Marine Pollution Bulletin 114 (2017) 1135–1140
Contents lists available at ScienceDirect
Marine Pollution Bulletin
journal homepage: www.elsevier.com/locate/marpolbul
Baseline
Coral benchmarks in the center of biodiversity
W.Y. Licuanan a,b,⁎, R. Robles a, M. Dygico c, A. Songco d, R. van Woesik e
a
Br. Alfred Shields FSC Ocean Research Center, De La Salle University Manila, Philippines
Biology Department, De La Salle University Manila, Philippines
c
World Wide Fund of Nature – Philippines, Puerto Princesa City, Palawan, Philippines
d
Tubbataha Management Office, Puerto Princesa City, Palawan, Philippines
e
Department of Biological Sciences, Florida Institute of Technology, Melbourne, FL, USA
b
a r t i c l e
i n f o
Article history:
Received 18 July 2016
Received in revised form 22 September 2016
Accepted 5 October 2016
Available online 19 October 2016
Keywords:
Benchmarks
Hard coral cover
Generic diversity
Philippines
Hierarchical sampling
a b s t r a c t
There is an urgent need to quantify coral reef benchmarks that assess changes and recovery rates through time
and serve as goals for management. Yet, few studies have identified benchmarks for hard coral cover and diversity in the center of marine diversity. In this study, we estimated coral cover and generic diversity benchmarks on
the Tubbataha reefs, the largest and best-enforced no-take marine protected area in the Philippines. The shallow
(2–6 m) reef slopes of Tubbataha were monitored annually, from 2012 to 2015, using hierarchical sampling.
Mean coral cover was 34% (σ ± 1.7) and generic diversity was 18 (σ ± 0.9) per 75 m by 25 m station. The southeastern leeward slopes supported on average 56% coral cover, whereas the northeastern windward slopes supported 30%, and the western slopes supported 18% coral cover. Generic diversity was more spatially
homogeneous than coral cover.
© 2016 Elsevier Ltd. All rights reserved.
Coral reefs are important to many tropical countries because they
support fisheries and tourism (Mumby et al., 2004), and protect shorelines from storm waves (Ferrario et al., 2014). Unfortunately, coral reefs
are declining at an alarming rate, with an estimated 75% of global reefs
under threat from local human pollution, and most reefs under threat
from climate-change-induced thermal stress (Burke et al., 2011). Already, approximately 19% of the world's coral reefs have been effectively lost, and another 15% may be lost in the next 10–20 years (Wilkinson,
2008). Even the iconic and well-managed Great Barrier Reef has lost half
of its coral cover from 1998 to 2012 (De'ath et al., 2012; but see also
Sweatman et al., 2011; Hughes et al., 2011; Osborne et al., 2011). Without corals, coral reefs will lose the major framework builders, along with
the architectural complexity needed to support fishes and other reef-associated organisms (Graham et al., 2006), and will lose their capacity to
grow and keep up with sea-level rise (van Woesik and Done, 1997;
Perry et al., 2013).
Benchmarks for common metrics, such as hard coral cover and diversity, are needed to assess the well-being of reef systems, and to determine management efficacy. Such benchmarks can: (i) provide
insights into background variability across reefs through time
(Murdoch and Aronson, 1999), (ii) determine what levels of change
can be effectively ignored, and (iii) suggest what levels of change are indicative of significant departures from normal states. Such knowledge
can be used to determine expected rates of recovery for different coral
⁎ Corresponding author.
E-mail address: wilfredo.licuanan@dlsu.edu.ph (W.Y. Licuanan).
http://dx.doi.org/10.1016/j.marpolbul.2016.10.017
0025-326X/© 2016 Elsevier Ltd. All rights reserved.
reef habitats (van Woesik, 2013), and used to improve the detectability
of adverse effects of different human activities. Information on the variability of these metrics, across habitats, reefs, and regions, may even
help refine appropriate scales of management for various human impacts. This knowledge could also provide a basis for evaluating the sensitivity of various assessment methodologies, and determine the
adequacy of sampling designs used in describing and monitoring coral
reefs. The aim of the present study is to provide new benchmarks for
coral cover and generic diversity (i.e., number of coral genera) using
data from the Tubbataha Reefs Natural Park, the largest and bestenforced no-take marine protected area in the Philippines (Dygico et
al., 2013). Strict enforcement has been in place at Tubbataha since
2001. The marine park is located in the Sulu Sea, which has been considered among the most diverse regions of the Coral Triangle, which itself
is the center of global marine diversity (Veron et al., 2009; Sanciangco et
al., 2013).
