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Resilience of coral recruits in Gulf of Mannar Marine Biosphere Reserve (GOMMBR), India
Journal Pre-proof Resilience of coral recruits in Gulf of Mannar Marine Biosphere Reserve (GOMMBR), India Machendiranathan M., R. Ranith, L. Senthilnathan, A. Saravanakumar, T. Thangaradjou
PII: DOI: Reference:
S2352-4855(19)30043-X https://doi.org/10.1016/j.rsma.2020.101055 RSMA 101055
To appear in:
Regional Studies in Marine Science
Received date : 18 January 2019 Revised date : 1 January 2020 Accepted date : 5 January 2020 Please cite this article as: Machendiranathan M., R. Ranith, L. Senthilnathan et al., Resilience of coral recruits in Gulf of Mannar Marine Biosphere Reserve (GOMMBR), India. Regional Studies in Marine Science (2020), doi: https://doi.org/10.1016/j.rsma.2020.101055. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
© 2020 Published by Elsevier B.V.
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RESILIENCE OF CORAL RECRUITS IN GULF OF MANNAR MARINE BIOSPHERE RESERVE (GOMMBR), INDIA Machendiranathan M*1, 2, R. Ranith3, L. Senthilnathan4, A. Saravanakumar2, T. Thangaradjou5
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1. College of Ocean and Meteorology, Guangdong Ocean University, Zhanjiang– 524088, Guangdong, China.
2. Centre of Advanced Studies in Marine Biology, Faculty of Marine Sciences, Annamalai University, Parangipettai – 608502, Tamilnadu, India.
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3. Fishery Environment Management Division, Central Marine Fisheries Research Institute (CMFRI), Kochi - 682018, Kerala, India.
4. Marine Science & Technology Lab, Department of Harbor and Ocean Engineering, Academy
Tamilnadu, India.
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of Maritime Education and Training AMET (Deemed to be University), Chennai - 603112,
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5. Science and Engineering Research Board (SERB), New Delhi – 110070
Corresponding Author:
Dr. M. Machendiranathan*1, 2
Email ID: [email protected]
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Phone: +86 18934225446
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ABSTRACT Interaction between climate change and resilience of the coral recruits will determine the future of the coral reefs. The recently emerged resilience mapping has provided adequate
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information on spatial planning for marine protected /unprotected area conservation measures. The present study has dealt with mapping the resilience of coral recruits in the Gulf of Mannar Marine Biosphere Reserve (GOMMBR), India. The resilience indicators are macroalgae, sedimentation, substratum, herbivore biomass, bleaching prevalence, disease prevalence, temperature variability, photosynthetically active radiation (PAR), and depth of the site. Our benthic survey encountered 103 coral recruits sites with selected coral species of Montipora digitata (41) Acropora nobilis
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(28), Montipora aequituberculata (23), Echinopora lamellosa (9) and Acropora humilis (2). Among the 103 sites, 12 coral recruits sites showed high resilience, while medium and low
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resilience was observed in 75 and 16 sites, respectively. Our survey observations evidently demonstrated that frequent macroalgae such as Caulerpa scalpelliformis (49), Caulerpa racemosa (29), Ulva reticulata (11), Turbinaria ornata (5), Chaetomorpha linum (4), Turbinaria conoides
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(3) and Kappaphycus alvarezii (2), were identified as a major hindrance to coral recruits. The results of principal component analysis (PCA) showed that sedimentation, macroalgae, and temperature variability were the factors playing a major role among different sites. Among the islands of GOMMBR high resilience of coral recruits found in the Pulivinichalli and Upputhanni islands. While, low resilience sites observed in the islands of Krusadai, Hare, Thalaiyari, Appa,
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Valimunai, Koswari, and Van. Altogether, the present study provides a clear spatial view on the resilience situation of the GOMMBR corals recruitment. Altogether, in order to save the coral recruits from multiple threats, a threat-specific conservation plan has to be established to conserve the corals in GOMMBR.
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Keywords: climate change; resilience; coral recruits; macroalgae; spatial map; phase shift; conservation.
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INTRODUCTION Coral reefs are outstanding among the marine ecosystems, because of its topographic complexity highly supports most of the reef-associated organisms (Idjadi and Edmunds, 2006). However, recent reports from global as well as regional, coral reefs are drastically declining due to climatic pressures coupled with human interventions (Hughes et al., 2003; Ateweberhan et al., 2013). The present scenario of anthropogenic and global climate change ultimately has reduced
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the live coral coverage, and it favored the macroalgae proliferations, which end up with phase shift scenarios (McManus and Polsenberg, 2004). Across the world coral reefs, many reports frequently
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concerning phase shift in terms of coral to macroalgae (Hughes, 1994; Done, 1992; Mumby, 2009; Bruno et al., 2009; Norstrom et al., 2009; Kelly et al., 2011). The phase shift can occur by various environmental disturbances such as diseases, predations, river run-off nutrients, hurricane, reduced
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herbivores and coral bleaching events (McManus and Polsenperg 2004; Rogers and Miller, 2006; Hughes et al., 2007; Ladlie et al., 2007). Besides, increased sedimentation load due to coastal development activities also affects the corals. Deposition of sediments on the coral surface, leading to retard the coral growth and thereby reducing its cover (Goatley and Bellwood, 2013). Recent decades, pressures exhibited by increased macroalgae and sedimentation is
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identified as a major hindrance to the survival of corals. Similarly, the Gulf of Mannar Marine Biosphere Reserve (GOMMBR) is not an exception to the global and regional scale threats. It is already reported that multiple threats such as bleaching events, phase shift, sedimentation and diseases (Arthur, 2000; Manikandan et al., 2014; Thangaradjou et al., 2014; Machendiranathan et
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al., 2014; Machendiranathan et al., 2016; Krishnan et al., 2018). Specific studies on enhanced macroalgal bloom due to increased nutrient load with increased reef fishing activities had been noticed and summarized in the process of Indian reef degradation (Manikandan and Ravindran,
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2016; Manikandan et al., 2014). It is evident that multiple threats suppress and alter the coral covers in GOMMBR, which resulted in the deterioration of corals from the last decade. Albeit, various disturbances altering the coral reef ecosystem, its recovering capability mainly depends on the resilience of newly settled coral recruits. It has well reported that the resilience of corals highly depends on the post-settlement survival rate of coral recruits that coincides with multiple environmental factors (Golbuu et al., 2007; Halford and Caley, 2009;
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McClanahan et al., 2012). All the resilience factors and indicators have been studied extensively for understanding the resilience of corals (Obura and Grimsditch, 2009; Maynard et al., 2010;
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McClanahan et al., 2012). Among the different environmental variables, such as resistant coral species, coral diversity, herbivore biomass, coral disease, macroalgae cover, and coral recruitment described as key indicators by Maynard et al. (2015). Based on the environmental factors,
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resilience scoring is an appropriate method to generate the spatial conservation plan to describe the protected/unprotected areas. There are few studies on the resilience of coral reefs were reported in the GOMMBR (Edward et al., 2012; Manikandan et al., 2017). However, spatial analysis of resilience mapping and conservation plan is lacking in the GOMMBR corals. Therefore, to fulfill the research gap the present study focused on the spatial resilience mapping of the coral recruits
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in GOMMBR.
