyfan@nmmba.gov.tw (T.-Y. Fan).

Abstract
Hsiaoliuchiu, a coral reef island located off southern Taiwan, wascharacterized by high coral cover in the 1970s but shifted from a coral- to an
algal-dominated system 20 years ago. That being said, there is little
information on the ecology of the coral reefs around Hsiaoliuchiu, nor do weknow what drove this dramatic decline in live coral cover. In this study,
comprehensive benthic community surveys were carried out at 36 sites around
Hsiaoliuchiu between 2010 and 2012, and four of these sites were surveyed ingreater detail to understand depth-related differences in benthic structure (to30 m). Turf algae dominated the benthic communities at most sites around theisland (% cover ranging from 35 to 81%). However, at Houshi fringing reef,
which was located at the southeastern side of the island, hard coral cover was
still 23.8 to 54.2%. At this site, encrusting Montipora spp. colonies dominatedthe shallows, while plating and massive corals were most common on the
deeper reefs. Also, at Houshi fringing reef, coral cover increased with depth,
while cover of macroalgae and turf algae were relatively rarer in deeper
waters. Based on these data, we recommend that Houshi fringing reef belegally designated as a marine protected area in order to conserve theseremaining coral communities of Hsiaoliuchiu.
Key words: algae, coral, coral reef ecology, marine protected area,
phase shift, upwelling

62

Platax 14: 62-81, 2017

Introduction

ultimately becoming dominated by turf ormacroalgae (McCook, 1999). Furthermore,as a result of rising seawater temperaturecaused by global climate change, corals
are currently disappearing at an alarming
rate (Hughes et al., 2010), and coraldisease prevalence is at an all-time high.
At some locations, coral reef ecosystems
are more prolific further offshore, as wellas in deeper waters, due to the better
water quality and cooler temperaturesassociated with such environments (Bakand Nieuwland, 1995; Bak et al., 2005;
Menza et al., 2008; Sommer et al., 2011).
One means of mitigating the effects
of anthropogenic disturbances on coral

Coral reefs are amongst the mostecologically and economically important
ecosystems in the world; unfortunately,
they are also amongst the most threatened(Pandolfi et al., 2003; Wilkinson, 2008),
and the costs to restore coral reefs arehigher than for all other ecosystems (DeGroot et al., 2013). Both natural andanthropogenic disturbances (Hughes,
1994; Hughes and Connell, 1999;
Knowlton, 2001; Bellwood et al., 2004;
Knowlton and Jackson, 2008), such as
overfishing, eutrophication, and coastal
development (associated with increased
sediment loads, amongst other issues), arepredominantly responsible for global
declines in coral reef health.
Anthropogenic disturbances cancause phase shifts in which hardcoral-dominated communities transition toalgal-dominated ones (Done, 1992;
Hughes, 1994; Connell, 1997; Gardner etal., 2003). For example, chronic
overfishing of reef herbivores can lead toalgal overgrowth, and these algae can thenout-compete corals for reef substrate(Hughes, 1994). Concurrently, coastal
development may also increase turbidity
and nutrient levels in the surrounding
waters, suffocating corals and limiting theability of coral larvae to recruit to thereefs (Gilmour, 1999; Malcolm et al.,2003). The eutrophication associated withsuch development also causes accelerated

reefs is the formation of marine protectedareas (MPA). In the course of establishingconservation areas, it is critical to identify
the capacity for resistance and resilienceof the existing coral reefs systems toenvironmental change (West and Salm,
2003). Additionally, determining thebenthic community composition also
provides a baseline against which futurechanges in the biota and habitat quality
can be quantified (Kuo et al., 2012;
Grizzle et al., 2015). This documentationof biodiversity is an important factor in
the designation of MPAs since marine
reserves are only useful when they can beproven to serve as spatial and temporalshelters for buffering the harmful effects
of anthropogenic disturbance (Allison etal., 1998).

algal growth, resulting in the reefs

63Platax 14: 62-81, 2017

Hsiaoliuchiu,

which

is

locatedgreatly. Results of a “Reef Check”

about 14 km from the southwestern coast

conducted in 2009 found that hard coralof mainland Taiwan, is the country’s only

cover at Hsiaoliuchiu was the lowest

coral reef island. Surveys carried out in(15%) in Taiwan and indicated that these