Annual monitoring of the Tubbataha reefs (Fig. 1) followed a hierarchical sampling design (Green et al., 2011). The hierarchical levels were
transects nested within stations, which were nested within study sites.
Two sites each were established in the north and south atolls of the
Tubbataha reefs. The sites were 6–28 km apart, and each site supported
two stations about 250–600 m apart (electronic supplementary material). Five 50-m transect lines were randomly placed within each station.
Each station was approximately 25 m × 75 m, and was located at 2–6 m
depth. The transects were re-randomized for every sampling period
(following Green et al., 2011). Monitoring involved photographing sections of the reef beneath each transect line, at 1-m intervals, using a
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W.Y. Licuanan et al. / Marine Pollution Bulletin 114 (2017) 1135–1140
Fig. 1. Map of the Tubbataha Reefs Natural Park showing the study stations monitored.
digital camera mounted on aluminum monopods. The camera was
contained in Ikelite® underwater housing, fitted with an Inon wide
angle (100o field of view) lens to allow each photograph to cover one
square meter of reef.
Digital images from 160 transects, sampled from 2012–2015 were
processed in the laboratory using Coral Point Count with Excel extensions (CPCe; Kohler and Gil, 2006). Ten points were randomly placed
on every 1 × 1 m digital image, and the corals under each point were
identified to genus. Some genera were also identified to growth form,
therefore in this paper taxa are occasionally referred to as Taxonomic
Amalgamation Units (electronic supplementary material).
A two-level analysis of variance using repeated measures (ANOVAR)
was used to examine the changes in percentage coral cover and generic
diversity that occurred across sites and through time. Post-hoc Tukey
tests were performed to specify which years and which sites significantly differed from each other. A two-level nested analysis of variance
(ANOVA) was also applied to both coral cover and generic diversity
data, collected in 2015, to compare the means and variances across
sites and stations. The program R (R Core Team, 2015), version 3.1.0,
was used to perform the ANOVAR and ANOVA tests. Power analysis
for a one-sample t-test (Zar, 2010; p. 117) was used to compute the
minimum detectable change in coral cover, and to compute the change
in generic diversity through time at the station, site, and location levels.
The alpha and beta values were arbitrarily set at 5% and 20%,
respectively.
From 2012 to 2015, the average coral cover and average generic diversity on the Tubbataha reefs were 34% (σ ± 1.7) and 18 (σ ± 0.9), respectively. Site 2, along the western slope, had the lowest coral cover at
18% (σ ± 5.3) and the lowest number of genera (15, σ ± 1.9), whereas
Site 3, on the southeastern slope, had the highest coral cover at 56%
(σ ± 4.1) (Fig. 2). Site 1, on the northeastern windward slope, supported the highest number of genera at 20 (σ ± 0.5) (Fig. 3). At the station
level, coral cover ranged from 14% to 57%, and the average number of
genera ranged from 15 to 22.
From 2012 to 2015, there were no significant changes in hard coral
cover (location level ANOVAR, p = 0.484) (Table 1), and no significant
changes in number of genera (location level ANOVAR, p = 0.299) on
the Tubbataha reefs (Table 1; Fig. 2). There were also no significant
changes in coral cover and generic diversity at the site level (p = 0.31
for hard coral cover, and p = 0.67 for generic diversity) (Fig. 3). Coral
cover was unchanged despite two thermal stress events — one in
2013, and the other in 2015 (Fig. 4).
The power analysis indicated that annual changes in coral cover as
small as 3% were detectable at the location level (Table 2), suggesting
that the current sampling protocol is adequate at Tubbataha reefs to detect changes in coral cover, should any changes occur. However, the
minimum detectable change was approximately 7% cover at the site
level, and 9% at the station level (Table 2). Sampling for the number of
genera also appeared adequate, at least at the location level. The
power analysis indicated that changes as small as two genera were detectable at the location level, and changes of three genera were detectable at the site and station levels (Table 2).
There were highly significant differences in coral cover across sites,
but only marginally significant differences in coral cover among stations
(Table 3, Fig. 2). Indeed, the greatest variance in coral cover was apparent among sites (10 km), at 71%, with only 9% variance in coral cover
among stations (Fig. 5). There were no significant differences in the
number of genera among sites and among stations (Table 3, Fig. 3), although most of the variance in the number of genera was apparent
among stations (25%), rather than among sites (13%) (Fig. 5).