Altogether, the present study aimed to map the resilience of coral recruits along GOMMBR islands, to understand spatial resilience and ultimately providing sites for implying conservation act towards the newly settled coral recruits.
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MATERIALS AND METHODS Study Area The Gulf of Mannar Marine Biosphere Reserve (GOMMBR) is located on the southeast
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coast of India. The GOMMBR (Fig.1) consists of 21 uninhabited islands, and conventionally the islands are categorized into four groups, which are Mandapam (Shingle, Krusadai, Pullivasal, Poomarichan, Manoliputti, Manoli, and Hare), Keezhakarai (Mulli, Valai, Thalaiyari, Appa, Poovarasanpatti, Vallimunai, and Anaipar), Vembar (Nallathanni, Puluvinichalli, and Upputhanni) and Tuticorin (Vilanguchalli, Kariyachalli, Koswari, and Van). Benthic Survey
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The study on the shallow water of GOMMBR corals assessed during the peak season of coral recruitment (from January to March 2014). Benthic surveys were conducted in and around
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the 20 islands, except submerged island of Poovarasanpatti due to difficulties in approachability. The resilience of coral recruits study only focused on highly distributed species such as, Acropora nobilis, Echinopora lamellosa, Montipora aequituberculata, Montipora digitata, and Acropora
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humilis. The survey was conducted by following the standard survey protocol (English et al., 1997). Based on the survey protocol, quadrats (0.25 m2) were placed randomly in and around the fore reef zone and observation made on percentage coverage of coral recruits, macroalgae, sedimentation, substratum suitability, bleaching prevalence, and disease prevalence. During the field survey, corals <5 cm size were considered as a coral recruit, as suggested by Edmunds et al.
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(1998). Notably, observations were made only on shallow water (0 to 6 m) corals of GOMMBR. Herbivore biomass was estimated based on the stationary point counts and observation denoted as g/m² (Green and Bellwood, 2009).
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Photosynthetically Active Radiation (PAR) Photosynthetically active radiation (PAR) data were downloaded from the MODIS (Moderate
Resolution
Imaging
Spectroradiometer)
ocean
color
data
portal
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(https://oceancolor.gsfc.nasa.gov/). The MODIS 4 km PAR (8-day composite unit Einstein E mday-1) data retrieved for the survey period (January to March 2014) and 103 coral recruits
locations corresponding to PAR values were extracted. Noise-free 43 composited PAR data were analyzed, and standard deviation values of that coral recruits locations used to perform the resilience calculation. The downloaded data processed with the help of desktop ArcGIS 10.1 version.
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Temperature Variability
Sea surface temperature (SST) changes were analyzed using the group for high-resolution
resolution
sea
surface
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sea surface temperature (GHRSST) data products with a spatial resolution of 1 km. Hightemperature
images
acquired
from
the
data
portal
(http://podaac.jpl.nasa.gov/GHRSST), and acquired SST data sets further processed in desktop
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ArcGIS 10.1 software. The standard deviation of temperature variability during the recruitment period (January to March 2014) for 103 coral recruits sites used in resilience calculation. GEBCO Bathymetry General
Bathymetric
Chart
of
the
Oceans
(GEBCO)
data
downloaded
(https://www.gebco.net/), and processed by using grid display software. Later, extracted depth data
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were included in the resilience index of coral recruits calculations and mapping section to provide a clear layout.
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Coral Resilience Index Assessment of resilience and anchored resilience score (ARS) are categorized into high (0.8-1.0 – low stress), medium (0.6-0.79), and low (<0.6 – high stress) as followed by Maynard
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and McLeod (2012). The assessment of the coral recruits resilience in this study carried out by the nine parameters. They are macroalgae proliferation, sedimentation cover, substratum suitability, herbivore biomass, bleaching prevalence, disease prevalence, temperature variability, photosynthetically active radiation (PAR) and depth of the sites. These parameters were chosen based on the benthic survey at GOMMBR and key variables of Maynard et al. (2015). Based on the quadrat observations, the percentage-based calculation applied for the variables such as coral
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recruits, macroalgae proliferation, sedimentation cover, substratum suitability, bleaching prevalence, and disease prevalence. The herbivore biomass (g/m2) measured as per the standard
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unit. Parameters such as temperature variability, photosynthetically active radiation (PAR), and depth data retrieved from the satellite observations and considered as unit less during the resilience index calculation.
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For example, the maximum coral recruits value in the region is 70%, the site with 70% receives a one, and the site with 60% gets a 0.86 (or 70 divided by 60). Anchoring values to the max value helps make clear exactly how different one site's value is from others. Anchored resilience scores of 0.8 to 1 represent high (relative) resilience potential, 0.6-0.79 medium, and low <0.6.
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Statistical Analysis
Principle component analyses (PCA) performed to find out the relative contribution of resilience indicators with its resilience scores of high (H), medium (M), and low (L). All statistical analyses performed using XLSTAT.
