Ocean Sci. J. (2019) Available online at http://link.springer.

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http://dx.doi.org/10.1007/s12601-019-0002-1

Article

pISSN 1738-5261
eISSN 2005-7172

Practical Resilience Index for Coral Reef Assessment

Imam Bachtiar1,2*, Suharsono3, Ario Damar4, and Neviaty P. Zamani5
1
Department of Math and Science Education, Faculty of Teacher Training and Education, University of Mataram, Kota Mataram
83125, Indonesia
2
Department of Magister Pendidikan IPA, Program Pascasarjana, University of Mataram, Kota Mataram 83125, Indonesia
3
Research Center for Oceanography, Indonesian Institute of Sciences, Jakarta 12710, Indonesia
4
Department of Aquatic Resources Management, Faculty of Fisheries and Marine Science, Bogor Agricultural University, West Java
16680, Indonesia
5
Department of Marine Science and Technology, Faculty of Fisheries and Marine Science, Bogor Agricultural University, West Java
16680, Indonesia

Received 14 January 2018; Revised 9 May 2018; Accepted 27 September 2018

 KSO, KIOST and Springer 2019

Abstract  Assessing coral reef resilience is an increasingly 2007) and human-induced stress and disturbances (Jackson
important component of coral reef management. Existing coral reef 1997; Jackson et al. 2001). Coral reef management can mitigate
resilience assessments are not practical, especially for developing the potential impact of these disturbances by improving
countries. South-east Asian countries have been using line-intercept- coral reef resilience (Hughes et al. 2007; Hoegh-Guldberg et
transect (LIT) in coral reef monitoring for a long time. The present al. 2007) regardless of its ecological limitations (Mora et al.
study proposes an index for assessing coral reef resilience based on
2016). Ecological resilience in terms of capacity to recover
data collected from the LIT method. The resilience index formula
was modified from an existing resilience index for soil communities from disturbance to the same level of organization (Holling
developed by Orwin and Wardle. We used an ideal resilient coral 1973) is increasingly important in coral reef management.
reef community as a reference point for the index. The ideal coral The theory of resilience has improved to the point where it
reef was defined from data collected from 1992 to 2009. Six variables should be able to be implemented in coral reef management
were statistically selected for the resilience indicators: coral functional practices (Nystrom et al. 2008).
group (CFG), coral habitat quality (CHQ), sand-silt cover (SSC),
Resilience assessment of coral reef ecosystems, however,
coral cover (COC), coral small-size number (CSN), and algae-
other-fauna (AOF) cover. Maximum values of five variables were is still at a development stage (Lam et al. 2017). At present,
determined as the best state, while the maximum value of CSN was two methods have been available for measuring coral reef
determined from 1240 data-sets of Indonesian reefs. The resilience resilience. Obura and Grimsditch (2009) provided a comprehensive
index performed well in relation to changes in COC, AOF, and SSC method which included 61 variables and 5 protocols. This
variables. Managers can use this tool to compare coral reef resilience large number of variables and protocols requires significant
levels among locations and times. This index would be applicable
financial support and considerable expertise, unlikely to be
for global coral reef resilience assessment.
available in developing countries. Maynard et al. (2010)
Keywords  recovery, food security, reef health, indicators, developed a more practical method in assessing coral reef
monitoring
resilience. This only needs a discussion forum to collect data
based on the personal judgment of managers, scientists, policy
1. Introduction makers, and other important stakeholders. This method could
be very practical in many countries, but it needs people with
Coral reef ecosystems are increasingly affected by global sufficient knowledge in coral reef ecology. In many developing
climate change (Kleypas et al. 1999; Hoegh-Guldberg et al. countries where coral reef scientists are rare, the Maynard
*Corresponding author. E-mail: [email protected] method might still be hard to implement. McClanahan et al.
2 Bachtiar, I. et al.