1970s (Yang et al., 1975; Randall andreefs have been severely damaged (Dai,Cheng, 1977) revealed that coral cover2010). However, data on coral reef

ranged from 50-80%, with a highecosystems around Hsiaoliuchiu are still

diversity of scleractinian corals andlimited; only a small number of reefs werevarious, huge coral colonies (e.g., tabulate

surveyed in 2009, and we have very

Acropora spp). Randall and Cheng (1977)

limitedindicated that the coral communities atcommunity structure of Hsiaoliuchiu’s

Hsiaoliuchiu were diverse and thriving,coral reefs (Fan, 2011). An updated,

and that the overall coral reef was moreaccurate,structurally developed and complex thancommunity structure is the foundation of aelsewhere in Taiwan. Since then, there hassuitable management plan needed for the

been no detailed study of the coral reef

conservation of coral reefs (Grizzle et al.,ecology of Hsiaoliuchiu, nor do we know2015). As such, to provide information for

how/if these reefs have been affected by

guiding coral reef conservation andlocal activities and global climate change.

management at Hsiaoliuchiu, we sought to

We do know that, for the past two
decades,

reefs

and

documentoncompletethethebenthic

reportcurrentofbenthic

surrounding

community composition, 2) assess the

Hsiaoliuchiu have been adversely affected

overall health of existing coral reefby various anthropogenic and natural

ecosystem, and 3) determine the influence

factors.

aof depth and temperature on coral coversignificant reduction in herbivorous fish

and composition around Hsiaoliuchiu. We

and invertebrate biomass (T.-Y. Fan,

hypothesized that reefs farther away frompersonal observation). As there is no

the island’s main population center on the

sewage system on the island, mostsouth coast would be characterized bydomestic waste is discharged directly intohigher hard coral cover. We also predicted

the

in

that coral cover would be higher at greater

eutrophication and numerous algal blooms.

depths due to the less anthropogenic

Due to these combined stressors, the hard

disturbances.

sea,

the

1)

knowledge

Over-fishing

which

has

has

causedresultedcoral cover around the island has reduced64Platax 14: 62-81, 2017

Fig. 1. Map of Hsiaoliuchiu featuring study sites. (A) Surveys were carriedout at 36 sites around Hsiaoliuchiu. Additional surveys were carried out
at four sites- Lobster Cave (LC), Houshi fringing reef (HSFR), Shanbay
Bay (SBB), and Hanban Bay (HBB)- to determine benthic covervariation across depths. Map of the location of the 17 study sites
surveyed between June and August 2011 (B). Map of the location of the
19 study sites surveyed between November 2011 and February 2012 (C).

65

Platax 14: 62-81, 2017

Materials and Methods

cover. Hanban Bay (HBB; 22°19’730”N,
120°21’161”E), located off the west coastof the island, is a key tourist spot with ahistory of coral harvesting. Lastly,
Shanban Bay (SBB; 22°21’048”N,
120°21’834”E) is located on the west
coast near marine cage fish cultures (Janet al., 2014).

Study sites
We surveyed 36 sites to characterize
the benthic cover around Hsiaoliuchiu(22°20’ N, 120°22’ E, Figure 1). In
addition, we also chose four locations
amongst these survey sites to further
investigate the impacts of depth andtemperature on the benthic communities.
Initial surveys were carried out across 17
study sites (June-August 2011) that were
evenly distributed around the island, while
the second set of surveys was carried out
on19
locations(November2011-February 2012); the latter weremainly on the eastern and southern sidesof Hsiaoliuchiu (Figure 1) since ourpreliminary surveys revealed that thesesides featured much higher coral coverand diversity coral reef communities.
Based on results from our initial
surveys, we further examined four
locations with a distinct history ofenvironmental and anthropogenic impacts.
Located at the east of the island, Lobster
Cave (LC; 22°20’891”N, 120°23’444”E)
abuts a heavily populated area, withhousing located right on the coast; sewage
runoff is therefore a potential problem atthis site. Houshi fringing reef (HSFR;
22°19’547”N, 120°22’137”E), the largest
and deepest reef area (Yang et al., 1975),
which is located in the south, is thefarthest from major population areas. It
was therefore hypothesized to be
characterized by higher live hard coral