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RESULTS AND DISCUSSION The present study observed 103 coral recruitment sites in GOMMBR. Among the observations, M.digitata observed maximum of 41 sites. The remaining coral recruits such as
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A.nobilis>M.aequituberculata>E.lamellosa>A.humilis as 28, 23, 9 and 2 sites respectively. Survey observations confirms that macroalgae such as Caulerpa scalpelliformis (49), Caulerpa racemosa (29), Ulva reticulata (11), Turbinaria ornata (5), Chaetomorpha linum (4), Turbinaria conoides (3) and Kappaphycus alvarezii (2) as a major hindrance to the coral recruits in GOMMBR. Spatial resilience maps illustrates that among 103 recruits, 12 sites possessed high resilience while medium and low resilience observed for 75 and 16 sites, respectively (Fig. 2a & 2b). Based on the
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coral resilience index, low resilience sites observed in the islands of Krusadai, Hare, Thalaiyari, Appa, Valimunai, Koswari, and Van coral recruits. Among the low resilience sites, Valimunai and
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Van islands are highly vulnerable.
Grounds behind the low resilience of coral recruits are due to reduced herbivore biomass which ultimately favoring over growth of macroalgae in the reef system. Globally, it is well known
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and documented that herbivore biomass plays an essential role in reducing macroalgae in the reef system (Heenan and Williams, 2013; Maynard et al., 2015). The Palk Bay reefs in India with severe fishing activities have enhanced 80% of corals associated with algal turf cover (Manikandan et al., 2014). The present study also found that the average herbivore biomass as 148 g/m2. It’s clearly indicating that herbivore biomass is one of the critical issues in GOMMBR. Another study
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has shown that GOMMBR lost 16.5% of live coral cover due to macroalgae blooms during 2013 (Manikandan et al., 2016). All the opportunistic macroalgae were degrading the live coral cover in GOMMBR reefs with the trend in a coral-algal phase shift; notably, it is not only because of the invasive species of K.alvarezii (Machendiranathan et al., 2014).
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PCA results depict that the influence of variables and the coral recruitment scenario (Fig. 3). The horizontal axis PC1 was responsible for 24.19% of the variation, and the PCA eigenvector values have shown that sedimentation (-1.359), macroalgae (-1.227), and temperature variability
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(-0.620). These above factors are playing a critical role in final resilience scores among coral recruitment sites. The vertical axis PC2, was responsible for 20.98% of the variation, with PCA eigenvector values indicating that coral recruits (-0.119) and macroalgae directly proportional to the coral recruits (1.936) which signify as a vital factor of the differences among sites in final resilience scores. There is a stable gradient of resilience scores across the x and y-axis, showing that increasing herbivore biomass, are always associated with higher resilience scores. In
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contradiction, medium and low resilience highly associated with counter sites (Fig. 3). In addition to PCA analysis, the box and whisker plot (Fig. 4) also showing variables
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influences in the anchored resilience score. It's revealing that the lowest influence variability with the indicators for temperature variability, coral bleaching, and disease prevalence (considering box height) and most significant for macroalgae and sedimentation. Irregularity found in scores for
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temperature variability, coral bleaching, and diseases is so low among the reef sites, and these indicators could have excluded with minimal impact on the final rankings. Notably, the plot explains that depth playing a significant role and it varying from the 0 to 6m with an average of 2.9 m. The plot purely explains that the resilience scores are within the range of 0.62 to 0.72. This demonstrate that resilience of coral recruits sites were different from each other. From this plot, it
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is clear that most of the surveyed sites are not equal, and hence specific actions to support resilience at these sites may be suitable. Medium resilience of coral recruits sites observed in the islands of Shingle, Manoliputti, Pullivasal, Poomarichan, Mulli, Valai, Anaipar, Nallathanni, Vilanguchalli and Kariyachalli. It
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illustrates that majority of the coral recruits influenced by any of the one variables. Apart from macroalgae bloom (Fig. 5b & 5e), variables such as sedimentation (Fig. 5c), coral bleaching, and diseases also disturbs the coral recruits. Although the present study observed with very sparse
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bleaching of coral recruits (Fig. 5f), it is not a good sign for corals of GOMMBR. Analyses of GOMMBR SST data during the settlement period evidently demonstrate that the temperature ranged between 24.6 °C to 30.92 °C with an average SST of 27.54 °C. This region already reported that coral bleaching getting started prior to summer in the Tuticorin group of islands (Machendiranathan et al., 2014). Later, the bleaching event of corals with different life forms summarized (Krishnan et al., 2018). In addition to SST, analyses on PAR availability of the
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GOMMBR during the survey period revealed that maximum as, 57.83 E m-2 day-1 and average of 46.92 E m-2 day-1. During 2010 and 2011, bleaching occurred in Lakshadweep corals of India with
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a PAR value of 48 - 50 E m-2 day-1 (Ranith et al., 2014), it corroborates with the present study. In this context, coral bleaching paves the way to increased fleshy macroalgae on the corals immediately after the bleaching event (Pulido and McCook 2002). Supporting to this recent post
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bleaching survey results in Indian reefs revealed that reduction of live coral cover with increased macroalgae (Ranith and Kripa, 2019). Overall, corals in this reserve are facing a declining trend from the past decades due to multiple threats such as bleaching events (1998, 2010, 2014 and 2016), coral-algal phase shift, sedimentation load and coral diseases (Arthur, 2000; Manikandan et al., 2014; Thangaradjou et al., 2014; Machendiranathan et al., 2014; Machendiranathan et al.,
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2016; Krishnan et al., 2018). It is evident that global climate change directly affects the highly sensitive coral reef ecosystem coupled with human interventions (Ateweberhan et al., 2013). Higher resilience of coral recruits found in the Pulivinichalli and Upputhanni islands (Fig. 5a & 5 d). These islands observed with an average herbivore biomass as 289.18 g/m2. Notably, the
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average herbivore biomass is one-fold high in this island group, while comparing the overall average. The coral recruits may hold higher possibilities of survival rate against all resilience indicators in these islands. PCA results indicating that the presence of herbivore biomass
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(maximum observed as 600 g/m2) associated with high resilience class (Fig. 3). Results of the present study shows that newly recruited corals of GOMMBR failed to express their resilience against the multiple threats. An increase in macroalgae cover, ultimately slowdown the recovery of corals. For example, Taiwan reefs experienced that Acropora and Montipora lost its resilience and disappeared from this region due to multiple threats (Kuo et al., 2012). Although GOMMBR reefs well recruited, the macroalgae reducing its survival rate. This
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resilience study alarms that these reefs are exceptionally vulnerable. Competition between corals and macroalgae is a pivotal ecological process, especially during reef degradation, which often
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involves a 'phase-shift' from coral to macroalgae dominated reefs (Jomba and McCook, 2003). Besides, the resilience of the reef system studies helps to plan the reversal of phase shift from macroalgae dominance (Hughes et al., 2010). For example, Island of Moorea, French Polynesia
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reefs demonstrated that nearshore nursery habitat of herbivorous fishes maintaining reef resilience (Adams et al., 2011). In spite, most of the reefs reported that Indo-Pacific corals were facing high degradation and lead to a shifted trend in coral-algal (Roff and Mumby, 2012). Understanding influences among different mechanisms of resilience variables in coral recruitment are critical for reef management. However, this present study attempted to identify the
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major threats in GOMMBR with coral recruitment. Overall, serious concern about reef conservation in GOMMBR is very urgent, a threat-specific action need especially during the recruitment period.