(2012) listed 11 key factors of coral reef resilience, but how the resilience index developed in the present study, a coral
the factors will be used in management is not yet formulated. reef manager will be working with multivariate data but
Cumming et al. (2016) reviewed resilience theory on social- interpreting them in a univariate way.
ecological systems that might be very difficult to use in
management because of its complexity. A new practical resilience 2. Methods
assessment is therefore needed for coral reef management in
developing countries with few coral reef ecologists. Data collection
The aim of the present study was to formulate an index for The present study used monitoring data collected by the
assessing the resilience state of a coral reef ecosystem using Research Center of Oceanography (RCO), Indonesian Institute
multivariate data extracted from line intercept transects of Sciences (Bahasa Indonesia, LIPI). All the collected data
(LIT). LIT has been widely used and extensively learned were taken from LIT methods by trained- and supervised-
about in the region of ASEAN countries, including Indonesia researchers of the same institution. Data were collected
(English et al. 1994; Suharsono 2008). This method would within the period of 1992–1998 and 2009; all 1240 transects
be practical in resilience assessment of the ASEAN countries. were 10 m length. This long period may provide samples of
Despite the range of multivariate data available from LIT the best and the worst coral reefs resilience levels in Indonesia.
(Marsh et al. 1984; English et al. 1994), the majority of In the first period LIT were laid at various depths, from 3 to
extracted data is merely living coral cover (%). Coral reef 15 m; in the second period LIT were at ~5 m depth. All
managers mostly did not know how to integrate multivariate positions of transect sites in 2009 were recorded aboard
data into a single interpretation of the quality of a coral reef using GPS (Global Positioning System).
ecosystem. Lam et al. (2017) found that existing coral reef The resilience index calculation is based on a transect unit.
resilience assessment and monitoring programs differ as The LIT data used in the present study could spatially represent
much as 75%. Here, we show that data collected on an the coral reefs of Indonesian waters (Fig. 1). Data collected
ordinary monitoring program can also be used in resilience in 2009 encompassed coral reefs of the Indian Ocean (Tapanuli
assessment. Coral reef resilience is defined as recovery Tengah, Nias, Nias Selatan, Mentawai), Indonesian Seas
potential to a coral predominated community. When using (Sunda Strait, Karimata Strait, Makassar Strait, Java Sea,

Fig. 1. Locations of data collection used in the present study. Locations with green background showed data collected in 1992–1998,
light-brown background showed data in 2009
 Practical Resilience Index for Coral Reef Assessment 3

Flores Sea, Arafura Sea), South China Sea (Natuna, Bintan), between before and after disturbance at impact community.
and Pacific Ocean (Biak, Raja Ampat). The older data The ecological index modification has two main processes,
(1992–1998) added locations at the Java Sea (Seribu Islands, i.e. determining indicator variables and building the formula.
Karimun Jawa), Sunda Strait (Bakahauni, Merak) and Raja Indicator variables were identified from a literature review
Ampat. The older data provided some reference to earlier coral and classified into six resilience components: biological
reef conditions when anthropogenic impacts were smaller legacy, structural legacy, and mobile link (Lundberg and
and the intervals between natural disturbances (bleaching) Moberg 2003), coral reef regimes (productivity), herbivory,
were longer. These data were all used to compose the “resilient and water quality. These variables are briefly discussed in
coral reef” as the reference point in the formulation of the this paper and listed in Table 1.
resilience index. (a) Biological legacy, i.e. surviving coral colonies. It has
been long understood that coral species exhibit different
Data analysis resistance to the same disturbance (Brown and Suharsono
The coral reef resilience index used in this study was a 1990; Ninio and Meekan 2002). Surviving colonies could
modification of the soil community resilience index developed enhance recolonization of opened spaces from both larvae
by Orwin and Wardle (2004). The modification included produced (Miller and Mundy 2003; Starger et al. 2010) and
redefining indicator variables and constructing a single vegetative propagation (Golbuu et al. 2007; Williams et al.
reference (control) community. The original formula of the 2008). Biological legacy is therefore related to biological
Orwin and Wardle (2004) index was diversity (Peterson et al. 1998) and larval dispersal. In the
present study, diversity at genera level (coral genera
2  D0 
RSt = ------------------------------- –1 richness, CGR) and functional level (coral functional group,
 D 0  +  Dx 
CFG) were used to represent biological diversity. Species
RSt = Resiliece index at t, D0 = difference between before and richness is hard to determine on LIT since coral taxonomists
after disturbance at control community, Dx = differerence are rare in many developing countries (Erdinger and Risk