Benthic cover and abiotic data acquisition
We deployed three, 10-m transects ateach site. The transect tapes werepositioned parallel to depth contours
between 5-8 m. We used a Canon G15
camera to photograph the benthos within a0.35 m x 0.35 m quadrat, resulting in a
total of 30 images per transect. We
constructed the quadrats according toTkachenko et al. (2007). The base frame(0.35 m x 0.35 m) of the quadrat had
0.4-m rods that were attached at each of
the four corners, which joined to a smallersquare frame above the base transect to fit
the camera lens. This set-up ensured thateach quadrat was the same size and thatthe camera was the same distance fromthe quadrat (0.4 m).
We investigated the impact of depth
and temperature on the benthic
community of four locations: LC, HSFR,HBB, and SBB. Due to unforeseen
circumstances (namely typhoons andunstable surf conditions), surveys wereconducted at different times. We
conducted photo surveys for LC and SBB
in November 2010, while surveys for66

Platax 14: 62-81, 2017

HBB and HSFR were performed in April
and August 2011, respectively. At the four
locations, five 10-m transects were
deployed 10-m apart and parallel to theshoreline at each depth. A total of 30
photos were taken along each transect tocompare the benthic community at
different depths. We started the survey
started at 5 m depth and deployed 10-mtransects at 5-m intervals (ensuring that
there were at least 10 m separation
between transects) until 30 m (5, 10, 15,
20, 25, and 30 m). If the reefs did notextend to 30 m, surveys were instead
conducted until the deepest 5-m increment.
Seawater temperature was recorded at
10-minintervals
using
HOBO
®
temperature recorders (Onset MA, USA)at 5 m at each of the four locations from
October 2010-May 2012. In addition,
temperatures were recorded at 12, 20 and
30 m at HSFR from March-September
2012. The HOBO recorders were set tomonitor and record the surrounding watertemperature every 10 mins.

of hard corals, it was further subdivided
into several different growth forms andgenera as described in Table 1: 1)
branching Acropora spp., 2) branching
Pocillopora spp., 3) massive andencrusting species, 4) foliaceous andplating species, 5) encrusting Montipora
spp., and 6) “other.” We used
one-way-ANOVA (Minitab ver. 14) on
normalized and transformed data,
followed by post-hoc Tukey’s honestly
significant difference (HSD) tests todetermine the effect of depth on thebenthic composition for each of four
locations (LC, HSFR, HBB, and SBB;
p<0.05).

Results
Benthic cover
Turf algae dominated the benthos
around Hsiaoliuchiu (35-81%; Figure 2),
with site 21 having the highest turf algal
cover (>80%). The cover of macroalgae(<23%) was lower than that of turf algae
at all sites. Hard coral cover was higher(21-45%) along the eastern and southerncoasts (sites 1-4 and 20-31), with highest
cover at sites 3 (45%) and 25 (44%). The
lowest hard coral cover was documented
along the western and northern coasts(Figure 2). Sites 17 and 18, which werelocated on the east coast, had the highest
soft coral cover (up to 42%; Figure 2).
The cover of hard corals was higher thansoft corals at most of the sites (excepting
17 and 18).

Data analysis
We used Coral Point Count with
Excel extensions (Kohler and Gill, 2006)
to analyze all survey images by randomly
selecting fifty points within the quadrat
and matching the points to a code thatindicated the coral morphology, coralgenus, and substrate type. The benthos
was categorized as hard corals, soft corals,
macroalgae, turf algae or other. In terms

67

Table 1. Classifications of hard corals at the four locations at which depth variation in the benthic community structure was
examined. Br= branching, M=massive, EC= encrusting, and F=foliaceous.

Platax 14: 62-81, 201768

Platax 14: 62-81, 2017

Fig. 2. Benthic cover data from Hsiaoliuchiu. Benthic cover data from the 17
Hsiaoliuchiu sites surveyed between June and August 2011 (sites 1-17) andthe 19 sites surveyed between November 2011 and February 2012 (sites
18-36). N=3/site.

69

Platax 14: 62-81, 2017

Fig. 3. Depth effects on benthic community structure. Variation (mean± standard
error [SE]) in benthic community structure at 3-6 depths at four locations:
Lobster Cave (LC), Houshi fringing reef (HSFR), Hanban Bay (HBB), andSanban Bay (SBB). Error bars represent standard deviation. N=5/depth.

70Platax 14: 62-81, 2017

Fig. 4. Seasonal variation in monthly mean seawater temperature at four study
sites around Hsiaoliuchiu, Taiwan: Lobster Cave=LC, Houshi fringing
reef=HSFR, Sanban Bay=SBB, and Hanban Bay=HBB. Error bars represent
standard deviation.