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Acknowledgment We thank the Director and Dean, CAS in Marine Biology, and the Authorities of Annamalai University for providing necessary facilities. We also thank National Remote Sensing
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Centre, ISRO-Hyderabad for providing financial support and also the Principal Chief Conservator of Forests, Government of Tamilnadu, and Wild Life Warden of the Gulf of Mannar Marine Biosphere Reserve for providing necessary permission and supports during the fieldwork. The contents and views expressed in the manuscript are of individual authors and not reflect the position of the institutions they hold. The authors are grateful to the reviewer's comments and suggestions.
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Conflicts of interest
The authors declare no conflicts of interest.
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Obura, D.O. and G. Grimsdith, 2009. Resilience Assessment of coral reefs – Assessment protocol for coral reefs, focusing on coral bleaching and thermal stress. IUCN working group on Climate Change and Coral Reefs. IUCN, Gland, Switzerland. 70 pages.
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Pulido, D. G. and L. J. McCook, 2002. The fate of bleached corals: patterns and dynamics of algal recruitment. Mar. Ecol. Prog. Ser., 232: 115-128. Ranith, R. and Kripa, V., 2019. Post-bleaching benthic status on reef sites of Mandapam group of
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islands and Palk Bay, Indian Ocean following the 2016 bleaching events. Regional Studies in Marine Science, 27, p.100525.
Ranith, R., Senthilnathan, L., Machendiranathan, M., Thangaradjou, T., Kumar, A. S., Sasamal, S. K., & Choudhury, S. B.2016. Integrated role of SST, PAR and CDOM in summer reef bleaching during 2010 and 2011 along the Lakshadweep Islands. CURRENT SCIENCE, 110(9), 1832.
& evolution, 27(7), pp.404-413.
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Roff, G. and Mumby, P.J., 2012. Global disparity in the resilience of coral reefs. Trends in ecology
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Rogers, C.S. and J. Miller, 2006. Permanent ‘phase shifts’ or rever- sible declines in coral cover? Lack of recovery of two coral reefs in St. John, US Virgin Islands. Mar. Ecol. Prog. Ser., 306: 103–114.
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Thangaradjou, T., M. Machendiranathan, R. Ranith, L. Senthilnathan, S.K. Sasamal, and S.B. Choudhury, 2016. Coral disease prevalence in Gulf of Mannar and Lakshadweep Islands.
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Indian Journal of Marine Sciences,Vol. 45(12), pp.1755- 1762.
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Figures and Legends:
Fig. 1 Study area map of GOMMBR islands
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Fig. 2a. Spatial resilience mapping of the selected coral species in Mandapam group of islands in GOMMBR.
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Fig. 2b. Spatial resilience mapping of the selected coral species in Keezhakarai, Vembar and Tuticorin group of islands in GOMMBR. 20
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Fig. 3. Principal component analysis (PCA; n= 103) coordinates showing the relative contribution of resilience factors with its resilience ranking of high (H), medium (M) and low (L) and resilience indicators short forms, CR -Coral recruits, MA -Macro Algae, S -Sedimentation, HB -Herbivore Biomass, D –Depth, CB – Coral Bleaching, DP -Disease Prevalence, SS -Substrate Suitability, TV
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-Temperature Variability, PAR -Photosynthetically Active Radiation.
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Fig. 4. Box-Whisker analysis for influences of variables in the resilience rank. Boxes indicate the 25th to 75th percentile range, band in the middle represent the median value, lower and upper bands indicate minimum and maximum values respectively, dot displays arithmetic mean (Variables short forms, CR -Coral recruits, MA -Macro Algae, S -Sedimentation, HB -Herbivore
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Biomass, D –Depth, CB – Coral Bleaching, DP -Disease Prevalence, SS -Substrate Suitability, TV
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-Temperature Variability, PAR -Photosynthetically Active Radiation, RS - Resilience Score).
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Fig. 5. Benthic photographs of corals in GOMMBR. Newly recruited Acropora nobilis (a), A.nobilis colony with overgrowth of U.reticulata (b), sedimentation with the coral E.lamellosa (c),
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newly recruited healthy colony of M.digitata (d), newly recruited M.aequituberculata surrounded with the macroalgae proliferation (e), bleached status of newly recruited coral M.digitata with macroalgae proliferation (f).
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Figure Legends 1. Study area map of GOMMBR islands 2. a & b Spatial resilience mapping of the selected coral species in Keezhakarai, Vembar and
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Tuticorin group of islands in GOMMBR & Spatial resilience mapping of the selected coral species in Keezhakarai, Vembar and Tuticorin group of islands in GOMMBR. 3. Principal component analysis (PCA) coordinates showing the relative contribution of resilience factors with its resilience ranking of high (H), medium (M) and low (L) and resilience indicators short forms, CR -Coral recruits, MA -Macro Algae, S -Sedimentation, HB -Herbivore Biomass, D –Depth, CB – Coral Bleaching, DP -Disease Prevalence, SS -
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Substrate Suitability, TV -Temperature Variability, PAR - Photosynthetically Active Radiation.