Ship groundings, typhoons, and thermal stress events disturbed the
reef slopes of Tubbataha during the four-year study period, yet the coral
assemblages appeared resilient. In 2013, two ship groundings were
monitored, one grounding occurred 1 km from Station 4A. From 2012
to 2015, five tropical storms passed within 350 km of the monitored
reefs. In 2013, one severe tropical storm passed within 40 km of the
reefs, and typhoon Haiyan, the strongest typhoon ever to hit land, was
a Category 3 typhoon when it passed within 350 km of Tubbataha
reefs. In addition, two thermal stress events, one in 2013 and the
other in 2015 (Fig. 4), had no detectable effect on coral cover and diversity, even though 2014 and 2015 were respectively the second warmest
and warmest years on record, globally (NOAA, 2015). Acroporids and
pocilloporids, known for their thermal sensitivity (Marshall and Baird,
2000; Loya et al., 2001; van Woesik et al., 2011, Furby et al., 2013),
remained among the most common genera on Tubbataha through the
study period (electronic supplementary material). Examination of past
data sets suggest no measureable changes have occurred to the
Tubbataha reefs since the declines associated with the 1998-thermal
stress event, from which the reef recovered rapidly (Ledesma and
Mejia, 2002; Dygico et al., 2013). Statistical power of these earlier monitoring studies, however, was limited (unpublished data), even though
the researchers surveyed some of the same stations used in the present
study.
W.Y. Licuanan et al. / Marine Pollution Bulletin 114 (2017) 1135–1140
1137
Fig. 2. Box and whiskers plot of coral cover for all Tubbataha stations monitored from 2012 to 2015. Plotted values are the median, the lower and upper quartiles (25% and 75%), and the
minimum and maximum values (denoted by the whiskers).
Fig. 3. Box and whiskers plot of generic diversity for all Tubbataha stations monitored from 2012 to 2015. Plotted values are the median, the lower and upper quartiles (25% and 75%), and
the minimum and maximum values (denoted by the whiskers).
Despite the lack of measureable change, Tubbataha had high spatial
variability in both coral cover and number of coral genera. There was
greatest variance among sites (10 km), than among transects
(0.01 km) and stations (0.5 km) (Fig. 5). These results suggest that the
reefs were broadly similar among habitats (0.5 km), but were patchy
(0.01 km) within those habitats. The considerable spatial differences
Table 1
Repeated measures ANOVA table for coral cover and generic diversity from 2012–2015,
where p is the probability.
Variable
Source
Degrees of
freedom
Sum of
Squares
Mean
Square
Coral cover
YEAR
SITE:YEAR
Residuals
YEAR
SITE:YEAR
Residuals
3
9
12
3
9
12
67.2
311.6
309.1
17.61
28.72
51.50
22.40
34.62
25.76
5.871
2.191
4.291
Generic diversity
F-value
p NF
0.870
1.344
0.484
0.310
1.368
0.744
0.299
0.666
in coral cover across sites is primarily a consequence of the culmination
of differences in exposure to waves, currents, and light (Done, 1982;
Storlazzi et al., 2005; DeVantier et al., 2006). In contrast, only 13% of
the total variability in generic diversity was due to differences among
sites, whereas 25% of the variability was due to differences among stations, and 62% was due to differences among transects (Fig. 5). This
spatial pattern was consistent over time, except for a slight shift in
variability in the number of genera from the site level to the transect
level in 2013. Such spatial variability is expected when transects are
re-randomized within stations every survey period (Green et al.,
2011). The variability in coral cover, and especially the variability
in number of genera among transects was likely because of small
differences in (i) depth profiles, (ii) monospecific stands of Isopora
brueggemanni, and (iii) the natural heterogeneity of reefs (Aronson
and Precht, 1995; Storlazzi et al., 2005). The consistency in the number of genera across sites suggests that the corals in the different
habitats were drawn from the same larval pool (Done et al., 1991;
Melbourne-Thomas et al., 2011).
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W.Y. Licuanan et al. / Marine Pollution Bulletin 114 (2017) 1135–1140
Fig. 4. Tubbataha sea surface temperature (SST) (°C) and degree heating weeks (DHW) data from January 2011 to January 2016 (data from NOAA Coral Reef Watch).
The average coral cover on the Tubbataha reefs was higher than that
currently found elsewhere in the Philippines, although coral cover was
comparable to other well-managed reefs in the central Philippines
(Stockwell et al., 2009), and on the relatively pristine reefs at Kingman
and Palmyra atolls (Sandin et al., 2008). In particular, coral cover averaged around 24% for 79 reef sites that are part of an ongoing nationwide
assessment in the Philippines (DM Licuanan personal communication).