71

Platax 14: 62-81, 2017

Benthic cover variation across depths
Turf algae was prevalent at LC,
HSFR, HBB, and SBB, with cover of 50%
or higher at all depths; the exception was
HSFR at 30 m (Figure 3). At LC, thecover of turf algae at 5 m depth was thehighest (86%), and it was almost doublethat of the other depths (Table 2). There
was also a significant difference inmacroalgal and soft coral cover acrossdepths at LC (Table 2). Less than 10% of
this site was covered by macroalgae, andwhile the soft coral cover was low (3%) at
5 m, there was an increase from 10 m anddeeper (30-40%; Figure 3). Hard coral
cover was low at all depths (4-8%) anddid not vary between them (Table 2).
At HSFR there was a significant
difference in all functional groupings oftaxa across depths (Table 2). Hard coral
cover was lowest (19%) at 10 m but
increased with depth (Figure 3). Highest
hard coral cover was documented at 30 m
(54%), followed by 5 m (40%). Although
soft coral cover was low (0.4-9%; Figure3), it did vary across depths (Table 2).
Finally, the cover of macroalgae
decreased significantly as the water depth
increased from 10 m (18%; the maximum)
to 30 m (1%; Figure 3 and Table 2).
Depth had no significant effect on
the benthic cover at HBB (Table 2). At all
depths, hard coral, macroalgal, and turf
algal cover were 8-15%, 4-8%, and 6-7%,
respectively (Figure 3). At SBB the coverof macroalgae (5%) and turf algae (84%)

was significantly higher at 5 m than atother depths (Table 2 and Figure 3). The
cover of hard corals (4-8%) and softcorals (<1%) was low.
Encrusting montiporids, such as
Montiporaaequituberculata,

weresignificantly more dominant at 5 m at
HSFR (Table 3). The plating coral growthform (e.g., Montipora spp., Turbinaria
spp., Echinophyllia spp., Merulina spp.,
Mycedium spp., and Pachyseris spp.)
dominated the coral cover at 30 m (Table3). We observed an approximately 2-foldincrease in the cover of massive andencrusting coral growth forms at depths
between 20-30 m as compared to theshallower waters (<20 m; Table 3).
Seawater temperature
The seasonal variation of seawatertemperature at 5 m was similar over both
space (across the four sites) and time(across different seasons; Figure 4).
However, the monthly mean seawatertemperature at LC and HSFR was lower
than

at

SBB

and

HBB

betweenMarch-September 2011 and April-May
2012. We observed a high temperaturefluctuation, especially during the summer,
at HSFR at various depths (Figure 5), witha higher fluctuation in deeper waters ( e.g.
26.1-28.0°C at 12 m, 23.7-27.8°C at 20 m,
and 21.8-27.5°C at 30m during 1 to 7 AM
on 25 June 2012).

72

Platax 14: 62-81, 2017

Fig. 5. Temperature variation at different depths – 12m, 20m and 30m at Houshi
Fringing Reef (HSFR).

73

Table 2. Summary table of 1-way ANOVA and Tukey’s honestly significant difference (HSD) tests comparing the benthic
cover of various functional groups between depths at four locations: Lobster Cave (LC), Houshi fringing reef
(HSFR), Hanban Bay (HBB), and Shanbay Bay (SBB). Lower-case letters (a, b, c) indicate Tukey’s HSD differences
between depths (p<0.05).

Platax 14: 62-81, 201774

Table 3. Summary table of 1-way ANOVA and Tukey’s honestly significant difference (HSD) tests comparing the cover ofvarious hard coral morphotypes between depths at four locations: Lobster Cave (LC), Houshi fringing reef (HSFR),
Hanban Bay (HBB), and Shanbay Bay (SBB). M=massive, EC=encrusting, and F=foliaceous. Lowercase lettersreflect Tukey’s HSD post-hoc differences between depths (p<0.05).

Platax 14: 62-81, 201775

Platax 14: 62-81, 2017

Discussion
Our survey revealed spatialdifferences in the benthic community
structure of reefs of the coral reef islandof Hsiaoliuchiu. Of note, the coral reefs
around the northern and western sides of
the island were seriously degraded andmostly overgrown by turf algae. Soft
corals were abundant in eastern
Hsiaoliuchiu, whereas some sites in thesoutheastern region maintained relatively
high coral cover. The coral community
varied across depths at these higher coral
cover sites.