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4. Box-Whisker analysis for influences of variables in the resilience rank (Variables short forms, CR -Coral recruits, MA -Macro Algae, S -Sedimentation, HB -Herbivore Biomass, D -Depth, CB -Coral Bleaching, DP -Disease Prevalence, SS -Substrate Suitability, TV -
Score).
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Temperature Variability, PAR -Photosynthetically Active Radiation, RS - Resilience
5. Benthic photographs of corals in GOMMBR. Newly recruited Acropora nobilis (a), A.nobilis colony with overgrowth of U.reticulata (b), sedimentation with the coral E.lamellosa (c), newly recruited healthy colony of M.digitata (d), newly recruited
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M.aequituberculata surrounded with the macroalgae proliferation (e), bleached status of newly recruited coral M.digitata with macroalgae proliferation (f).
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Declaration of interests ☒ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:
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Author Statement: Machendiranathan: Conceptualization, Methodology, Software, Data curation, Writing- Original draft preparation.
Thangaradjou and Saravanakumar: Supervision
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Machendiranathan: Writing-Reviewing and Editing
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Machendiranathan, Ranith, Senthilnathan and team: Visualization and Investigation.
PII: DOI: Reference:
S2352-4855(19)30043-X https://doi.org/10.1016/j.rsma.2020.101055 RSMA 101055
To appear in:
Regional Studies in Marine Science
Received date : 18 January 2019 Revised date : 1 January 2020 Accepted date : 5 January 2020 Please cite this article as: Machendiranathan M., R. Ranith, L. Senthilnathan et al., Resilience of coral recruits in Gulf of Mannar Marine Biosphere Reserve (GOMMBR), India. Regional Studies in Marine Science (2020), doi: https://doi.org/10.1016/j.rsma.2020.101055. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
© 2020 Published by Elsevier B.V.
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RESILIENCE OF CORAL RECRUITS IN GULF OF MANNAR MARINE BIOSPHERE RESERVE (GOMMBR), INDIA Machendiranathan M*1, 2, R. Ranith3, L. Senthilnathan4, A. Saravanakumar2, T. Thangaradjou5
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1. College of Ocean and Meteorology, Guangdong Ocean University, Zhanjiang– 524088, Guangdong, China.
2. Centre of Advanced Studies in Marine Biology, Faculty of Marine Sciences, Annamalai University, Parangipettai – 608502, Tamilnadu, India.
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3. Fishery Environment Management Division, Central Marine Fisheries Research Institute (CMFRI), Kochi - 682018, Kerala, India.
4. Marine Science & Technology Lab, Department of Harbor and Ocean Engineering, Academy
Tamilnadu, India.
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of Maritime Education and Training AMET (Deemed to be University), Chennai - 603112,
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5. Science and Engineering Research Board (SERB), New Delhi – 110070
Corresponding Author:
Dr. M. Machendiranathan*1, 2
Email ID: [email protected]
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Phone: +86 18934225446
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ABSTRACT Interaction between climate change and resilience of the coral recruits will determine the future of the coral reefs. The recently emerged resilience mapping has provided adequate
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information on spatial planning for marine protected /unprotected area conservation measures. The present study has dealt with mapping the resilience of coral recruits in the Gulf of Mannar Marine Biosphere Reserve (GOMMBR), India. The resilience indicators are macroalgae, sedimentation, substratum, herbivore biomass, bleaching prevalence, disease prevalence, temperature variability, photosynthetically active radiation (PAR), and depth of the site. Our benthic survey encountered 103 coral recruits sites with selected coral species of Montipora digitata (41) Acropora nobilis
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(28), Montipora aequituberculata (23), Echinopora lamellosa (9) and Acropora humilis (2). Among the 103 sites, 12 coral recruits sites showed high resilience, while medium and low
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resilience was observed in 75 and 16 sites, respectively. Our survey observations evidently demonstrated that frequent macroalgae such as Caulerpa scalpelliformis (49), Caulerpa racemosa (29), Ulva reticulata (11), Turbinaria ornata (5), Chaetomorpha linum (4), Turbinaria conoides
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(3) and Kappaphycus alvarezii (2), were identified as a major hindrance to coral recruits. The results of principal component analysis (PCA) showed that sedimentation, macroalgae, and temperature variability were the factors playing a major role among different sites. Among the islands of GOMMBR high resilience of coral recruits found in the Pulivinichalli and Upputhanni islands. While, low resilience sites observed in the islands of Krusadai, Hare, Thalaiyari, Appa,
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Valimunai, Koswari, and Van. Altogether, the present study provides a clear spatial view on the resilience situation of the GOMMBR corals recruitment. Altogether, in order to save the coral recruits from multiple threats, a threat-specific conservation plan has to be established to conserve the corals in GOMMBR.
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Keywords: climate change; resilience; coral recruits; macroalgae; spatial map; phase shift; conservation.