Table 1. Indicator variables used in development of the coral reef resilience index
Components Variables Unit Justifications References
a) Biological legacy Coral genera richness (CGR) # genera High resistance, surviving Miller and Mundy (2003);
(Biodiversity) colonies contribute to sexual Williams et al. (2008);
and asexual recruitment Starger et al. (2010)
Coral functional group (CFG) # life form Functional diversity augment Bellwood et al. (2004)
robust community
b) Structural legacy Coral massive and sub-mas- % CM+CS covers High resistance, high habitat com- Erdinger and Risk (2000);
(Complexity) sive cover (CMS) plexity, but low water quality Ninio and Meekan (2002)
Unsuitable settlement % sand and silt covers Inhibit coral settlement and Hodgson (1990);
substrate (SSC) growth Babcock and Davies (1991)
c) Mobile link Coral colony size (CCS) #size classes Continuing recruitment Peterson et al. (1998)
(Recruitment) classes; 10 cm interval increase recovery
Coral small-size colonies #small colonies Existing recruitment enhance Van Moorsel (1985);
(CSN); D  10 cm recovery Golbuu et al. (2007)
d) Productivity Coral cover (COC) % coral cover Healthy coral reef, high Done (1992); Hughes (1994)
(Regimes) productivity
Algal total cover (ATC) % algal cover Unhealthy reef, low herbivory Done (1992); Hughes (1994);
Bahartan et al. (2010)
Other fauna cover (OTF) % OTF cover Unhealthy reef, low productivity Tkachenko et al. (2007);
Cruz et al. (2016)
e) Herbivory Macroalgal cover (AMC) % cover Unhealthy reef, low herbivory Hughes et al. (2007);
Roff and Mumby (2012)
f) Water quality Coral acroporiid cover (CAC) % acroporidae cover Good water quality, rapid Done (1982);
recovery, but low habitat Erdinger and Risk (2000);
complexity Roff and Mumby (2012)
4 Bachtiar, I. et al.