around the island, especially in theshallow areas. The local islanders havehistorically collected coral colonies,
especially around the northern andwestern sides of the island (i.e., SBB and
HBB) to supply to tourist gift shops (Yanget al., 1975). Another key factor in thehard coral decline is over-harvesting of
herbivorous fish and invertebrates (Dai,2010). In a top-down controlled
ecosystem (Hughes, 1987; Bellwood et al.,2004), without these herbivorous fishes
and invertebrates to remove fast-growing
algae on the reefs, the algae can dominate;
this increase in algal biomass can thenlimit the growth of existing corals andinhibit coral larvae settlement (Sammarco,
1980; Wilkinson, 2008).
Increased eutrophication andsedimentation might be another reason for
the reefs’ decline. Hsiaoliuchiu lacks asewage treatment system, and wastewaterfrom both the locals and tourists isdischarged directly into coastal waters(Dai, 2010). Recently, tourism has
increased on the island, and more than 1
million people are visiting the island
every year at current estimates; as only
12,000 people currently live on
Hsiaoliuchiu, new hotels and otherbuildings will likely be required toaccommodate this rising influx of tourists.
These tourists are likely to contribute toelevated seawater pollution levels, as well(Fan, 2011). Furthermore, land-derived
nutrients and sedimentation are washed

Phase shift
The coral cover around Hsiaoliuchiu
was typically < 20%, and turf algae
dominated all surveyed sites. Yang et al.
(1975) noted that the coral community
along the west coast of Hsiaoliuchiu wasmore developed than that of the east coast,
while Randall and Cheng (1977) reported
that coral cover was between 50 and 80%
in the shallow reef and 20-40% in the
deeper reef. However, we could not findthe high coral cover described in theseolder works; instead, an algal-dominatedsystem was documented. The possible
reasons for this coral-to-algae phase shift
are
coral
harvesting,overfishing,eutrophication, and sedimentation, as now
discussed in further detail.
The excessive collection of corals
has clearly played a role in the rapid
decline in the coral reef ecosystems

76

Platax 14: 62-81, 2017

directly into the surrounding waters
during heavy rainfall events.
Exacerbating the issue ofeutrophication, a commercial fish farm
was developed near the inshore coral reefs
off the northern coast of Hsiaoliuchiu
since 1994. Fish farms can release large
quantities of excessive feed and fecal
material, mostly as dissolved nutrients andorganic particles, into the surrounding
marine environment, and this may lead toalgal blooms and coral reef degradation(Huang et al., 2011, 2012). At
Hsiaoliuchiu, it has been shown that theparticulate organic matter released by thefarm may have entered the coral reef
ecosystem through the pelagic food chain(Jan et al., 2014). The phase shift fromcoral-dominated to turf algal- or
macroalgal-dominated ecosystems at
Hsiaoliuchiu may, then, be the result of
not only overfishing, but also increased
eutrophication from terrestrial wastewaterand sediment runoff.

anthropogenic
impacthave
been
documented
elsewhere(Bak
and
Nieuwland, 1995; Bak et al., 2005; Menzaet al., 2008). Regarding the second
hypothesis, hard coral cover may,alternatively, have increased with depth at
HSFR because of the differential
influence of upwelling on deep reefs
relative to shallow ones. Shih (2006)
documented spring tide upwelling insoutheastern Hsiaoliuchiu in which deep
ocean seawater characterized by low
temperature, high salinity, high oxygen
concentration, and low chlorophyll-aconcentration was brought to the shallow
water. Our temperature data shown the
deeper water more influenced by the cold
water (Figure 5). Such deep ocean
seawater is likely to be more amenable tocoral growth than the relatively polluted
seawater coming from the island(Fabricius, 2005; Fabricius et al., 2012),
though whether the cooler temperature or
the lower pollutant levels associated withthis upwelled water is more important inpromoting coral growth over the shallow
areas should be investigated morethoroughly in future works (Schmidt et al.,2012).
Encrusting Montipora species,
such as M. aequituberculata, were thedominant hard corals at 5 m at HSFR.
Encrusting Montipora spp. are well
adapted to turbulent conditions in Hawaii(Jokiel et al., 2004), and this relatively
wave-resistant morphotype appear to have

Houshi fringing reef
The higher coral cover (24-44%)
off the southeastern coast of Hsiaoliuchiu
may be partly due to 1) lower humanpopulation density and human activity ingeneral (Fan, 2011) and 2) upwelling.
Regarding the former hypothesis, deeper
waters are likely to be less affected byland-based anthropogenic factors, andsuch shallow-deep gradients in coral
cover as a result of dampening of77