This estimate was derived using field methods identical to that of the
present work, following a stratified (by biogeographic zone) random
sampling scheme. In comparison, Magdaong et al. (2014) reported a
higher average coral cover of ~36% at 317 sites surveyed from 1981 to
2010 in the Philippines. The discrepancies between these two Philippine
averages are potentially a consequence of: (i) the use of different
methods, (ii) sampling at different depths, (iii) biases involved with
sampling in protected areas. The same authors found coral cover was
5.8% higher in the protected areas in the Philippines than outside the
protected areas. In addition, estimates of coral cover from Tubbataha
are comparable with the 22% (95% confidence intervals of 21% and
23%) coral cover reported in 2003 from 390 sites in the Indo-Pacific
(Bruno and Selig, 2007), and the 33% (± 0.6 SE) coral cover reported
from 1996–2003 from 963 sites in the Indo-Pacific (Bruno et al.,
2009). Yet, Bruno and Selig (2007) estimated that coral cover in the
Indo-Pacific is at least 20% lower than the best estimates of historical
Table 2
Minimum detectable changes in coral cover (delta in absolute percent coral cover) and generic diversity (number of TAUs) using power analysis at various hierarchical levels based
on power analysis of 2012–2015 data; alpha = 5%, beta = 20%.
Coral cover
Location
Site
Station
Tubbataha
Site 1
Site 2
Site 3
Site 4
S1 A
S1 B
S2 A
S2 B
S3 A
S3 B
S4 A
S4 B
baselines. Thus, any new baseline proposed for coral cover can be already considered as ‘shifted’.
The low levels of terrigenous influences and the open ocean setting
produce coral assemblages on atolls, such as Tubbataha, that are different from assemblages on fringing reefs. For example, Acropora tends to
be more common on offshore reefs than on nearshore fringing reefs
(Licuanan et al., 2002; DeVantier et al., 2006). Monospecific stands of
branching and corymbose Acropora frequently lead to high coral
cover, but low generic diversity, on Tubbataha. Therefore, the benchmark for generic diversity may be on average lower on Tubbataha
than elsewhere in the Philippines. This contrast is evident when comparing the work by Huang et al. (2014, 2016), who showed high diversities (398 coral species) in northern Palawan, and in western Luzon
(433 coral species), with work by van Woesik (1996), who reported
260 coral species on Tubbataha. Note that the diversity presented in
the present study are derived from quantitative sampling, within set
areas (75 m × 25 m stations), and should not be directly compared
with systematic searches for species over large extents of reef.
The Tubbataha reefs are relatively undisturbed by local human populations, and are as close to pristine as is possible, for a modern reef in
Asia (Nañola et al., 2011). Moreover, the reefs are under a high level of
management, and are protected from fishing pressure. Considering
the diversity, and the high threat levels to Philippine reefs in general
(Burke et al., 2011), coral cover on Tubbataha can serve as a useful
benchmark for what is currently possible in the region. The relative geographic remoteness and high conservation status of Tubbataha also appear to provide relatively high resilience to regional stresses, at least for
now, although a rapidly warming ocean will test that resilience.
Generic diversity
Variance
Delta
Variance
Delta
2.8
8.01
28.2
16.91
10.01
6.71
18.46
16.72
64.04
78.05
15.96
25.94
3.39
3%
5%
9%
7%
6%
5%
8%
7%
14%
15%
7%
9%
4%
0.73
0.26
3.62
1.91
1.93
2.47
0.36
4.68
13.26
0.87
6.67
3.21
1.1
2
1
4
3
3
3
1
4
7
2
5
3
2
Table 3
Two-level nested ANOVA table for coral cover and generic diversity in 2015, where p is the
probability.
Variable
Source
Degrees of
freedom
Sum of
Squares
Mean
Square
F-Value
p NF
Coral Cover
SITE
STATION(SITE)
Error
Total
SITE
STATION(SITE)
Error
Total
3
4
32
39
3
4
32
39
6568
1051
2990
10,609
26.8
69.2
253.6
349.6
2189.4
262.8
93.4
23.43
2.81
b0.0001
0.0416
8.933
17.3
7.925
1.13
2.18
0.3527
0.0933
Generic
Diversity
W.Y. Licuanan et al. / Marine Pollution Bulletin 114 (2017) 1135–1140
1139
Fig. 5. Percentage variance in coral cover and in generic diversity per level of sampling, from 2012 to 2015.
Acknowledgments
We thank the editor and the anonymous reviewer for comments and
suggestions that greatly improved the manuscript. This work was partially supported by the Department of Science and Technology and the
respective organizations of the authors.
Appendix A. Supplementary data
Supplementary data to this article can be found online at http://dx.
doi.org/10.1016/j.marpolbul.2016.10.017.
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