2000). It is assumed that adequate coral larval recruitment indicator variable of herbivory intensity, however, might not
will occur with sufficient coral colonies. be very appropriate. Phase-shift could happen without
(b) Structural legacy, i.e. habitat complexity and settlement reduction on herbivorous fishes abundance, e.g. in the Great
substrate availability. A complex habitat provides a suitable Barrier Reefs (Cheal et al. 2010). Important herbivores are
substrate for larval settlement, hosts fish diversity (Wilson et dependent on the composition of the algal community (Fox
al. 2007), and maintains herbivory processes (Ledlie et al. and Bellwood 2008; Hoey and Bellwood 2008). Redundancy
2007). Previous studies measured habitat complexity using of herbivory roles between herbivorous fishes and sea urchins
a spatial index (Rogers et al. 1983), surface index (Robert could also vary among locations (Carpenter 1990). A coral
and Ormond 1987), or visual assessment (Wilson et al. 2007). In reef could still maintain its resilience in conditions of low
the present study, habitat complexity was indicated by abundance abundance of herbivorous fishes, when sea urchins are
of massive- and sub-massive- corals (CMS). Both coral life sufficiently abundant (Hughes 1994). Furthermore, important
forms are structurally resistant to biological and physical herbivory could be carried out by non-herbivorous fishes,
disturbances when other coral life forms (branching, foliose, such as Platax pinnatus (Bellwood et al. 2006). In the present
encrusting, etc.) become rubble. Availability of settlement study, abundance of macroalgae (AMC) and total algal
substrate is also very important to facilitate sexual coral abundance (ATC) were used as indicator variables of
recruitment. Measuring unsuitable settlement substrate (USS) herbivory. Both indicator variables could represent the impact
is easier than the opposite, since some suitable settlement of herbivory intensity and nutrient availability (Littler et al.
substrates may have been temporarily occupied by benthic 2006).
community. (e) Ecosystem productivity. Coral reefs exhibit multi-stable
(c) Mobile link, i.e. incoming mobile organism. Planulae states with different productivity levels. Highly productive
larvae are one of the important mobile link organisms that coral dominated communities could shift into alternate
facilitate coral recolonization. Incoming fish and other benthic stable states which are predominated by macroalgae (Hughes
larvae and juveniles are also important but indirectly related 1994), soft corals (Fox et al. 2003), or anemone (Tkachenko
to coral recolonization and therefore do not directly affect et al. 2007). Indicator variables that represent the productivity
coral reef recovery. In the present study, coral colony size of a coral reef ecosystem are COC (coral cover), OTF (other
was chosen as an indicator of incoming coral recruitment. fauna cover), and ATC (algae total cover). A high productivity
When recruitment is continuing, the range of the coral colony coral reef should be high in COC but low in OTF and ATC
size should be wide. This condition could be indicated by the variables.
number of colony size classes (coral colony size-classes, (f) Water quality. While temperature, chlorophyll and turbidity
CCS), at 10 cm intervals. The abundance of the smallest can be easier to measure than nutrients and contaminants in
colony size ( 10 cm) could also indicate current coral reef waters, they still require more specialized equipment
recruitment. Indicator variable of coral small-size number and training, difficult to access in a developing country. To
(CSN) is chosen to represent the mobile link, coral recruitment simplify assessment, a bioindicator can be chosen to represent
or colonization. Marsh et al. (1984) provided a formula for water quality. Particular coral species such as Acropora have
measuring colony diameter on a line transect which is too been linked with good water quality (Done 1982; Erdinger
complex for coral reef managers. In this study, colony size and Risk 2000). Thus the cover acroporid corals (CAC)
was defined as the length of colony size at the intercept. This were used as an indicator variable of good water quality.
approach would not affect the results of the study as colony Among the 11 variables in Table 1, there were variables
size measurement was not one of the objectives. Confounding that need to be combined. There were variables having small
data on CSN might happen whether it comes from recruitment abundance but high variances, i.e. algae total cover (ATC),
or coral fragment. This could also be neglected since index macroalgae cover (AMC), and other fauna cover (OTF).
as an ecological indicator will be working on a macro scale These variables are ecologically important but statistically
instead. McClanahan et al. (2012) also recognized coral size too small to detect their effect. ATC, AMC and OTF variables
distribution as important factor in coral reef resilience. were therefore combined as one variable AOF (algae and
(d) Intensity of herbivory is an important factor controlling other fauna) so that its importance will not be neglected in
algal abundance on reefs. Using herbivorous fishes as an statistical analysis.
 Practical Resilience Index for Coral Reef Assessment 5