Platax 14: 62-81, 2017

adapted to the strong waves and swellcharacteristic of HSFR, a reef that also
experiences boreal summer typhoons (Fan,
2011). On the other hand, the coral
community in the deeper waters at HSFR
was dominated by massive, encrusting,and plating (foliaceous) growth forms andfeatured corals such as Turbinaria spp.
(plating form), Echinophyllia spp. (platingform), Merulina spp. (plating form),
Mycedium spp. (plating form), andPachyseris spp. (plating form). These
species are also common on reef slopes insouthern Taiwan (Dai, 1993), and, likeother encrusting, massive, and platingcorals, have a relatively greater surface
area for capturing light compared tobranching corals; this allows them tothrive in low-light areas (Goh et al., 1994;
Dikou and van Woesik, 2006; Erftemeijer
et al., 2012).

tool by comparison to the baseline dataset
presented
herein(Connell,
1997;
Tkachenko and Soong, 2010; Kuo et al.,2012). Establishment of no-take MPAs
could promote the repopulation ofherbivorous
fishes,which
couldconsequently control algal densities andfacilitate coral re-population (Lester et al.,2009). Houbihu in Nanwan Bay
represents a successful MPA in Southern
Taiwan; the closing of the area to fishinghas resulted in relative higher coral coverand fish densities than non-protectedareas in the near vicinity (Tkachenko
and Soong, 2010). The formation andeffective management of an MPA at
Hsiaoliuchiu will ideally benefit its
coral reefs in a similar manner.

Acknowledgments
We thank the Pingtung County
Government for funding this study, as
well as Z. G. Chen for his assistance withfieldwork.

Management implications
Thesoutheasternregionsof
Hsiaoliuchiu, including HSFR, should beprioritized for coral reef protection
because they are characterized by thelargest and deepest reefs (Yang et al.,1975), the highest coral cover (This study),
and, presumably, the lowest human levelof human and land-based impact. Given
the aforementioned increase in tourism at
Hsiaoliuchiu, it will be critical to establish
a MPA around HSFR and then trackchanges in the benthic community todetermine its efficacy as a conservation

References
Allison, G.W., J. Lubchenco & M.H. Carr M.H.
1998. Marine reserves are necessary but
not sufficient for marine conservation.
Ecological Applications, 8:S79-S92.
Bak, R.P.M. & G. Nieuwland. 1995.
Long-term change in coral communities
along depth gradients over leeward reefs
in the Netherlands Antilles. Bulletin ofMarine Science, 56:609-619.
Bak, R.P.M., G. Nieuwland & E.H. Meesters.
2005. Coral reef crisis in deep andshallow reefs: 30 years of constancy andchange in reefs of Curacao and Bonaire.

78

Platax 14: 62-81, 2017

Coral Reefs, 24:475-479.
Bellwood, D.R., T.P. Hughes, C. Folke & M.
Nystrom. 2004. Confronting the coral
reef crisis. Nature, 429:827-833.
Carilli, J., S.D. Donner & A.C. Hartmann.
2012. Historical temperature variability
affects coral response to heat stress.
PLoS ONE, 7(3):e34418.
Connell, J.H. 1997. Disturbance and recoveryof coral communities. Coral Reefs,
16:S101-S113.
Dai, C.F. 1993. Patterns of coral distribution
and benthic space partitioning on thefringing reefs of southern Taiwan. Marine
Ecology, 42:185-204.
Dai, C.F., 2010, Status of Coral Reefs in
Taiwan. In: Kimura T (ed.) Status ofCoral Reefs in East Asian Sea Region:
2010,
pp.
79-87.
MinistryofEnvironment, Japan.
De Groot, R.S., J. Blignaut J, A. Van Der
Ploeg, J. Aronson, T. Elmqvist & J.
Farley. 2013. Benefits of investing inecosystem restoration. Conservation
Biology, 27:1286-1293.
Dikou, A. & R. van Woesik. 2006. Partial
colonymortalityreflects
coralcommunity dynamics: a fringing reef
study near a small river in Okinawa,
Japan. Marine Pollution Bulletin,
52:269-280.
Done, T.J. 1992, Phase shifts in coral
communities and their ecologicalsignificance.
Hydrobiologia,
247:121-132.
Erftemeijer, P.L.A., B. Riegl, B.W. Hoeksema& P.A. Todd. 2012. Environmental
impacts of dredging and other sedimentdisturbances on corals: a review. Marine
Pollution Bulletin, 64:1737-1765.
Fabricius, K. 2005. Effects of terrestrial runoff
on the ecology of corals and coral reefs:
review and synthesis. Marine Pollution
Bulletin, 50:125-146.
Fabricius, K., T.F. Cooper, C. Humphrey, S.
Uthicke, G. De’ath, J. Davidson, H.
LeGrand, A. Thompson A & B.
Schaffelke. 2012. A bioindicator system