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INTRODUCTION Coral reefs are outstanding among the marine ecosystems, because of its topographic complexity highly supports most of the reef-associated organisms (Idjadi and Edmunds, 2006). However, recent reports from global as well as regional, coral reefs are drastically declining due to climatic pressures coupled with human interventions (Hughes et al., 2003; Ateweberhan et al., 2013). The present scenario of anthropogenic and global climate change ultimately has reduced
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the live coral coverage, and it favored the macroalgae proliferations, which end up with phase shift scenarios (McManus and Polsenberg, 2004). Across the world coral reefs, many reports frequently
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concerning phase shift in terms of coral to macroalgae (Hughes, 1994; Done, 1992; Mumby, 2009; Bruno et al., 2009; Norstrom et al., 2009; Kelly et al., 2011). The phase shift can occur by various environmental disturbances such as diseases, predations, river run-off nutrients, hurricane, reduced
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herbivores and coral bleaching events (McManus and Polsenperg 2004; Rogers and Miller, 2006; Hughes et al., 2007; Ladlie et al., 2007). Besides, increased sedimentation load due to coastal development activities also affects the corals. Deposition of sediments on the coral surface, leading to retard the coral growth and thereby reducing its cover (Goatley and Bellwood, 2013). Recent decades, pressures exhibited by increased macroalgae and sedimentation is
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identified as a major hindrance to the survival of corals. Similarly, the Gulf of Mannar Marine Biosphere Reserve (GOMMBR) is not an exception to the global and regional scale threats. It is already reported that multiple threats such as bleaching events, phase shift, sedimentation and diseases (Arthur, 2000; Manikandan et al., 2014; Thangaradjou et al., 2014; Machendiranathan et
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al., 2014; Machendiranathan et al., 2016; Krishnan et al., 2018). Specific studies on enhanced macroalgal bloom due to increased nutrient load with increased reef fishing activities had been noticed and summarized in the process of Indian reef degradation (Manikandan and Ravindran,
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2016; Manikandan et al., 2014). It is evident that multiple threats suppress and alter the coral covers in GOMMBR, which resulted in the deterioration of corals from the last decade. Albeit, various disturbances altering the coral reef ecosystem, its recovering capability mainly depends on the resilience of newly settled coral recruits. It has well reported that the resilience of corals highly depends on the post-settlement survival rate of coral recruits that coincides with multiple environmental factors (Golbuu et al., 2007; Halford and Caley, 2009;
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McClanahan et al., 2012). All the resilience factors and indicators have been studied extensively for understanding the resilience of corals (Obura and Grimsditch, 2009; Maynard et al., 2010;
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McClanahan et al., 2012). Among the different environmental variables, such as resistant coral species, coral diversity, herbivore biomass, coral disease, macroalgae cover, and coral recruitment described as key indicators by Maynard et al. (2015). Based on the environmental factors,
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resilience scoring is an appropriate method to generate the spatial conservation plan to describe the protected/unprotected areas. There are few studies on the resilience of coral reefs were reported in the GOMMBR (Edward et al., 2012; Manikandan et al., 2017). However, spatial analysis of resilience mapping and conservation plan is lacking in the GOMMBR corals. Therefore, to fulfill the research gap the present study focused on the spatial resilience mapping of the coral recruits
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in GOMMBR.
Altogether, the present study aimed to map the resilience of coral recruits along GOMMBR islands, to understand spatial resilience and ultimately providing sites for implying conservation act towards the newly settled coral recruits.
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MATERIALS AND METHODS Study Area The Gulf of Mannar Marine Biosphere Reserve (GOMMBR) is located on the southeast
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coast of India. The GOMMBR (Fig.1) consists of 21 uninhabited islands, and conventionally the islands are categorized into four groups, which are Mandapam (Shingle, Krusadai, Pullivasal, Poomarichan, Manoliputti, Manoli, and Hare), Keezhakarai (Mulli, Valai, Thalaiyari, Appa, Poovarasanpatti, Vallimunai, and Anaipar), Vembar (Nallathanni, Puluvinichalli, and Upputhanni) and Tuticorin (Vilanguchalli, Kariyachalli, Koswari, and Van). Benthic Survey
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The study on the shallow water of GOMMBR corals assessed during the peak season of coral recruitment (from January to March 2014). Benthic surveys were conducted in and around
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the 20 islands, except submerged island of Poovarasanpatti due to difficulties in approachability. The resilience of coral recruits study only focused on highly distributed species such as, Acropora nobilis, Echinopora lamellosa, Montipora aequituberculata, Montipora digitata, and Acropora
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humilis. The survey was conducted by following the standard survey protocol (English et al., 1997). Based on the survey protocol, quadrats (0.25 m2) were placed randomly in and around the fore reef zone and observation made on percentage coverage of coral recruits, macroalgae, sedimentation, substratum suitability, bleaching prevalence, and disease prevalence. During the field survey, corals <5 cm size were considered as a coral recruit, as suggested by Edmunds et al.
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(1998). Notably, observations were made only on shallow water (0 to 6 m) corals of GOMMBR. Herbivore biomass was estimated based on the stationary point counts and observation denoted as g/m² (Green and Bellwood, 2009).
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Photosynthetically Active Radiation (PAR) Photosynthetically active radiation (PAR) data were downloaded from the MODIS (Moderate
Resolution
Imaging
Spectroradiometer)
ocean
color
data
portal
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(https://oceancolor.gsfc.nasa.gov/). The MODIS 4 km PAR (8-day composite unit Einstein E mday-1) data retrieved for the survey period (January to March 2014) and 103 coral recruits
locations corresponding to PAR values were extracted. Noise-free 43 composited PAR data were analyzed, and standard deviation values of that coral recruits locations used to perform the resilience calculation. The downloaded data processed with the help of desktop ArcGIS 10.1 version.
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Temperature Variability
Sea surface temperature (SST) changes were analyzed using the group for high-resolution
resolution
sea
surface
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sea surface temperature (GHRSST) data products with a spatial resolution of 1 km. Hightemperature
images
acquired
from
the
data
portal
(http://podaac.jpl.nasa.gov/GHRSST), and acquired SST data sets further processed in desktop
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ArcGIS 10.1 software. The standard deviation of temperature variability during the recruitment period (January to March 2014) for 103 coral recruits sites used in resilience calculation. GEBCO Bathymetry General
Bathymetric
Chart
of
the
Oceans
(GEBCO)
data
downloaded
(https://www.gebco.net/), and processed by using grid display software. Later, extracted depth data
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were included in the resilience index of coral recruits calculations and mapping section to provide a clear layout.
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Coral Resilience Index Assessment of resilience and anchored resilience score (ARS) are categorized into high (0.8-1.0 – low stress), medium (0.6-0.79), and low (<0.6 – high stress) as followed by Maynard
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and McLeod (2012). The assessment of the coral recruits resilience in this study carried out by the nine parameters. They are macroalgae proliferation, sedimentation cover, substratum suitability, herbivore biomass, bleaching prevalence, disease prevalence, temperature variability, photosynthetically active radiation (PAR) and depth of the sites. These parameters were chosen based on the benthic survey at GOMMBR and key variables of Maynard et al. (2015). Based on the quadrat observations, the percentage-based calculation applied for the variables such as coral
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recruits, macroalgae proliferation, sedimentation cover, substratum suitability, bleaching prevalence, and disease prevalence. The herbivore biomass (g/m2) measured as per the standard
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unit. Parameters such as temperature variability, photosynthetically active radiation (PAR), and depth data retrieved from the satellite observations and considered as unit less during the resilience index calculation.