There were also variables with contrasting characteristics. select environmental variables or species that best explain
Coral massive + sub-massive (CMS) cover and coral acroporid community pattern. Reduction of the number of variables
cover (CAC) play different roles in ecosystem resilience. could be carried out using BEST analysis, as long as its
High CMS cover could indicate high coral reef complexity correlation coefficient is higher than 95% (Clarke et al. 2008).
but it could also indicate poorer water quality and slow recovery. Prior to data analysis, data were transformed into log (x + 1)
Massive and sub-massive corals found on inshore reefs are and normalized, since some variables had different scales.
relatively tolerant to low water quality from sedimentation PCA (Principal Component Analysis) was performed to
and land-based pollution (Erdinger and Risk 2000). In contrast, weight each indicator variable based on its contribution to
high CAC could indicate less coral reef complexity but also the first principal component, as suggested in Primpas et al.
indicates rapid recovery (Ninio and Meekan 2002). Both (2010). All multivariate statistics were carried out using
CMS and CAC are equally important in determining coral Primer 6 version 6.1.13 software.
reef resilience.
Combining CMS and CAC into a single variable CHQ 3. Results
(coral habitat quality) needs a special approach, based on
existing studies on Indo-Pacific reefs. Cumulative coverage Refining indicators
of CMS and CAC has a maximum value of 100%. It was After grouping the five indicator variables (CAC and
therefore assumed that the best resilience of a coral reef CMS as CHQ; AMC, ATC, and OTF as AOF), there were 8
would be composed of 50% of CMS and 50% of CAC. This remaining indicator variables of coral reef resilience. Among
composition ensures rapid coral recovery as CAC (Ninio these, three variables were interdependently related, i.e. COC,
and Meekan 2002) promotes high growth rates and adaptation AOF and SSC. Potentially, coverage of COC and AOF is
(Guest et al. 2016), and CMS promotes habitat complexity dependent on the coverage of SSC, i.e. sand and silt covers.
by maintaining the abundance and diversity of herbivorous Maximum cover of COC and AOF is 100%, when SSC is
fishes (Ledlie et al. 2007; Guest et al. 2016). CHQ is mathematically zero. The maximum cover of COC and AOF decreases with
calculated as follows: increasing SSC.
Among 8 indicator variables of the resilience index, many
CHQ = CAC*  CMC + CSC  variables showed significant correlation, as the number of
CAC=coral Acropora cover, CMC=coral massive cover, data was robust (N = 1240 transects). Two pairs of variables
CSC=coral sub-massive cover showed a considerably high correlation index. Correlation
indices between CFG and CGR was 0.691, and between
Algal and other fauna (AOF) was defined to integrate COC and CCS was 0.833 (Table 2). The number of variables
AMC, ATC and OTF. Data of Indonesian coral reefs showed needs to be reduced, to avoid redundancy and to improve its
that each AMC, ATC and OTF variables have a very high applicability without significant reduction in the quality of
coefficient of variability, i.e. 349%, 87%, and 140% respectively. the index.
The three variables were then pooled into a new variable, BEST analysis provided combinations of seven and six
AOF, which is the sum of total algal cover (ATC) and other variables that may be used to reduce the number of variables.
fauna cover (OTF). Macroalgal cover (AMC) is part of the The highest priority for omission is the coral genera richness
ATC. They were separately measured as different variables (CGR) due to difficulties in underwater genera identification.
since macroalgae predominance has been shown to be the From the BEST combinations (Table 3), while six or seven
most common phase shift condition on coral reefs (Hughes variables do not reduce the performance very much, in contrast
1994; Hughes et al. 2007). there is a huge difference in the effort spent on measurement.
Statistical analysis was applied to refine indicator variables. It was decided to omit CGR and CCS from indicators of
Pearson correlation index was calculated to identify redundancies coral reef resilience. Leaving out CGR and CCS variables
among variables. Non-parametric multivariate statistics, BEST the index still maintained representativeness of each resilience
(Biological Environmental STepwise) analysis was applied component, CFG represents biodiversity and CSN represents
to find the best combinations in variable reduction for mobile link resilience components.
several correlated variables. BEST is a multivariate tool to
6 Bachtiar, I. et al.

Table 2. Matrix of correlation coefficients among eight resilience variables (N = 1060)

CGR CFG SSC CHQ CCS CSN COC AOF
CGR 1.000
CFG 0.691 1.000
SSC -0.224 -0.277 1.000
CHQ 0.299 0.550 -0.222 1.000
CCS 0.343 0.382 -0.287 0.395 1.000
CSN 0.512 0.443 -0.155 0.055 0.015 1.000
COC 0.511 0.526 -0.389 0.478 0.833 0.175 1.000
AOF 0.046 0.023 -0.113 -0.100 -0.280 0.123 -0.313 1.000

Table 3. Combinations of seven and six variables provided by BEST analysis

No. Number variables Correlation index Variable combinations Omitted variable
1 7 0.992 CGR, SSC, CHQ, CCS, CSN, COC, AOF CFG
2 7 0.991 CFG, SSC, CHQ, CCS, CSN, COC, AOF CGR
3 7 0.990 CGR, CFG, SSC, CHQ, CCS, CSN, AOF COC
4 7 0.988 CGR, CFG, SSC, CHQ, CSN, COC, AOF CCS
5 6 0.974 CGR, SSC, CHQ, CSN, COC, AOF CFG, CCS
6 6 0.973 CGR, SSC, CHQ, CCS, CSN, AOF CFG, COC
7 6 0.973 CFG, SSC, CHQ, CSN, COC, AOF CGR, CCS
8 6 0.971 CFG, SSC, CHQ, CCS, CSN, AOF CGR, COC
9 6 0.970 CHQ, CCS, CSN, SSC, COC, AOF CGR, CFG
10 7 0.969 CGR, CFG, CHQ, CCS, SSC, COC, AOF CSN