for water quality on inshore coral reefs ofthe Great Barrier Reef. Marine Pollution
Bulletin, 65:320-332.
Fan, T.Y. 2011. Ecology and conservation of
Hsiaoliuchiu coral reefs. PingtungCounty Government. Chinese withEnglish abstract.
Gardner, T.A., I.M. Cote, J. A. Gill, A. Grant
A & A.R. Watkinson A. 2003. Long-term
region-wide declines in Caribbean corals.
Science, 301:958-960.Gilmour, J. 1999.
Experimental investigation into theeffects of suspended sediment on
fertilization,
larvalsurvival
andsettlement in a scleractinian coral. Marine
Biology, 135:451-462.
Goh, N.K.C., C.Y.Y. Chua & L.M. Chou L.
1994. Depth-related morphology ofscleractinian corals on Singapore reefs. In:
Proceedings
of
the
Third
ASEAN-Australia Symposium on Living
Coastal Resources, vol. 2, pp. 61-67.
Graham, N.A.J., D.R. Bellwood, J.E. Cinner,
T.P. Hughes, A.V. Norström & M.
Nyström M. 2013. Managing resilience
to reverse phase shifts in coral reefs.
Frontier in Ecology and the Environment,
11:541-548.
Grizzle, R.E., K.M. Ward, R.M.S. AlShihi &J.A. Burt. 2016. Current status of coral
reefs in the United Arab Emirates:
distribution, extent, and community
structurewithimplications
formanagement. Marine Pollution Bulletin,
105:515-523.
Huang, Y.A., S.C. Huang, P.J. Meng, H.J.
Hsieh & C.A. Chen. 2012. Influence of
seasonal monsoon winds on the water
quality around a marine cage-culturezone in a semi-closed embayment in
Taiwan. Marine Pollution Bulletin,
64:851-860.
Huang, Y.A., H.J. Hsieh, S.C. Huang, P.J.
Meng, Y.S. Chen, S. Kevashavamurthy,
Y. Nozawa & C.A. Chen. 2011. Nutrient
enrichment caused by marine cage
culture and its influence on subtropicalcoral communities in turbid waters.