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For example, the maximum coral recruits value in the region is 70%, the site with 70% receives a one, and the site with 60% gets a 0.86 (or 70 divided by 60). Anchoring values to the max value helps make clear exactly how different one site's value is from others. Anchored resilience scores of 0.8 to 1 represent high (relative) resilience potential, 0.6-0.79 medium, and low <0.6.
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Statistical Analysis
Principle component analyses (PCA) performed to find out the relative contribution of resilience indicators with its resilience scores of high (H), medium (M), and low (L). All statistical analyses performed using XLSTAT.
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RESULTS AND DISCUSSION The present study observed 103 coral recruitment sites in GOMMBR. Among the observations, M.digitata observed maximum of 41 sites. The remaining coral recruits such as
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A.nobilis>M.aequituberculata>E.lamellosa>A.humilis as 28, 23, 9 and 2 sites respectively. Survey observations confirms that macroalgae such as Caulerpa scalpelliformis (49), Caulerpa racemosa (29), Ulva reticulata (11), Turbinaria ornata (5), Chaetomorpha linum (4), Turbinaria conoides (3) and Kappaphycus alvarezii (2) as a major hindrance to the coral recruits in GOMMBR. Spatial resilience maps illustrates that among 103 recruits, 12 sites possessed high resilience while medium and low resilience observed for 75 and 16 sites, respectively (Fig. 2a & 2b). Based on the
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coral resilience index, low resilience sites observed in the islands of Krusadai, Hare, Thalaiyari, Appa, Valimunai, Koswari, and Van coral recruits. Among the low resilience sites, Valimunai and
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Van islands are highly vulnerable.
Grounds behind the low resilience of coral recruits are due to reduced herbivore biomass which ultimately favoring over growth of macroalgae in the reef system. Globally, it is well known
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and documented that herbivore biomass plays an essential role in reducing macroalgae in the reef system (Heenan and Williams, 2013; Maynard et al., 2015). The Palk Bay reefs in India with severe fishing activities have enhanced 80% of corals associated with algal turf cover (Manikandan et al., 2014). The present study also found that the average herbivore biomass as 148 g/m2. It’s clearly indicating that herbivore biomass is one of the critical issues in GOMMBR. Another study
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has shown that GOMMBR lost 16.5% of live coral cover due to macroalgae blooms during 2013 (Manikandan et al., 2016). All the opportunistic macroalgae were degrading the live coral cover in GOMMBR reefs with the trend in a coral-algal phase shift; notably, it is not only because of the invasive species of K.alvarezii (Machendiranathan et al., 2014).
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PCA results depict that the influence of variables and the coral recruitment scenario (Fig. 3). The horizontal axis PC1 was responsible for 24.19% of the variation, and the PCA eigenvector values have shown that sedimentation (-1.359), macroalgae (-1.227), and temperature variability
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(-0.620). These above factors are playing a critical role in final resilience scores among coral recruitment sites. The vertical axis PC2, was responsible for 20.98% of the variation, with PCA eigenvector values indicating that coral recruits (-0.119) and macroalgae directly proportional to the coral recruits (1.936) which signify as a vital factor of the differences among sites in final resilience scores. There is a stable gradient of resilience scores across the x and y-axis, showing that increasing herbivore biomass, are always associated with higher resilience scores. In
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contradiction, medium and low resilience highly associated with counter sites (Fig. 3). In addition to PCA analysis, the box and whisker plot (Fig. 4) also showing variables
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influences in the anchored resilience score. It's revealing that the lowest influence variability with the indicators for temperature variability, coral bleaching, and disease prevalence (considering box height) and most significant for macroalgae and sedimentation. Irregularity found in scores for
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temperature variability, coral bleaching, and diseases is so low among the reef sites, and these indicators could have excluded with minimal impact on the final rankings. Notably, the plot explains that depth playing a significant role and it varying from the 0 to 6m with an average of 2.9 m. The plot purely explains that the resilience scores are within the range of 0.62 to 0.72. This demonstrate that resilience of coral recruits sites were different from each other. From this plot, it
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is clear that most of the surveyed sites are not equal, and hence specific actions to support resilience at these sites may be suitable. Medium resilience of coral recruits sites observed in the islands of Shingle, Manoliputti, Pullivasal, Poomarichan, Mulli, Valai, Anaipar, Nallathanni, Vilanguchalli and Kariyachalli. It
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illustrates that majority of the coral recruits influenced by any of the one variables. Apart from macroalgae bloom (Fig. 5b & 5e), variables such as sedimentation (Fig. 5c), coral bleaching, and diseases also disturbs the coral recruits. Although the present study observed with very sparse
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bleaching of coral recruits (Fig. 5f), it is not a good sign for corals of GOMMBR. Analyses of GOMMBR SST data during the settlement period evidently demonstrate that the temperature ranged between 24.6 °C to 30.92 °C with an average SST of 27.54 °C. This region already reported that coral bleaching getting started prior to summer in the Tuticorin group of islands (Machendiranathan et al., 2014). Later, the bleaching event of corals with different life forms summarized (Krishnan et al., 2018). In addition to SST, analyses on PAR availability of the
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GOMMBR during the survey period revealed that maximum as, 57.83 E m-2 day-1 and average of 46.92 E m-2 day-1. During 2010 and 2011, bleaching occurred in Lakshadweep corals of India with
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a PAR value of 48 - 50 E m-2 day-1 (Ranith et al., 2014), it corroborates with the present study. In this context, coral bleaching paves the way to increased fleshy macroalgae on the corals immediately after the bleaching event (Pulido and McCook 2002). Supporting to this recent post
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bleaching survey results in Indian reefs revealed that reduction of live coral cover with increased macroalgae (Ranith and Kripa, 2019). Overall, corals in this reserve are facing a declining trend from the past decades due to multiple threats such as bleaching events (1998, 2010, 2014 and 2016), coral-algal phase shift, sedimentation load and coral diseases (Arthur, 2000; Manikandan et al., 2014; Thangaradjou et al., 2014; Machendiranathan et al., 2014; Machendiranathan et al.,
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2016; Krishnan et al., 2018). It is evident that global climate change directly affects the highly sensitive coral reef ecosystem coupled with human interventions (Ateweberhan et al., 2013). Higher resilience of coral recruits found in the Pulivinichalli and Upputhanni islands (Fig. 5a & 5 d). These islands observed with an average herbivore biomass as 289.18 g/m2. Notably, the
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average herbivore biomass is one-fold high in this island group, while comparing the overall average. The coral recruits may hold higher possibilities of survival rate against all resilience indicators in these islands. PCA results indicating that the presence of herbivore biomass
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(maximum observed as 600 g/m2) associated with high resilience class (Fig. 3). Results of the present study shows that newly recruited corals of GOMMBR failed to express their resilience against the multiple threats. An increase in macroalgae cover, ultimately slowdown the recovery of corals. For example, Taiwan reefs experienced that Acropora and Montipora lost its resilience and disappeared from this region due to multiple threats (Kuo et al., 2012). Although GOMMBR reefs well recruited, the macroalgae reducing its survival rate. This
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resilience study alarms that these reefs are exceptionally vulnerable. Competition between corals and macroalgae is a pivotal ecological process, especially during reef degradation, which often
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involves a 'phase-shift' from coral to macroalgae dominated reefs (Jomba and McCook, 2003). Besides, the resilience of the reef system studies helps to plan the reversal of phase shift from macroalgae dominance (Hughes et al., 2010). For example, Island of Moorea, French Polynesia
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reefs demonstrated that nearshore nursery habitat of herbivorous fishes maintaining reef resilience (Adams et al., 2011). In spite, most of the reefs reported that Indo-Pacific corals were facing high degradation and lead to a shifted trend in coral-algal (Roff and Mumby, 2012). Understanding influences among different mechanisms of resilience variables in coral recruitment are critical for reef management. However, this present study attempted to identify the
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major threats in GOMMBR with coral recruitment. Overall, serious concern about reef conservation in GOMMBR is very urgent, a threat-specific action need especially during the recruitment period.