Defining a reference community its maximum value from transects was 23 colonies, the
An ideal ‘resilient’ coral reef must be set up as a reference maximum value of CSN was set up at 25, which has a very
community of the index. It must show a maximum value of low probability of occurrence (0.048%).
resilience index, which happens when it has maximum
values in all six indicator variables. On the other hand, a Formulating resilience index
‘non-resilient’ coral reef must have a minimum value of index. The coral reef resilience index uses a single reference
Among the six indicator variables, the maximum and minimum community, the ideal resilient coral reef community, i.e. a
theoretical values of five variables are known. Coral cover community with the best (maximum) values in all n indicator
(COC), for example, theoretically has a minimum and variables. Orwin-Wardle index modification resulted in a
maximum value of 0.00 and 100.00% respectively (Table 4). coral reef resilience index as described in Eq. 1.
Coral functional group (CFG), i.e. coral life form, theoretically n 2  Xi max – Xi min 
between 0–13 groups, as it has been standardized in English RIj = 
i=1
------------------------------------------------------------------------------
 Xi max – Xi min  +  Xij – Xi min 
-–1 (1)
et al. (1994). The theoretical maximum value of one variable,
CSN, however, was not known. The maximum value of RIj = Resilience index of transect j, Ximax = maximum
CSN was therefore determined from 1240 transects. Since value of variable Xi., Xi.min = minimum value of variable Xi.,

Table 4. Variable composition of the “super coral reef” as the reference point of the resilience index assessment
Resilience indicator From transects Unit Minimum Maximum
1) Coral Functional Group (CFG) 0–10 Group 0 13
2) Sand and Silt cover (SSC) 100–0 % 100 0
3) Coral Habitat Quality (CHQ) 0–42 % 0 50
4) Coral Small-size Number (CSN) 0–23 Colony 0 25
5) Coral Cover (COC) 0–100 % 0 100
6) Algae-Other-Fauna cover (AOF) 100–0 % 100 0
 Practical Resilience Index for Coral Reef Assessment 7

Table 5. Weighting factors of the indicator variables Using the present index, a single transect has a theoretically
Indicator variables PC 1 resilience index between 0.000 and 2.130, but we hardly find
CFG -0.560 coral reef with a resilience index more than 1.00. Assessment of
SSC 0.204 ~1240 transects from Indonesian reefs revealed a range
CHQ -0.423 between 0.021 and 1.070, with an average (± SD) of 0.468 ±
CSN -0.430
0.225, and a median of 0.469. Proportion of transects with a
COC -0.520
resilience index  1.000 was only 0.403%. This proportion
AOF 0.103
is very small and not usually found in natural habitats.
Furthermore, resilience index assessment on a reef must be
Xij = real value of Xi at transect j. carried out using more than one transect, as such assessment
Using data of the resilient coral reef, the formula for the needs replications. From the present data, at any location
coral reef resilience index is defined as follows. (site) with a minimum of three transects, there was no reef
with an average resilience index of  1.000. The highest
2  13 – 0  2  50 – 0 
RI =  -------------------------------------------------- – 1 +  -------------------------------------------------- – 1 average resilience index (± SD) found was 0.976 ± 0.107.
  13 – 0  +  13 – CFG     50 – 0 +  50 – CHQ  
Theoretically, we rarely encounter any reefs with a resilience
2  25 – 0  2  100 – 0 
+  ------------------------------------------------
- – 1 +  -------------------------------------------------------- – 1
   index  1.000.
 25 – 0 +  25 – CSN   100 – 0  +  100 – COC

2  100 – 0  2  100 – 0 
  -----------------------------------------------
- – 1 –  ------------------------------------------------- – 1
  