79

Platax 14: 62-81, 2017

Marine Ecology Progress Series,
423:83-93.
Hughes, T.P. 1994. Catastrophes, phase shifts,
and large-scale degradation of a
Caribbean
coral
reef.
Science,
265:1547-1551.
Hughes, T.P. & J.H. Connell. 1999. Multiple
stressors on coral reefs: a long-term
perspective.
Limnology
andOceanography, 44(3 II):932-940.
Hughes, T.P., D.C. Reed & M.J. Boyle. 1987.
Herbivory on coral reefs: community
structure following mass mortalities of
sea urchins. Journal of Experimental
Marine Biology and Ecology, 113:39-59.
Hughes, T.P., N.A.J. Graham, J.B.C. Jackson,
P.J. Mumby & R.S. Steneck. 2010. Rising
to the challenge of sustaining coral reef
resilience. Trends in Ecology and
Evolution, 25:633-642.
Jan, R.Q., S.J. Kao, C.F. Dai & C.T. Ho. 2014.
Assessment of the effects of cagefish-farming on damselfish-associatedfood chains using stable-isotope analyses.
Marine Pollution Bulletin, 86:111-121.
Jokiel, P.L., E.K. Brown, A. Friedlander, S.K.
Rodgers & W.R. Smith. 2004. Hawaii
coral reef assessment and monitoring
program: Spatial patterns and temporal
dynamics in reef coral communities.
Pacific Science, 58:159-174.
Jouffray, J.B., M. Nystrom, A.V. Norstrom,
I.D. Williams, L.M. Wedding, J.N.
Kittinger, & G.J. Williams. 2015.
Identifying multiple coral reef regimes
and their drivers across the Hawaiianarchipelago. Philosophical Transactionsof Royal Society, 370B:20130268.
Knowlton, N. 1992. Thresholds and multiple
stable states in coral reef community
dynamics.
AmericanZoologist,
32:674-682.
Knowlton, N. 2001. The future of coral reefs.
Proceedings of the National Academy of
Sciences of the United States ofAmerican, 98:5419-5425.
Knowlton, N. & J.B.C. Jackson. 2008.
Shifting baselines, local impacts, andglobal change on coral reefs. PLoS
Biology, 6(2):e54.
Kohler, K.E. & S.M. Gill. 2006. Coral point
count with Excel extension (CPCe): avisual basic program for determination ofcoral and substrate coverage using
random point count methodology.
ComputersandGeosciences,32;1259-1269.
Kuo, C.Y., P.J. Meng, P.H. Ho, J.T. Wang, J.P.
Chen, Y.W. Chiu, H.J. Lin, Y.C. Chang,
T.Y. Fan, A.H. Baird & C.A. Chen. 2012.
Recurrent
disturbancesandthedegradation of hard coral communities in
Taiwan. PLoS One, 7(8):e44364.
Lester, S.E., B.S. Halpern, K. Grorud-Colvert,
J Lubchenco, B.I. Ruttenberg, S.D.
Gaines, S. Airamé & R.R. Warner. 2009.
Biological effects within no-take marine
reserves: a global synthesis. Marine
Ecology Progress Series, 384:33-46.
Malcolm, M., F. Stewart, W. Timothy, H. Erica
H, L. Janice L & B. David. 2003. Coral
record of increased sediment flux to theinner Great Barrier Reef since European
settlement. Nature, 421:727-730.
Maynard, J.A., P.A. Marshall, J.E. Johnson &S. Harman. 2010. Building resilience into
practical conservation: identifying local
management responses to global climatechange in the southern Great Barrier Reef.
Coral Reefs, 29:381-391.
McCook L.J. 1999. Macroalgae, nutrients andphase shifts on coral reefs: scientiﬁcissues and management consequences for
the Great Barrier Reef. Coral Reefs,
18:357-367.
Menza, C., M. Kendall & S. Hile. 2008. The
deeper we go the less we know. Revista
de Biologia Tropical, 56:11-24.
Pandolfi, J.M., R.H. Bradbury, E. Sala, T.P.
Hughes, K.A. Bjorndal, R.G. Cooke, D.
McArdle, L. McClenachan, M.J.H.
Newman, G. Paredes, R.R. Warner, J.B.C.
Jackson. 2003. Global trajectories of thelong-term decline of coral reef
ecosystems. Science, 301:955-958.
Randall, R.H. & Y.M. Cheng. 1977. Recent

80Platax 14: 62-81, 2017

corals of Taiwan. Part I. Description ofreefs and coral environments. Acta
Geologica Taiwanica 19:79-102.
Sammarco, P.W. 1980. Diadema and its
relationship to coral spat mortality:
grazing, competition, and biologicaldisturbance. Journal of Experimental
MarineBiologyandEcology,
45:245-272.
Schmidt, G.M., N. Phongsuwan, C. Jantzen, C.
Roder, S. Khokiattiwong & C. Richter.
2012. Coral community composition andreef development at the Similan Islands,
Andaman Sea, in response to strong
environmental
variations.
MarineEcology Progress Series, 456:113-126.
Shih, H.E. 2006. Investigation of flow pattern
and upwelling characteristics near the
wakes of Liu-Chiu-Yu Island. Master’s
thesis,Department
ofMarineBiotechnology and Resources, National
Sun Yat-Sen University.
Sommer, B., P.L. Harrison, L. Brooks L & S.R.
Scheffers. 2011. Coral community
decline at Bonaire, Southern Caribbean.
Bulletin of Marine Science, 87:541-565.

Tkachenko, K.S. & K. Soong. 2010.
Protection of habitat types: a case studyof the effectiveness of a small marine
reserve and impacts of different habitats
on the diversity and abundance of coral
reef fishes. Zoological Studies, 49:195-210.
Tkachenko, K.S., B.J. Wu, L.S. Fang L.S. &T.Y. Fan. 2007. Dynamics of a coral reef
community after mass mortality of
branching Acropora corals and an
outbreak of anemones. Marine Biology,
151:185-194.
West, J.M. & R.V. Salm. 2003. Resistance andresilience to coral bleaching: implications
for coral reef conservation andmanagement. Conservation Biology,
17:956-967.
Wilkinson, C.R. 2008. Status of the coral reefsof the world: Global Coral Reef
Monitoring Network and AustralianInstitute of Marine Science, Townsville.
Yang, R.T., K.S. Chi, S.C. Hu & H.T. Chen.
1975. Corals, fishes and benthic biota of
Hsiao-Liuchiu. Spec Publication No 7,
Institute of Oceanography, National
Taiwan University.

81