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Acknowledgment We thank the Director and Dean, CAS in Marine Biology, and the Authorities of Annamalai University for providing necessary facilities. We also thank National Remote Sensing
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Centre, ISRO-Hyderabad for providing financial support and also the Principal Chief Conservator of Forests, Government of Tamilnadu, and Wild Life Warden of the Gulf of Mannar Marine Biosphere Reserve for providing necessary permission and supports during the fieldwork. The contents and views expressed in the manuscript are of individual authors and not reflect the position of the institutions they hold. The authors are grateful to the reviewer's comments and suggestions.
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Conflicts of interest
The authors declare no conflicts of interest.
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Figures and Legends:
Fig. 1 Study area map of GOMMBR islands
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Fig. 2a. Spatial resilience mapping of the selected coral species in Mandapam group of islands in GOMMBR.
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Fig. 2b. Spatial resilience mapping of the selected coral species in Keezhakarai, Vembar and Tuticorin group of islands in GOMMBR. 20
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Fig. 3. Principal component analysis (PCA; n= 103) coordinates showing the relative contribution of resilience factors with its resilience ranking of high (H), medium (M) and low (L) and resilience indicators short forms, CR -Coral recruits, MA -Macro Algae, S -Sedimentation, HB -Herbivore Biomass, D –Depth, CB – Coral Bleaching, DP -Disease Prevalence, SS -Substrate Suitability, TV
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-Temperature Variability, PAR -Photosynthetically Active Radiation.
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Fig. 4. Box-Whisker analysis for influences of variables in the resilience rank. Boxes indicate the 25th to 75th percentile range, band in the middle represent the median value, lower and upper bands indicate minimum and maximum values respectively, dot displays arithmetic mean (Variables short forms, CR -Coral recruits, MA -Macro Algae, S -Sedimentation, HB -Herbivore
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Biomass, D –Depth, CB – Coral Bleaching, DP -Disease Prevalence, SS -Substrate Suitability, TV
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-Temperature Variability, PAR -Photosynthetically Active Radiation, RS - Resilience Score).
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Fig. 5. Benthic photographs of corals in GOMMBR. Newly recruited Acropora nobilis (a), A.nobilis colony with overgrowth of U.reticulata (b), sedimentation with the coral E.lamellosa (c),
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newly recruited healthy colony of M.digitata (d), newly recruited M.aequituberculata surrounded with the macroalgae proliferation (e), bleached status of newly recruited coral M.digitata with macroalgae proliferation (f).
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Figure Legends 1. Study area map of GOMMBR islands 2. a & b Spatial resilience mapping of the selected coral species in Keezhakarai, Vembar and
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Tuticorin group of islands in GOMMBR & Spatial resilience mapping of the selected coral species in Keezhakarai, Vembar and Tuticorin group of islands in GOMMBR. 3. Principal component analysis (PCA) coordinates showing the relative contribution of resilience factors with its resilience ranking of high (H), medium (M) and low (L) and resilience indicators short forms, CR -Coral recruits, MA -Macro Algae, S -Sedimentation, HB -Herbivore Biomass, D –Depth, CB – Coral Bleaching, DP -Disease Prevalence, SS -
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Substrate Suitability, TV -Temperature Variability, PAR - Photosynthetically Active Radiation.
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4. Box-Whisker analysis for influences of variables in the resilience rank (Variables short forms, CR -Coral recruits, MA -Macro Algae, S -Sedimentation, HB -Herbivore Biomass, D -Depth, CB -Coral Bleaching, DP -Disease Prevalence, SS -Substrate Suitability, TV -
Score).
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Temperature Variability, PAR -Photosynthetically Active Radiation, RS - Resilience
5. Benthic photographs of corals in GOMMBR. Newly recruited Acropora nobilis (a), A.nobilis colony with overgrowth of U.reticulata (b), sedimentation with the coral E.lamellosa (c), newly recruited healthy colony of M.digitata (d), newly recruited
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M.aequituberculata surrounded with the macroalgae proliferation (e), bleached status of newly recruited coral M.digitata with macroalgae proliferation (f).
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Declaration of interests ☒ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:
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Author Statement: Machendiranathan: Conceptualization, Methodology, Software, Data curation, Writing- Original draft preparation.
Thangaradjou and Saravanakumar: Supervision
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Machendiranathan: Writing-Reviewing and Editing
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Machendiranathan, Ranith, Senthilnathan and team: Visualization and Investigation.