(2) Validating resilience index
 100 – 0  +  SSC – 0   100 – 0 +  AOF – 0 
Comparing resilience index with COC, AOF and SSC
Each indicator variable in Eq. 2 might have a different showed a positive relationship between the increase of COC
magnitude of contribution to the index, as they could have and an increase in the resilience index. On the other hand, an
different variances. Indicator variables need to be weighted increase in AOF and SSC coincided in a decrease in the
to improve index sensitivity. PCA was performed to objectively resilience index. Recovery of a coral dominated community
weight each of the resilience indicators. PCA showed that depends on the composition of the coral community and the
the PC1 contributed 47.7% of the total variances. This number other two opposing factors, AOF and SSC. This suggests
determined its liability to be used as a weighting factor. that coral cover alone may not be a good measure of coral
Variables were weighted using PC1 as listed in Table 5. reef resilience since it does not necessarily show diversity of
Weighting of indicator variables changed the index value. coral functional group and coral recruitment.
The maximum value of the resilience index was 1.930, while The resilience index provides a more meaningful metric
the minimum was -0.200. A correction factor is required to for assessment of resilience levels than coral cover, although
ensure that the minimum value was close to 0.000, i.e. when regression analysis for both variables COC and AOF shows
a coral reef was 100% covered by SSC (sand and silt). The its significant dependency. Resilience index increases with
final formula of the coral reef resilience index is as Eq. 3 or 4. increasing coral cover but decreases with increasing algal-
2  13 – 0  2  50 – 0 
other-fauna and sand-silt covers (Fig. 2). Coral reefs with poor
RI = 0.56  -------------------------------------------------- – 1 + 0.42  -------------------------------------------------- – 1 coral cover (< 25%) show a wide range of resilience levels,
  13 – 0  +  13 – CFG     50 – 0  +  50 – CHQ 
from 0.021 to 0.663. Coral reefs with algal cover > 50%,
2  25 – 0  2  100 – 0 
+ 0.43  ------------------------------------------------
- – 1 + 0.52  -------------------------------------------------------- – 1
   however, have a resilience index range between 0.100 and
 25 – 0  +  25 – CSN   100 – 0 +  100 – COC 
0.802. This high resilience index was found at a transect in
2  100 – 0  2  100 – 0 
0.20  -----------------------------------------------
 100 – 0  +  SSC – 0  
- – 1 – 0.10  ------------------------------------------------- – 1 +0.20 (3)
  100 – 0  +  AOF – 0  
Biak (BIALT11) which has 36.0% COC and 52.4% AOF.
Coral reef with the best resilience index (1.000) may still
26 100
RI = 0.56  -------------------------------------- – 1 + 0.42  -------------------------------------- – 1 have AOF about 0 and 17%, with coral cover ranging from
 13 +  13 – CFG    50 +  50 – CHQ 
71.0 to 89.70%.
50 200 The present resilience index is also readily applicable for
+ 0.43  ------------------------------------
- – 1 + 0.52  -------------------------------------------
 
- – 1

25 +  25 – CSN  100 +  100 – COC 
extreme situations. An extreme reef which is covered by
200 200 100% sand and silt (SSC) will have a resilience index of
 0.20 ---------------------------------------
- – 1 – 0.10  ------------------------------------------ – 1 + 0.20 (4)
  
 100  +  SSC – 0   100  +  AOF – 0  0.000. This means that such a reef would never be recolonized
8 Bachtiar, I. et al.

Fig. 2. Performance of resilience index in relation to COC, AOF, and SSC

by coral communities. A transect with 100% algal or soft

coral (AOF) covers will have a resilience index of 0.047,
while a transect that has 100% ruble cover will have a resilience
index of 0.094. Regarding these situations, coral population
recovery is still possible and dependent on other ecological
processes.
The present index can be used to compare the resilience
status of coral reefs among locations and times. Fig. 3A
shows coral reef resilience indices among four locations in
the Province of Kepulauan Riau, Indonesia. Using this index
we could also determine that coral reef resilience was
significantly different among the four locations (F = 3.935,
df = 3,225, P < 0.01). Coral reef resilience is dynamic as a
results of its interaction with fluctuating stress and disturbances
from the surrounding environment over time. Fig. 3B shows
how the present index compares temporal variation in coral
reef resilience. These figures confirmed the practical uses
of the index to detect resilience variation spatially and
temporally.

4. Discussion

The present study shows that assessment of coral reef

resilience level can be carried out using LIT data. Using this
index, managers are able to more objectively compare resilience
Fig. 3. Comparison of coral reef resilience indices among locations
levels spatially among coral reefs and more accurately make
(A) and times (B). Error bars indicate 1 SE decisions on coral reef management. They could also describe
 Practical Resilience Index for Coral Reef Assessment 9

temporal variation of the resilience level to predict future cover (Golbuu et al. 2007; Gilmour et al. 2013; Graham et al.
trends for management purposes. 2015) and community composition or species diversity
The present resilience index is merely ecological resilience. (Brown and Suharsono 1990; Done et al. 1991; Smith et al.
Several authors have proposed employing a more complicated 2008). Returning coral cover could take place over a decade,
resilience measurement which covers not only ecological but returning species diversity might need many decades.
but also physical oceanography, social factors, and management The present index supports the efforts of Timpane-Padgham
practices (Maynard et al. 2010; Obura and Grimsditch 2009; et al. (2017) to integrate resilience metrics in coral reef
Cumming et al. 2016). Such coral reef resilience measurements restoration efforts. Using the resilience index, coral reef recovery
are more comprehensive than the present study, but they are does not only mean recovery of coral cover but also functional
also impractical for coral reef managers. The present study group diversity, habitat quality and recruitment.
provides a complementary resilience index to Maynard’s The present resilience index would be globally applicable,
index. The Maynard’s index provides a broad assessment of since reference points of all variable indicators were theoretically
the resilience state, while this present resilience index focuses their maximum values. Only the CSN value was determined
on ecological assessment. from data collected from Indonesian waters. Since many
The resilience state represented by the index may only Indonesian waters show the best places for coral growth
operate maximally under good management practices. Improper (Tomascik et al. 1996) and center of coral diversity (Veron et
management could impose additional stress and disturbances al. 2009), it might be inferred that the best in Indonesia might
on coral reefs. The resilience index should be viewed as the also represent the best state worldwide. This means that the
resilience state of coral reef ecosystems at the time of assessment. maximum value of CSN on the index would also be the
A resilience index will likely decrease in response to maximum value in most other coral reef areas in the world.
disturbances, due to reduction in coral cover, loss of coral Furthermore, the index can be easily adapted to various
functional groups, increasing coverage of rubble, or increasing transect lengths by using new CSN values related to the
algae and other fauna cover. transect length, for example 30 or 50 meter length. The CSN
The present index is very practical. A coral taxonomist or variable is additively linear to transect length.
biologist is not always available in many provinces in The resilience index needs to be interpreted in relation to a
Indonesia. Coral genera richness (CGR) is therefore omitted specific disturbance. Carpenter et al. (2001) advised that
from the operational resilience indicators. Obura and Grimsditch resilience measurement should clearly compare the resilience of
(2009) resilience assessment uses 61 indicators covering ‘what to what’. Interpretation of the resilience index used in
ecological, social, physical, and management factors. This this study should be developed for that purpose. When a
complex resilience measurement would require a high level coral reef with a resilience index of 0.450, for example, is
of financial support and a lot of expertise. On the other hand, reduced to 0.250 due to coral bleaching, the length of time
the use of the present index can be utilized by nearly all coral for recovery to its former state is important. Time series data
reef managers with basic training experience in the LIT from permanently laid LIT, particularly in areas of mass
method and a spreadsheet computer program. coral mortality related to bleaching, will assist in further
The resilience index enable managers to make the right development and interpretation of the resilience index. It is
management decisions. When SSC is high due to coastal recommended that the index should be validated through
erosion, a possible management response is to deploy suitable application by coral reef researchers from other Indo-Pacific
settlement substrate to reduce SSC cover, for example concrete regions.
blocks (Bachtiar 2002) or reef balls (Bachtiar and Prayogo In the future, index interpretation should also be developed
2010). However this would only be practical if erosion or the in relation to human-induced acute disturbances, such as
disturbance could be reduced over the long term. blast fishing and ship grounding. Index interpretation in relation
The index may be used as an alternative and predictive to chronic disturbance might be best used as a warning signal of
measurement of coral reef recovery after disturbance. Recovery a potential greater ecological loss if it is accompanied by an
of the ecosystem may be measured in terms of time to return acute disturbance. This system of resilience index assessment
to a former pre-disturbance resilience index. Conventional needs to be developed as a standard protocol.
recovery time has mostly been measured as returning coral
10 Bachtiar, I. et al.

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